Chapter 3 Anatomy, Structure, and Function of the Periodontium

C H A P T E R 3
Anatomy, Structure,
and Function of the
Periodontium
Joseph P. Fiorellini, David Kim, Yu-Cheng Chang
CHAPTER OUTLINE
Oral Mucosa
Gingiva
Periodontal Ligament
Cementum
Alveolar Process
Development of the Attachment Apparatus
External Forces and the Periodontium
Vascularization of the Supporting Structures
The normal periodontium provides the support necessary to
maintain teeth in function. It consists of four principal components:
181
gingiva, periodontal ligament, cementum, and alveolar bone. Each
of these periodontal components is distinct in its location, tissue
architecture, biochemical composition, and chemical composition,
but all of these components function together as a single unit.
Research has revealed that the extracellular matrix components of
one periodontal compartment can influence the cellular activities of
adjacent structures. Therefore the pathologic changes that occur in
one periodontal component may have significant ramifications for
the maintenance, repair, or regeneration of other components of the
periodontium.
18
This chapter first discusses the structural components of the
normal periodontium; it then describes their development,
vascularization, innervation, and functions.
Oral Mucosa
The oral mucosa consists of the following three zones:
1. The gingiva and the covering of the hard palate, termed the
masticatory mucosa (the gingiva is the part of the oral mucosa
that covers the alveolar processes of the jaws and surrounds
the necks of the teeth)
2. The dorsum of the tongue, covered by specialized mucosa
3. The oral mucous membrane lining the remainder of the oral
cavity
Gingiva
Clinical Features
In an adult, normal gingiva covers the alveolar bone and tooth root
to a level just coronal to the cementoenamel junction. The gingiva is
divided anatomically into marginal, attached, and interdental areas.
Although each type of gingiva exhibits considerable variation in
differentiation, histology, and thickness according to its functional
demands, all types are specifically structured to function
appropriately against mechanical and microbial damage.
7
In other
words, the specific structure of different types of gingiva reflects
182
each one's effectiveness as a barrier to the penetration by microbes
and noxious agents into the deeper tissue.
Marginal Gingiva
The marginal or unattached gingiva is the terminal edge or border
of the gingiva that surrounds the teeth in collar-like fashion (Figs.
3.1 and 3.2).
6
In about 50% of cases, it is demarcated from the
adjacent attached gingiva by a shallow linear depression called the
free gingival groove.
6
The marginal gingiva is usually about 1 mm
wide, and it forms the soft-tissue wall of the gingival sulcus. It may
be separated from the tooth surface with a periodontal probe. The
most apical point of the marginal gingival scallop is called the
gingival zenith. Its apicocoronal and mesiodistal dimensions vary
between 0.06 and 0.96 mm.
171
FIG. 3.1 Normal gingiva in a young adult. Note the
demarcation (mucogingival line) (arrows) between the
attached gingiva and the darker alveolar mucosa.
183
FIG. 3.2 Diagram showing the anatomic landmarks of
the gingiva.
Gingival Sulcus
The gingival sulcus is the shallow crevice or space around the tooth
bounded by the surface of the tooth on one side and the epithelium
lining the free margin of the gingiva on the other side. It is V-
shaped and barely permits the entrance of a periodontal probe. The
clinical determination of the depth of the gingival sulcus is an
important diagnostic parameter. Under absolutely normal or ideal
conditions, the depth of the gingival sulcus is 0 mm or close to 0
mm.
105
These strict conditions of normalcy can be produced
experimentally only in germ-free animals or after intense and
prolonged plaque control.
13,49
In clinically healthy human gingiva, a sulcus of some depth can
be found. The depth of this sulcus, as determined in histologic
sections, has been reported as 1.8 mm, with variations from 0 to 6
mm
195
; other studies have reported 1.5 mm
289
and 0.69 mm.
93
The
clinical evaluation used to determine the depth of the sulcus
involves the introduction of a metallic instrument (i.e., the
periodontal probe) and the estimation of the distance it penetrates
(i.e., the probing depth). The histologic depth of a sulcus does not
need to be exactly equal to the depth of penetration of the probe.
The penetration of the probe depends on several factors, such as
184
probe diameter, probing force, and level of inflammation.
91
Consequently, the probing depth is not necessarily exactly equal to
the histologic depth of the sulcus. The so-called probing depth of a
clinically normal gingival sulcus in humans is 2 to 3 mm (see
Chapter 32).
Attached Gingiva
The attached gingiva is continuous with the marginal gingiva. It is
firm, resilient, and tightly bound to the underlying periosteum of
alveolar bone. The facial aspect of the attached gingiva extends to
the relatively loose and movable alveolar mucosa; it is demarcated
by the mucogingival junction (see Fig. 3.2).
The width of the attached gingiva is another important clinical
parameter.
7
It is the distance between the mucogingival junction
and the projection on the external surface of the bottom of the
gingival sulcus or the periodontal pocket. It should not be confused
with the width of the keratinized gingiva, although this also includes
the marginal gingiva (see Fig. 3.2).
The width of the attached gingiva on the facial aspect differs in
different areas of the mouth.
40
It is generally greatest in the incisor
region (i.e., 3.5 to 4.5 mm in the maxilla, 3.3 to 3.9 mm in the
mandible) and narrower in the posterior segments (i.e., 1.9 mm in
the maxillary first premolars and 1.8 mm in the mandibular first
premolars)
6
(Fig. 3.3).
FIG. 3.3 Mean width of the attached gingiva in the
185
human permanent dentition.
Because the mucogingival junction remains stationary
throughout adult life,
4
changes in the width of the attached gingiva
are caused by modifications in the position of its coronal portion.
The width of the attached gingiva increases by the age of 4 years
and in supraerupted teeth.
5
On the lingual aspect of the mandible,
the attached gingiva terminates at the junction of the lingual
alveolar mucosa, which is continuous with the mucous membrane
that lines the floor of the mouth. The palatal surface of the attached
gingiva in the maxilla blends imperceptibly with the equally firm
and resilient palatal mucosa.
Interdental Gingiva
The interdental gingiva occupies the gingival embrasure, which is
the interproximal space beneath the area of tooth contact. The
interdental gingiva can be pyramidal, or it can have a “col” shape.
In the former, the tip of one papilla is located immediately beneath
the contact point; the latter presents a valley-like depression that
connects a facial and lingual papilla and that conforms to the shape
of the interproximal contact
62
(Figs. 3.4 and 3.5). The shape of the
gingiva in a given interdental space depends on the presence or
absence of a contact point between the adjacent teeth, the distance
between the contact point and the osseous crest,
260
and the presence
or absence of some degree of recession. Fig. 3.6 depicts the
variations in normal interdental gingiva.
186
FIG. 3.4 Site of extraction showing the facial and
palatal interdental papillae and the intervening col
(arrow).
FIG. 3.5 Faciolingual section of a monkey showing the
col between the facial and lingual interdental papillae.
The col is covered with nonkeratinized stratified
squamous epithelium.
187
FIG. 3.6 A diagram that compares anatomic variations
of the interdental col in the normal gingiva (left side)
and after gingival recession (right side). (A–B)
Mandibular anterior segment, facial and buccolingual
views, respectively. (C–D) Mandibular posterior region,
facial and buccolingual views, respectively. Tooth
contact points are shown with black marks in the lower
individual teeth.
The facial and lingual surfaces are tapered toward the
interproximal contact area, whereas the mesial and distal surfaces
are slightly concave. The lateral borders and tips of the interdental
papillae are formed by the marginal gingiva of the adjoining teeth.
The intervening portion consists of attached gingiva (Fig. 3.7). If a
diastema is present, the gingiva is firmly bound over the interdental
bone to form a smooth, rounded surface without interdental
papillae (Fig. 3.8).
FIG. 3.7 Interdental papillae (arrow) with a central
portion formed by the attached gingiva. The shape of
188
the papillae varies according to the dimension of the
gingival embrasure. (Courtesy Dr. Osvaldo Costa.)
FIG. 3.8 An absence of interdental papillae and col
where the proximal tooth contact is missing. (Courtesy Dr.
Osvaldo Costa.)
Microscopic Features
Microscopic examination reveals that gingiva is composed of the
overlying stratified squamous epithelium and the underlying
central core of connective tissue. Although the epithelium is
predominantly cellular in nature, the connective tissue is less
cellular and composed primarily of collagen fibers and ground
substance. These two tissues are considered separately. (A detailed
description of gingival histology can be found in Schroeder HE: The
periodontium, New York, 1986, Springer-Verlag; and in Biological
structure of the normal and diseased periodontium, Periodontol 2000
13:1, 1997.)
Gingival Epithelium
General Aspects of Gingival Epithelium Biology
Historically, the epithelial compartment was thought to provide
only a physical barrier to infection and the underlying gingival
attachment. However, we now believe that epithelial cells play an
active role in innate host defense by responding to bacteria in an
189
interactive manner,
67
which means that the epithelium participates
actively in responding to infection, in signaling further host
reactions, and in integrating innate and acquired immune
responses. For example, epithelial cells may respond to bacteria by
increased proliferation, the alteration of cell-signaling events,
changes in differentiation and cell death, and, ultimately, the
alteration of tissue homeostasis.
67
To understand this new
perspective of the epithelial innate defense responses and the role
of epithelium in gingival health and disease, it is important to
understand its basic structure and function (Box 3.1).
Box 3.1
Functions and Features of Gingival
Epithelium
Functions
Mechanical, chemical, water, and microbial barrier
Signaling functions
Architectural Integrity
Cell–cell attachments
Basal lamina
Keratin cytoskeleton
Major Cell Type
Keratinocyte
Other Cell Types
Langerhans cells
Melanocytes
Merkel cells
190
Constant Renewal
Replacement of damaged cells
Cell–Cell Attachments
Desmosomes
Adherens junctions
Tight junctions
Gap junctions
Cell–Basal Lamina
Synthesis of basal lamina components
Hemidesmosome
Modified from Dale BA: Periodontal epithelium: a newly recognized role in health and
disease. Periodontol 2000 30:71, 2002.
The gingival epithelium consists of a continuous lining of
stratified squamous epithelium. There are three different areas that
can be defined from the morphologic and functional points of view:
the oral or outer epithelium, the sulcular epithelium, and the
junctional epithelium.
The principal cell type of the gingival epithelium—as well as of
other stratified squamous epithelia—is the keratinocyte. Other cells
found in the epithelium are the clear cells or nonkeratinocytes,
which include the Langerhans cells, the Merkel cells, and the
melanocytes.
The main function of the gingival epithelium is to protect the
deep structures while allowing for a selective interchange with the
oral environment. This is achieved via the proliferation and
differentiation of the keratinocytes. The proliferation of keratinocytes
takes place by mitosis in the basal layer and less frequently in the
suprabasal layers, in which a small proportion of cells remain as a
proliferative compartment while a larger number begin to migrate
to the surface.
Differentiation involves the process of keratinization, which
191
consists of progressions of biochemical and morphologic events
that occur in the cell as they migrate from the basal layer (Fig. 3.9).
The main morphologic changes include the following: (1) the
progressive flattening of the cell with an increasing prevalence of
tonofilaments; (2) the couple of intercellular junctions with the
production of keratohyalin granules; and (3) the disappearance of
the nucleus. (See Schroeder
230
for further details.)
FIG. 3.9 Diagram showing representative cells from
the various layers of stratified squamous epithelium as
seen by electron microscopy. (Modified from Weinstock A: In Ham
AW: Histology, ed 7, Philadelphia, 1974, Lippincott.)
A complete keratinization process leads to the production of an
orthokeratinized superficial horny layer similar to that of the skin,
with no nuclei in the stratum corneum and a well-defined stratum
granulosum (Fig. 3.10). Only some areas of the outer gingival
epithelium are orthokeratinized; the other gingival areas are
covered by parakeratinized or nonkeratinized epithelium
45
and are
considered to be at intermediate stages of keratinization. These
areas can progress to maturity or dedifferentiate under different
192
physiologic or pathologic conditions.
FIG. 3.10 (A) Scanning electron micrograph of
keratinized gingiva showing the flattened keratinocytes
and their boundaries on the surface of the gingiva
(×1000). (B) Scanning electron micrograph of the
gingival margin at the edge of the gingival sulcus
showing several keratinocytes about to be exfoliated
(×3000). (From Kaplan GB, Pameijer CH, Ruben MP: J Periodontol 48:446,
1977.)
In parakeratinized epithelia, the stratum corneum retains pyknotic
nuclei, and the keratohyalin granules are dispersed rather than
giving rise to a stratum granulosum. The nonkeratinized epithelium
(although cytokeratins are the major component, as in all epithelia)
has neither granulosum nor corneum strata, whereas superficial
cells have viable nuclei.
Immunohistochemistry, gel electrophoresis, and immunoblot
techniques have made the identification of the characteristic pattern
of cytokeratins possible in each epithelial type. The keratin proteins
are composed of different polypeptide subunits characterized by
their isoelectric points and molecular weights. They are numbered
in a sequence that is contrary to their molecular weight. In general,
193
basal cells begin synthesizing lower-molecular-weight keratins
(e.g., K19 [40 kD]), and they express other higher-molecular-weight
keratins as they migrate to the surface. K1 keratin polypeptide (68
kD) is the main component of the stratum corneum.
60
Other proteins unrelated to keratins are synthesized during the
maturation process. The most extensively studied are keratolinin
and involucrin, which are precursors of a chemically resistant
structure (the envelope) located below the cell membrane, and
filaggrin, which has precursors that are packed into the keratohyalin
granules. At the sudden transition to the horny layer, the
keratohyalin granules disappear and give rise to filaggrin, which
forms the matrix of the most differentiated epithelial cell, the
corneocyte.
Thus in the fully differentiated state, the corneocytes are mainly
formed by bundles of keratin tonofilaments embedded in an
amorphous matrix of filaggrin and surrounded by a resistant
envelope under the cell membrane. The immunohistochemical
patterns of the different keratin types, envelope proteins, and
filaggrin change under normal or pathologic stimuli, thereby
modifying the keratinization process.
128130
Electron microscopy reveals that keratinocytes are interconnected
by structures on the cell periphery called desmosomes.
154
These
desmosomes have a typical structure that consists of two dense
attachment plaques into which tonofibrils insert and an
intermediate, electron-dense line in the extracellular compartment.
Tonofilaments, which are the morphologic expression of the
cytoskeleton of keratin proteins, radiate in brushlike fashion from
the attachment plaques into the cytoplasm of the cells. The space
between the cells shows cytoplasmic projections that resemble
microvilli and that extend into the intercellular space and often
interdigitate.
Less frequently observed forms of epithelial cell connections are
tight junctions (zonae occludens), in which the membranes of the
adjoining cells are thought to be fused.
268,287
Evidence suggests that
these structures allow ions and small molecules to pass from one
cell to another.
Cytoplasmic organelle concentration varies among different
epithelial strata. Mitochondria are more numerous in deeper strata
194
and decrease toward the surface of the cell.
Accordingly, the histochemical demonstration of succinic
dehydrogenase, nicotinamide-adenine dinucleotide, cytochrome
oxidase, and other mitochondrial enzymes reveals a more active
tricarboxylic cycle in basal and parabasal cells, in which the
proximity of the blood supply facilitates energy production through
aerobic glycolysis.
Conversely, enzymes of the pentose shunt (an alternative
pathway of glycolysis), such as glucose-6-phosphatase, increase
their activity toward the surface. This pathway produces a larger
amount of intermediate products for the production of ribonucleic
acid (RNA), which in turn can be used for the synthesis of
keratinization proteins. This histochemical pattern is in accordance
with the increased volume and the amount of tonofilaments
observed in cells reaching the surface; the intensity of the activity is
proportional to the degree of differentiation.
72,82,127,202
The uppermost cells of the stratum spinosum contain numerous
dense granules called keratinosomes or Odland bodies, which are
modified lysosomes. They contain a large amount of acid
phosphatase, an enzyme involved in the destruction of organelle
membranes, which occurs suddenly between the granulosum and
corneum strata and during the intercellular cementation of
cornified cells. Thus acid phosphatase is another enzyme that is
closely related to the degree of keratinization.
46,125,284
These contain
tyrosinase, which hydroxylates tyrosine to dihydroxyphenylalanine
(dopa), which in turn is progressively converted to melanin.
Melanin granules are phagocytosed and contained within other
cells of the epithelium and connective tissue called melanophages or
melanophores.
Nonkeratinocyte cells are present in gingival epithelium as in
other malpighian epithelia. Melanocytes are dendritic cells located in
the basal and spinous layers of the gingival epithelium. They
synthesize melanin in organelles called premelanosomes or
melanosomes
61,228,252
(Fig. 3.11).
195
FIG. 3.11 Pigmented gingiva of dog showing
melanocytes (M) in the basal epithelial layer and
melanophores (C) in the connective tissue (Glucksman
technique).
Langerhans cells are dendritic cells located among keratinocytes at
all suprabasal levels (Fig. 3.12). They belong to the mononuclear
phagocyte system (reticuloendothelial system) as modified
monocytes derived from the bone marrow. They contain elongated
granules, and they are considered macrophages with possible
antigenic properties.
72
Langerhans cells have an important role in
the immune reaction as antigen-presenting cells for lymphocytes.
They contain g-specific granules (Birbeck granules), and they have
marked adenosine triphosphatase activity. They are found in the
oral epithelium of normal gingiva and in smaller amounts in the
sulcular epithelium; they are probably absent from the junctional
epithelium of normal gingiva.
196
FIG. 3.12 Human gingival epithelium, oral aspect.
Immunoperoxidase technique showing Langerhans
cells.
Merkel cells are located in the deeper layers of the epithelium;
they harbor nerve endings, and they are connected to adjacent cells
by desmosomes. They have been identified as tactile perceptors.
188
The epithelium is joined to the underlying connective tissue by a
basal lamina 300 to 400 Å thick and lying approximately 400 Å
beneath the epithelial basal layer.
147,235,254
The basal lamina consists
of lamina lucida and lamina densa. Hemidesmosomes of the basal
epithelial cells abut the lamina lucida, which is mainly composed of
the glycoprotein laminin. The lamina densa is composed of type IV
collagen.
The basal lamina, which is clearly distinguishable at the
ultrastructural level, is connected to a reticular condensation of the
underlying connective tissue fibrils (mainly collagen type IV) by the
anchoring fibrils.
183,213,257
Anchoring fibrils have been measured at
750 nm in length from their epithelial end to their connective tissue
end, where they appear to form loops around collagen fibers. The
complex of basal lamina and fibrils is the periodic acid–Schiff–
positive and argyrophilic line observed at the optical level
237,258
(Fig.
3.13). The basal lamina is permeable to fluids, but it acts as a barrier
to particulate matter.
197
FIG. 3.13 Normal human gingiva stained with the
periodic acid–Schiff histochemical method. The
basement membrane (B) is seen between the
epithelium (E) and the underlying connective tissue
(C). In the epithelium, glycoprotein material occurs in
cells and cell membranes of the superficial hornified
(H) and underlying granular layers (G). The connective
tissue presents a diffuse, amorphous ground
substance and collagen fibers. The blood vessel walls
stand out clearly in the papillary projections of the
connective tissue (P).
Structural and Metabolic Characteristics of Different Areas
of Gingival Epithelium
The epithelial component of the gingiva shows regional
morphologic variations that reflect tissue adaptation to the tooth
and alveolar bone.
231
These variations include the oral epithelium,
the sulcular epithelium, and the junctional epithelium. Whereas the
oral epithelium and the sulcular epithelium are largely protective in
function, the junctional epithelium serves many more roles and is of
considerable importance in the regulation of tissue health.
18
It is
now recognized that epithelial cells are not passive bystanders in
the gingival tissues; rather, they are metabolically active and
capable of reacting to external stimuli by synthesizing a number of
cytokines, adhesion molecules, growth factors, and enzymes.
18
The degree of gingival keratinization diminishes with age and the
onset of menopause,
199
but it is not necessarily related to the
different phases of the menstrual cycle.
131
Keratinization of the oral
198
mucosa varies in different areas in the following order: palate (most
keratinized), gingiva, ventral aspect of the tongue, and cheek (least
keratinized).
181
Keratins K1, K2, and K10 through K12, which are specific to
epidermal-type differentiation, are immunohistochemically
expressed with high intensity in orthokeratinized areas and with
less intensity in parakeratinized areas. K6 and K16, which are
characteristic of highly proliferative epithelia, and K5 and K14,
which are stratification-specific cytokeratins, also are present.
Parakeratinized areas express K19, which is usually absent from
orthokeratinized normal epithelia.
37,205
In keeping with the complete or almost-complete maturation,
histoenzyme reactions for acid phosphatase and pentose-shunt
enzymes are very strong.
47,127
Glycogen can accumulate intracellularly when it is not
completely degraded by any of the glycolytic pathways. Thus its
concentration in normal gingiva is inversely related to the degree of
keratinization
236,285
and inflammation.
71,273,276
Oral (Outer) Epithelium
The oral or outer epithelium covers the crest and outer surface of
the marginal gingiva and the surface of the attached gingiva. On
average, the oral epithelium is 0.2 to 0.3 mm in thickness. It is
keratinized or parakeratinized, or it may present various
combinations of these conditions (Fig. 3.14). The prevalent surface,
however, is parakeratinized.
32,45,285
The oral epithelium is composed
of four layers: stratum basale (basal layer), stratum spinosum
(prickle cell layer), stratum granulosum (granular layer), and
stratum corneum (cornified layer).
199
FIG. 3.14 Variations in the gingival epithelium. (A)
Keratinized. (B) Nonkeratinized. (C) Parakeratinized.
Horny layer (H), granular layer (G), prickle cell layer
(P), basal cell layer (Ba), flattened surface cells (S),
and parakeratotic layer (Pk).
Sulcular Epithelium
The sulcular epithelium lines the gingival sulcus (Fig. 3.15). It is a
thin, nonkeratinized stratified squamous epithelium without rete
pegs, and it extends from the coronal limit of the junctional
epithelium to the crest of the gingival margin (Fig. 3.16). It usually
shows many cells with hydropic degeneration.
32
FIG. 3.15 Scanning electron microscopic view of the
200
epithelial surface facing the tooth in a normal human
gingival sulcus. The epithelium (Ep) shows
desquamating cells, some scattered erythrocytes (E),
and a few emerging leukocytes (L). (×1000.)
FIG. 3.16 Epon-embedded human biopsy specimen
showing a relatively normal gingival sulcus. The soft-
tissue wall of the gingival sulcus is made up of the oral
sulcular epithelium (ose) and its underlying connective
tissue (ct), whereas the base of the gingival sulcus is
formed by the sloughing surface of the junctional
epithelium (je). The enamel space is delineated by a
dense cuticular structure (dc). A relatively sharp line of
demarcation exists between the junctional epithelium
and the oral sulcular epithelium (arrow), and several
polymorphonuclear leukocytes (pmn) can be seen
traversing the junctional epithelium. The sulcus
contains red blood cells that resulted from the
hemorrhage that occurred at the time of biopsy. (×391;
inset ×55.) (From Schluger S, Youdelis R, Page RC: Periodontal disease, ed
2, Philadelphia, 1990, Lea & Febiger.)
201
As with other nonkeratinized epithelia, the sulcular epithelium
lacks granulosum and corneum strata and K1, K2, and K10 through
K12 cytokeratins, but it contains K4 and K13, the so-called
esophageal-type cytokeratins. It also expresses K19, and it normally
does not contain Merkel cells.
Histochemical studies of enzymes have consistently revealed a
lower degree of activity in the sulcular than in the outer epithelium,
particularly in the case of enzymes related to keratinization.
Glucose-6-phosphate dehydrogenase expresses a faint and
homogeneous reaction in all strata, unlike the increasing gradient
toward the surface observed in cornified epithelia.
127
Acid
phosphatase staining is negative,
46
although lysosomes have been
described in exfoliated cells.
148
Despite these morphologic and chemical characteristics, the
sulcular epithelium has the potential to keratinize if it is reflected
and exposed to the oral cavity
44,48
or if the bacterial flora of the
sulcus is totally eliminated.
50
Conversely, the outer epithelium loses
its keratinization when it is placed in contact with the tooth.
50
These
findings suggest that the local irritation of the sulcus prevents
sulcular keratinization.
The sulcular epithelium is extremely important; it may act as a
semipermeable membrane through which injurious bacterial
products pass into the gingiva and through which tissue fluid from
the gingiva seeps into the sulcus.
267
Unlike the junctional
epithelium, however, the sulcular epithelium is not heavily
infiltrated by polymorphonuclear neutrophil leukocytes, and it
appears to be less permeable.
18
Junctional Epithelium
The junctional epithelium consists of a collar-like band of stratified
squamous nonkeratinizing epithelium. It is 3 to 4 layers thick in
early life, but that number increases with age to 10 or even 20
layers. In addition, the junctional epithelium tapers from its coronal
end, which may be 10 to 29 cells wide to 1 or 2 cells wide at its
apical termination, which is located at the cementoenamel junction
in healthy tissue. These cells can be grouped in two strata: the basal
layer that faces the connective tissue and the suprabasal layer that
extends to the tooth surface. The length of the junctional epithelium
202
ranges from 0.25 to 1.35 mm (Fig. 3.17).
FIG. 3.17 Eruption process in cat's tooth. (A)
Unerupted tooth. Dentin (D), remnants of enamel
matrix (E), reduced enamel epithelium (REE), oral
epithelium (OE), and artifact (a). (B) Erupting tooth
forming junctional epithelium (JE). (C) Completely
erupted tooth. Sulcus with epithelial debris (S),
cementum (C), and epithelial rests (ER).
The junctional epithelium is formed by the confluence of the oral
epithelium and the reduced enamel epithelium during tooth
eruption. However, the reduced enamel epithelium is not essential
for its formation; in fact, the junctional epithelium is completely
restored after pocket instrumentation or surgery, and it forms
around an implant.
151
Cell layers that are not juxtaposed to the tooth exhibit numerous
free ribosomes, prominent membrane-bound structures (e.g., Golgi
complexes), and cytoplasmic vacuoles that are presumably
phagocytic. Lysosome-like bodies also are present, but the absence
of keratinosomes (Odland bodies) and histochemically
demonstrable acid phosphatase, which are correlated with the low
degree of differentiation, may reflect a low-defense power against
microbial plaque accumulation in the gingival sulcus. Similar
morphologic findings have been described in the gingiva of germ-
free rats. Polymorphonuclear neutrophil leukocytes are found
203
routinely in the junctional epithelium of both conventional rats and
germ-free rats.
296
Research has shown that, although numerous
migrating polymorphonuclear neutrophil leukocytes are evident
and present around healthy junctional epithelium, a considerable
increase in polymorphonuclear neutrophil leukocyte numbers can
be expected with the accumulation of dental plaque and gingival
inflammation.
18
The different keratin polypeptides of the junctional epithelium
have a particular histochemical pattern. Junctional epithelium
expresses K19, which is absent from keratinized epithelia, and the
stratification-specific cytokeratins K5 and K14.
224
Morgan and
colleagues
182
reported that reactions to demonstrate K4 or K13
reveal a sudden change between sulcular and junctional epithelia;
the junctional area is the only stratified nonkeratinized epithelium
in the oral cavity that does not synthesize these specific
polypeptides. Another particular behavior of junctional epithelium
is the lack of expression of K6 and K16, which is usually linked to
highly proliferative epithelia, although the turnover of the cells is
very high.
Similar to sulcular epithelium, junctional epithelium exhibits
lower glycolytic enzyme activity than outer epithelium, and it also
lacks acid phosphatase activity.
46,127
The junctional epithelium is attached to the tooth surface
(epithelial attachment) by means of an internal basal lamina. It is
attached to the gingival connective tissue by an external basal
lamina that has the same structure as other epithelial–connective
tissue attachments elsewhere in the body.
155,161
The internal basal lamina consists of a lamina densa (adjacent to
the enamel) and a lamina lucida to which hemidesmosomes are
attached. Hemidesmosomes have a decisive role in the firm
attachment of the cells to the internal basal lamina on the tooth
surface.
Data suggest that the hemidesmosomes may also act as specific
sites of signal transduction and thus may participate in the
regulation of gene expression, cell proliferation, and cell
differentiation.
134
Organic strands from the enamel appear to extend
into the lamina densa.
256
The junctional epithelium attaches to
afibrillar cementum that is present on the crown (usually restricted
204
to an area within 1 mm of the cementoenamel junction)
233
and root
cementum in a similar manner.
Histochemical evidence for the presence of neutral
polysaccharides in the zone of the epithelial attachment has been
reported.
272
Data also have shown that the basal lamina of the
junctional epithelium resembles that of endothelial and epithelial
cells in its laminin content but differs in its internal basal lamina,
which has no type IV collagen.
142,223
These findings indicate that the
cells of the junctional epithelium are involved in the production of
laminin and play a key role in the adhesion mechanism.
The attachment of the junctional epithelium to the tooth is
reinforced by the gingival fibers, which brace the marginal gingiva
against the tooth surface. For this reason, the junctional epithelium
and the gingival fibers are considered together as a functional unit
referred to as the dentogingival unit.
158
In conclusion, it is usually accepted that the junctional epithelium
exhibits several unique structural and functional features that
contribute to preventing pathogenic bacterial flora from colonizing
the subgingival tooth surface.
205
First, junctional epithelium is
firmly attached to the tooth surface, thereby forming an epithelial
barrier against plaque bacteria. Second, it allows access of gingival
fluid, inflammatory cells, and components of the immunologic host
defense to the gingival margin. Third, junctional epithelial cells
exhibit rapid turnover, which contributes to the host–parasite
equilibrium and the rapid repair of damaged tissue. Some
investigators have also indicated that the cells of the junctional
epithelium have an endocytic capacity equal to that of macrophages
and neutrophils and that this activity may be protective in nature.
57
Development of Gingival Sulcus
After enamel formation is complete, the enamel is covered with
reduced enamel epithelium (REE), which is attached to the tooth by a
basal lamina and hemidesmosomes.
156,255
When the tooth penetrates
the oral mucosa, the REE unites with the oral epithelium and
transforms into the junctional epithelium. As the tooth erupts, this
united epithelium condenses along the crown, and the ameloblasts,
which form the inner layer of the REE (see Fig. 3.17), gradually
become squamous epithelial cells. The transformation of the REE
205
into a junctional epithelium proceeds in an apical direction without
interrupting the attachment to the tooth. According to Schroeder
and Listgarten,
233
this process takes between 1 and 2 years.
The junctional epithelium is a continually self-renewing
structure, with mitotic activity occurring in all cell layers.
156,255
The
regenerating epithelial cells move toward the tooth surface and
along it in a coronal direction to the gingival sulcus, where they are
shed
22
(Fig. 3.18). The migrating daughter cells provide a
continuous attachment to the tooth surface. The strength of the
epithelial attachment to the tooth has not been measured.
FIG. 3.18 Junctional epithelium on an erupting tooth.
The junctional epithelium (JE) is formed by the joining
of the oral epithelium (OE) and the reduced enamel
epithelium (REE). Afibrillar cementum (AC) is
sometimes formed on enamel after the degeneration of
the REE. The arrows indicate the coronal movement of
the regenerating epithelial cells, which multiply more
rapidly in the JE than in the OE. E, Enamel; C, root
cementum. A similar cell turnover pattern exists in the
fully erupted tooth. (Modified from Listgarten MA: J Can Dent Assoc
36:70, 1970.)
206
The gingival sulcus is formed when the tooth erupts into the oral
cavity. At that time, the junctional epithelium and the REE form a
broad band that is attached to the tooth surface from near the tip of
the crown to the cementoenamel junction. The gingival sulcus is the
shallow, V-shaped space or groove between the tooth and the
gingiva that encircles the newly erupted tip of the crown. In the
fully erupted tooth, only the junctional epithelium persists. The
sulcus consists of the shallow space that is coronal to the attachment of the
junctional epithelium and bounded by the tooth on one side and the
sulcular epithelium on the other. The coronal extent of the gingival sulcus
is the gingival margin.
Renewal of Gingival Epithelium
The oral epithelium undergoes continuous renewal. Its thickness is
maintained by a balance between new cell formation in the basal
and spinous layers and the shedding of old cells at the surface. The
mitotic activity exhibits a 24-hour periodicity, with the highest and
lowest rates occurring in the morning and evening, respectively.
256
The mitotic rate is higher in nonkeratinized areas and increased in
gingivitis, without significant gender differences. Opinions differ
with regard to whether the mitotic rate is increased
160,161,179
or
decreased
15
with age.
The mitotic rate in experimental animals varies among different
areas of the oral epithelium in descending order: buccal mucosa,
hard palate, sulcular epithelium, junctional epithelium, outer
surface of the marginal gingiva, and attached gingiva.
9,112,160,274
The
following have been reported as turnover times for different areas
of the oral epithelium in experimental animals: palate, tongue, and
cheek, 5 to 6 days; gingiva, 10 to 12 days, with the same or more
time required with age; and junctional epithelium, 1 to 6 days.
22,249
With regard to junctional epithelium, it was previously thought
that only epithelial cells facing the external basal lamina were
rapidly dividing. However, evidence indicates that a significant
number of the cells (e.g., the basal cells along the connective tissue)
are capable of synthesizing deoxyribonucleic acid (DNA), thereby
demonstrating their mitotic activity.
221,222
The rapid shedding of
cells effectively removes bacteria that adhere to the epithelial cells
and therefore is an important part of the antimicrobial defense
207
mechanisms at the dentogingival junction.
205
Cuticular Structures on the Tooth
The term cuticle describes a thin acellular structure with a
homogeneous matrix that is sometimes enclosed within clearly
demarcated linear borders.
Listgarten
159
has classified cuticular structures into coatings of
developmental origin and acquired coatings. Acquired coatings
include those of exogenous origin such as saliva, bacteria, calculus,
and surface stains (see Chapters 7 and 13). Coatings of developmental
origin are those that are normally formed as part of tooth
development. They include the REE, the coronal cementum, and the
dental cuticle.
After enamel formation is completed, the ameloblastic epithelium
is reduced to one or two layers of cells that remain attached to the
enamel surface by hemidesmosomes and a basal lamina. This REE
consists of postsecretory ameloblasts and cells from the stratum
intermedium of the enamel organ. In some animal species, the REE
disappears entirely and rapidly, thereby placing the enamel surface
in contact with the connective tissue. Connective tissue cells then
deposit a thin layer of cementum known as coronal cementum on the
enamel. In humans, thin patches of afibrillar cementum sometimes
may be seen in the cervical half of the crown.
Electron microscopy has demonstrated a dental cuticle that
consists of a layer of homogeneous organic material of variable
thickness (approximately 0.25 µm) overlying the enamel surface. It
is nonmineralized, and it is not always present. In some cases, near
the cementoenamel junction, it is deposited over a layer of afibrillar
cementum, which in turn overlies enamel. The cuticle may be
present between the junctional epithelium and the tooth.
Ultrastructural histochemical studies have shown that the dental
cuticle is proteinaceous,
143
and it may be an accumulation of tissue
fluid components.
87,232
Gingival Fluid (Sulcular Fluid)
The value of the gingival fluid is that it can be represented as either
a transudate or an exudate. The gingival fluid contains a vast array
of biochemical factors, thereby offering its potential use as a
208
diagnostic or prognostic biomarker of the biologic state of the
periodontium in health and disease
81
(see Chapter 16). It also
contains components of connective tissue, epithelium,
inflammatory cells, serum, and microbial flora that inhabit the
gingival margin or the sulcus (pocket).
79
In the healthy sulcus, the amount of gingival fluid is very small.
During inflammation, however, the gingival fluid flow increases,
and its composition starts to resemble that of an inflammatory
exudate.
59
The main route of the gingival fluid diffusion is through
the basement membrane, through the relatively wide intercellular
spaces of the junctional epithelium, and then into the sulcus.
205
The
gingival fluid is believed to do the following: (1) cleanse material
from the sulcus; (2) contain plasma proteins that may improve
adhesion of the epithelium to the tooth; (3) possess antimicrobial
properties; and (4) exert antibody activity to defend the gingiva.
Gingival Connective Tissue
The major components of the gingival connective tissue are
collagen fibers (about 60% by volume), fibroblasts (5%), vessels,
nerves, and matrix (about 35%). The connective tissue of the
gingiva is known as the lamina propria, and it consists of two layers:
(1) a papillary layer subjacent to the epithelium that consists of
papillary projections between the epithelial rete pegs and (2) a
reticular layer that is contiguous with the periosteum of the alveolar
bone.
Connective tissue has a cellular compartment and an extracellular
compartment composed of fibers and ground substance. Thus the
gingival connective tissue is largely a fibrous connective tissue that
has elements that originate directly from the oral mucosal
connective tissue as well as some fibers (dentogingival) that
originate from the developing dental follicle.
18
The ground substance fills the space between fibers and cells; it is
amorphous, and it has a high water content. It is composed of
proteoglycans (mainly hyaluronic acid and chondroitin sulfate) and
glycoproteins (mainly fibronectin). Glycoproteins account for the
faint periodic acid–Schiff–positive reaction of the ground
substance.
82
Fibronectin binds fibroblasts to the fibers and many
other components of the intercellular matrix, thereby helping to
209
mediate cell adhesion and migration. Laminin, which is another
glycoprotein found in the basal lamina, serves to attach it to
epithelial cells.
The three types of connective tissue fibers are collagen, reticular,
and elastic. Collagen type I forms the bulk of the lamina propria
and provides the tensile strength to the gingival tissue. Type IV
collagen (argyrophilic reticulum fiber) branches between the
collagen type I bundles, and it is continuous with fibers of the
basement membrane and the blood vessel walls.
161
The elastic fiber system is composed of oxytalan, elaunin, and
elastin fibers distributed among collagen fibers.
56
Therefore densely
packed collagen bundles that are anchored into the acellular
extrinsic fiber cementum just below the terminal point of the
junctional epithelium form the connective tissue attachment. The
stability of this attachment is a key factor in the limitation of the
migration of junctional epithelium.
57
Gingival Fibers
The connective tissue of the marginal gingiva is densely
collagenous, and it contains a prominent system of collagen fiber
bundles called the gingival fibers. These fibers consist of type I
collagen.
213
The gingival fibers have the following functions:
1. To brace the marginal gingiva firmly against the tooth
2. To provide the rigidity necessary to withstand the forces of
mastication without being deflected away from the tooth
surface
3. To unite the free marginal gingiva with the cementum of the
root and the adjacent attached gingiva
The gingival fibers are arranged in three groups: gingivodental,
circular, and transseptal.
146
The gingivodental fibers are those on the facial, lingual, and
interproximal surfaces. They are embedded in the cementum just
beneath the epithelium at the base of the gingival sulcus. On the
facial and lingual surfaces, they project from the cementum in a
fanlike conformation toward the crest and outer surface of the
marginal gingiva, where they terminate short of the epithelium
210
(Figs. 3.19 and 3.20). They also extend externally to the periosteum
of the facial and lingual alveolar bones, terminating in the attached
gingiva or blending with the periosteum of the bone.
Interproximally, the gingivodental fibers extend toward the crest of
the interdental gingiva.
FIG. 3.19 Faciolingual section of marginal gingiva
showing gingival fibers (F) that extend from the
cementum (C) to the crest of the gingiva, to the outer
gingival surface, and external to the periosteum of the
bone (B). Circular fibers (CF) are shown in cross-
section between the other groups. (Courtesy Sol Bernick.)
211
FIG. 3.20 Diagram of the gingivodental fibers that
extend from the cementum (1) to the crest of the
gingiva, (2) to the outer surface, and (3) external to the
periosteum of the labial plate. Circular fibers (4) are
shown in cross-section.
The circular fibers course through the connective tissue of the
marginal and interdental gingivae and encircle the tooth in ringlike
fashion.
The transseptal fibers, which are located interproximally, form
horizontal bundles that extend between the cementum of the
approximating teeth into which they are embedded. They lie in the
area between the epithelium at the base of the gingival sulcus and
the crest of the interdental bone, and they are sometimes classified
with the principal fibers of the periodontal ligament.
Page and colleagues
198
described a group of semicircular fibers that
attach at the proximal surface of a tooth immediately below the
cementoenamel junction, go around the facial or lingual marginal
gingiva of the tooth, and attach on the other proximal surface of the
same tooth; they also discussed a group of transgingival fibers that
212
attach in the proximal surface of one tooth, traverse the interdental
space diagonally, go around the facial or lingual surface of the
adjacent tooth, again traverse the interdental space diagonally, and
then attach in the proximal surface of the next tooth.
Tractional forces in the extracellular matrix produced by
fibroblasts are believed to be responsible for generating tension in
the collagen. This keeps the teeth tightly bound to each other and to
the alveolar bone.
Cellular Elements
The preponderant cellular element in the gingival connective tissue
is the fibroblast. Numerous fibroblasts are found between the fiber
bundles. Fibroblasts are of mesenchymal origin and play a major
role in the development, maintenance, and repair of gingival
connective tissue. As with connective tissue elsewhere in the body,
fibroblasts synthesize collagen and elastic fibers as well as the
glycoproteins and glycosaminoglycans of the amorphous
intercellular substance. Fibroblasts also regulate collagen
degradation through phagocytosis and the secretion of
collagenases.
Fibroblast heterogeneity is now a well-established feature of
fibroblasts in the periodontium.
226
Although the biologic and
clinical significance of such heterogeneity is not yet clear, it seems
that this is necessary for the normal functioning of tissues in health,
disease, and repair.
18
Mast cells, which are distributed throughout the body, are
numerous in the connective tissue of the oral mucosa and the
gingiva.
52,244,245,288
Fixed macrophages and histiocytes are present in the
gingival connective tissue as components of the mononuclear
phagocyte system (reticuloendothelial system) and are derived
from blood monocytes. Adipose cells and eosinophils, although scarce,
are also present in the lamina propria.
In clinically normal gingiva, small foci of plasma cells and
lymphocytes are found in the connective tissue near the base of the
sulcus (Fig. 3.21). Neutrophils can be seen in relatively high
numbers in both the gingival connective tissue and the sulcus.
These inflammatory cells are usually present in small amounts in
clinically normal gingiva.
213
FIG. 3.21 Section of clinically normal gingiva showing
some degree of inflammation, which is almost always
present near the base of the sulcus.
Speculations about whether small amounts of leukocytes should
be considered a normal component of the gingiva or an incipient
inflammatory infiltrate without clinical expression are of theoretic
rather than practical importance. Lymphocytes are absent when
gingival normalcy is judged by strict clinical criteria or under
special experimental conditions,
13,192
but they are practically
constant in healthy, normal gingiva, even before complete tooth
eruption.
150,167,229
Immunohistochemical studies involving monoclonal antibodies
have identified the different lymphocyte subpopulations. The
infiltrate in the area below the junctional epithelium of healthy
gingiva in newly erupted teeth in children is mainly composed of T
lymphocytes (helper, cytotoxic, suppressor, and natural killer)
12,98,242
and thus could be interpreted as a normal lymphoid tissue involved
in the early defense recognition system. As time elapses, B
lymphocytes and plasma cells appear in greater proportions to
elaborate specific antibodies against already-recognized antigens
that are always present in the sulcus of clinically normal gingiva.
234
Repair of Gingival Connective Tissue
Because of the high turnover rate, the connective tissue of the
gingiva has remarkably good healing and regenerative capacity.
Indeed, it may be one of the best healing tissues in the body, and it
generally shows little evidence of scarring after surgical procedures.
This is likely caused by the rapid reconstruction of the fibrous
214
architecture of the tissues.
178
However, the reparative capacity of
gingival connective tissue is not as great as that of the periodontal
ligament or the epithelial tissue.
Blood Supply, Lymphatics, and Nerves
Microcirculatory tracts, blood vessels, and lymphatic vessels play
an important role in the drainage of tissue fluid and in the spread of
inflammation. In individuals with gingivitis and periodontitis, the
microcirculation and vascular formation change greatly in the
vascular network directly under the gingival sulcular epithelium
and the junctional epithelium.
170
Blood vessels are easily evidenced in tissue sections by means of
immunohistochemical reactions against proteins of endothelial cells
(i.e., factor VIII and adhesion molecules). Before these techniques
were developed, vascularization patterns of periodontal tissues had
been described using histoenzymatic reactions for alkaline
phosphatase and adenosine triphosphatase because of the great
activity of these enzymes in endothelial cells.
54,297
In experimental animals, perfusion with India ink also was used
to study vascular distribution. The injection and subsequent
demonstration of peroxidase allow for blood vessel identification
and permeability studies.
239
The periodic acid–Schiff reaction also
outlines vascular walls by revealing a positive line in the basal
membrane.
237
Endothelial cells express 5-nucleotidase activity as
well.
126
Scanning electron microscopy can be used after the injection
of plastic into the vessels through the carotid artery, which is
followed by the corrosion of the soft tissues.
84
In addition, laser
Doppler flow measurement provides a noninvasive means for the
observation of blood flow modifications related to disease.
8
Three sources of blood supply to the gingiva are as follows (Figs.
3.22 and 3.23):
215
FIG. 3.22 Diagram of an arteriole penetrating the
interdental alveolar bone to supply the interdental
tissues (left) and a supraperiosteal arteriole overlying
the facial alveolar bone, sending branches to the
surrounding tissue (right).
FIG. 3.23 Blood supply and peripheral circulation of
the gingiva. Tissues perfused with India ink. Note the
216
capillary plexus parallel to the sulcus (S) and the
capillary loops in the outer papillary layer. Note also
the supraperiosteal vessels external to the bone (B),
which supply the gingiva, and a periodontal ligament
vessel anastomosing with the sulcus plexus. (Courtesy Sol
Bernick.)
1. Supraperiosteal arterioles along the facial and lingual surfaces
of the alveolar bone from which capillaries extend along the
sulcular epithelium and between the rete pegs of the
external gingival surface
8,76,113
: Occasional branches of the
arterioles pass through the alveolar bone to the periodontal
ligament or run over the crest of the alveolar bone.
2. Vessels of the periodontal ligament, which extend into the
gingiva and anastomose with capillaries in the sulcus area.
3. Arterioles, which emerge from the crest of the interdental
septa
84
and extend parallel to the crest of the bone to
anastomose with vessels of the periodontal ligament, with
capillaries in the gingival crevicular areas and vessels that
run over the alveolar crest.
Beneath the epithelium on the outer gingival surface, capillaries
extend into the papillary connective tissue between the epithelial
rete pegs in the form of terminal hairpin loops with efferent and
afferent branches, spirals, and varices
54,113
(Fig. 3.24; also see Fig.
3.23). The loops are sometimes linked by cross-communications,
86
and flattened capillaries serve as reserve vessels when the
circulation is increased in response to irritation.
99
217
FIG. 3.24 Scanning electron microscopic view of the
gingival tissues of rat molar palatal gingiva after the
vascular perfusion of plastic and the corrosion of soft
tissue. (A) Oral view of gingival capillaries: t, tooth;
interdental papilla (arrowhead) (×180). (B) View from
the tooth side. Note the vessels of the plexus next to
the sulcular and junctional epithelium. The arrowheads
point to vessels in the sulcus area with mild
inflammatory changes. g, Crest of the marginal
gingiva; s, bottom of the gingival sulcus; pl, periodontal
ligament vessels. (×150.) (Courtesy NJ Selliseth and K Selvig,
University of Bergen, Norway.)
Along the sulcular epithelium, capillaries are arranged in a flat,
218
anastomosing plexus that extends parallel to the enamel from the
base of the sulcus to the gingival margin.
54
In the col area, a mixed
pattern of anastomosing capillaries and loops occurs.
As mentioned previously, anatomic and histologic changes have
been shown to occur in the gingival microcirculation of individuals
with gingivitis. Prospective studies of the gingival vasculature in
animals have demonstrated that, in the absence of inflammation,
the vascular network is arranged in a regular, repetitive, and
layered pattern.
54,216
By contrast, the inflamed gingival vasculature
exhibits an irregular vascular plexus pattern, with the microvessels
exhibiting a looped, dilated, and convoluted appearance.
216
The role of the lymphatic system in removing excess fluids,
cellular and protein debris, microorganisms, and other elements is
important for controlling diffusion and the resolution of
inflammatory processes.
168
The lymphatic drainage of the gingiva
brings in the lymphatics of the connective tissue papillae.
238
It
progresses into the collecting network external to the periosteum of
the alveolar process and then moves to the regional lymph nodes,
particularly the submaxillary group. In addition, lymphatics just
beneath the junctional epithelium extend into the periodontal
ligament and accompany the blood vessels.
Neural elements are extensively distributed throughout the
gingival tissues. Within the gingival connective tissues, most nerve
fibers are myelinated and closely associated with the blood
vessels.
162
Gingival innervation is derived from fibers that arise from
nerves in the periodontal ligament and from the labial, buccal, and
palatal nerves.
30
The following nerve structures are present in the
connective tissue: a meshwork of terminal argyrophilic fibers, some
of which extend into the epithelium; Meissner-type tactile
corpuscles; Krause-type end bulbs, which are temperature
receptors; and encapsulated spindles.
14
Correlation of Clinical and Microscopic
Features
An understanding of the normal clinical features of the gingiva
requires the ability to interpret them in terms of the microscopic
structures that they represent.
219
Color
The color of the attached and marginal gingiva is generally
described as “coral pink”; it is produced by the vascular supply, the
thickness and degree of keratinization of the epithelium, and the
presence of pigment-containing cells. The color varies among
different persons and appears to be correlated with the cutaneous
pigmentation. It is lighter in blond individuals with fair
complexions than in swarthy, dark-haired individuals (Fig. 3.25).
FIG. 3.25 (A) Clinically normal gingiva in a young
adult. (B) Heavily pigmented (melanotic) gingiva in a
middle-aged adult. (From Glickman I, Smulow JB: Periodontal disease:
clinical, radiographic, and histopathologic features, Philadelphia, 1974, Saunders.)
The attached gingiva is demarcated from the adjacent alveolar
mucosa on the buccal aspect by a clearly defined mucogingival line.
The alveolar mucosa is red, smooth, and shiny rather than pink and
stippled. A comparison of the microscopic structure of the attached
gingiva with that of the alveolar mucosa provides an explanation
for the difference in appearance. The epithelium of the alveolar
mucosa is thinner and nonkeratinized, and it contains no rete pegs
(Fig. 3.26). The connective tissue of the alveolar mucosa is loosely
220
arranged, and the blood vessels are more numerous.
FIG. 3.26 Oral mucosa, facial and palatal surfaces.
The facial surface (F) shows the marginal gingiva
(MG), the attached gingiva (AG), and the alveolar
mucosa (AM). The double line marks the mucogingival
junction. Note the differences in the epithelium and the
connective tissue in the attached gingiva and the
alveolar mucosa. The palatal surface (P) shows the
marginal gingiva (MG) and the thick, keratinized palatal
mucosa (PM).
Physiologic Pigmentation (Melanin)
Melanin is a non–hemoglobin-derived brown pigment with the
following characteristics:
• Melanin is responsible for the normal
pigmentation of the skin, the gingiva, and the
remainder of the oral mucous membrane.
• Melanin is present in all normal individuals
(often not in sufficient quantities to be detected
221
clinically), but it is absent or severely diminished
in albinos.
• Melanin pigmentation in the oral cavity is
prominent in black individuals (see Fig. 3.25).
• Ascorbic acid directly down-regulates melanin
pigmentation in gingival tissues.
246
According to Dummett,
73
the distribution of oral pigmentation in
black individuals is as follows: gingiva, 60%; hard palate, 61%;
mucous membrane, 22%; and tongue, 15%. Gingival pigmentation
occurs as a diffuse, deep-purplish discoloration or as irregularly
shaped brown and light-brown patches. It may appear in the
gingiva as early as 3 hours after birth, and it is often the only
evidence of pigmentation.
73
Oral repigmentation refers to the clinical reappearance of
melanin pigment after a period of clinical depigmentation of the
oral mucosa as a result of chemical, thermal, surgical,
pharmacologic, or idiopathic factors.
74
Information about the
repigmentation of oral tissues after surgical procedures is extremely
limited, and no definitive treatment is offered at this time.
Size
The size of the gingiva corresponds with the sum total of the bulk
of cellular and intercellular elements and their vascular supply.
Alteration in size is a common feature of gingival disease.
Contour
The contour or shape of the gingiva varies considerably and
depends on the shape of the teeth and their alignment in the arch,
the location and size of the area of proximal contact, and the
dimensions of the facial and lingual gingival embrasures.
The marginal gingiva envelops the teeth in collar-like fashion and
follows a scalloped outline on the facial and lingual surfaces. It
forms a straight line along teeth with relatively flat surfaces. On
teeth with pronounced mesiodistal convexity (e.g., maxillary
canines) or teeth in labial version, the normal arcuate contour is
222
accentuated, and the gingiva is located farther apically. On teeth in
lingual version, the gingiva is horizontal and thickened (Fig. 3.27).
In addition, the gingival tissue biotype varies significantly. A thin
and clear gingiva is found in one-third of the population and
primarily in females with slender teeth with a narrow zone of
keratinized tissue, whereas a clear, thick gingiva with a broad zone
of keratinized tissue is present in two-thirds of the population and
primarily in males.
70
FIG. 3.27 A thickened, shelflike contour of gingiva on a
tooth in lingual version aggravated by local irritation
caused by plaque accumulation.
Shape
The shape of the interdental gingiva is governed by the contour of
the proximal tooth surfaces and the location and shape of the
gingival embrasures.
When the proximal surfaces of the crowns are relatively flat
faciolingually, the roots are close together, the interdental bone is
thin mesiodistally, and the gingival embrasures and interdental
gingiva are narrow mesiodistally. Conversely, with proximal
surfaces that flare away from the area of contact, the mesiodistal
diameter of the interdental gingiva is broad (Fig. 3.28). The height
of the interdental gingiva varies with the location of the proximal
contact. Thus in the anterior region of the dentition, the interdental
223
papilla is pyramidal in form, whereas the papilla is more flattened
in a buccolingual direction in the molar region.
FIG. 3.28 Shape of the interdental gingival papillae
correlated with the shape of the teeth and the
embrasures. (A) Broad interdental papillae. (B) Narrow
interdental papillae.
Consistency
The gingiva is firm and resilient and, with the exception of the
movable free margin, tightly bound to the underlying bone. The
collagenous nature of the lamina propria and its contiguity with the
mucoperiosteum of the alveolar bone determine the firmness of the
attached gingiva. The gingival fibers contribute to the firmness of
the gingival margin.
Surface Texture
The gingiva presents a textured surface similar to that of an orange
peel and is referred to as stippled (see Fig. 3.25). Stippling is best
viewed by drying the gingiva. The attached gingiva is stippled; the
marginal gingiva is not. The central portion of the interdental
papillae is usually stippled, but the marginal borders are smooth.
The pattern and extent of stippling vary among individuals and
among different areas of the same mouth.
108,216
Stippling is less
prominent on lingual than facial surfaces and may be absent in
some persons.
Stippling varies with age. It is absent during infancy, it appears in
some children at about 5 years of age, it increases until adulthood,
and it frequently begins to disappear during old age.
Microscopically, stippling is produced by alternate rounded
224
protuberances and depressions in the gingival surface. The
papillary layer of the connective tissue projects into the elevations,
and the elevated and depressed areas are covered by stratified
squamous epithelium (Fig. 3.29). The degree of keratinization and
the prominence of stippling appear to be related.
FIG. 3.29 Gingival biopsy of the patient shown in Fig.
3.7 demonstrating alternate elevations and
depressions (arrows) in the attached gingiva that are
responsible for the stippled appearance.
Scanning electron microscopy has shown considerable variation
in shape but a relatively constant depth of stippling. At low
magnification, a rippled surface is seen, and this is interrupted by
irregular depressions that are 50 µm in diameter. At higher
magnification, cell micropits are seen.
61
Stippling is a form of adaptive specialization or reinforcement for
function. It is a feature of healthy gingiva, and the reduction or loss
of stippling is a common sign of gingival disease. When the gingiva
is restored to health after treatment, the stippled appearance
returns.
225
The surface texture of the gingiva is also related to the presence
and degree of epithelial keratinization. Keratinization is considered
a protective adaptation to function. It increases when the gingiva is
stimulated by toothbrushing. However, research on free gingival
grafts (see Chapter 65) has shown that when connective tissue is
transplanted from a keratinized area to a nonkeratinized area, it
becomes covered by a keratinized epithelium.
140
This finding
suggests a connective-tissue–based genetic determination of the
type of epithelial surface.
Position
The position of the gingiva is the level at which the gingival margin
is attached to the tooth. When the tooth erupts into the oral cavity,
the margin and sulcus are at the tip of the crown; as eruption
progresses, they are seen closer to the root. During this eruption
process, as described previously, the junctional epithelium, the oral
epithelium, and the reduced enamel epithelium undergo extensive
alterations and remodeling while maintaining the shallow
physiologic depth of the sulcus. Without this remodeling of the
epithelia, an abnormal anatomic relationship between the gingiva
and the tooth would result.
Continuous Tooth Eruption
According to the concept of continuous eruption,
105
eruption does
not cease when the teeth meet their functional antagonists; rather, it
continues throughout life. Eruption consists of an active phase and
a passive phase. Active eruption is the movement of the teeth in the
direction of the occlusal plane, whereas passive eruption is the
exposure of the teeth via apical migration of the gingiva.
This concept distinguishes between the anatomic crown (i.e., the
portion of the tooth covered by enamel) and the anatomic root (i.e.,
the portion of the tooth covered by cementum) and between the
clinical crown (i.e., the part of the tooth that has been denuded of its
gingiva and projects into the oral cavity) and the clinical root (i.e.,
the portion of the tooth covered by periodontal tissues). When the
teeth reach their functional antagonists, the gingival sulcus and the
junctional epithelium are still on the enamel, and the clinical crown
is approximately two-thirds of the anatomic crown.
226
Gottlieb and Orban
105
believed that active and passive eruption
proceed together. Active eruption is coordinated with attrition; the
teeth erupt to compensate for tooth substance that has been worn
away by attrition. Attrition reduces the clinical crown and prevents
it from becoming disproportionately long in relation to the clinical
root, thus avoiding excessive leverage on the periodontal tissues.
Ideally, the rate of active eruption keeps pace with tooth wear,
thereby preserving the vertical dimension of the dentition.
As teeth erupt, cementum is deposited at the apices and
furcations of the roots, and bone is formed along the fundus of the
alveolus and at the crest of the alveolar bone. In this way, part of
the tooth substance lost by attrition is replaced by the lengthening
of the root, and the socket depth is maintained to support the root.
Although originally thought to be a normal physiologic process,
passive eruption is now considered a pathologic process. Passive
eruption is divided into the following four stages (Fig. 3.30):
FIG. 3.30 Diagrammatic representation of the four
steps of passive eruption according to Gottlieb and
Orban.
105
1, The base of the gingival sulcus (arrow)
and the junctional epithelium (JE) are on the enamel.
2, The base of the gingival sulcus (arrow) is on the
enamel, and part of the junctional epithelium is on the
root. 3, The base of the gingival sulcus (arrow) is at the
cementoenamel line, and the entire junctional
epithelium is on the root. 4, The base of the gingival
sulcus (arrow) and the junctional epithelium are on the
root.
227
Stage 1: The teeth reach the line of occlusion. The junctional
epithelium and the base of the gingival sulcus are on the
enamel.
Stage 2: The junctional epithelium proliferates so that part is on
the cementum and part is on the enamel. The base of the
sulcus is still on the enamel.
Stage 3: The entire junctional epithelium is on the cementum,
and the base of the sulcus is at the cementoenamel junction.
As the junctional epithelium proliferates from the crown
onto the root, it does not remain at the cementoenamel
junction any longer than at any other area of the tooth.
Stage 4: The junctional epithelium has proliferated farther on
the cementum. The base of the sulcus is on the cementum, a
portion of which is exposed. Proliferation of the junctional
epithelium onto the root is accompanied by degeneration of
the gingival and periodontal ligament fibers and their
detachment from the tooth. The cause of this degeneration is
not understood. At present, it is believed to be the result of
chronic inflammation and therefore a pathologic process.
As noted, apposition of bone accompanies active eruption. The
distance between the apical end of the junctional epithelium and
the crest of the alveolus remains constant throughout continuous
tooth eruption (i.e., 1.07 mm).
93
Exposure of the tooth via the apical migration of the gingiva is
called gingival recession or atrophy. According to the concept of
continuous eruption, the gingival sulcus may be located on the
crown, the cementoenamel junction, or the root, depending on the
age of the patient and the stage of eruption. Therefore some root
exposure with age would be considered normal and referred to as
physiologic recession. Again, this concept is not accepted at present.
Excessive exposure is termed pathologic recession (see Chapter 23).
Periodontal Ligament
The periodontal ligament is composed of a complex vascular and
highly cellular connective tissue that surrounds the tooth root and
connects it to the inner wall of the alveolar bone.
175
It is continuous
228
with the connective tissue of the gingiva, and it communicates with
the marrow spaces through vascular channels in the bone.
Although the average width of the periodontal ligament space is
documented to be about 0.2 mm, considerable variation exists. The
periodontal space is diminished around teeth that are not in
function and in unerupted teeth, but it is increased in teeth that
have been subjected to hyperfunction.
Periodontal Fibers
The most important elements of the periodontal ligament are the
principal fibers, which are collagenous and arranged in bundles and
which follow a wavy course when viewed in longitudinal section
(Fig. 3.31). The terminal portions of the principal fibers that are
inserted into cementum and bone are termed Sharpey fibers (Fig.
3.32). The principal fiber bundles consist of individual fibers that
form a continuous anastomosing network between tooth and
bone.
25,58
Once embedded in the wall of the alveolus or in the tooth,
Sharpey fibers calcify to a significant degree. They are associated
with abundant noncollagenous proteins that are typically found in
bone, and they have also been identified in tooth cementum.
33,132,175
Notable among these proteins are osteopontin and bone
sialoprotein. These proteins are thought to contribute to the
regulation of mineralization and to tissue cohesion at sites of
increased biomechanical strain.
175
229
FIG. 3.31 Principal fibers of the periodontal ligament
follow a wavy course when sectioned longitudinally.
The formative function of the periodontal ligament is
illustrated by the newly formed osteoid and osteoblasts
along a previously resorbed bone surface (left) and the
cementoid and cementoblasts (right). Note the fibers
embedded in the forming calcified tissues (arrows). V,
Vascular channels.
230
FIG. 3.32 Collagen fibers embedded in the cementum
(left) and the bone (right) (silver stain). Note the
Sharpey fibers within the bundle bone (BB) overlying
the lamellar bone.
Collagen is a protein that is composed of different amino acids,
the most important of which are glycine, proline, hydroxylysine,
and hydroxyproline.
51
The amount of collagen in a tissue can be
determined by its hydroxyproline content. Collagen is responsible
for the maintenance of the framework and the tone of tissue, and it
exhibits a wide range of diversity.
80
There are at least 19 recognized
collagen species encoded by at least 25 separate genes dispersed
among 12 chromosomes.
80
Collagen biosynthesis occurs inside the fibroblasts to form
tropocollagen molecules. These aggregate into microfibrils that are
packed together to form fibrils. Collagen fibrils have a transverse
striation with a characteristic periodicity of 64 µm; this striation is
caused by the overlapping arrangement of the tropocollagen
molecules. In collagen types I and III, these fibrils associate to form
fibers; in collagen type I, the fibers associate to form bundles (Fig.
3.33).
231
FIG. 3.33 Collagen microfibrils, fibrils, fibers, and
bundles.
Collagen is synthesized by fibroblasts, chondroblasts, osteoblasts,
odontoblasts, and other cells. The several types of collagen are all
distinguishable by their chemical composition, distribution,
function, and morphology.
138
The principal fibers are composed
mainly of collagen type I,
211
whereas reticular fibers are composed
of collagen type III. Collagen type IV is found in the basal
lamina.
212,214
The expression of type XII collagen during tooth
development is timed with the alignment and organization of
periodontal fibers and is limited in tooth development to cells
within the periodontal ligament.
164
Type VI collagen has also been
immunolocalized in the periodontal ligament and the gingiva.
83
The molecular configuration of collagen fibers provides them
with a tensile strength that is greater than that of steel.
Consequently, collagen imparts a unique combination of flexibility
and strength to the tissues.
138
The principal fibers of the periodontal ligament are arranged in
six groups that develop sequentially in the developing root: the
transseptal, alveolar crest, horizontal, oblique, apical, and
interradicular fibers (Fig. 3.34).
232
FIG. 3.34 Diagram of the principal fiber groups.
Transseptal fibers extend interproximally over the alveolar bone
crest and are embedded in the cementum of adjacent teeth (Fig.
3.35). They are reconstructed even after destruction of the alveolar
bone that results from periodontal disease. These fibers may be
considered as belonging to the gingiva, because they do not have
osseous attachment.
FIG. 3.35 Transseptal fibers (F) at the crest of the
interdental bone.
Alveolar crest fibers extend obliquely from the cementum just
233
beneath the junctional epithelium to the alveolar crest (Fig. 3.36).
Fibers also run from the cementum over the alveolar crest and to
the fibrous layer of the periosteum that covers the alveolar bone.
The alveolar crest fibers prevent the extrusion of the tooth
53
and
resist lateral tooth movements. The incision of these fibers during
periodontal surgery does not increase tooth mobility unless
significant attachment loss has occurred.
97
FIG. 3.36 Rat molar section showing alveolar crest
fibers radiating coronally.
Horizontal fibers extend at right angles to the long axis of the tooth
from the cementum to the alveolar bone.
Oblique fibers, which constitute the largest group in the
periodontal ligament, extend from the cementum in a coronal
direction obliquely to the bone (see Fig. 3.34). They bear the brunt
of vertical masticatory stresses and transform such stresses into
tension on the alveolar bone.
234
The apical fibers radiate in a rather irregular manner from the
cementum to the bone at the apical region of the socket. They do
not occur on incompletely formed roots.
The interradicular fibers fan out from the cementum to the tooth in
the furcation areas of multirooted teeth.
Other well-formed fiber bundles interdigitate at right angles or
splay around and between regularly arranged fiber bundles. Less
regularly arranged collagen fibers are found in the interstitial
connective tissue between the principal fiber groups; this tissue
contains the blood vessels, lymphatics, and nerves.
Although the periodontal ligament does not contain mature
elastin, two immature forms are found: oxytalan and elaunin. The
so-called oxytalan fibers
89,103
run parallel to the root surface in a
vertical direction and bend to attach to the cementum
89
in the
cervical third of the root. They are thought to regulate vascular
flow.
88
An elastic meshwork has been described in the periodontal
ligament
133
as being composed of many elastin lamellae with
peripheral oxytalan fibers and elaunin fibers. Oxytalan fibers have
been shown to develop de novo in the regenerated periodontal
ligament.
219
The principal fibers are remodeled by the periodontal ligament
cells to adapt to physiologic needs
265,295
and in response to different
stimuli.
277
In addition to these fiber types, small collagen fibers
associated with the larger principal collagen fibers have been
described. These fibers run in all directions and form a plexus
called the indifferent fiber plexus.
243
Cellular Elements
Four types of cells have been identified in the periodontal ligament:
connective tissue cells, epithelial rest cells, immune system cells,
and cells associated with neurovascular elements.
26,27
Connective tissue cells include fibroblasts, cementoblasts, and
osteoblasts. Fibroblasts are the most common cells in the
periodontal ligament; they appear as ovoid or elongated cells
oriented along the principal fibers, and they exhibit pseudopodia-
like processes.
210
These cells synthesize collagen and possess the
capacity to phagocytose “old” collagen fibers and degrade them
265
235
via enzyme hydrolysis. Thus collagen turnover appears to be
regulated by fibroblasts in a process of intracellular degradation of
collagen that does not involve the action of collagenase.
24
Phenotypically distinct and functionally different subpopulations
of fibroblasts exist in the adult periodontal ligament. They appear
to be identical at both the light and electron microscopic levels,
115
but they may have different functions, such as the secretion of
different collagen types and the production of collagenase.
Osteoblasts, cementoblasts, osteoclasts, and odontoclasts are also
seen in the cemental and osseous surfaces of the periodontal
ligament.
The epithelial rests of Malassez form a latticework in the
periodontal ligament and appear as either isolated clusters of cells
or interlacing strands (Fig. 3.37), depending on the plane in which
the microscopic section is cut. Continuity with the junctional
epithelium has been suggested in experimental animals.
106
The
epithelial rests are considered remnants of the Hertwig root sheath,
which disintegrates during root development (Fig. 3.37A).
FIG. 3.37 Epithelial rests of Malassez. (A) Erupting
236
tooth in a cat. Note the fragmentation of the Hertwig
epithelial root sheath giving rise to epithelial rests
located along and close to the root surface. (B) Human
periodontal ligament with rosette-shaped epithelial
rests (arrows) lying close to the cementum (C).
Epithelial rests are distributed close to the cementum throughout
the periodontal ligament of most teeth; they are most numerous in
the apical area
207
and the cervical area.
279,280
They diminish in
number with age
248
by degenerating and disappearing or by
undergoing calcification to become cementicles. The cells are
surrounded by a distinct basal lamina, they are interconnected by
hemidesmosomes, and they contain tonofilaments.
24
Although their functional properties are still considered to be
unclear,
259
the epithelial rests are reported to contain keratinocyte
growth factors, and they have been shown to be positive for
tyrosine kinase A neurotrophin receptor.
92,281,291
In addition,
epithelial rests proliferate when stimulated,
261,266,275
and they
participate in the formation of periapical cysts and lateral root cysts.
The defense cells in the periodontal ligament include neutrophils,
lymphocytes, macrophages, mast cells, and eosinophils. These cells,
as well as those associated with neurovascular elements, are similar
to the cells found in other connective tissues.
Ground Substance
The periodontal ligament also contains a large proportion of
ground substance that fills the spaces between fibers and cells. This
substance consists of two main components: glycosaminoglycans,
such as hyaluronic acid and proteoglycans, and glycoproteins, such
as fibronectin and laminin. It also has a high water content (i.e.,
70%).
The cell surface proteoglycans participate in several biologic
functions, including cell adhesion, cell–cell and cell–matrix
interactions, binding to various growth factors as coreceptors, and
cell repair.
292
For example, fibromodulin (a small proteoglycan rich
in keratan sulfate and leucine) has been identified in bovine
periodontal ligament.
283
The most comprehensive study of the
proteoglycans in periodontal ligament was performed with the use
237
of fibroblast cultures of human ligament.
149
The periodontal ligament may also contain calcified masses
called cementicles, which are adherent to or detached from the root
surfaces (Fig. 3.38).
FIG. 3.38 Cementicles in the periodontal ligament.
One is lying free and the other is adherent to the tooth
surface.
Cementicles may develop from calcified epithelial rests; around
small spicules of cementum or alveolar bone traumatically
displaced into the periodontal ligament; from calcified Sharpey
fibers; and from calcified, thrombosed vessels within the
periodontal ligament.
180
Functions of Periodontal Ligament
The functions of the periodontal ligament are categorized as
physical, formative and remodeling, nutritional, and sensory.
Physical Functions
The physical functions of the periodontal ligament entail the
following:
238
1. Provision of a soft-tissue “casing” to protect the vessels and
nerves from injury by mechanical forces
2. Transmission of occlusal forces to the bone
3. Attachment of the teeth to the bone
4. Maintenance of the gingival tissues in their proper
relationship to the teeth
5. Resistance to the impact of occlusal forces (i.e., shock
absorption)
Resistance to Impact of Occlusal Forces (Shock
Absorption)
Two theories pertaining to the mechanism of tooth support have
been considered: the tensional theory and the viscoelastic system
theory.
The tensional theory of tooth support states that the principal
fibers of the periodontal ligament are the major factor in supporting
the tooth and transmitting forces to the bone. When a force is
applied to the crown, the principal fibers first unfold and
straighten, and they then transmit forces to the alveolar bone,
thereby causing an elastic deformation of the bony socket. Finally,
when the alveolar bone has reached its limit, the load is transmitted
to the basal bone. Many investigators find this theory insufficient to
explain available experimental evidence.
The viscoelastic system theory states that the displacement of the
tooth is largely controlled by fluid movements, with fibers having
only a secondary role.
31,43
When forces are transmitted to the tooth,
the extracellular fluid passes from the periodontal ligament into the
marrow spaces of the bone through the foramina in the cribriform
plate. These perforations of the cribriform plate link the periodontal
ligament with the cancellous portion of the alveolar bone; they are
more abundant in the cervical third than in the middle and apical
thirds (Fig. 3.39).
239
FIG. 3.39 Foramina perforating the lamina dura of a
dog jaw.
After the depletion of tissue fluids, the fiber bundles absorb the
slack and tighten. This leads to a blood vessel stenosis. Arterial back
pressure causes ballooning of the vessels and passage of the blood
ultrafiltrates into the tissues, thereby replenishing the tissue fluids.
31
Transmission of Occlusal Forces to Bone
The arrangement of the principal fibers is similar to that of a
suspension bridge or a hammock. When an axial force is applied to
a tooth, a tendency toward displacement of the root into the
alveolus occurs. The oblique fibers alter their wavy, untensed
pattern, assume their full length, and sustain the major part of the
axial force. When a horizontal or tipping force is applied, two
phases of tooth movement occur. The first is within the confines of
the periodontal ligament, and the second produces a displacement
of the facial and lingual bony plates.
69
The tooth rotates about an
axis that may change as the force is increased.
The apical portion of the root moves in a direction that is
opposite to the coronal portion. In areas of tension, the principal
fiber bundles are taut rather than wavy. In areas of pressure, the
fibers are compressed, the tooth is displaced, and a corresponding
distortion of bone exists in the direction of root movement.
203
In single-rooted teeth, the axis of rotation is located in the area
between the apical third and the middle third of the root (Fig. 3.40).
The root apex
184
and the coronal half of the clinical root have been
240
suggested as other locations of the axis of rotation. The periodontal
ligament, which has an hourglass shape, is narrowest in the region
of the axis of rotation
65,145
(Table 3.1). In multirooted teeth, the axis
of rotation is located in the bone between the roots (Fig. 3.41). In
compliance with the physiologic mesial migration of the teeth, the
periodontal ligament is thinner on the mesial root surface than on
the distal surface.
FIG. 3.40 Left, Diagram of a mandibular premolar in a
resting state. Right, When a force is exerted on the
tooth—in this case, in faciolingual direction (arrow)
the tooth rotates around the fulcrum or axis of rotation
(black circle on root). The periodontal ligament is
compressed in areas of pressure and distended in
areas of tension.
TABLE 3.1
Thickness of the Periodontal Ligaments of 172 Teeth From 15
Human Subjects
Average of Alveolar
Crest (mm)
Average of
Midroot (mm)
Average of
Apex (mm)
Average of
Tooth (mm)
Ages 11
through 16
years
0.23 0.17 0.24 0.21
83 teeth from 4
jaws
241
Ages 32
through 50
years
0.20 0.14 0.19 0.18
36 teeth from 5
jaws
Ages 51
through 67
years
0.17 0.12 0.16 0.15
35 teeth from 5
jaws
Age 24 years (1
case)
0.16 0.09 0.15 0.13
18 teeth from 1
jaw
Modified from Coolidge ED: The thickness of the human periodontal membrane. J
Am Dent Assoc 24:1260, 1937.
FIG. 3.41 Microscopic view of a rat molar subjected to
occlusohorizontal forces. Note the alternating widened
and narrowed areas of the periodontal ligament as the
tooth rotates around its axis of rotation. The axis of
rotation is in the interradicular space.
Formative and Remodeling Function
242
Periodontal ligament and alveolar bone cells are exposed to
physical forces in response to mastication, parafunction, speech,
and orthodontic tooth movement.
173
Cells of the periodontal
ligament participate in the formation and resorption of cementum
and bone, which occur during physiologic tooth movement, during
the accommodation of the periodontium to occlusal forces, and
during the repair of injuries.
Variations in cellular enzyme activity are correlated with the
remodeling process.
9496
Although applied loads may induce
vascular and inflammatory reactive changes in periodontal
ligament cells, current evidence suggests that these cells have a
mechanism to respond directly to mechanical forces via the
activation of various mechanosensory signaling systems, including
adenylate cyclase, stretch-activated ion channels, and via changes in
cytoskeletal organization.
173
Cartilage formation in the periodontal ligament, although
unusual, may represent a metaplastic phenomenon in the repair of
this ligament after injury.
20
The periodontal ligament is constantly undergoing remodeling.
Old cells and fibers are broken down and replaced by new ones,
and mitotic activity can be observed in the fibroblasts and the
endothelial cells.
185
Fibroblasts form the collagen fibers, and the
residual mesenchymal cells develop into osteoblasts and
cementoblasts. Therefore the rate of formation and the
differentiation of osteoblasts, cementoblasts, and fibroblasts affect
the rate of formation of collagen, cementum, and bone.
Radioautographic studies with radioactive thymidine, proline,
and glycine indicate a high turnover rate of collagen in the
periodontal ligament. The rate of collagen synthesis is twice as fast
as that in the gingiva and four times as fast as that in the skin, as
established in the rat molar.
250
A rapid turnover of sulfated
glycosaminoglycans in the cells and amorphous ground substance
of the periodontal ligament also occurs.
21
It should be noted that
most of these studies have been performed in rodents and that
information about primates and humans is scarce.
232
Nutritional and Sensory Functions
The periodontal ligament supplies nutrients to the cementum, bone,
243
and gingiva by way of the blood vessels, and it also provides
lymphatic drainage as discussed later in this chapter. In relation to
other ligaments and tendons, the periodontal ligament is highly
vascularized tissue; almost 10% of its volume in the rodent molar is
blood vessels.
35,174
This relatively high blood vessel content may
provide hydrodynamic damping to applied forces as well as high
perfusion rates to the periodontal ligament.
173
The periodontal ligament is abundantly supplied with sensory
nerve fibers that are capable of transmitting tactile, pressure, and
pain sensations via the trigeminal pathways.
14,30
Nerve bundles pass
into the periodontal ligament from the periapical area and through
channels from the alveolar bone that follow the course of the blood
vessels. The bundles divide into single myelinated fibers, which
ultimately lose their myelin sheaths and end in one of four types of
neural termination: (1) free endings, which have a treelike
configuration and carry pain sensation; (2) Ruffini-like
mechanoreceptors, which are located primarily in the apical area;
(3) coiled Meissner corpuscles and mechanoreceptors, which are
found mainly in the midroot region; and (4) spindle-like pressure
and vibration endings, which are surrounded by a fibrous capsule
and located mainly in the apex.
88,166
Regulation of Periodontal Ligament Width
Some of the most interesting features of the periodontal ligament in
animals are its adaptability to rapidly changing applied force and
its capacity to maintain its width at constant dimensions
throughout its lifetime.
174
These are important measures of
periodontal ligament homeostasis that provide insight into the
function of the biologic mechanisms that tightly regulate the
metabolism and spatial locations of the cell populations involved in
the formation of bone, cementum, and periodontal ligament fibers.
In addition, the ability of periodontal ligament cells to synthesize
and secrete a wide range of regulatory molecules is an essential
component of tissue remodeling and periodontal ligament
homeostasis.
173
Cementum
244
Cementum is the calcified, avascular mesenchymal tissue that
forms the outer covering of the anatomic root. The two main types
of cementum are acellular (primary) and cellular (secondary)
cementum.
104
Both consist of a calcified interfibrillar matrix and
collagen fibrils.
The two main sources of collagen fibers in cementum are Sharpey
fibers (extrinsic), which are the embedded portion of the principal
fibers of the periodontal ligament
214
and which are formed by the
fibroblasts, and fibers that belong to the cementum matrix
(intrinsic), which are produced by the cementoblasts.
240
Cementoblasts also form the noncollagenous components of the
interfibrillar ground substance, such as proteoglycans,
glycoproteins, and phosphoproteins. Proteoglycans are most likely
to play a role in regulating cell–cell and cell–matrix interactions,
both during normal development and during the regeneration of
the cementum.
17
In addition, immunohistochemical studies have
shown that the distribution of proteoglycans is closely associated
with the cementoblasts and the cementocytes.
1,2
The major proportion of the organic matrix of cementum is
composed of type I (90%) and type III (about 5%) collagens.
Sharpey fibers, which constitute a considerable proportion of the
bulk of cementum, are composed of mainly type I collagen.
206
Type
III collagen appears to coat the type I collagen of the Sharpey
fibers.
16
Acellular cementum is the first cementum formed; it covers
approximately the cervical third or half of the root, and it does not
contain cells (Fig. 3.42). This cementum is formed before the tooth
reaches the occlusal plane, and its thickness ranges from 30 to 230
µm.
248
Sharpey fibers make up most of the structure of acellular
cementum, which has a principal role in supporting the tooth. Most
fibers are inserted at approximately right angles into the root
surface and penetrate deep into the cementum, but others enter
from several different directions. Their size, number, and
distribution increase with function.
123
Sharpey fibers are completely
calcified, with the mineral crystals oriented parallel to the fibrils as
in dentin and bone, except in a 10- to 50-µm–wide zone near the
cementodentinal junction, where they are only partially calcified.
The peripheral portions of Sharpey fibers in actively mineralizing
245
cementum tend to be more calcified than the interior regions,
according to evidence obtained by scanning electron microscopy.
137
Acellular cementum also contains intrinsic collagen fibrils that are
calcified and irregularly arranged or parallel to the surface.
232
FIG. 3.42 Acellular cementum (AC) showing
incremental lines running parallel to the long axis of the
tooth. These lines represent the appositional growth of
cementum. Note the thin, light lines running into the
cementum perpendicular to the surface; these
represent the Sharpey fibers of the periodontal
ligament (PL). D, Dentin. (×300.)
Cellular cementum, which is formed after the tooth reaches the
occlusal plane, is more irregular and contains cells (cementocytes)
in individual spaces (lacunae) that communicate with each other
through a system of anastomosing canaliculi (Fig. 3.43). Cellular
cementum is less calcified than the acellular type.
124
Sharpey fibers
occupy a smaller portion of cellular cementum and are separated by
other fibers that are arranged either parallel to the root surface or at
random. Sharpey fibers may be completely or partially calcified, or
246
they may have a central, uncalcified core surrounded by a calcified
border.
135,240
FIG. 3.43 Cellular cementum (CC) showing
cementocytes lying within the lacunae. Cellular
cementum is thicker than acellular cementum. The
evidence of incremental lines also exists, but they are
less distinct than in the acellular cementum. The cells
adjacent to the surface of the cementum in the
periodontal ligament (PL) space are cementoblasts. D,
Dentin. (×300.)
Both acellular cementum and cellular cementum are arranged in
lamellae separated by incremental lines parallel to the long axis of
the root (see Figs. 3.42 and 3.43). These lines represent “rest
periods” in cementum formation, and they are more mineralized
than the adjacent cementum.
215
In addition, the loss of the cervical
part of the reduced enamel epithelium at the time of tooth eruption
may place portions of mature enamel in contact with the connective
tissue, which then will deposit an acellular and afibrillar type of
cementum over the enamel.
157
247
On the basis of these findings, Schroeder
133,134
has classified
cementum as follows:
• Acellular afibrillar cementum contains neither
cells nor extrinsic or intrinsic collagen fibers,
except for a mineralized ground substance.
Acellular afibrillar cementum is a product of
cementoblasts and found as coronal cementum in
humans, with a thickness of 1 to 15 µm.
• Acellular extrinsic fiber cementum is composed
almost entirely of densely packed bundles of
Sharpey fibers and lacks cells. Acellular extrinsic
fiber cementum is a product of fibroblasts and
cementoblasts. It is found in the cervical third of
roots in humans, but it may extend farther
apically. Its thickness is between 30 and 230 µm.
• Cellular mixed stratified cementum is composed
of extrinsic (Sharpey) and intrinsic fibers, and it
may contain cells. Cellular mixed stratified
cementum is a co-product of fibroblasts and
cementoblasts. In humans, it appears primarily in
the apical third of the roots and apices and in
furcation areas. Its thickness ranges from 100 to
1000 µm.
• Cellular intrinsic fiber cementum contains cells
but no extrinsic collagen fibers. Cellular intrinsic
fiber cementum is formed by cementoblasts, and,
in humans, it fills the resorption lacunae.
Intermediate cementum is a poorly defined zone near the
cementodentinal junction of certain teeth that appears to contain
cellular remnants of the Hertwig sheath embedded in a calcified
248
ground substance.
77,153
Inorganic content of cementum (hydroxyapatite;
Ca10[Po4]6[OH]2) is 45% to 50%, which is less than that of bone
(65%), enamel (97%), or dentin (70%).
299
Opinions differ with regard
to whether the microhardness increases
189
or decreases with age,
282
and no relationship has been established between aging and the
mineral content of cementum.
It is well known that the protein extracts of mature cementum
promote cell attachment and cell migration and stimulate the
protein synthesis of gingival fibroblasts and periodontal ligament
cells.
225
Studies of cementum have identified adhesion proteins with
arginyl–glycyl–aspartic acid sequences: bone sialoprotein,
osteopontin, and osteonectin.
39,175
Bone sialoprotein and osteopontin
are expressed during early tooth root development by cells along
the root surface, and they are thought to play a major role in the
differentiation of the cementoblast progenitor cells to the
cementoblasts.
109,225
Some of the molecules unique to the cementum have been
described. Researchers have investigated the role of cementum
attachment protein, which is a collagenous cementum-derived
protein. Cementum attachment protein has been shown to promote
the adhesion and spreading of mesenchymal cell types, with
osteoblasts and periodontal ligament fibroblasts showing better
adhesion than gingival fibroblasts and keratinocytes.
220
In addition,
Ikezawa and colleagues
122
described the characterization of
cementum-derived growth factor, which is an insulin-like, growth
factor-I–like molecule. Cementum-derived growth factor has been
shown to enhance the proliferation of gingival fibroblasts and
periodontal ligament cells.
Permeability of Cementum
In very young animals, acellular cementum and cellular cementum
are very permeable and permit the diffusion of dyes from the pulp
and the external root surface. In cellular cementum, the canaliculi in
some areas are contiguous with the dentinal tubuli. The
permeability of cementum diminishes with age.
36
249
Cementoenamel Junction
The cementum at and immediately subjacent to the cementoenamel
junction is of particular clinical importance in root-scaling
procedures. Three types of relationships involving the cementum
may exist at the cementoenamel junction.
190
In about 60% to 65% of
cases, cementum overlaps the enamel (Fig. 3.44); in about 30%, an
edge-to-edge butt joint exists; and in 5% to 10%, the cementum and
enamel fail to meet. In the last case, gingival recession may result in
accentuated sensitivity as a result of exposed dentin.
FIG. 3.44 Normal variations in tooth morphology at the
cementoenamel junction. (A) Space between the
enamel and the cementum with the dentin (D)
exposed. (B) End-to-end relationship of enamel and
cementum. (C) Cementum overlapping the enamel.
Cementodentinal Junction
The terminal apical area of the cementum where it joins the internal
root canal dentin is known as the cementodentinal junction. When
root canal treatment is performed, the obturating material should
be at the cementodentinal junction. There appears to be no increase
or decrease in the width of the cementodentinal junction with age;
its width appears to remain relatively stable.
253
Scanning electron
microscopy of the human teeth reveals that the cementodentinal
junction is 2 to 3 µm wide. The fibril-poor layer contains a
significant amount of proteoglycans, and fibrils intermingle
between the cementum and the dentin.
293,294
250
Thickness of Cementum
Cementum deposition is a continuous process that proceeds at
varying rates throughout life. Cementum formation is most rapid in
the apical regions, where it compensates for tooth eruption, which
itself compensates for attrition.
The thickness of cementum on the coronal half of the root varies
from 16 to 60 µm, which is about the thickness of a hair. It attains its
greatest thickness (≤150 to 200 µm) in the apical third and in the
furcation areas. It is thicker in distal surfaces than in mesial
surfaces, probably because of functional stimulation from mesial
drift over time.
68
Between the ages of 11 and 70 years, the average
thickness of the cementum increases threefold, with the greatest
increase seen in the apical region. Average thicknesses of 95 µm at
the age of 20 years and of 215 µm at the age of 60 years have been
reported.
298
Abnormalities in the thickness of cementum may range from an
absence or paucity of cellular cementum (i.e., cemental aplasia or
hypoplasia) to an excessive deposition of cementum (i.e., cemental
hyperplasia or hypercementosis).
152
The term hypercementosis refers to a prominent thickening of the
cementum. It is largely an age-related phenomenon, and it may be
localized to one tooth or affect the entire dentition. As a result of
considerable physiologic variation in the thickness of cementum
among different teeth in the same person and also among different
persons, distinguishing between hypercementosis and the
physiologic thickening of cementum is sometimes difficult.
Nevertheless, the excessive proliferation of cementum may occur
with a broad spectrum of neoplastic and nonneoplastic conditions,
including benign cementoblastoma, cementifying fibroma,
periapical cemental dysplasia, florid cemento-osseous dysplasia,
and other benign fibro-osseous lesions.
152
Hypercementosis occurs as a generalized thickening of the
cementum, with nodular enlargement of the apical third of the root.
It also appears in the form of spikelike excrescences (i.e., cemental
spikes) created by either the coalescence of cementicles that adhere
to the root or the calcification of periodontal fibers at the sites of
insertion into the cementum.
153
Radiographically, the radiolucent shadow of the periodontal
251
ligament and the radiopaque lamina dura are always seen on the
outer border of an area of hypercementosis, enveloping it as it
would in normal cementum.
152
On the other hand, from a
diagnostic standpoint, periapical cemental dysplasia, condensing
osteitis, and focal periapical osteopetrosis may be differentiated
from hypercementosis, because all of these entities are located
outside of the shadow of the periodontal ligament and the lamina
dura.
290
The cause of hypercementosis varies and is not completely
understood. The spikelike type of hypercementosis generally
results from excessive tension caused by orthodontic appliances or
occlusal forces. The generalized type occurs in a variety of
circumstances. In teeth without antagonists, hypercementosis is
interpreted as an effort to keep pace with excessive tooth eruption.
In teeth that are subject to low-grade periapical irritation that arises
from pulp disease, it is considered compensation for the destroyed
fibrous attachment to the tooth. The cementum is deposited
adjacent to the inflamed periapical tissue. Hypercementosis of the
entire dentition may occur in patients with Paget disease.
218
Other
systemic disturbances that may lead to or may be associated with
hypercementosis include acromegaly, arthritis, calcinosis,
rheumatic fever, and thyroid goiter.
152
Hypercementosis itself does not require treatment. It could pose a
problem if an affected tooth requires extraction. In a multirooted
tooth, sectioning of the tooth may be required before extraction.
19
Cementum Resorption and Repair
Permanent teeth do not undergo physiologic resorption as primary
teeth do. However, the cementum of erupted (as well as unerupted)
teeth is subject to resorptive changes that may be of microscopic
proportion or sufficiently extensive to present a radiographically
detectable alteration in the root contour.
Microscopic cementum resorption is extremely common; in one
study, it occurred in 236 of 261 teeth (90.5%).
118
The average number
of resorption areas per tooth was 3.5. Of the 922 areas of resorption,
708 (76.8%) were located in the apical third of the root, 177 (19.2%)
in the middle third, and 37 (4.0%) in the gingival third.
252
Approximately 70% of all resorption areas were confined to the
cementum without involving the dentin.
Cementum resorption may be caused by local or systemic factors,
or it may occur without apparent etiology (i.e., idiopathic). Local
conditions that cause cementum resorption include trauma from
occlusion
194
(Fig. 3.45); orthodontic movement
117,193,217
; pressure from
malaligned erupting teeth, cysts, and tumors
144
; teeth without
functional antagonists; embedded teeth; replanted and transplanted
teeth
3,135
; periapical disease; and periodontal disease. Systemic
conditions that are cited as predisposing an individual to or
inducing cemental resorption include calcium deficiency,
136
hypothyroidism,
23
hereditary fibrous osteodystrophy,
269
and Paget
disease.
218
FIG. 3.45 Cemental resorption associated with
excessive occlusal forces. (A) Low-power histologic
section of the mandibular anterior teeth. (B) High-
power micrograph of the apex of the left central incisor
shortened by the resorption of cementum and dentin.
Note the partial repair of the eroded areas (arrows)
and the cementicle at the upper right.
Cementum resorption appears microscopically as baylike
253
concavities in the root surface. (Fig. 3.46) Multinucleated giant cells
and large mononuclear macrophages are generally found adjacent
to cementum that is undergoing active resorption (Fig. 3.47).
Several sites of resorption may coalesce to form a large area of
destruction. The resorptive process may extend into the underlying
dentin and even into the pulp, but it is usually painless. Cementum
resorption is not necessarily continuous and may alternate with
periods of repair and the deposition of new cementum. The newly
formed cementum is demarcated from the root by a deeply staining
irregular line termed a reversal line, which delineates the border of
the previous resorption. One study showed that the reversal lines of
human teeth contain a few collagen fibrils and highly accumulated
proteoglycans with mucopolysaccharides (glycosaminoglycans)
and that fibril intermingling occurs only in some places between
reparative cementum and resorbed dentin or cementum.
293,294
Embedded fibers of the periodontal ligament reestablish a
functional relationship in the new cementum.
FIG. 3.46 Scanning electron micrograph of a root
exposed by periodontal disease showing a large
resorption bay (R). Remnants of the periodontal
ligament (P) and calculus (C) are visible. Cracking of
the tooth surface occurs as a result of the preparation
technique. (×160.) (Courtesy Dr. John Sottosanti, La Jolla, California.)
254
FIG. 3.47 Resorption of cementum and dentin. A
multinuclear osteoclast in seen (X). The direction of
resorption is indicated by the arrow. Note the scalloped
resorption front in the dentin (D). The cementum is the
darkly stained band at the upper and lower right. P,
Periodontal ligament.
Cementum repair requires the presence of viable connective
tissue. If epithelium proliferates into an area of resorption, repair
will not take place. Cementum repair can occur in devitalized as
well as vital teeth.
Histologic evidence demonstrates that cementum formation is
critical for the appropriate maturation of the periodontium, both
during development and during the regeneration of lost
periodontal tissues.
225
In other words, a variety of macromolecules
present in the extracellular matrix of the periodontium are likely to
play a regulatory role in cementogenesis.
169
The regeneration of cementum requires cementoblasts, but the
origin of the cementoblasts and the molecular factors that regulate
their recruitment and differentiation are not fully understood.
However, research provides a better understanding; for example,
the epithelial cell rests of Malassez are the only odontogenic
epithelial cells that remain in the periodontium after the eruption of
teeth, and they may have some function in cementum repair and
255
regeneration under specific conditions.
114
The rests of Malassez may
be related to cementum repair by activating their potential to
secrete matrix proteins that have been expressed in tooth
development, such as amelogenins, enamelins, and sheath proteins.
Several growth factors have been shown to be effective in
cementum regeneration, including members of the transforming
growth factor superfamily (i.e., bone morphogenetic proteins),
platelet-derived growth factor, insulin-like growth factor, and
enamel matrix derivatives
139,225
(Fig. 3.48).
FIG. 3.48 A clinical human histology shows that new
cementum and new periodontal ligament fiber formed
at a previous periodontal defect treated with
recombinant human platelet-derived growth factor-BB
with β-tricalcium phosphate. (Courtesy Dr. Daniel WK Kao,
Philadelphia, Pennsylvania.)
Ankylosis
Fusion of the cementum and the alveolar bone with obliteration of
the periodontal ligament is termed ankylosis. Ankylosis occurs in
teeth with cemental resorption, which suggests that it may
represent a form of abnormal repair. Ankylosis may also develop
after chronic periapical inflammation, tooth replantation, and
occlusal trauma and around embedded teeth. This condition is
relatively uncommon, and it occurs most frequently in the primary
256
dentition.
176
Ankylosis results in the resorption of the root and its gradual
replacement by bone tissue. For this reason, reimplanted teeth that
ankylose will lose their roots after 4 to 5 years and will be
exfoliated. Clinically, ankylosed teeth lack the physiologic mobility
of normal teeth, which is one diagnostic sign for ankylotic
resorption. In addition, these teeth usually have a special metallic
percussion sound; if the ankylotic process continues, they will be in
infraocclusion.
90
However, the clinical diagnosis of ankylosis by
mobility and percussion tests alone is only reliable when at least
20% of the root surface is affected.
10
As the periodontal ligament is replaced with bone during
ankylosis, proprioception is lost, because pressure receptors in the
periodontal ligament are deleted or do not function correctly.
Furthermore, the physiologic drifting and eruption of teeth can no
longer occur, and thus the ability of the teeth and periodontium to
adapt to altered force levels or directions of force is greatly
reduced.
173
Radiographically, resorption lacunae are filled with
bone, and the periodontal ligament space is missing.
Because no definitive causes can be found in ankylotic root
resorption, no predictable treatment can be suggested. Treatment
modalities range from a conservative approach, such as restorative
intervention, to surgical, such as the extraction of the affected
tooth.
186
When titanium implants are placed in the jaw, healing results in
bone that is formed in direct apposition to the implant without
intervening connective tissue. This may be interpreted as a form of
ankylosis. Because resorption of the metallic implant cannot occur,
the implant remains indefinitely “ankylosed” to the bone. In
addition, a true periodontal pocket will not form; the apical
proliferation of the epithelium along the root, which is a key
element of pocket formation, is not possible because of the
ankylosis.
Exposure of Cementum to the Oral
Environment
Cementum becomes exposed to the oral environment in cases of
257
gingival recession and as a result of the loss of attachment in pocket
formation. The cementum is sufficiently permeable to be penetrated
in these cases by organic substances, inorganic ions, and bacteria.
Bacterial invasion of the cementum occurs frequently in individuals
with periodontal disease, and cementum caries can develop (see
Chapter 23).
Alveolar Process
The alveolar process is the portion of the maxilla and mandible that
forms and supports the tooth sockets (alveoli). It forms when the
tooth erupts to provide the osseous attachment to the forming
periodontal ligament; it disappears gradually after the tooth is lost.
Because the alveolar processes develop and undergo remodeling
with tooth formation and eruption, they are tooth-dependent bony
structures.
227
Therefore the size, shape, location, and function of the
teeth determine their morphology. Interestingly, although the
growth and development of the bones of the jaw determine the
position of the teeth, a certain degree of repositioning of the teeth
can be accomplished through occlusal forces and in response to
orthodontic procedures that rely on the adaptability of the alveolar
bone and the associated periodontal tissues.
251
The alveolar process consists of the following:
1. An external plate of cortical bone is formed by haversian
bone and compacted bone lamellae.
2. The inner socket wall of thin, compact bone called the
alveolar bone proper is seen as the lamina dura in radiographs.
Histologically, it contains a series of openings (i.e., the
cribriform plate) through which neurovascular bundles link
the periodontal ligament with the central component of the
alveolar bone: the cancellous bone.
3. Cancellous trabeculae between these two compact layers act
as supporting alveolar bone. The interdental septum consists
of cancellous supporting bone enclosed within a compact
border (Fig. 3.49).
258
FIG. 3.49 Mesiodistal section through the mandibular
molars of a 17-year-old girl obtained at autopsy. Note the
interdental bony septa between the first and second
molars. The dense cortical bony plates represent the
alveolar bone proper (i.e., the cribriform plates) and are
supported by cancellous bony trabeculae. The third molar
is still in the early stages of root formation and eruption.
In addition, the bones of the jaw include the basal bone, which is
the portion of the jaw located apically but unrelated to the teeth
(Fig. 3.50).
259
FIG. 3.50 Section through a human jaw with a tooth in
situ. The dotted line indicates the separation between
the basal bone and the alveolar bone. (Redrawn from Ten Cate
AR: Oral histology: development, structure, and function, ed 4, St Louis, 1994,
Mosby.)
The alveolar process is divisible into separate areas on an
anatomic basis, but it functions as a unit, with all parts interrelated
in the support of the teeth. Figs. 3.51 and 3.52 show the relative
proportions of cancellous bone and compact bone that form the
alveolar process. Most of the facial and lingual portions of the
sockets are formed by compact bone alone; cancellous bone
surrounds the lamina dura in apical, apicolingual, and
interradicular areas.
260
FIG. 3.51 Relative proportions of cancellous bone and
compact bone in a longitudinal faciolingual section of
(A) mandibular molars, (B) lateral incisors, (C) canines,
(D) first premolars, (E) second premolars, (F) first
molars, (G) second molars, and (H) third molars.
261
FIG. 3.52 The shape of the roots and the surrounding
bone distribution in a transverse section of maxilla and
mandible at the midroot level.
Bone consists of two-thirds inorganic matter and one-third
organic matrix. The inorganic matter is composed principally of the
minerals calcium and phosphate, along with hydroxyl, carbonate,
citrate, and trace amounts of other ions
101,102
such as sodium,
magnesium, and fluorine. The mineral salts are in the form of
hydroxyapatite crystals of ultramicroscopic size and constitute
approximately two-thirds of the bone structure.
The organic matrix
75
consists mainly of collagen type I (90%),
185
with small amounts of noncollagenous proteins such as osteocalcin,
osteonectin, bone morphogenetic protein, phosphoproteins, and
proteoglycans.
209
Osteopontin and bone sialoprotein are cell-
adhesion proteins that appear to be important for the adhesion of
both osteoclasts and osteoblasts.
163
In addition, paracrine factors,
including cytokines, chemokines, and growth factors, have been
implicated in the local control of mesenchymal condensations that
occur at the onset of organogenesis. These factors probably play a
prominent role in the development of the alveolar processes.
251
Although the alveolar bone tissue is constantly changing its
internal organization, it retains approximately the same form from
childhood through adult life. Bone deposition by osteoblasts is
balanced by resorption by osteoclasts during tissue remodeling and
renewal. It is well known that the number of osteoblasts decreases
with aging; however, no remarkable change in the number of
osteoclasts has ever been reported.
191
Remodeling is the major pathway of bony changes in shape,
resistance to forces, repair of wounds, and calcium and phosphate
homeostasis in the body. Indeed, the coupling of bone resorption
with bone formation constitutes one of the fundamental principles
by which bone is necessarily remodeled throughout its life. Bone
remodeling involves the coordination of activities of cells from two
distinct lineages, the osteoblasts and the osteoclasts, which form
and resorb the mineralized connective tissues of bone.
251
The regulation of bone remodeling is a complex process that
involves hormones and local factors acting in an autocrine and a
paracrine manner on the generation and activity of differentiated
262
bone cells.
251
Bone contains 99% of the body's calcium ions and
therefore is the major source for calcium release when the calcium
blood levels decrease; this is monitored by the parathyroid gland. A
decrease in blood calcium is mediated by receptors on the chief cells
of the parathyroid glands, which then release parathyroid hormone.
Parathyroid hormone stimulates osteoblasts to release interleukin-1
and interleukin-6, which stimulate monocytes to migrate into the
bone area. Leukemia-inhibiting factor, which is secreted by
osteoblasts, coalesces monocytes into multinucleated osteoclasts,
which then resorb bone, thereby releasing calcium ions from
hydroxyapatite into the blood. This release normalizes the blood
level of calcium. A feedback mechanism of normal blood levels of
calcium turns off the secretion of parathyroid hormone. Meanwhile,
osteoclasts have resorbed organic matrix along with
hydroxyapatite. The breakdown of collagen from the organic matrix
releases various osteogenic substrates, which are covalently bound
to collagen. This in turn stimulates the differentiation of osteoblasts,
which ultimately deposit bone. This interdependency of osteoblasts
and osteoclasts in remodeling is called coupling.
The bone matrix that is laid down by osteoblasts is
nonmineralized osteoid. While new osteoid is being deposited, the
older osteoid located below the surface becomes mineralized as the
mineralization front advances.
Bone resorption is a complex process that is morphologically
related to the appearance of eroded bone surfaces (i.e., Howship
lacunae) and large, multinucleated cells (osteoclasts) (Fig. 3.53).
Osteoclasts originate from hematopoietic tissue
55,110,197
and are
formed by the fusion of mononuclear cells of asynchronous
populations.
141,201,264
When osteoclasts are active rather than resting,
they possess an elaborately developed ruffled border from which
hydrolytic enzymes are thought to be secreted.
278
These enzymes
digest the organic portion of bone. The activity of osteoclasts and
the morphology of the ruffled border can be modified and
regulated by hormones such as parathyroid hormone (indirectly)
and calcitonin, which has receptors on the osteoclast membrane.
263
FIG. 3.53 Rat alveolar bone. This histologic view show
two multinucleated osteoclasts in the Howship lacuna.
Another mechanism of bone resorption involves the creation of
an acidic environment on the bone surface, thereby leading to the
dissolution of the mineral component of bone. This event can be
produced by different conditions, including a proton pump
through the cell membrane of the osteoclast,
34
bone tumors, and
local pressure
197
translated through the secretory activity of the
osteoclast.
Ten Cate
264
described the sequence of events in the resorptive
process as follows:
1. Attachment of osteoclasts to the mineralized surface of bone
2. Creation of a sealed acidic environment through the action
of the proton pump, which demineralizes bone and exposes
the organic matrix
3. Degradation of the exposed organic matrix to its constituent
amino acids via the action of released enzymes (e.g., acid
phosphatase, cathepsin)
4. Sequestering of mineral ions and amino acids within the
osteoclast
264
Notably, the cellular and molecular events involved in bone
remodeling have a strong similarity to many aspects of
inflammation and repair. The relationships among matrix
molecules (e.g., osteopontin, bone sialoprotein, SPARC [secreted
protein, acidic, rich in cysteine], osteocalcin), blood clotting, and
wound healing are clearly evident.
251
Cells and Intercellular Matrix
Osteoblasts, which are the cells that produce the organic matrix of
bone, are differentiated from pluripotent follicle cells. Alveolar
bone is formed during fetal growth by intramembranous
ossification, and it consists of a calcified matrix with osteocytes
enclosed within spaces called lacunae. The osteocytes extend
processes into canaliculi that radiate from the lacunae. The canaliculi
form an anastomosing system through the intercellular matrix of
the bone, which brings oxygen and nutrients to the osteocytes
through the blood and removes metabolic waste products. Blood
vessels branch extensively and travel through the periosteum. The
endosteum lies adjacent to the marrow vasculature. Bone growth
occurs via the apposition of an organic matrix that is deposited by
osteoblasts. Haversian systems (i.e., osteons) are the internal
mechanisms that bring a vascular supply to bones that are too thick
to be supplied only by surface vessels. These are found primarily in
the outer cortical plates and the alveolar bone proper.
Socket Wall
The socket wall consists of dense, lamellated bone, some of which is
arranged in haversian systems and bundle bone. Bundle bone is the
term given to bone adjacent to the periodontal ligament that
contains a great number of Sharpey fibers
286
(Fig. 3.54). It is
characterized by thin lamellae arranged in layers parallel to the
root, with intervening appositional lines (Fig. 3.55). Bundle bone is
localized within the alveolar bone proper. Some Sharpey fibers are
completely calcified, but most contain an uncalcified central core
within a calcified outer layer.
240
Bundle bone is not unique to the
jaws; it occurs throughout the skeletal system wherever ligaments
and muscles are attached.
265
FIG. 3.54 Deep penetration of Sharpey fibers into
bundle bone of a rat molar.
266
FIG. 3.55 Bundle bone associated with the physiologic
mesial migration of the teeth. (A) Horizontal section
through the molar roots during the process of mesial
migration (left, mesial; right, distal). (B) Mesial root
surface showing osteoclasis of bone (arrows). (C)
Distal root surface showing bundle bone that has been
partially replaced with dense bone on the marrow side.
PL, Periodontal ligament.
The cancellous portion of the alveolar bone consists of trabeculae
that enclose irregularly shaped marrow spaces lined with a layer of
thin, flattened endosteal cells. Wide variation occurs in the
trabecular pattern of cancellous bone,
200
which is affected by
occlusal forces. The matrix of the cancellous trabeculae consists of
irregularly arranged lamellae separated by deeply staining
incremental and resorption lines indicative of previous bone
activity, with an occasional haversian system.
Cancellous bone is found predominantly in the interradicular
and interdental spaces and in limited amounts facially or lingually,
except in the palate. In the adult human, more cancellous bone
exists in the maxilla than in the mandible.
Bone Marrow
In the embryo and the newborn, the cavities of all bones are
occupied by red hematopoietic marrow. The red marrow gradually
undergoes a physiologic change to the fatty or yellow inactive type
of marrow. In the adult, the marrow of the jaw is normally of the
latter type, and red marrow is found only in the ribs, sternum,
vertebrae, skull, and humerus. However, foci of the red bone
marrow are occasionally seen in the jaws, often accompanied by the
resorption of bony trabeculae.
41
Common locations are the
maxillary tuberosity, the maxillary and mandibular molar and
premolar areas, and the mandibular symphysis and ramus angle,
which may be visible radiographically as zones of radiolucency.
Periosteum and Endosteum
Layers of differentiated osteogenic connective tissue cover all of the
bone surfaces. The tissue that covers the outer surface of bone is
267
termed periosteum, whereas the tissue that lines the internal bone
cavities is called endosteum.
The periosteum consists of an inner layer composed of osteoblasts
surrounded by osteoprogenitor cells, which have the potential to
differentiate into osteoblasts, and an outer layer rich in blood vessels
and nerves and composed of collagen fibers and fibroblasts.
Bundles of periosteal collagen fibers penetrate the bone, thereby
binding the periosteum to the bone. The endosteum is composed of
a single layer of osteoblasts and sometimes a small amount of
connective tissue. The inner layer is the osteogenic layer, and the
outer layer is the fibrous layer.
Cellular events at the periosteum modulate bone size throughout
an individual's life span, and a change in bone size is probably the
result of the balance between periosteal osteoblastic and osteoclastic
activities. Little is currently known about the control of periosteal
osteoblastic activity or the clinical importance of variations in
periosteal bone formation.
196
Moreover, the nature and impact of
periosteal bone resorption are virtually unexplored.
Interdental Septum
The interdental septum consists of cancellous bone that is bordered
by the socket wall cribriform plates (i.e., lamina dura or alveolar
bone proper) of approximating teeth and the facial and lingual
cortical plates (Fig. 3.56). If the interdental space is narrow, the
septum may consist of only the cribriform plate. In one study, for
example, the space between the mandibular second premolars and
first molars consisted of cribriform plate and cancellous bone in
85% of the cases and of only cribriform plate in the remaining
15%.
116
If the roots are too close together, an irregular “window”
can appear in the bone between adjacent roots (Fig. 3.57). Between
maxillary molars, the septum consisted of cribriform plate and
cancellous bone in 66.6% of cases; it was composed of only
cribriform plate in 20.8%, and it had a fenestration in 12.5%.
116
268
FIG. 3.56 Interdental septa. (A) Radiograph of the
mandibular incisor area. Note the prominent lamina
dura. (B) Interdental septa between the mandibular
anterior teeth shown in A. There is a slight reduction in
bone height with widening of the periodontal ligament
in the coronal areas. The central cancellous portion is
bordered by the dense bony cribriform plates of the
socket, which form the lamina dura around the teeth in
the radiograph. Attachments for the mentalis muscle
are seen between the canine and lateral incisors. (From
Glickman I, Smulow J: Periodontal disease: clinical, radiographic, and
histopathologic features, Philadelphia, 1974, Saunders.)
269
FIG. 3.57 Boneless “window” between adjoining close
roots of molars.
Determining root proximity radiographically is important (see
Chapters 33 and 35). The mesiodistal angulation of the crest of the
interdental septum usually parallels a line drawn between the
cementoenamel junctions of the approximating teeth.
209
The
distance between the crest of the alveolar bone and the
cementoenamel junction in young adults varies between 0.75 and
1.49 mm (average, 1.08 mm). This distance increases with age to an
average of 2.81 mm.
93
However, this phenomenon may not be as
much a function of age as of periodontal disease.
The mesiodistal and faciolingual dimensions and shape of the
interdental septum are governed by the size and convexity of the
crowns of the two approximating teeth as well as by the position of
the teeth in the jaw and their degree of eruption.
209
Osseous Topography
The bone contour normally conforms to the prominence of the
roots, with intervening vertical depressions that taper toward the
margin (Fig. 3.58). Alveolar bone anatomy varies among patients
and has important clinical implications. The height and thickness of
the facial and lingual bony plates are affected by the alignment of
the teeth, the angulation of the root to the bone, and occlusal forces.
FIG. 3.58 Normal that the bone contour conforms to
the prominence of the roots.
270
On teeth in labial version, the margin of the labial bone is located
farther apically than it is on teeth that are in proper alignment. The
bone margin is thinned to a knife edge, and it presents an
accentuated arc in the direction of the apex. On teeth in lingual
version, the facial bony plate is thicker than normal. The margin is
blunt, rounded, and horizontal rather than arcuate. The effect of the
root-to-bone angulation on the height of alveolar bone is most
noticeable on the palatal roots of the maxillary molars. The bone
margin is located farther apically on the roots, and it forms
relatively acute angles with the palatal bone.
120
The cervical portion
of the alveolar plate is sometimes considerably thickened on the
facial surface, apparently as reinforcement against occlusal forces
(Fig. 3.59).
FIG. 3.59 Variations in the cervical portion of the
buccal alveolar plate. (A) Shelflike conformation. (B)
Comparatively thin buccal plate.
Fenestration and Dehiscence
Isolated areas in which the root is denuded of bone and the root
surface is covered only by periosteum and overlying gingiva are
termed fenestrations. In these areas, the marginal bone is intact.
When the denuded areas extend through the marginal bone, the
defect is called a dehiscence (Fig. 3.60).
271
FIG. 3.60 Dehiscence on the canine and fenestration
of the first premolar.
Such defects occur on approximately 20% of the teeth; they occur
more often on the facial bone than on the lingual bone, they are
more common on anterior teeth than on posterior teeth, and they
are frequently bilateral. Microscopic evidence of lacunar resorption
may be present at the margins. The cause of these defects is not
clear. Prominent root contours, malposition, and labial protrusion
of the root in combination with a thin bony plate are predisposing
factors.
78
Fenestration and dehiscence are important because they
may complicate the outcome of periodontal surgery.
Remodeling of Alveolar Bone
In contrast with its apparent rigidity, alveolar bone is the least
stable of the periodontal tissues, because its structure is in a
constant state of flux. A considerable amount of internal
remodeling takes place by means of resorption and formation, and
this is regulated by local and systemic influences. Local influences
include functional requirements on the tooth and age-related
changes in bone cells. Systemic influences are probably hormonal
(e.g., parathyroid hormone, calcitonin, vitamin D
3
).
The remodeling of the alveolar bone affects its height, contour,
and density and is manifested in the following three areas: adjacent
272
to the periodontal ligament, in relation to the periosteum of the
facial and lingual plates, and along the endosteal surface of the
marrow spaces.
Development of the Attachment
Apparatus
After the crown has formed, the stratum intermedium and the
stellate reticulum of the enamel organ disappear. The outer and
inner epithelia of the enamel organ remain and form REE. The
apical portion of this constitutes the Hertwig epithelial root sheath,
which will continue to grow apically and which determines the
shape of the root. Before the beginning of root formation, the root
sheath bends horizontally at the future cementoenamel junction,
thereby narrowing the cervical opening and forming the epithelial
diaphragm. The epithelial diaphragm separates the dental follicle
from the dental papilla.
After root dentin formation begins, the Hertwig root sheath
breaks up and partially disappears; the remaining cells form the
epithelial clusters or strands known as the epithelial rests of Malassez
(see Fig. 3.37A). In multirooted teeth, the epithelial diaphragm
grows in such a way that tonguelike extensions develop
horizontally, thereby leaving spaces for each of the future roots to
form.
The role of the Hertwig epithelial root sheath in root
development, especially as it relates to the initiation of
cementogenesis, has become a focus of research.
271
On the basis of
various studies, it is now generally accepted that there is a transient
period of the secretion of proteins (e.g., bone sialoprotein,
osteopontin, amelin) by the cells of the Hertwig epithelial root
sheath.
38,85
In addition, research shows that growth and
differentiation factors may play roles in the development of the
attachment apparatus of periodontal tissues. Pluripotent dental
follicle cells have been shown to differentiate into osteoblasts,
cementoblasts, and periodontal fibroblasts.
241
Cementum
273
The rupture of the Hertwig root sheath allows the mesenchymal
cells of the dental follicle to contact the dentin, where they start
forming a continuous layer of cementoblasts. On the basis of
immunochemical and ultrastructural studies, Thomas
270
and
others
35,165
have speculated that cementoblasts can be of epithelial
origin (i.e., the Hertwig root sheath), having undergone an
epithelial mesenchymal transformation.
Cementum formation begins with the deposition of a meshwork
of irregularly arranged collagen fibrils sparsely distributed in a
ground substance or matrix called precementum or cementoid. This is
followed by a phase of matrix maturation, which subsequently
mineralizes to form cementum. Cementoblasts, which are initially
separated from the cementum by uncalcified cementoid, sometimes
become enclosed within the matrix and are trapped. After they are
enclosed, they are referred to as cementocytes, and they will remain
viable in a manner similar to that of osteocytes.
A layer of connective tissue known as the dental sac surrounds the
enamel organ and includes the epithelial root sheath as it develops.
The zone that is immediately in contact with the dental organ and
continuous with the ectomesenchyme of the dental papilla is called
the dental follicle,
262,263,266
and it consists of undifferentiated
fibroblasts.
Periodontal Ligament
As the crown approaches the oral mucosa during tooth eruption,
these fibroblasts become active and start producing collagen fibrils.
They initially lack orientation, but they soon acquire an orientation
that is oblique to the tooth. The first collagen bundles then appear
in the region immediately apical to the cementoenamel junction and
give rise to the gingivodental fiber groups. As tooth eruption
progresses, additional oblique fibers appear and become attached to
the newly formed cementum and bone. The transseptal and
alveolar crest fibers develop when the tooth merges into the oral
cavity. Alveolar bone deposition occurs simultaneously with
periodontal ligament organization.
250
Studies of the squirrel monkey have shown that, during eruption,
cemental Sharpey fibers appear first, followed by Sharpey fibers
274
emerging from the bone.
107
Sharpey fibers are fewer in number and
more widely spaced than those that emerge from the cementum. At
a later stage, alveolar fibers extend into the middle zone to join the
lengthening cemental fibers and to attain their classic orientation,
thickness, and strength when occlusal function is established.
Early investigators suggested that the individual fibers, rather
than being continuous, consisted of two separate parts spliced
together midway between the cementum and the bone in a zone
called the intermediate plexus. The plexus has been reported in the
periodontal ligament of continuously growing incisors but not in
the posterior teeth of rodents
119,177,300
or in actively erupting human
and monkey teeth
107
and not after teeth reach occlusal contact. The
rearrangement of the fiber ends in the plexus is supposed to
accommodate tooth eruption without necessitating the embedding
of new fibers into the tooth and the bone.
177
The existence of such a
plexus, however, has not been confirmed by radioautographic data
and other studies, and it is considered a microscopic artifact.
232
The developing periodontal ligament and the mature periodontal
ligament contain undifferentiated stem cells that retain the potential
to differentiate into osteoblasts, cementoblasts, and fibroblasts.
172
Alveolar Bone
Just before mineralization, osteoblasts start producing matrix
vesicles. These vesicles contain enzymes (e.g., alkaline phosphatase)
that help to jump-start the nucleation of hydroxyapatite crystals. As
these crystals grow and develop, they form coalescing bone
nodules, which, with fast-growing nonoriented collagen fibers, are
the substructure of woven bone and the first bone formed in the
alveolus. Later, through bone deposition, remodeling, and the
secretion of oriented collagen fibers in sheets, mature lamellar bone
is formed.
28,29
The hydroxyapatite crystals are generally aligned with their long
axes parallel to the collagen fibers, and they appear to be deposited
on and within the collagen fibers in mature lamellar bone. In this
way, bone matrix is able to withstand the heavy mechanical stresses
applied to it during function.
The alveolar bone develops around each tooth follicle during
275
odontogenesis. When a deciduous tooth is shed, its alveolar bone is
resorbed. The succedaneous permanent tooth moves into place and
develops its own alveolar bone from its own dental follicle. As the
tooth root forms and the surrounding tissues develop and mature,
alveolar bone merges with the separately developing basal bone,
and the two become one continuous structure. Although alveolar
bone and basal bone have different intermediate origins, both are
ultimately derived from neural crest ectomesenchyme.
Mandibular basal bone begins mineralization at the exit of the
mental nerve from the mental foramen, whereas the maxillary basal
bone begins at the exit of the infraorbital nerve from the infraorbital
foramen.
Physiologic Migration of the Teeth
Tooth movement does not end when active eruption is completed
and the tooth is in functional occlusion. With time and wear, the
proximal contact areas of the teeth are flattened, and the teeth tend
to move mesially. This is referred to as physiologic mesial migration.
By the age of 40 years, this process results in a reduction of about
0.5 cm in the length of the dental arch from the midline to the third
molars. Alveolar bone is reconstructed in compliance with the
physiologic mesial migration of the teeth. Bone resorption is
increased in areas of pressure along the mesial surfaces of the teeth,
and new layers of bundle bone are formed in areas of tension on the
distal surfaces (see Fig. 3.55).
External Forces and the Periodontium
The periodontium exists for the purpose of supporting teeth during
function, and it depends on the stimulation that it receives from
function for the preservation of its structure. Therefore a constant
and sensitive balance is present between external forces and the
periodontal structures.
Alveolar bone undergoes constant physiologic remodeling in
response to external forces, particularly occlusal forces. Bone is
removed from areas where it is no longer needed and added to
areas where it is presently needed.
276
The socket wall reflects the responsiveness of alveolar bone to
external forces. Osteoblasts and newly formed osteoid line the
socket in areas of tension; osteoclasts and bone resorption occur in
areas of pressure. Forces exerted on the tooth also influence the
number, density, and alignment of cancellous trabeculae. The bony
trabeculae are aligned in the path of the tensile and compressive
stresses to provide maximal resistance to the occlusal force with a
minimum of bone substance
100,247
(Fig. 3.61). When forces are
increased, the cancellous bony trabeculae increase in number and
thickness, and bone may be added to the external surface of the
labial and lingual plates.
FIG. 3.61 Bony trabeculae realigned perpendicular to
the mesial root of a tilted molar.
A study has shown that the presence of antagonists of occlusal
force and the severity of periodontal disease increase the extension
of periodontal tissue resorption.
66
The periodontal ligament also depends on the stimulation
provided by function to preserve its structure. Within physiologic
limits, the periodontal ligament can accommodate increased
function with an increase in width (Table 3.2), a thickening of its
fiber bundles, and an increase in the diameter and number of
Sharpey fibers. Forces that exceed the adaptive capacity of the
periodontium produce injury called trauma from occlusion. Because
277
trauma from occlusion can only be confirmed histologically, the
clinician is challenged to use clinical and radiographic surrogate
indicators in an attempt to facilitate and assist with its diagnosis
111
(see Chapter 26).
TABLE 3.2
Comparison of Periodontal Width of Functioning and Functionless
Teeth in a 38-Year-Old Man
AVERAGE WIDTH OF PERIODONTAL SPACE
Entrance of Alveolus
(mm)
Middle of Alveolus
(mm)
Fundus of Alveolus
(mm)
Heavy Function 0.35 0.28 0.30
Left upper second
bicuspid
Light Function 0.14 0.10 0.12
Left lower first
bicuspid
Functionless 0.10 0.06 0.06
Left upper third
molar
Modified from Kronfeld R: Histologic study of the influence of function on the human
periodontal membrane. J Am Dent Assoc 18:1242, 1931.
When occlusal forces are reduced, the number and thickness of
the trabeculae are reduced.
64
The periodontal ligament also
atrophies and appears thinned; the fibers are reduced in number
and density, disoriented,
11,208
and ultimately arranged parallel to the
root surface (Fig. 3.62). This phenomenon is termed disuse atrophy or
afunctional atrophy. With this condition, the cementum is either
unaffected
64
or thickened, and the distance from the cementoenamel
junction to the alveolar crest is increased.
204
278
FIG. 3.62 Atrophic periodontal ligament (P) of a tooth
devoid of function. Note the scalloped edge of the
alveolar bone (B), which indicates that resorption has
occurred. C, Cementum.
Decreased occlusal function causes changes in the periodontal
microvasculature, such as the occlusion of blood vessels and a
decrease in the number of blood vessels.
121
For example, Murrell
and colleagues
187
reported that the application and removal of
orthodontic force produced significant changes in blood vessel
number and density; however, no evidence-based explanation
exists for why the force stimulated such changes in the number of
blood vessels.
Orthodontic tooth movement is thought to result from site-
specific bone remodeling in the absence of inflammation. It is well
recognized that tensional forces will stimulate the formation and
activity of osteoblastic cells, whereas compressive forces promote
osteoclastic activity.
251
Vascularization of the Supporting
Structures
The blood supply to the supporting structures of the tooth is
279
derived from the inferior and superior alveolar arteries to the
mandible and maxilla, and it reaches the periodontal ligament from
three sources: apical vessels, penetrating vessels from the alveolar
bone, and anastomosing vessels from the gingiva.
63
The branches of the apical vessels supply the apical region of the
periodontal ligament before the vessels enter the dental pulp. The
transalveolar vessels are branches of the intraseptal vessels that
perforate the lamina dura and enter the ligament. The intraseptal
vessels continue to vascularize the gingiva; these gingival vessels in
turn anastomose with the periodontal ligament vessels of the
cervical region.
84
The vessels within the periodontal ligament are contained in the
interstitial spaces of loose connective tissue between the principal
fibers, and they are connected in a netlike plexus that runs
longitudinally and closer to the bone than the cementum
54
(Figs.
3.63 and 3.64). The blood supply increases from the incisors to the
molars; it is greatest in the gingival third of single-rooted teeth, less
in the apical third, and least in the middle; it is equal in the apical
and middle thirds of multirooted teeth; it is slightly greater on the
mesial and distal surfaces than on the facial and lingual surfaces;
and it is greater on the mesial surfaces of the mandibular molars
than on the distal surfaces.
33
280
FIG. 3.63 Vascular supply of a monkey periodontium
perfused with India ink. Note the longitudinal vessels in
the periodontal ligament and the alveolar arteries
passing through channels between the bone marrow
(M) and the periodontal ligament. D, Dentin. (Courtesy Dr.
Sol Bernick, Los Angeles, California.)
281
FIG. 3.64 Vascular supply to the periodontal ligament
in a rat molar as viewed by scanning electron
microscopy after perfusion with plastic and tissue
corrosion. Middle and apical areas of the periodontal
ligament are shown with longitudinal blood vessels
from the apex (below) to the gingiva (above),
perforating vessels entering the bone (b), and many
transverse connections (arrowheads). Apical vessels
(a) form a cap that connects with the pulpal vessels.
(Courtesy NJ Selliseth and K Selvig, University of Bergen, Norway.)
The vascular supply to the bone enters the interdental septa
through nutrient canals together with veins, nerves, and
lymphatics. Dental arterioles, which also branch off the alveolar
arteries, send tributaries through the periodontal ligament, and
some small branches enter the marrow spaces of the bone through
the perforations in the cribriform plate. Small vessels that emanate
from the facial and lingual compact bone also enter the marrow and
spongy bone.
The venous drainage of the periodontal ligament accompanies the
arterial supply. Venules receive the blood through the abundant
capillary network. In addition, arteriovenous anastomoses bypass
the capillaries and are seen more frequently in apical and
interradicular regions; their significance is unknown.
Lymphatics supplement the venous drainage system. Lymphatic
channels that drain the region just beneath the junctional
epithelium pass into the periodontal ligament and accompany the
blood vessels into the periapical region.
42
From there, they pass
through the alveolar bone to the inferior dental canal in the
mandible or the infraorbital canal in the maxilla and then go on to
the submaxillary lymph nodes.
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C H A P T E R 3Anatomy, Structure,and Function of thePeriodontiumJoseph P. Fiorellini, David Kim, Yu-Cheng ChangCHAPTER OUTLINEOral MucosaGingivaPeriodontal LigamentCementumAlveolar ProcessDevelopment of the Attachment ApparatusExternal Forces and the PeriodontiumVascularization of the Supporting StructuresThe normal periodontium provides the support necessary tomaintain teeth in function. It consists of four principal components:181 gingiva, periodontal ligament, cementum, and alveolar bone. Eachof these periodontal components is distinct in its location, tissuearchitecture, biochemical composition, and chemical composition,but all of these components function together as a single unit.Research has revealed that the extracellular matrix components ofone periodontal compartment can influence the cellular activities ofadjacent structures. Therefore the pathologic changes that occur inone periodontal component may have significant ramifications forthe maintenance, repair, or regeneration of other components of theperiodontium.18This chapter first discusses the structural components of thenormal periodontium; it then describes their development,vascularization, innervation, and functions.Oral MucosaThe oral mucosa consists of the following three zones:1. The gingiva and the covering of the hard palate, termed themasticatory mucosa (the gingiva is the part of the oral mucosathat covers the alveolar processes of the jaws and surroundsthe necks of the teeth)2. The dorsum of the tongue, covered by specialized mucosa3. The oral mucous membrane lining the remainder of the oralcavityGingivaClinical FeaturesIn an adult, normal gingiva covers the alveolar bone and tooth rootto a level just coronal to the cementoenamel junction. The gingiva isdivided anatomically into marginal, attached, and interdental areas.Although each type of gingiva exhibits considerable variation indifferentiation, histology, and thickness according to its functionaldemands, all types are specifically structured to functionappropriately against mechanical and microbial damage.7 In otherwords, the specific structure of different types of gingiva reflects182 each one's effectiveness as a barrier to the penetration by microbesand noxious agents into the deeper tissue.Marginal GingivaThe marginal or unattached gingiva is the terminal edge or borderof the gingiva that surrounds the teeth in collar-like fashion (Figs.3.1 and 3.2).6 In about 50% of cases, it is demarcated from theadjacent attached gingiva by a shallow linear depression called thefree gingival groove.6 The marginal gingiva is usually about 1 mmwide, and it forms the soft-tissue wall of the gingival sulcus. It maybe separated from the tooth surface with a periodontal probe. Themost apical point of the marginal gingival scallop is called thegingival zenith. Its apicocoronal and mesiodistal dimensions varybetween 0.06 and 0.96 mm.171FIG. 3.1 Normal gingiva in a young adult. Note thedemarcation (mucogingival line) (arrows) between theattached gingiva and the darker alveolar mucosa.183 FIG. 3.2 Diagram showing the anatomic landmarks ofthe gingiva.Gingival SulcusThe gingival sulcus is the shallow crevice or space around the toothbounded by the surface of the tooth on one side and the epitheliumlining the free margin of the gingiva on the other side. It is V-shaped and barely permits the entrance of a periodontal probe. Theclinical determination of the depth of the gingival sulcus is animportant diagnostic parameter. Under absolutely normal or idealconditions, the depth of the gingival sulcus is 0 mm or close to 0mm.105 These strict conditions of normalcy can be producedexperimentally only in germ-free animals or after intense andprolonged plaque control.13,49In clinically healthy human gingiva, a sulcus of some depth canbe found. The depth of this sulcus, as determined in histologicsections, has been reported as 1.8 mm, with variations from 0 to 6mm195; other studies have reported 1.5 mm289 and 0.69 mm.93 Theclinical evaluation used to determine the depth of the sulcusinvolves the introduction of a metallic instrument (i.e., theperiodontal probe) and the estimation of the distance it penetrates(i.e., the probing depth). The histologic depth of a sulcus does notneed to be exactly equal to the depth of penetration of the probe.The penetration of the probe depends on several factors, such as184 probe diameter, probing force, and level of inflammation.91Consequently, the probing depth is not necessarily exactly equal tothe histologic depth of the sulcus. The so-called probing depth of aclinically normal gingival sulcus in humans is 2 to 3 mm (seeChapter 32).Attached GingivaThe attached gingiva is continuous with the marginal gingiva. It isfirm, resilient, and tightly bound to the underlying periosteum ofalveolar bone. The facial aspect of the attached gingiva extends tothe relatively loose and movable alveolar mucosa; it is demarcatedby the mucogingival junction (see Fig. 3.2).The width of the attached gingiva is another important clinicalparameter.7 It is the distance between the mucogingival junctionand the projection on the external surface of the bottom of thegingival sulcus or the periodontal pocket. It should not be confusedwith the width of the keratinized gingiva, although this also includesthe marginal gingiva (see Fig. 3.2).The width of the attached gingiva on the facial aspect differs indifferent areas of the mouth.40 It is generally greatest in the incisorregion (i.e., 3.5 to 4.5 mm in the maxilla, 3.3 to 3.9 mm in themandible) and narrower in the posterior segments (i.e., 1.9 mm inthe maxillary first premolars and 1.8 mm in the mandibular firstpremolars)6 (Fig. 3.3).FIG. 3.3 Mean width of the attached gingiva in the185 human permanent dentition.Because the mucogingival junction remains stationarythroughout adult life,4 changes in the width of the attached gingivaare caused by modifications in the position of its coronal portion.The width of the attached gingiva increases by the age of 4 yearsand in supraerupted teeth.5 On the lingual aspect of the mandible,the attached gingiva terminates at the junction of the lingualalveolar mucosa, which is continuous with the mucous membranethat lines the floor of the mouth. The palatal surface of the attachedgingiva in the maxilla blends imperceptibly with the equally firmand resilient palatal mucosa.Interdental GingivaThe interdental gingiva occupies the gingival embrasure, which isthe interproximal space beneath the area of tooth contact. Theinterdental gingiva can be pyramidal, or it can have a “col” shape.In the former, the tip of one papilla is located immediately beneaththe contact point; the latter presents a valley-like depression thatconnects a facial and lingual papilla and that conforms to the shapeof the interproximal contact62 (Figs. 3.4 and 3.5). The shape of thegingiva in a given interdental space depends on the presence orabsence of a contact point between the adjacent teeth, the distancebetween the contact point and the osseous crest,260 and the presenceor absence of some degree of recession. Fig. 3.6 depicts thevariations in normal interdental gingiva.186 FIG. 3.4 Site of extraction showing the facial andpalatal interdental papillae and the intervening col(arrow).FIG. 3.5 Faciolingual section of a monkey showing thecol between the facial and lingual interdental papillae.The col is covered with nonkeratinized stratifiedsquamous epithelium.187 FIG. 3.6 A diagram that compares anatomic variationsof the interdental col in the normal gingiva (left side)and after gingival recession (right side). (A–B)Mandibular anterior segment, facial and buccolingualviews, respectively. (C–D) Mandibular posterior region,facial and buccolingual views, respectively. Toothcontact points are shown with black marks in the lowerindividual teeth.The facial and lingual surfaces are tapered toward theinterproximal contact area, whereas the mesial and distal surfacesare slightly concave. The lateral borders and tips of the interdentalpapillae are formed by the marginal gingiva of the adjoining teeth.The intervening portion consists of attached gingiva (Fig. 3.7). If adiastema is present, the gingiva is firmly bound over the interdentalbone to form a smooth, rounded surface without interdentalpapillae (Fig. 3.8).FIG. 3.7 Interdental papillae (arrow) with a centralportion formed by the attached gingiva. The shape of188 the papillae varies according to the dimension of thegingival embrasure. (Courtesy Dr. Osvaldo Costa.)FIG. 3.8 An absence of interdental papillae and colwhere the proximal tooth contact is missing. (Courtesy Dr.Osvaldo Costa.)Microscopic FeaturesMicroscopic examination reveals that gingiva is composed of theoverlying stratified squamous epithelium and the underlyingcentral core of connective tissue. Although the epithelium ispredominantly cellular in nature, the connective tissue is lesscellular and composed primarily of collagen fibers and groundsubstance. These two tissues are considered separately. (A detaileddescription of gingival histology can be found in Schroeder HE: Theperiodontium, New York, 1986, Springer-Verlag; and in Biologicalstructure of the normal and diseased periodontium, Periodontol 200013:1, 1997.)Gingival EpitheliumGeneral Aspects of Gingival Epithelium BiologyHistorically, the epithelial compartment was thought to provideonly a physical barrier to infection and the underlying gingivalattachment. However, we now believe that epithelial cells play anactive role in innate host defense by responding to bacteria in an189 interactive manner,67 which means that the epithelium participatesactively in responding to infection, in signaling further hostreactions, and in integrating innate and acquired immuneresponses. For example, epithelial cells may respond to bacteria byincreased proliferation, the alteration of cell-signaling events,changes in differentiation and cell death, and, ultimately, thealteration of tissue homeostasis.67 To understand this newperspective of the epithelial innate defense responses and the roleof epithelium in gingival health and disease, it is important tounderstand its basic structure and function (Box 3.1). Box 3.1Functions and Features of GingivalEpitheliumFunctionsMechanical, chemical, water, and microbial barrierSignaling functionsArchitectural IntegrityCell–cell attachmentsBasal laminaKeratin cytoskeletonMajor Cell TypeKeratinocyteOther Cell TypesLangerhans cellsMelanocytesMerkel cells190 Constant RenewalReplacement of damaged cellsCell–Cell AttachmentsDesmosomesAdherens junctionsTight junctionsGap junctionsCell–Basal LaminaSynthesis of basal lamina componentsHemidesmosomeModified from Dale BA: Periodontal epithelium: a newly recognized role in health anddisease. Periodontol 2000 30:71, 2002.The gingival epithelium consists of a continuous lining ofstratified squamous epithelium. There are three different areas thatcan be defined from the morphologic and functional points of view:the oral or outer epithelium, the sulcular epithelium, and thejunctional epithelium.The principal cell type of the gingival epithelium—as well as ofother stratified squamous epithelia—is the keratinocyte. Other cellsfound in the epithelium are the clear cells or nonkeratinocytes,which include the Langerhans cells, the Merkel cells, and themelanocytes.The main function of the gingival epithelium is to protect thedeep structures while allowing for a selective interchange with theoral environment. This is achieved via the proliferation anddifferentiation of the keratinocytes. The proliferation of keratinocytestakes place by mitosis in the basal layer and less frequently in thesuprabasal layers, in which a small proportion of cells remain as aproliferative compartment while a larger number begin to migrateto the surface.Differentiation involves the process of keratinization, which191 consists of progressions of biochemical and morphologic eventsthat occur in the cell as they migrate from the basal layer (Fig. 3.9).The main morphologic changes include the following: (1) theprogressive flattening of the cell with an increasing prevalence oftonofilaments; (2) the couple of intercellular junctions with theproduction of keratohyalin granules; and (3) the disappearance ofthe nucleus. (See Schroeder230 for further details.)FIG. 3.9 Diagram showing representative cells fromthe various layers of stratified squamous epithelium asseen by electron microscopy. (Modified from Weinstock A: In HamAW: Histology, ed 7, Philadelphia, 1974, Lippincott.)A complete keratinization process leads to the production of anorthokeratinized superficial horny layer similar to that of the skin,with no nuclei in the stratum corneum and a well-defined stratumgranulosum (Fig. 3.10). Only some areas of the outer gingivalepithelium are orthokeratinized; the other gingival areas arecovered by parakeratinized or nonkeratinized epithelium45 and areconsidered to be at intermediate stages of keratinization. Theseareas can progress to maturity or dedifferentiate under different192 physiologic or pathologic conditions.FIG. 3.10 (A) Scanning electron micrograph ofkeratinized gingiva showing the flattened keratinocytesand their boundaries on the surface of the gingiva(×1000). (B) Scanning electron micrograph of thegingival margin at the edge of the gingival sulcusshowing several keratinocytes about to be exfoliated(×3000). (From Kaplan GB, Pameijer CH, Ruben MP: J Periodontol 48:446,1977.)In parakeratinized epithelia, the stratum corneum retains pyknoticnuclei, and the keratohyalin granules are dispersed rather thangiving rise to a stratum granulosum. The nonkeratinized epithelium(although cytokeratins are the major component, as in all epithelia)has neither granulosum nor corneum strata, whereas superficialcells have viable nuclei.Immunohistochemistry, gel electrophoresis, and immunoblottechniques have made the identification of the characteristic patternof cytokeratins possible in each epithelial type. The keratin proteinsare composed of different polypeptide subunits characterized bytheir isoelectric points and molecular weights. They are numberedin a sequence that is contrary to their molecular weight. In general,193 basal cells begin synthesizing lower-molecular-weight keratins(e.g., K19 [40 kD]), and they express other higher-molecular-weightkeratins as they migrate to the surface. K1 keratin polypeptide (68kD) is the main component of the stratum corneum.60Other proteins unrelated to keratins are synthesized during thematuration process. The most extensively studied are keratolininand involucrin, which are precursors of a chemically resistantstructure (the envelope) located below the cell membrane, andfilaggrin, which has precursors that are packed into the keratohyalingranules. At the sudden transition to the horny layer, thekeratohyalin granules disappear and give rise to filaggrin, whichforms the matrix of the most differentiated epithelial cell, thecorneocyte.Thus in the fully differentiated state, the corneocytes are mainlyformed by bundles of keratin tonofilaments embedded in anamorphous matrix of filaggrin and surrounded by a resistantenvelope under the cell membrane. The immunohistochemicalpatterns of the different keratin types, envelope proteins, andfilaggrin change under normal or pathologic stimuli, therebymodifying the keratinization process.128-130Electron microscopy reveals that keratinocytes are interconnectedby structures on the cell periphery called desmosomes.154 Thesedesmosomes have a typical structure that consists of two denseattachment plaques into which tonofibrils insert and anintermediate, electron-dense line in the extracellular compartment.Tonofilaments, which are the morphologic expression of thecytoskeleton of keratin proteins, radiate in brushlike fashion fromthe attachment plaques into the cytoplasm of the cells. The spacebetween the cells shows cytoplasmic projections that resemblemicrovilli and that extend into the intercellular space and ofteninterdigitate.Less frequently observed forms of epithelial cell connections aretight junctions (zonae occludens), in which the membranes of theadjoining cells are thought to be fused.268,287 Evidence suggests thatthese structures allow ions and small molecules to pass from onecell to another.Cytoplasmic organelle concentration varies among differentepithelial strata. Mitochondria are more numerous in deeper strata194 and decrease toward the surface of the cell.Accordingly, the histochemical demonstration of succinicdehydrogenase, nicotinamide-adenine dinucleotide, cytochromeoxidase, and other mitochondrial enzymes reveals a more activetricarboxylic cycle in basal and parabasal cells, in which theproximity of the blood supply facilitates energy production throughaerobic glycolysis.Conversely, enzymes of the pentose shunt (an alternativepathway of glycolysis), such as glucose-6-phosphatase, increasetheir activity toward the surface. This pathway produces a largeramount of intermediate products for the production of ribonucleicacid (RNA), which in turn can be used for the synthesis ofkeratinization proteins. This histochemical pattern is in accordancewith the increased volume and the amount of tonofilamentsobserved in cells reaching the surface; the intensity of the activity isproportional to the degree of differentiation.72,82,127,202The uppermost cells of the stratum spinosum contain numerousdense granules called keratinosomes or Odland bodies, which aremodified lysosomes. They contain a large amount of acidphosphatase, an enzyme involved in the destruction of organellemembranes, which occurs suddenly between the granulosum andcorneum strata and during the intercellular cementation ofcornified cells. Thus acid phosphatase is another enzyme that isclosely related to the degree of keratinization.46,125,284 These containtyrosinase, which hydroxylates tyrosine to dihydroxyphenylalanine(dopa), which in turn is progressively converted to melanin.Melanin granules are phagocytosed and contained within othercells of the epithelium and connective tissue called melanophages ormelanophores.Nonkeratinocyte cells are present in gingival epithelium as inother malpighian epithelia. Melanocytes are dendritic cells located inthe basal and spinous layers of the gingival epithelium. Theysynthesize melanin in organelles called premelanosomes ormelanosomes61,228,252 (Fig. 3.11).195 FIG. 3.11 Pigmented gingiva of dog showingmelanocytes (M) in the basal epithelial layer andmelanophores (C) in the connective tissue (Glucksmantechnique).Langerhans cells are dendritic cells located among keratinocytes atall suprabasal levels (Fig. 3.12). They belong to the mononuclearphagocyte system (reticuloendothelial system) as modifiedmonocytes derived from the bone marrow. They contain elongatedgranules, and they are considered macrophages with possibleantigenic properties.72 Langerhans cells have an important role inthe immune reaction as antigen-presenting cells for lymphocytes.They contain g-specific granules (Birbeck granules), and they havemarked adenosine triphosphatase activity. They are found in theoral epithelium of normal gingiva and in smaller amounts in thesulcular epithelium; they are probably absent from the junctionalepithelium of normal gingiva.196 FIG. 3.12 Human gingival epithelium, oral aspect.Immunoperoxidase technique showing Langerhanscells.Merkel cells are located in the deeper layers of the epithelium;they harbor nerve endings, and they are connected to adjacent cellsby desmosomes. They have been identified as tactile perceptors.188The epithelium is joined to the underlying connective tissue by abasal lamina 300 to 400 Å thick and lying approximately 400 Åbeneath the epithelial basal layer.147,235,254 The basal lamina consistsof lamina lucida and lamina densa. Hemidesmosomes of the basalepithelial cells abut the lamina lucida, which is mainly composed ofthe glycoprotein laminin. The lamina densa is composed of type IVcollagen.The basal lamina, which is clearly distinguishable at theultrastructural level, is connected to a reticular condensation of theunderlying connective tissue fibrils (mainly collagen type IV) by theanchoring fibrils.183,213,257 Anchoring fibrils have been measured at750 nm in length from their epithelial end to their connective tissueend, where they appear to form loops around collagen fibers. Thecomplex of basal lamina and fibrils is the periodic acid–Schiff–positive and argyrophilic line observed at the optical level 237,258 (Fig.3.13). The basal lamina is permeable to fluids, but it acts as a barrierto particulate matter.197 FIG. 3.13 Normal human gingiva stained with theperiodic acid–Schiff histochemical method. Thebasement membrane (B) is seen between theepithelium (E) and the underlying connective tissue(C). In the epithelium, glycoprotein material occurs incells and cell membranes of the superficial hornified(H) and underlying granular layers (G). The connectivetissue presents a diffuse, amorphous groundsubstance and collagen fibers. The blood vessel wallsstand out clearly in the papillary projections of theconnective tissue (P).Structural and Metabolic Characteristics of Different Areasof Gingival EpitheliumThe epithelial component of the gingiva shows regionalmorphologic variations that reflect tissue adaptation to the toothand alveolar bone.231 These variations include the oral epithelium,the sulcular epithelium, and the junctional epithelium. Whereas theoral epithelium and the sulcular epithelium are largely protective infunction, the junctional epithelium serves many more roles and is ofconsiderable importance in the regulation of tissue health.18 It isnow recognized that epithelial cells are not passive bystanders inthe gingival tissues; rather, they are metabolically active andcapable of reacting to external stimuli by synthesizing a number ofcytokines, adhesion molecules, growth factors, and enzymes.18The degree of gingival keratinization diminishes with age and theonset of menopause,199 but it is not necessarily related to thedifferent phases of the menstrual cycle.131 Keratinization of the oral198 mucosa varies in different areas in the following order: palate (mostkeratinized), gingiva, ventral aspect of the tongue, and cheek (leastkeratinized).181Keratins K1, K2, and K10 through K12, which are specific toepidermal-type differentiation, are immunohistochemicallyexpressed with high intensity in orthokeratinized areas and withless intensity in parakeratinized areas. K6 and K16, which arecharacteristic of highly proliferative epithelia, and K5 and K14,which are stratification-specific cytokeratins, also are present.Parakeratinized areas express K19, which is usually absent fromorthokeratinized normal epithelia.37,205In keeping with the complete or almost-complete maturation,histoenzyme reactions for acid phosphatase and pentose-shuntenzymes are very strong.47,127Glycogen can accumulate intracellularly when it is notcompletely degraded by any of the glycolytic pathways. Thus itsconcentration in normal gingiva is inversely related to the degree ofkeratinization236,285 and inflammation.71,273,276Oral (Outer) EpitheliumThe oral or outer epithelium covers the crest and outer surface ofthe marginal gingiva and the surface of the attached gingiva. Onaverage, the oral epithelium is 0.2 to 0.3 mm in thickness. It iskeratinized or parakeratinized, or it may present variouscombinations of these conditions (Fig. 3.14). The prevalent surface,however, is parakeratinized.32,45,285 The oral epithelium is composedof four layers: stratum basale (basal layer), stratum spinosum(prickle cell layer), stratum granulosum (granular layer), andstratum corneum (cornified layer).199 FIG. 3.14 Variations in the gingival epithelium. (A)Keratinized. (B) Nonkeratinized. (C) Parakeratinized.Horny layer (H), granular layer (G), prickle cell layer(P), basal cell layer (Ba), flattened surface cells (S),and parakeratotic layer (Pk).Sulcular EpitheliumThe sulcular epithelium lines the gingival sulcus (Fig. 3.15). It is athin, nonkeratinized stratified squamous epithelium without retepegs, and it extends from the coronal limit of the junctionalepithelium to the crest of the gingival margin (Fig. 3.16). It usuallyshows many cells with hydropic degeneration.32FIG. 3.15 Scanning electron microscopic view of the200 epithelial surface facing the tooth in a normal humangingival sulcus. The epithelium (Ep) showsdesquamating cells, some scattered erythrocytes (E),and a few emerging leukocytes (L). (×1000.)FIG. 3.16 Epon-embedded human biopsy specimenshowing a relatively normal gingival sulcus. The soft-tissue wall of the gingival sulcus is made up of the oralsulcular epithelium (ose) and its underlying connectivetissue (ct), whereas the base of the gingival sulcus isformed by the sloughing surface of the junctionalepithelium (je). The enamel space is delineated by adense cuticular structure (dc). A relatively sharp line ofdemarcation exists between the junctional epitheliumand the oral sulcular epithelium (arrow), and severalpolymorphonuclear leukocytes (pmn) can be seentraversing the junctional epithelium. The sulcuscontains red blood cells that resulted from thehemorrhage that occurred at the time of biopsy. (×391;inset ×55.) (From Schluger S, Youdelis R, Page RC: Periodontal disease, ed2, Philadelphia, 1990, Lea & Febiger.)201 As with other nonkeratinized epithelia, the sulcular epitheliumlacks granulosum and corneum strata and K1, K2, and K10 throughK12 cytokeratins, but it contains K4 and K13, the so-calledesophageal-type cytokeratins. It also expresses K19, and it normallydoes not contain Merkel cells.Histochemical studies of enzymes have consistently revealed alower degree of activity in the sulcular than in the outer epithelium,particularly in the case of enzymes related to keratinization.Glucose-6-phosphate dehydrogenase expresses a faint andhomogeneous reaction in all strata, unlike the increasing gradienttoward the surface observed in cornified epithelia.127 Acidphosphatase staining is negative,46 although lysosomes have beendescribed in exfoliated cells.148Despite these morphologic and chemical characteristics, thesulcular epithelium has the potential to keratinize if it is reflectedand exposed to the oral cavity44,48 or if the bacterial flora of thesulcus is totally eliminated.50 Conversely, the outer epithelium losesits keratinization when it is placed in contact with the tooth.50 Thesefindings suggest that the local irritation of the sulcus preventssulcular keratinization.The sulcular epithelium is extremely important; it may act as asemipermeable membrane through which injurious bacterialproducts pass into the gingiva and through which tissue fluid fromthe gingiva seeps into the sulcus.267 Unlike the junctionalepithelium, however, the sulcular epithelium is not heavilyinfiltrated by polymorphonuclear neutrophil leukocytes, and itappears to be less permeable.18Junctional EpitheliumThe junctional epithelium consists of a collar-like band of stratifiedsquamous nonkeratinizing epithelium. It is 3 to 4 layers thick inearly life, but that number increases with age to 10 or even 20layers. In addition, the junctional epithelium tapers from its coronalend, which may be 10 to 29 cells wide to 1 or 2 cells wide at itsapical termination, which is located at the cementoenamel junctionin healthy tissue. These cells can be grouped in two strata: the basallayer that faces the connective tissue and the suprabasal layer thatextends to the tooth surface. The length of the junctional epithelium202 ranges from 0.25 to 1.35 mm (Fig. 3.17).FIG. 3.17 Eruption process in cat's tooth. (A)Unerupted tooth. Dentin (D), remnants of enamelmatrix (E), reduced enamel epithelium (REE), oralepithelium (OE), and artifact (a). (B) Erupting toothforming junctional epithelium (JE). (C) Completelyerupted tooth. Sulcus with epithelial debris (S),cementum (C), and epithelial rests (ER).The junctional epithelium is formed by the confluence of the oralepithelium and the reduced enamel epithelium during tootheruption. However, the reduced enamel epithelium is not essentialfor its formation; in fact, the junctional epithelium is completelyrestored after pocket instrumentation or surgery, and it formsaround an implant.151Cell layers that are not juxtaposed to the tooth exhibit numerousfree ribosomes, prominent membrane-bound structures (e.g., Golgicomplexes), and cytoplasmic vacuoles that are presumablyphagocytic. Lysosome-like bodies also are present, but the absenceof keratinosomes (Odland bodies) and histochemicallydemonstrable acid phosphatase, which are correlated with the lowdegree of differentiation, may reflect a low-defense power againstmicrobial plaque accumulation in the gingival sulcus. Similarmorphologic findings have been described in the gingiva of germ-free rats. Polymorphonuclear neutrophil leukocytes are found203 routinely in the junctional epithelium of both conventional rats andgerm-free rats.296 Research has shown that, although numerousmigrating polymorphonuclear neutrophil leukocytes are evidentand present around healthy junctional epithelium, a considerableincrease in polymorphonuclear neutrophil leukocyte numbers canbe expected with the accumulation of dental plaque and gingivalinflammation.18The different keratin polypeptides of the junctional epitheliumhave a particular histochemical pattern. Junctional epitheliumexpresses K19, which is absent from keratinized epithelia, and thestratification-specific cytokeratins K5 and K14.224 Morgan andcolleagues182 reported that reactions to demonstrate K4 or K13reveal a sudden change between sulcular and junctional epithelia;the junctional area is the only stratified nonkeratinized epitheliumin the oral cavity that does not synthesize these specificpolypeptides. Another particular behavior of junctional epitheliumis the lack of expression of K6 and K16, which is usually linked tohighly proliferative epithelia, although the turnover of the cells isvery high.Similar to sulcular epithelium, junctional epithelium exhibitslower glycolytic enzyme activity than outer epithelium, and it alsolacks acid phosphatase activity.46,127The junctional epithelium is attached to the tooth surface(epithelial attachment) by means of an internal basal lamina. It isattached to the gingival connective tissue by an external basallamina that has the same structure as other epithelial–connectivetissue attachments elsewhere in the body.155,161The internal basal lamina consists of a lamina densa (adjacent tothe enamel) and a lamina lucida to which hemidesmosomes areattached. Hemidesmosomes have a decisive role in the firmattachment of the cells to the internal basal lamina on the toothsurface.Data suggest that the hemidesmosomes may also act as specificsites of signal transduction and thus may participate in theregulation of gene expression, cell proliferation, and celldifferentiation.134 Organic strands from the enamel appear to extendinto the lamina densa.256 The junctional epithelium attaches toafibrillar cementum that is present on the crown (usually restricted204 to an area within 1 mm of the cementoenamel junction)233 and rootcementum in a similar manner.Histochemical evidence for the presence of neutralpolysaccharides in the zone of the epithelial attachment has beenreported.272 Data also have shown that the basal lamina of thejunctional epithelium resembles that of endothelial and epithelialcells in its laminin content but differs in its internal basal lamina,which has no type IV collagen.142,223 These findings indicate that thecells of the junctional epithelium are involved in the production oflaminin and play a key role in the adhesion mechanism.The attachment of the junctional epithelium to the tooth isreinforced by the gingival fibers, which brace the marginal gingivaagainst the tooth surface. For this reason, the junctional epitheliumand the gingival fibers are considered together as a functional unitreferred to as the dentogingival unit.158In conclusion, it is usually accepted that the junctional epitheliumexhibits several unique structural and functional features thatcontribute to preventing pathogenic bacterial flora from colonizingthe subgingival tooth surface.205 First, junctional epithelium isfirmly attached to the tooth surface, thereby forming an epithelialbarrier against plaque bacteria. Second, it allows access of gingivalfluid, inflammatory cells, and components of the immunologic hostdefense to the gingival margin. Third, junctional epithelial cellsexhibit rapid turnover, which contributes to the host–parasiteequilibrium and the rapid repair of damaged tissue. Someinvestigators have also indicated that the cells of the junctionalepithelium have an endocytic capacity equal to that of macrophagesand neutrophils and that this activity may be protective in nature.57Development of Gingival SulcusAfter enamel formation is complete, the enamel is covered withreduced enamel epithelium (REE), which is attached to the tooth by abasal lamina and hemidesmosomes.156,255 When the tooth penetratesthe oral mucosa, the REE unites with the oral epithelium andtransforms into the junctional epithelium. As the tooth erupts, thisunited epithelium condenses along the crown, and the ameloblasts,which form the inner layer of the REE (see Fig. 3.17), graduallybecome squamous epithelial cells. The transformation of the REE205 into a junctional epithelium proceeds in an apical direction withoutinterrupting the attachment to the tooth. According to Schroederand Listgarten,233 this process takes between 1 and 2 years.The junctional epithelium is a continually self-renewingstructure, with mitotic activity occurring in all cell layers.156,255 Theregenerating epithelial cells move toward the tooth surface andalong it in a coronal direction to the gingival sulcus, where they areshed22 (Fig. 3.18). The migrating daughter cells provide acontinuous attachment to the tooth surface. The strength of theepithelial attachment to the tooth has not been measured.FIG. 3.18 Junctional epithelium on an erupting tooth.The junctional epithelium (JE) is formed by the joiningof the oral epithelium (OE) and the reduced enamelepithelium (REE). Afibrillar cementum (AC) issometimes formed on enamel after the degeneration ofthe REE. The arrows indicate the coronal movement ofthe regenerating epithelial cells, which multiply morerapidly in the JE than in the OE. E, Enamel; C, rootcementum. A similar cell turnover pattern exists in thefully erupted tooth. (Modified from Listgarten MA: J Can Dent Assoc36:70, 1970.)206 The gingival sulcus is formed when the tooth erupts into the oralcavity. At that time, the junctional epithelium and the REE form abroad band that is attached to the tooth surface from near the tip ofthe crown to the cementoenamel junction. The gingival sulcus is theshallow, V-shaped space or groove between the tooth and thegingiva that encircles the newly erupted tip of the crown. In thefully erupted tooth, only the junctional epithelium persists. Thesulcus consists of the shallow space that is coronal to the attachment of thejunctional epithelium and bounded by the tooth on one side and thesulcular epithelium on the other. The coronal extent of the gingival sulcusis the gingival margin.Renewal of Gingival EpitheliumThe oral epithelium undergoes continuous renewal. Its thickness ismaintained by a balance between new cell formation in the basaland spinous layers and the shedding of old cells at the surface. Themitotic activity exhibits a 24-hour periodicity, with the highest andlowest rates occurring in the morning and evening, respectively.256The mitotic rate is higher in nonkeratinized areas and increased ingingivitis, without significant gender differences. Opinions differwith regard to whether the mitotic rate is increased160,161,179 ordecreased15 with age.The mitotic rate in experimental animals varies among differentareas of the oral epithelium in descending order: buccal mucosa,hard palate, sulcular epithelium, junctional epithelium, outersurface of the marginal gingiva, and attached gingiva.9,112,160,274 Thefollowing have been reported as turnover times for different areasof the oral epithelium in experimental animals: palate, tongue, andcheek, 5 to 6 days; gingiva, 10 to 12 days, with the same or moretime required with age; and junctional epithelium, 1 to 6 days.22,249With regard to junctional epithelium, it was previously thoughtthat only epithelial cells facing the external basal lamina wererapidly dividing. However, evidence indicates that a significantnumber of the cells (e.g., the basal cells along the connective tissue)are capable of synthesizing deoxyribonucleic acid (DNA), therebydemonstrating their mitotic activity.221,222 The rapid shedding ofcells effectively removes bacteria that adhere to the epithelial cellsand therefore is an important part of the antimicrobial defense207 mechanisms at the dentogingival junction.205Cuticular Structures on the ToothThe term cuticle describes a thin acellular structure with ahomogeneous matrix that is sometimes enclosed within clearlydemarcated linear borders.Listgarten159 has classified cuticular structures into coatings ofdevelopmental origin and acquired coatings. Acquired coatingsinclude those of exogenous origin such as saliva, bacteria, calculus,and surface stains (see Chapters 7 and 13). Coatings of developmentalorigin are those that are normally formed as part of toothdevelopment. They include the REE, the coronal cementum, and thedental cuticle.After enamel formation is completed, the ameloblastic epitheliumis reduced to one or two layers of cells that remain attached to theenamel surface by hemidesmosomes and a basal lamina. This REEconsists of postsecretory ameloblasts and cells from the stratumintermedium of the enamel organ. In some animal species, the REEdisappears entirely and rapidly, thereby placing the enamel surfacein contact with the connective tissue. Connective tissue cells thendeposit a thin layer of cementum known as coronal cementum on theenamel. In humans, thin patches of afibrillar cementum sometimesmay be seen in the cervical half of the crown.Electron microscopy has demonstrated a dental cuticle thatconsists of a layer of homogeneous organic material of variablethickness (approximately 0.25 µm) overlying the enamel surface. Itis nonmineralized, and it is not always present. In some cases, nearthe cementoenamel junction, it is deposited over a layer of afibrillarcementum, which in turn overlies enamel. The cuticle may bepresent between the junctional epithelium and the tooth.Ultrastructural histochemical studies have shown that the dentalcuticle is proteinaceous,143 and it may be an accumulation of tissuefluid components.87,232Gingival Fluid (Sulcular Fluid)The value of the gingival fluid is that it can be represented as eithera transudate or an exudate. The gingival fluid contains a vast arrayof biochemical factors, thereby offering its potential use as a208 diagnostic or prognostic biomarker of the biologic state of theperiodontium in health and disease81 (see Chapter 16). It alsocontains components of connective tissue, epithelium,inflammatory cells, serum, and microbial flora that inhabit thegingival margin or the sulcus (pocket).79In the healthy sulcus, the amount of gingival fluid is very small.During inflammation, however, the gingival fluid flow increases,and its composition starts to resemble that of an inflammatoryexudate.59 The main route of the gingival fluid diffusion is throughthe basement membrane, through the relatively wide intercellularspaces of the junctional epithelium, and then into the sulcus.205 Thegingival fluid is believed to do the following: (1) cleanse materialfrom the sulcus; (2) contain plasma proteins that may improveadhesion of the epithelium to the tooth; (3) possess antimicrobialproperties; and (4) exert antibody activity to defend the gingiva.Gingival Connective TissueThe major components of the gingival connective tissue arecollagen fibers (about 60% by volume), fibroblasts (5%), vessels,nerves, and matrix (about 35%). The connective tissue of thegingiva is known as the lamina propria, and it consists of two layers:(1) a papillary layer subjacent to the epithelium that consists ofpapillary projections between the epithelial rete pegs and (2) areticular layer that is contiguous with the periosteum of the alveolarbone.Connective tissue has a cellular compartment and an extracellularcompartment composed of fibers and ground substance. Thus thegingival connective tissue is largely a fibrous connective tissue thathas elements that originate directly from the oral mucosalconnective tissue as well as some fibers (dentogingival) thatoriginate from the developing dental follicle.18The ground substance fills the space between fibers and cells; it isamorphous, and it has a high water content. It is composed ofproteoglycans (mainly hyaluronic acid and chondroitin sulfate) andglycoproteins (mainly fibronectin). Glycoproteins account for thefaint periodic acid–Schiff–positive reaction of the groundsubstance.82 Fibronectin binds fibroblasts to the fibers and manyother components of the intercellular matrix, thereby helping to209 mediate cell adhesion and migration. Laminin, which is anotherglycoprotein found in the basal lamina, serves to attach it toepithelial cells.The three types of connective tissue fibers are collagen, reticular,and elastic. Collagen type I forms the bulk of the lamina propriaand provides the tensile strength to the gingival tissue. Type IVcollagen (argyrophilic reticulum fiber) branches between thecollagen type I bundles, and it is continuous with fibers of thebasement membrane and the blood vessel walls.161The elastic fiber system is composed of oxytalan, elaunin, andelastin fibers distributed among collagen fibers.56 Therefore denselypacked collagen bundles that are anchored into the acellularextrinsic fiber cementum just below the terminal point of thejunctional epithelium form the connective tissue attachment. Thestability of this attachment is a key factor in the limitation of themigration of junctional epithelium.57Gingival FibersThe connective tissue of the marginal gingiva is denselycollagenous, and it contains a prominent system of collagen fiberbundles called the gingival fibers. These fibers consist of type Icollagen.213 The gingival fibers have the following functions:1. To brace the marginal gingiva firmly against the tooth2. To provide the rigidity necessary to withstand the forces ofmastication without being deflected away from the toothsurface3. To unite the free marginal gingiva with the cementum of theroot and the adjacent attached gingivaThe gingival fibers are arranged in three groups: gingivodental,circular, and transseptal.146The gingivodental fibers are those on the facial, lingual, andinterproximal surfaces. They are embedded in the cementum justbeneath the epithelium at the base of the gingival sulcus. On thefacial and lingual surfaces, they project from the cementum in afanlike conformation toward the crest and outer surface of themarginal gingiva, where they terminate short of the epithelium210 (Figs. 3.19 and 3.20). They also extend externally to the periosteumof the facial and lingual alveolar bones, terminating in the attachedgingiva or blending with the periosteum of the bone.Interproximally, the gingivodental fibers extend toward the crest ofthe interdental gingiva.FIG. 3.19 Faciolingual section of marginal gingivashowing gingival fibers (F) that extend from thecementum (C) to the crest of the gingiva, to the outergingival surface, and external to the periosteum of thebone (B). Circular fibers (CF) are shown in cross-section between the other groups. (Courtesy Sol Bernick.)211 FIG. 3.20 Diagram of the gingivodental fibers thatextend from the cementum (1) to the crest of thegingiva, (2) to the outer surface, and (3) external to theperiosteum of the labial plate. Circular fibers (4) areshown in cross-section.The circular fibers course through the connective tissue of themarginal and interdental gingivae and encircle the tooth in ringlikefashion.The transseptal fibers, which are located interproximally, formhorizontal bundles that extend between the cementum of theapproximating teeth into which they are embedded. They lie in thearea between the epithelium at the base of the gingival sulcus andthe crest of the interdental bone, and they are sometimes classifiedwith the principal fibers of the periodontal ligament.Page and colleagues198 described a group of semicircular fibers thatattach at the proximal surface of a tooth immediately below thecementoenamel junction, go around the facial or lingual marginalgingiva of the tooth, and attach on the other proximal surface of thesame tooth; they also discussed a group of transgingival fibers that212 attach in the proximal surface of one tooth, traverse the interdentalspace diagonally, go around the facial or lingual surface of theadjacent tooth, again traverse the interdental space diagonally, andthen attach in the proximal surface of the next tooth.Tractional forces in the extracellular matrix produced byfibroblasts are believed to be responsible for generating tension inthe collagen. This keeps the teeth tightly bound to each other and tothe alveolar bone.Cellular ElementsThe preponderant cellular element in the gingival connective tissueis the fibroblast. Numerous fibroblasts are found between the fiberbundles. Fibroblasts are of mesenchymal origin and play a majorrole in the development, maintenance, and repair of gingivalconnective tissue. As with connective tissue elsewhere in the body,fibroblasts synthesize collagen and elastic fibers as well as theglycoproteins and glycosaminoglycans of the amorphousintercellular substance. Fibroblasts also regulate collagendegradation through phagocytosis and the secretion ofcollagenases.Fibroblast heterogeneity is now a well-established feature offibroblasts in the periodontium.226 Although the biologic andclinical significance of such heterogeneity is not yet clear, it seemsthat this is necessary for the normal functioning of tissues in health,disease, and repair.18Mast cells, which are distributed throughout the body, arenumerous in the connective tissue of the oral mucosa and thegingiva.52,244,245,288 Fixed macrophages and histiocytes are present in thegingival connective tissue as components of the mononuclearphagocyte system (reticuloendothelial system) and are derivedfrom blood monocytes. Adipose cells and eosinophils, although scarce,are also present in the lamina propria.In clinically normal gingiva, small foci of plasma cells andlymphocytes are found in the connective tissue near the base of thesulcus (Fig. 3.21). Neutrophils can be seen in relatively highnumbers in both the gingival connective tissue and the sulcus.These inflammatory cells are usually present in small amounts inclinically normal gingiva.213 FIG. 3.21 Section of clinically normal gingiva showingsome degree of inflammation, which is almost alwayspresent near the base of the sulcus.Speculations about whether small amounts of leukocytes shouldbe considered a normal component of the gingiva or an incipientinflammatory infiltrate without clinical expression are of theoreticrather than practical importance. Lymphocytes are absent whengingival normalcy is judged by strict clinical criteria or underspecial experimental conditions,13,192 but they are practicallyconstant in healthy, normal gingiva, even before complete tootheruption.150,167,229Immunohistochemical studies involving monoclonal antibodieshave identified the different lymphocyte subpopulations. Theinfiltrate in the area below the junctional epithelium of healthygingiva in newly erupted teeth in children is mainly composed of Tlymphocytes (helper, cytotoxic, suppressor, and natural killer)12,98,242and thus could be interpreted as a normal lymphoid tissue involvedin the early defense recognition system. As time elapses, Blymphocytes and plasma cells appear in greater proportions toelaborate specific antibodies against already-recognized antigensthat are always present in the sulcus of clinically normal gingiva.234Repair of Gingival Connective TissueBecause of the high turnover rate, the connective tissue of thegingiva has remarkably good healing and regenerative capacity.Indeed, it may be one of the best healing tissues in the body, and itgenerally shows little evidence of scarring after surgical procedures.This is likely caused by the rapid reconstruction of the fibrous214 architecture of the tissues.178 However, the reparative capacity ofgingival connective tissue is not as great as that of the periodontalligament or the epithelial tissue.Blood Supply, Lymphatics, and NervesMicrocirculatory tracts, blood vessels, and lymphatic vessels playan important role in the drainage of tissue fluid and in the spread ofinflammation. In individuals with gingivitis and periodontitis, themicrocirculation and vascular formation change greatly in thevascular network directly under the gingival sulcular epitheliumand the junctional epithelium.170Blood vessels are easily evidenced in tissue sections by means ofimmunohistochemical reactions against proteins of endothelial cells(i.e., factor VIII and adhesion molecules). Before these techniqueswere developed, vascularization patterns of periodontal tissues hadbeen described using histoenzymatic reactions for alkalinephosphatase and adenosine triphosphatase because of the greatactivity of these enzymes in endothelial cells.54,297In experimental animals, perfusion with India ink also was usedto study vascular distribution. The injection and subsequentdemonstration of peroxidase allow for blood vessel identificationand permeability studies.239 The periodic acid–Schiff reaction alsooutlines vascular walls by revealing a positive line in the basalmembrane.237 Endothelial cells express 5-nucleotidase activity aswell.126 Scanning electron microscopy can be used after the injectionof plastic into the vessels through the carotid artery, which isfollowed by the corrosion of the soft tissues.84 In addition, laserDoppler flow measurement provides a noninvasive means for theobservation of blood flow modifications related to disease.8Three sources of blood supply to the gingiva are as follows (Figs.3.22 and 3.23):215 FIG. 3.22 Diagram of an arteriole penetrating theinterdental alveolar bone to supply the interdentaltissues (left) and a supraperiosteal arteriole overlyingthe facial alveolar bone, sending branches to thesurrounding tissue (right).FIG. 3.23 Blood supply and peripheral circulation ofthe gingiva. Tissues perfused with India ink. Note the216 capillary plexus parallel to the sulcus (S) and thecapillary loops in the outer papillary layer. Note alsothe supraperiosteal vessels external to the bone (B),which supply the gingiva, and a periodontal ligamentvessel anastomosing with the sulcus plexus. (Courtesy SolBernick.)1. Supraperiosteal arterioles along the facial and lingual surfacesof the alveolar bone from which capillaries extend along thesulcular epithelium and between the rete pegs of theexternal gingival surface8,76,113: Occasional branches of thearterioles pass through the alveolar bone to the periodontalligament or run over the crest of the alveolar bone.2. Vessels of the periodontal ligament, which extend into thegingiva and anastomose with capillaries in the sulcus area.3. Arterioles, which emerge from the crest of the interdentalsepta84 and extend parallel to the crest of the bone toanastomose with vessels of the periodontal ligament, withcapillaries in the gingival crevicular areas and vessels thatrun over the alveolar crest.Beneath the epithelium on the outer gingival surface, capillariesextend into the papillary connective tissue between the epithelialrete pegs in the form of terminal hairpin loops with efferent andafferent branches, spirals, and varices54,113 (Fig. 3.24; also see Fig.3.23). The loops are sometimes linked by cross-communications,86and flattened capillaries serve as reserve vessels when thecirculation is increased in response to irritation.99217 FIG. 3.24 Scanning electron microscopic view of thegingival tissues of rat molar palatal gingiva after thevascular perfusion of plastic and the corrosion of softtissue. (A) Oral view of gingival capillaries: t, tooth;interdental papilla (arrowhead) (×180). (B) View fromthe tooth side. Note the vessels of the plexus next tothe sulcular and junctional epithelium. The arrowheadspoint to vessels in the sulcus area with mildinflammatory changes. g, Crest of the marginalgingiva; s, bottom of the gingival sulcus; pl, periodontalligament vessels. (×150.) (Courtesy NJ Selliseth and K Selvig,University of Bergen, Norway.)Along the sulcular epithelium, capillaries are arranged in a flat,218 anastomosing plexus that extends parallel to the enamel from thebase of the sulcus to the gingival margin.54 In the col area, a mixedpattern of anastomosing capillaries and loops occurs.As mentioned previously, anatomic and histologic changes havebeen shown to occur in the gingival microcirculation of individualswith gingivitis. Prospective studies of the gingival vasculature inanimals have demonstrated that, in the absence of inflammation,the vascular network is arranged in a regular, repetitive, andlayered pattern.54,216 By contrast, the inflamed gingival vasculatureexhibits an irregular vascular plexus pattern, with the microvesselsexhibiting a looped, dilated, and convoluted appearance.216The role of the lymphatic system in removing excess fluids,cellular and protein debris, microorganisms, and other elements isimportant for controlling diffusion and the resolution ofinflammatory processes.168 The lymphatic drainage of the gingivabrings in the lymphatics of the connective tissue papillae.238 Itprogresses into the collecting network external to the periosteum ofthe alveolar process and then moves to the regional lymph nodes,particularly the submaxillary group. In addition, lymphatics justbeneath the junctional epithelium extend into the periodontalligament and accompany the blood vessels.Neural elements are extensively distributed throughout thegingival tissues. Within the gingival connective tissues, most nervefibers are myelinated and closely associated with the bloodvessels.162 Gingival innervation is derived from fibers that arise fromnerves in the periodontal ligament and from the labial, buccal, andpalatal nerves.30 The following nerve structures are present in theconnective tissue: a meshwork of terminal argyrophilic fibers, someof which extend into the epithelium; Meissner-type tactilecorpuscles; Krause-type end bulbs, which are temperaturereceptors; and encapsulated spindles.14Correlation of Clinical and MicroscopicFeaturesAn understanding of the normal clinical features of the gingivarequires the ability to interpret them in terms of the microscopicstructures that they represent.219 ColorThe color of the attached and marginal gingiva is generallydescribed as “coral pink”; it is produced by the vascular supply, thethickness and degree of keratinization of the epithelium, and thepresence of pigment-containing cells. The color varies amongdifferent persons and appears to be correlated with the cutaneouspigmentation. It is lighter in blond individuals with faircomplexions than in swarthy, dark-haired individuals (Fig. 3.25).FIG. 3.25 (A) Clinically normal gingiva in a youngadult. (B) Heavily pigmented (melanotic) gingiva in amiddle-aged adult. (From Glickman I, Smulow JB: Periodontal disease:clinical, radiographic, and histopathologic features, Philadelphia, 1974, Saunders.)The attached gingiva is demarcated from the adjacent alveolarmucosa on the buccal aspect by a clearly defined mucogingival line.The alveolar mucosa is red, smooth, and shiny rather than pink andstippled. A comparison of the microscopic structure of the attachedgingiva with that of the alveolar mucosa provides an explanationfor the difference in appearance. The epithelium of the alveolarmucosa is thinner and nonkeratinized, and it contains no rete pegs(Fig. 3.26). The connective tissue of the alveolar mucosa is loosely220 arranged, and the blood vessels are more numerous.FIG. 3.26 Oral mucosa, facial and palatal surfaces.The facial surface (F) shows the marginal gingiva(MG), the attached gingiva (AG), and the alveolarmucosa (AM). The double line marks the mucogingivaljunction. Note the differences in the epithelium and theconnective tissue in the attached gingiva and thealveolar mucosa. The palatal surface (P) shows themarginal gingiva (MG) and the thick, keratinized palatalmucosa (PM).Physiologic Pigmentation (Melanin)Melanin is a non–hemoglobin-derived brown pigment with thefollowing characteristics:• Melanin is responsible for the normalpigmentation of the skin, the gingiva, and theremainder of the oral mucous membrane.• Melanin is present in all normal individuals(often not in sufficient quantities to be detected221 clinically), but it is absent or severely diminishedin albinos.• Melanin pigmentation in the oral cavity isprominent in black individuals (see Fig. 3.25).• Ascorbic acid directly down-regulates melaninpigmentation in gingival tissues.246According to Dummett,73 the distribution of oral pigmentation inblack individuals is as follows: gingiva, 60%; hard palate, 61%;mucous membrane, 22%; and tongue, 15%. Gingival pigmentationoccurs as a diffuse, deep-purplish discoloration or as irregularlyshaped brown and light-brown patches. It may appear in thegingiva as early as 3 hours after birth, and it is often the onlyevidence of pigmentation.73Oral repigmentation refers to the clinical reappearance ofmelanin pigment after a period of clinical depigmentation of theoral mucosa as a result of chemical, thermal, surgical,pharmacologic, or idiopathic factors.74 Information about therepigmentation of oral tissues after surgical procedures is extremelylimited, and no definitive treatment is offered at this time.SizeThe size of the gingiva corresponds with the sum total of the bulkof cellular and intercellular elements and their vascular supply.Alteration in size is a common feature of gingival disease.ContourThe contour or shape of the gingiva varies considerably anddepends on the shape of the teeth and their alignment in the arch,the location and size of the area of proximal contact, and thedimensions of the facial and lingual gingival embrasures.The marginal gingiva envelops the teeth in collar-like fashion andfollows a scalloped outline on the facial and lingual surfaces. Itforms a straight line along teeth with relatively flat surfaces. Onteeth with pronounced mesiodistal convexity (e.g., maxillarycanines) or teeth in labial version, the normal arcuate contour is222 accentuated, and the gingiva is located farther apically. On teeth inlingual version, the gingiva is horizontal and thickened (Fig. 3.27).In addition, the gingival tissue biotype varies significantly. A thinand clear gingiva is found in one-third of the population andprimarily in females with slender teeth with a narrow zone ofkeratinized tissue, whereas a clear, thick gingiva with a broad zoneof keratinized tissue is present in two-thirds of the population andprimarily in males.70FIG. 3.27 A thickened, shelflike contour of gingiva on atooth in lingual version aggravated by local irritationcaused by plaque accumulation.ShapeThe shape of the interdental gingiva is governed by the contour ofthe proximal tooth surfaces and the location and shape of thegingival embrasures.When the proximal surfaces of the crowns are relatively flatfaciolingually, the roots are close together, the interdental bone isthin mesiodistally, and the gingival embrasures and interdentalgingiva are narrow mesiodistally. Conversely, with proximalsurfaces that flare away from the area of contact, the mesiodistaldiameter of the interdental gingiva is broad (Fig. 3.28). The heightof the interdental gingiva varies with the location of the proximalcontact. Thus in the anterior region of the dentition, the interdental223 papilla is pyramidal in form, whereas the papilla is more flattenedin a buccolingual direction in the molar region.FIG. 3.28 Shape of the interdental gingival papillaecorrelated with the shape of the teeth and theembrasures. (A) Broad interdental papillae. (B) Narrowinterdental papillae.ConsistencyThe gingiva is firm and resilient and, with the exception of themovable free margin, tightly bound to the underlying bone. Thecollagenous nature of the lamina propria and its contiguity with themucoperiosteum of the alveolar bone determine the firmness of theattached gingiva. The gingival fibers contribute to the firmness ofthe gingival margin.Surface TextureThe gingiva presents a textured surface similar to that of an orangepeel and is referred to as stippled (see Fig. 3.25). Stippling is bestviewed by drying the gingiva. The attached gingiva is stippled; themarginal gingiva is not. The central portion of the interdentalpapillae is usually stippled, but the marginal borders are smooth.The pattern and extent of stippling vary among individuals andamong different areas of the same mouth.108,216 Stippling is lessprominent on lingual than facial surfaces and may be absent insome persons.Stippling varies with age. It is absent during infancy, it appears insome children at about 5 years of age, it increases until adulthood,and it frequently begins to disappear during old age.Microscopically, stippling is produced by alternate rounded224 protuberances and depressions in the gingival surface. Thepapillary layer of the connective tissue projects into the elevations,and the elevated and depressed areas are covered by stratifiedsquamous epithelium (Fig. 3.29). The degree of keratinization andthe prominence of stippling appear to be related.FIG. 3.29 Gingival biopsy of the patient shown in Fig.3.7 demonstrating alternate elevations anddepressions (arrows) in the attached gingiva that areresponsible for the stippled appearance.Scanning electron microscopy has shown considerable variationin shape but a relatively constant depth of stippling. At lowmagnification, a rippled surface is seen, and this is interrupted byirregular depressions that are 50 µm in diameter. At highermagnification, cell micropits are seen.61Stippling is a form of adaptive specialization or reinforcement forfunction. It is a feature of healthy gingiva, and the reduction or lossof stippling is a common sign of gingival disease. When the gingivais restored to health after treatment, the stippled appearancereturns.225 The surface texture of the gingiva is also related to the presenceand degree of epithelial keratinization. Keratinization is considereda protective adaptation to function. It increases when the gingiva isstimulated by toothbrushing. However, research on free gingivalgrafts (see Chapter 65) has shown that when connective tissue istransplanted from a keratinized area to a nonkeratinized area, itbecomes covered by a keratinized epithelium.140 This findingsuggests a connective-tissue–based genetic determination of thetype of epithelial surface.PositionThe position of the gingiva is the level at which the gingival marginis attached to the tooth. When the tooth erupts into the oral cavity,the margin and sulcus are at the tip of the crown; as eruptionprogresses, they are seen closer to the root. During this eruptionprocess, as described previously, the junctional epithelium, the oralepithelium, and the reduced enamel epithelium undergo extensivealterations and remodeling while maintaining the shallowphysiologic depth of the sulcus. Without this remodeling of theepithelia, an abnormal anatomic relationship between the gingivaand the tooth would result.Continuous Tooth EruptionAccording to the concept of continuous eruption,105 eruption doesnot cease when the teeth meet their functional antagonists; rather, itcontinues throughout life. Eruption consists of an active phase anda passive phase. Active eruption is the movement of the teeth in thedirection of the occlusal plane, whereas passive eruption is theexposure of the teeth via apical migration of the gingiva.This concept distinguishes between the anatomic crown (i.e., theportion of the tooth covered by enamel) and the anatomic root (i.e.,the portion of the tooth covered by cementum) and between theclinical crown (i.e., the part of the tooth that has been denuded of itsgingiva and projects into the oral cavity) and the clinical root (i.e.,the portion of the tooth covered by periodontal tissues). When theteeth reach their functional antagonists, the gingival sulcus and thejunctional epithelium are still on the enamel, and the clinical crownis approximately two-thirds of the anatomic crown.226 Gottlieb and Orban105 believed that active and passive eruptionproceed together. Active eruption is coordinated with attrition; theteeth erupt to compensate for tooth substance that has been wornaway by attrition. Attrition reduces the clinical crown and preventsit from becoming disproportionately long in relation to the clinicalroot, thus avoiding excessive leverage on the periodontal tissues.Ideally, the rate of active eruption keeps pace with tooth wear,thereby preserving the vertical dimension of the dentition.As teeth erupt, cementum is deposited at the apices andfurcations of the roots, and bone is formed along the fundus of thealveolus and at the crest of the alveolar bone. In this way, part ofthe tooth substance lost by attrition is replaced by the lengtheningof the root, and the socket depth is maintained to support the root.Although originally thought to be a normal physiologic process,passive eruption is now considered a pathologic process. Passiveeruption is divided into the following four stages (Fig. 3.30):FIG. 3.30 Diagrammatic representation of the foursteps of passive eruption according to Gottlieb andOrban.105 1, The base of the gingival sulcus (arrow)and the junctional epithelium (JE) are on the enamel.2, The base of the gingival sulcus (arrow) is on theenamel, and part of the junctional epithelium is on theroot. 3, The base of the gingival sulcus (arrow) is at thecementoenamel line, and the entire junctionalepithelium is on the root. 4, The base of the gingivalsulcus (arrow) and the junctional epithelium are on theroot.227 Stage 1: The teeth reach the line of occlusion. The junctionalepithelium and the base of the gingival sulcus are on theenamel.Stage 2: The junctional epithelium proliferates so that part is onthe cementum and part is on the enamel. The base of thesulcus is still on the enamel.Stage 3: The entire junctional epithelium is on the cementum,and the base of the sulcus is at the cementoenamel junction.As the junctional epithelium proliferates from the crownonto the root, it does not remain at the cementoenameljunction any longer than at any other area of the tooth.Stage 4: The junctional epithelium has proliferated farther onthe cementum. The base of the sulcus is on the cementum, aportion of which is exposed. Proliferation of the junctionalepithelium onto the root is accompanied by degeneration ofthe gingival and periodontal ligament fibers and theirdetachment from the tooth. The cause of this degeneration isnot understood. At present, it is believed to be the result ofchronic inflammation and therefore a pathologic process.As noted, apposition of bone accompanies active eruption. Thedistance between the apical end of the junctional epithelium andthe crest of the alveolus remains constant throughout continuoustooth eruption (i.e., 1.07 mm).93Exposure of the tooth via the apical migration of the gingiva iscalled gingival recession or atrophy. According to the concept ofcontinuous eruption, the gingival sulcus may be located on thecrown, the cementoenamel junction, or the root, depending on theage of the patient and the stage of eruption. Therefore some rootexposure with age would be considered normal and referred to asphysiologic recession. Again, this concept is not accepted at present.Excessive exposure is termed pathologic recession (see Chapter 23).Periodontal LigamentThe periodontal ligament is composed of a complex vascular andhighly cellular connective tissue that surrounds the tooth root andconnects it to the inner wall of the alveolar bone.175 It is continuous228 with the connective tissue of the gingiva, and it communicates withthe marrow spaces through vascular channels in the bone.Although the average width of the periodontal ligament space isdocumented to be about 0.2 mm, considerable variation exists. Theperiodontal space is diminished around teeth that are not infunction and in unerupted teeth, but it is increased in teeth thathave been subjected to hyperfunction.Periodontal FibersThe most important elements of the periodontal ligament are theprincipal fibers, which are collagenous and arranged in bundles andwhich follow a wavy course when viewed in longitudinal section(Fig. 3.31). The terminal portions of the principal fibers that areinserted into cementum and bone are termed Sharpey fibers (Fig.3.32). The principal fiber bundles consist of individual fibers thatform a continuous anastomosing network between tooth andbone.25,58 Once embedded in the wall of the alveolus or in the tooth,Sharpey fibers calcify to a significant degree. They are associatedwith abundant noncollagenous proteins that are typically found inbone, and they have also been identified in tooth cementum.33,132,175Notable among these proteins are osteopontin and bonesialoprotein. These proteins are thought to contribute to theregulation of mineralization and to tissue cohesion at sites ofincreased biomechanical strain.175229 FIG. 3.31 Principal fibers of the periodontal ligamentfollow a wavy course when sectioned longitudinally.The formative function of the periodontal ligament isillustrated by the newly formed osteoid and osteoblastsalong a previously resorbed bone surface (left) and thecementoid and cementoblasts (right). Note the fibersembedded in the forming calcified tissues (arrows). V,Vascular channels.230 FIG. 3.32 Collagen fibers embedded in the cementum(left) and the bone (right) (silver stain). Note theSharpey fibers within the bundle bone (BB) overlyingthe lamellar bone.Collagen is a protein that is composed of different amino acids,the most important of which are glycine, proline, hydroxylysine,and hydroxyproline.51 The amount of collagen in a tissue can bedetermined by its hydroxyproline content. Collagen is responsiblefor the maintenance of the framework and the tone of tissue, and itexhibits a wide range of diversity.80 There are at least 19 recognizedcollagen species encoded by at least 25 separate genes dispersedamong 12 chromosomes.80Collagen biosynthesis occurs inside the fibroblasts to formtropocollagen molecules. These aggregate into microfibrils that arepacked together to form fibrils. Collagen fibrils have a transversestriation with a characteristic periodicity of 64 µm; this striation iscaused by the overlapping arrangement of the tropocollagenmolecules. In collagen types I and III, these fibrils associate to formfibers; in collagen type I, the fibers associate to form bundles (Fig.3.33).231 FIG. 3.33 Collagen microfibrils, fibrils, fibers, andbundles.Collagen is synthesized by fibroblasts, chondroblasts, osteoblasts,odontoblasts, and other cells. The several types of collagen are alldistinguishable by their chemical composition, distribution,function, and morphology.138 The principal fibers are composedmainly of collagen type I,211 whereas reticular fibers are composedof collagen type III. Collagen type IV is found in the basallamina.212,214 The expression of type XII collagen during toothdevelopment is timed with the alignment and organization ofperiodontal fibers and is limited in tooth development to cellswithin the periodontal ligament.164 Type VI collagen has also beenimmunolocalized in the periodontal ligament and the gingiva.83The molecular configuration of collagen fibers provides themwith a tensile strength that is greater than that of steel.Consequently, collagen imparts a unique combination of flexibilityand strength to the tissues.138The principal fibers of the periodontal ligament are arranged insix groups that develop sequentially in the developing root: thetransseptal, alveolar crest, horizontal, oblique, apical, andinterradicular fibers (Fig. 3.34).232 FIG. 3.34 Diagram of the principal fiber groups.Transseptal fibers extend interproximally over the alveolar bonecrest and are embedded in the cementum of adjacent teeth (Fig.3.35). They are reconstructed even after destruction of the alveolarbone that results from periodontal disease. These fibers may beconsidered as belonging to the gingiva, because they do not haveosseous attachment.FIG. 3.35 Transseptal fibers (F) at the crest of theinterdental bone.Alveolar crest fibers extend obliquely from the cementum just233 beneath the junctional epithelium to the alveolar crest (Fig. 3.36).Fibers also run from the cementum over the alveolar crest and tothe fibrous layer of the periosteum that covers the alveolar bone.The alveolar crest fibers prevent the extrusion of the tooth53 andresist lateral tooth movements. The incision of these fibers duringperiodontal surgery does not increase tooth mobility unlesssignificant attachment loss has occurred.97FIG. 3.36 Rat molar section showing alveolar crestfibers radiating coronally.Horizontal fibers extend at right angles to the long axis of the toothfrom the cementum to the alveolar bone.Oblique fibers, which constitute the largest group in theperiodontal ligament, extend from the cementum in a coronaldirection obliquely to the bone (see Fig. 3.34). They bear the bruntof vertical masticatory stresses and transform such stresses intotension on the alveolar bone.234 The apical fibers radiate in a rather irregular manner from thecementum to the bone at the apical region of the socket. They donot occur on incompletely formed roots.The interradicular fibers fan out from the cementum to the tooth inthe furcation areas of multirooted teeth.Other well-formed fiber bundles interdigitate at right angles orsplay around and between regularly arranged fiber bundles. Lessregularly arranged collagen fibers are found in the interstitialconnective tissue between the principal fiber groups; this tissuecontains the blood vessels, lymphatics, and nerves.Although the periodontal ligament does not contain matureelastin, two immature forms are found: oxytalan and elaunin. Theso-called oxytalan fibers89,103 run parallel to the root surface in avertical direction and bend to attach to the cementum89 in thecervical third of the root. They are thought to regulate vascularflow.88 An elastic meshwork has been described in the periodontalligament133 as being composed of many elastin lamellae withperipheral oxytalan fibers and elaunin fibers. Oxytalan fibers havebeen shown to develop de novo in the regenerated periodontalligament.219The principal fibers are remodeled by the periodontal ligamentcells to adapt to physiologic needs265,295 and in response to differentstimuli.277 In addition to these fiber types, small collagen fibersassociated with the larger principal collagen fibers have beendescribed. These fibers run in all directions and form a plexuscalled the indifferent fiber plexus.243Cellular ElementsFour types of cells have been identified in the periodontal ligament:connective tissue cells, epithelial rest cells, immune system cells,and cells associated with neurovascular elements.26,27Connective tissue cells include fibroblasts, cementoblasts, andosteoblasts. Fibroblasts are the most common cells in theperiodontal ligament; they appear as ovoid or elongated cellsoriented along the principal fibers, and they exhibit pseudopodia-like processes.210 These cells synthesize collagen and possess thecapacity to phagocytose “old” collagen fibers and degrade them265235 via enzyme hydrolysis. Thus collagen turnover appears to beregulated by fibroblasts in a process of intracellular degradation ofcollagen that does not involve the action of collagenase.24Phenotypically distinct and functionally different subpopulationsof fibroblasts exist in the adult periodontal ligament. They appearto be identical at both the light and electron microscopic levels,115but they may have different functions, such as the secretion ofdifferent collagen types and the production of collagenase.Osteoblasts, cementoblasts, osteoclasts, and odontoclasts are alsoseen in the cemental and osseous surfaces of the periodontalligament.The epithelial rests of Malassez form a latticework in theperiodontal ligament and appear as either isolated clusters of cellsor interlacing strands (Fig. 3.37), depending on the plane in whichthe microscopic section is cut. Continuity with the junctionalepithelium has been suggested in experimental animals.106 Theepithelial rests are considered remnants of the Hertwig root sheath,which disintegrates during root development (Fig. 3.37A).FIG. 3.37 Epithelial rests of Malassez. (A) Erupting236 tooth in a cat. Note the fragmentation of the Hertwigepithelial root sheath giving rise to epithelial restslocated along and close to the root surface. (B) Humanperiodontal ligament with rosette-shaped epithelialrests (arrows) lying close to the cementum (C).Epithelial rests are distributed close to the cementum throughoutthe periodontal ligament of most teeth; they are most numerous inthe apical area207 and the cervical area.279,280 They diminish innumber with age248 by degenerating and disappearing or byundergoing calcification to become cementicles. The cells aresurrounded by a distinct basal lamina, they are interconnected byhemidesmosomes, and they contain tonofilaments.24Although their functional properties are still considered to beunclear,259 the epithelial rests are reported to contain keratinocytegrowth factors, and they have been shown to be positive fortyrosine kinase A neurotrophin receptor.92,281,291 In addition,epithelial rests proliferate when stimulated,261,266,275 and theyparticipate in the formation of periapical cysts and lateral root cysts.The defense cells in the periodontal ligament include neutrophils,lymphocytes, macrophages, mast cells, and eosinophils. These cells,as well as those associated with neurovascular elements, are similarto the cells found in other connective tissues.Ground SubstanceThe periodontal ligament also contains a large proportion ofground substance that fills the spaces between fibers and cells. Thissubstance consists of two main components: glycosaminoglycans,such as hyaluronic acid and proteoglycans, and glycoproteins, suchas fibronectin and laminin. It also has a high water content (i.e.,70%).The cell surface proteoglycans participate in several biologicfunctions, including cell adhesion, cell–cell and cell–matrixinteractions, binding to various growth factors as coreceptors, andcell repair.292 For example, fibromodulin (a small proteoglycan richin keratan sulfate and leucine) has been identified in bovineperiodontal ligament.283 The most comprehensive study of theproteoglycans in periodontal ligament was performed with the use237 of fibroblast cultures of human ligament.149The periodontal ligament may also contain calcified massescalled cementicles, which are adherent to or detached from the rootsurfaces (Fig. 3.38).FIG. 3.38 Cementicles in the periodontal ligament.One is lying free and the other is adherent to the toothsurface.Cementicles may develop from calcified epithelial rests; aroundsmall spicules of cementum or alveolar bone traumaticallydisplaced into the periodontal ligament; from calcified Sharpeyfibers; and from calcified, thrombosed vessels within theperiodontal ligament.180Functions of Periodontal LigamentThe functions of the periodontal ligament are categorized asphysical, formative and remodeling, nutritional, and sensory.Physical FunctionsThe physical functions of the periodontal ligament entail thefollowing:238 1. Provision of a soft-tissue “casing” to protect the vessels andnerves from injury by mechanical forces2. Transmission of occlusal forces to the bone3. Attachment of the teeth to the bone4. Maintenance of the gingival tissues in their properrelationship to the teeth5. Resistance to the impact of occlusal forces (i.e., shockabsorption)Resistance to Impact of Occlusal Forces (ShockAbsorption)Two theories pertaining to the mechanism of tooth support havebeen considered: the tensional theory and the viscoelastic systemtheory.The tensional theory of tooth support states that the principalfibers of the periodontal ligament are the major factor in supportingthe tooth and transmitting forces to the bone. When a force isapplied to the crown, the principal fibers first unfold andstraighten, and they then transmit forces to the alveolar bone,thereby causing an elastic deformation of the bony socket. Finally,when the alveolar bone has reached its limit, the load is transmittedto the basal bone. Many investigators find this theory insufficient toexplain available experimental evidence.The viscoelastic system theory states that the displacement of thetooth is largely controlled by fluid movements, with fibers havingonly a secondary role.31,43 When forces are transmitted to the tooth,the extracellular fluid passes from the periodontal ligament into themarrow spaces of the bone through the foramina in the cribriformplate. These perforations of the cribriform plate link the periodontalligament with the cancellous portion of the alveolar bone; they aremore abundant in the cervical third than in the middle and apicalthirds (Fig. 3.39).239 FIG. 3.39 Foramina perforating the lamina dura of adog jaw.After the depletion of tissue fluids, the fiber bundles absorb theslack and tighten. This leads to a blood vessel stenosis. Arterial backpressure causes ballooning of the vessels and passage of the bloodultrafiltrates into the tissues, thereby replenishing the tissue fluids.31Transmission of Occlusal Forces to BoneThe arrangement of the principal fibers is similar to that of asuspension bridge or a hammock. When an axial force is applied toa tooth, a tendency toward displacement of the root into thealveolus occurs. The oblique fibers alter their wavy, untensedpattern, assume their full length, and sustain the major part of theaxial force. When a horizontal or tipping force is applied, twophases of tooth movement occur. The first is within the confines ofthe periodontal ligament, and the second produces a displacementof the facial and lingual bony plates.69 The tooth rotates about anaxis that may change as the force is increased.The apical portion of the root moves in a direction that isopposite to the coronal portion. In areas of tension, the principalfiber bundles are taut rather than wavy. In areas of pressure, thefibers are compressed, the tooth is displaced, and a correspondingdistortion of bone exists in the direction of root movement.203In single-rooted teeth, the axis of rotation is located in the areabetween the apical third and the middle third of the root (Fig. 3.40).The root apex184 and the coronal half of the clinical root have been240 suggested as other locations of the axis of rotation. The periodontalligament, which has an hourglass shape, is narrowest in the regionof the axis of rotation65,145 (Table 3.1). In multirooted teeth, the axisof rotation is located in the bone between the roots (Fig. 3.41). Incompliance with the physiologic mesial migration of the teeth, theperiodontal ligament is thinner on the mesial root surface than onthe distal surface.FIG. 3.40 Left, Diagram of a mandibular premolar in aresting state. Right, When a force is exerted on thetooth—in this case, in faciolingual direction (arrow)—the tooth rotates around the fulcrum or axis of rotation(black circle on root). The periodontal ligament iscompressed in areas of pressure and distended inareas of tension.TABLE 3.1Thickness of the Periodontal Ligaments of 172 Teeth From 15Human SubjectsAverage of AlveolarCrest (mm)Average ofMidroot (mm)Average ofApex (mm)Average ofTooth (mm)Ages 11through 16years0.23 0.17 0.24 0.2183 teeth from 4jaws241 Ages 32through 50years0.20 0.14 0.19 0.1836 teeth from 5jawsAges 51through 67years0.17 0.12 0.16 0.1535 teeth from 5jawsAge 24 years (1case)0.16 0.09 0.15 0.1318 teeth from 1jawModified from Coolidge ED: The thickness of the human periodontal membrane. JAm Dent Assoc 24:1260, 1937.FIG. 3.41 Microscopic view of a rat molar subjected toocclusohorizontal forces. Note the alternating widenedand narrowed areas of the periodontal ligament as thetooth rotates around its axis of rotation. The axis ofrotation is in the interradicular space.Formative and Remodeling Function242 Periodontal ligament and alveolar bone cells are exposed tophysical forces in response to mastication, parafunction, speech,and orthodontic tooth movement.173 Cells of the periodontalligament participate in the formation and resorption of cementumand bone, which occur during physiologic tooth movement, duringthe accommodation of the periodontium to occlusal forces, andduring the repair of injuries.Variations in cellular enzyme activity are correlated with theremodeling process.94-96 Although applied loads may inducevascular and inflammatory reactive changes in periodontalligament cells, current evidence suggests that these cells have amechanism to respond directly to mechanical forces via theactivation of various mechanosensory signaling systems, includingadenylate cyclase, stretch-activated ion channels, and via changes incytoskeletal organization.173Cartilage formation in the periodontal ligament, althoughunusual, may represent a metaplastic phenomenon in the repair ofthis ligament after injury.20The periodontal ligament is constantly undergoing remodeling.Old cells and fibers are broken down and replaced by new ones,and mitotic activity can be observed in the fibroblasts and theendothelial cells.185 Fibroblasts form the collagen fibers, and theresidual mesenchymal cells develop into osteoblasts andcementoblasts. Therefore the rate of formation and thedifferentiation of osteoblasts, cementoblasts, and fibroblasts affectthe rate of formation of collagen, cementum, and bone.Radioautographic studies with radioactive thymidine, proline,and glycine indicate a high turnover rate of collagen in theperiodontal ligament. The rate of collagen synthesis is twice as fastas that in the gingiva and four times as fast as that in the skin, asestablished in the rat molar.250 A rapid turnover of sulfatedglycosaminoglycans in the cells and amorphous ground substanceof the periodontal ligament also occurs.21 It should be noted thatmost of these studies have been performed in rodents and thatinformation about primates and humans is scarce.232Nutritional and Sensory FunctionsThe periodontal ligament supplies nutrients to the cementum, bone,243 and gingiva by way of the blood vessels, and it also provideslymphatic drainage as discussed later in this chapter. In relation toother ligaments and tendons, the periodontal ligament is highlyvascularized tissue; almost 10% of its volume in the rodent molar isblood vessels.35,174 This relatively high blood vessel content mayprovide hydrodynamic damping to applied forces as well as highperfusion rates to the periodontal ligament.173The periodontal ligament is abundantly supplied with sensorynerve fibers that are capable of transmitting tactile, pressure, andpain sensations via the trigeminal pathways.14,30 Nerve bundles passinto the periodontal ligament from the periapical area and throughchannels from the alveolar bone that follow the course of the bloodvessels. The bundles divide into single myelinated fibers, whichultimately lose their myelin sheaths and end in one of four types ofneural termination: (1) free endings, which have a treelikeconfiguration and carry pain sensation; (2) Ruffini-likemechanoreceptors, which are located primarily in the apical area;(3) coiled Meissner corpuscles and mechanoreceptors, which arefound mainly in the midroot region; and (4) spindle-like pressureand vibration endings, which are surrounded by a fibrous capsuleand located mainly in the apex.88,166Regulation of Periodontal Ligament WidthSome of the most interesting features of the periodontal ligament inanimals are its adaptability to rapidly changing applied force andits capacity to maintain its width at constant dimensionsthroughout its lifetime.174 These are important measures ofperiodontal ligament homeostasis that provide insight into thefunction of the biologic mechanisms that tightly regulate themetabolism and spatial locations of the cell populations involved inthe formation of bone, cementum, and periodontal ligament fibers.In addition, the ability of periodontal ligament cells to synthesizeand secrete a wide range of regulatory molecules is an essentialcomponent of tissue remodeling and periodontal ligamenthomeostasis.173Cementum244 Cementum is the calcified, avascular mesenchymal tissue thatforms the outer covering of the anatomic root. The two main typesof cementum are acellular (primary) and cellular (secondary)cementum.104 Both consist of a calcified interfibrillar matrix andcollagen fibrils.The two main sources of collagen fibers in cementum are Sharpeyfibers (extrinsic), which are the embedded portion of the principalfibers of the periodontal ligament214 and which are formed by thefibroblasts, and fibers that belong to the cementum matrix(intrinsic), which are produced by the cementoblasts.240Cementoblasts also form the noncollagenous components of theinterfibrillar ground substance, such as proteoglycans,glycoproteins, and phosphoproteins. Proteoglycans are most likelyto play a role in regulating cell–cell and cell–matrix interactions,both during normal development and during the regeneration ofthe cementum.17 In addition, immunohistochemical studies haveshown that the distribution of proteoglycans is closely associatedwith the cementoblasts and the cementocytes.1,2The major proportion of the organic matrix of cementum iscomposed of type I (90%) and type III (about 5%) collagens.Sharpey fibers, which constitute a considerable proportion of thebulk of cementum, are composed of mainly type I collagen.206 TypeIII collagen appears to coat the type I collagen of the Sharpeyfibers.16Acellular cementum is the first cementum formed; it coversapproximately the cervical third or half of the root, and it does notcontain cells (Fig. 3.42). This cementum is formed before the toothreaches the occlusal plane, and its thickness ranges from 30 to 230µm.248 Sharpey fibers make up most of the structure of acellularcementum, which has a principal role in supporting the tooth. Mostfibers are inserted at approximately right angles into the rootsurface and penetrate deep into the cementum, but others enterfrom several different directions. Their size, number, anddistribution increase with function.123 Sharpey fibers are completelycalcified, with the mineral crystals oriented parallel to the fibrils asin dentin and bone, except in a 10- to 50-µm–wide zone near thecementodentinal junction, where they are only partially calcified.The peripheral portions of Sharpey fibers in actively mineralizing245 cementum tend to be more calcified than the interior regions,according to evidence obtained by scanning electron microscopy.137Acellular cementum also contains intrinsic collagen fibrils that arecalcified and irregularly arranged or parallel to the surface.232FIG. 3.42 Acellular cementum (AC) showingincremental lines running parallel to the long axis of thetooth. These lines represent the appositional growth ofcementum. Note the thin, light lines running into thecementum perpendicular to the surface; theserepresent the Sharpey fibers of the periodontalligament (PL). D, Dentin. (×300.)Cellular cementum, which is formed after the tooth reaches theocclusal plane, is more irregular and contains cells (cementocytes)in individual spaces (lacunae) that communicate with each otherthrough a system of anastomosing canaliculi (Fig. 3.43). Cellularcementum is less calcified than the acellular type.124 Sharpey fibersoccupy a smaller portion of cellular cementum and are separated byother fibers that are arranged either parallel to the root surface or atrandom. Sharpey fibers may be completely or partially calcified, or246 they may have a central, uncalcified core surrounded by a calcifiedborder.135,240FIG. 3.43 Cellular cementum (CC) showingcementocytes lying within the lacunae. Cellularcementum is thicker than acellular cementum. Theevidence of incremental lines also exists, but they areless distinct than in the acellular cementum. The cellsadjacent to the surface of the cementum in theperiodontal ligament (PL) space are cementoblasts. D,Dentin. (×300.)Both acellular cementum and cellular cementum are arranged inlamellae separated by incremental lines parallel to the long axis ofthe root (see Figs. 3.42 and 3.43). These lines represent “restperiods” in cementum formation, and they are more mineralizedthan the adjacent cementum.215 In addition, the loss of the cervicalpart of the reduced enamel epithelium at the time of tooth eruptionmay place portions of mature enamel in contact with the connectivetissue, which then will deposit an acellular and afibrillar type ofcementum over the enamel.157247 On the basis of these findings, Schroeder133,134 has classifiedcementum as follows:• Acellular afibrillar cementum contains neithercells nor extrinsic or intrinsic collagen fibers,except for a mineralized ground substance.Acellular afibrillar cementum is a product ofcementoblasts and found as coronal cementum inhumans, with a thickness of 1 to 15 µm.• Acellular extrinsic fiber cementum is composedalmost entirely of densely packed bundles ofSharpey fibers and lacks cells. Acellular extrinsicfiber cementum is a product of fibroblasts andcementoblasts. It is found in the cervical third ofroots in humans, but it may extend fartherapically. Its thickness is between 30 and 230 µm.• Cellular mixed stratified cementum is composedof extrinsic (Sharpey) and intrinsic fibers, and itmay contain cells. Cellular mixed stratifiedcementum is a co-product of fibroblasts andcementoblasts. In humans, it appears primarily inthe apical third of the roots and apices and infurcation areas. Its thickness ranges from 100 to1000 µm.• Cellular intrinsic fiber cementum contains cellsbut no extrinsic collagen fibers. Cellular intrinsicfiber cementum is formed by cementoblasts, and,in humans, it fills the resorption lacunae.Intermediate cementum is a poorly defined zone near thecementodentinal junction of certain teeth that appears to containcellular remnants of the Hertwig sheath embedded in a calcified248 ground substance.77,153Inorganic content of cementum (hydroxyapatite;Ca10[Po4]6[OH]2) is 45% to 50%, which is less than that of bone(65%), enamel (97%), or dentin (70%).299 Opinions differ with regardto whether the microhardness increases189 or decreases with age,282and no relationship has been established between aging and themineral content of cementum.It is well known that the protein extracts of mature cementumpromote cell attachment and cell migration and stimulate theprotein synthesis of gingival fibroblasts and periodontal ligamentcells.225 Studies of cementum have identified adhesion proteins witharginyl–glycyl–aspartic acid sequences: bone sialoprotein,osteopontin, and osteonectin.39,175 Bone sialoprotein and osteopontinare expressed during early tooth root development by cells alongthe root surface, and they are thought to play a major role in thedifferentiation of the cementoblast progenitor cells to thecementoblasts.109,225Some of the molecules unique to the cementum have beendescribed. Researchers have investigated the role of cementumattachment protein, which is a collagenous cementum-derivedprotein. Cementum attachment protein has been shown to promotethe adhesion and spreading of mesenchymal cell types, withosteoblasts and periodontal ligament fibroblasts showing betteradhesion than gingival fibroblasts and keratinocytes.220 In addition,Ikezawa and colleagues122 described the characterization ofcementum-derived growth factor, which is an insulin-like, growthfactor-I–like molecule. Cementum-derived growth factor has beenshown to enhance the proliferation of gingival fibroblasts andperiodontal ligament cells.Permeability of CementumIn very young animals, acellular cementum and cellular cementumare very permeable and permit the diffusion of dyes from the pulpand the external root surface. In cellular cementum, the canaliculi insome areas are contiguous with the dentinal tubuli. Thepermeability of cementum diminishes with age.36249 Cementoenamel JunctionThe cementum at and immediately subjacent to the cementoenameljunction is of particular clinical importance in root-scalingprocedures. Three types of relationships involving the cementummay exist at the cementoenamel junction.190 In about 60% to 65% ofcases, cementum overlaps the enamel (Fig. 3.44); in about 30%, anedge-to-edge butt joint exists; and in 5% to 10%, the cementum andenamel fail to meet. In the last case, gingival recession may result inaccentuated sensitivity as a result of exposed dentin.FIG. 3.44 Normal variations in tooth morphology at thecementoenamel junction. (A) Space between theenamel and the cementum with the dentin (D)exposed. (B) End-to-end relationship of enamel andcementum. (C) Cementum overlapping the enamel.Cementodentinal JunctionThe terminal apical area of the cementum where it joins the internalroot canal dentin is known as the cementodentinal junction. Whenroot canal treatment is performed, the obturating material shouldbe at the cementodentinal junction. There appears to be no increaseor decrease in the width of the cementodentinal junction with age;its width appears to remain relatively stable.253 Scanning electronmicroscopy of the human teeth reveals that the cementodentinaljunction is 2 to 3 µm wide. The fibril-poor layer contains asignificant amount of proteoglycans, and fibrils interminglebetween the cementum and the dentin.293,294250 Thickness of CementumCementum deposition is a continuous process that proceeds atvarying rates throughout life. Cementum formation is most rapid inthe apical regions, where it compensates for tooth eruption, whichitself compensates for attrition.The thickness of cementum on the coronal half of the root variesfrom 16 to 60 µm, which is about the thickness of a hair. It attains itsgreatest thickness (≤150 to 200 µm) in the apical third and in thefurcation areas. It is thicker in distal surfaces than in mesialsurfaces, probably because of functional stimulation from mesialdrift over time.68 Between the ages of 11 and 70 years, the averagethickness of the cementum increases threefold, with the greatestincrease seen in the apical region. Average thicknesses of 95 µm atthe age of 20 years and of 215 µm at the age of 60 years have beenreported.298Abnormalities in the thickness of cementum may range from anabsence or paucity of cellular cementum (i.e., cemental aplasia orhypoplasia) to an excessive deposition of cementum (i.e., cementalhyperplasia or hypercementosis).152The term hypercementosis refers to a prominent thickening of thecementum. It is largely an age-related phenomenon, and it may belocalized to one tooth or affect the entire dentition. As a result ofconsiderable physiologic variation in the thickness of cementumamong different teeth in the same person and also among differentpersons, distinguishing between hypercementosis and thephysiologic thickening of cementum is sometimes difficult.Nevertheless, the excessive proliferation of cementum may occurwith a broad spectrum of neoplastic and nonneoplastic conditions,including benign cementoblastoma, cementifying fibroma,periapical cemental dysplasia, florid cemento-osseous dysplasia,and other benign fibro-osseous lesions.152Hypercementosis occurs as a generalized thickening of thecementum, with nodular enlargement of the apical third of the root.It also appears in the form of spikelike excrescences (i.e., cementalspikes) created by either the coalescence of cementicles that adhereto the root or the calcification of periodontal fibers at the sites ofinsertion into the cementum.153Radiographically, the radiolucent shadow of the periodontal251 ligament and the radiopaque lamina dura are always seen on theouter border of an area of hypercementosis, enveloping it as itwould in normal cementum.152 On the other hand, from adiagnostic standpoint, periapical cemental dysplasia, condensingosteitis, and focal periapical osteopetrosis may be differentiatedfrom hypercementosis, because all of these entities are locatedoutside of the shadow of the periodontal ligament and the laminadura.290The cause of hypercementosis varies and is not completelyunderstood. The spikelike type of hypercementosis generallyresults from excessive tension caused by orthodontic appliances orocclusal forces. The generalized type occurs in a variety ofcircumstances. In teeth without antagonists, hypercementosis isinterpreted as an effort to keep pace with excessive tooth eruption.In teeth that are subject to low-grade periapical irritation that arisesfrom pulp disease, it is considered compensation for the destroyedfibrous attachment to the tooth. The cementum is depositedadjacent to the inflamed periapical tissue. Hypercementosis of theentire dentition may occur in patients with Paget disease.218 Othersystemic disturbances that may lead to or may be associated withhypercementosis include acromegaly, arthritis, calcinosis,rheumatic fever, and thyroid goiter.152Hypercementosis itself does not require treatment. It could pose aproblem if an affected tooth requires extraction. In a multirootedtooth, sectioning of the tooth may be required before extraction.19Cementum Resorption and RepairPermanent teeth do not undergo physiologic resorption as primaryteeth do. However, the cementum of erupted (as well as unerupted)teeth is subject to resorptive changes that may be of microscopicproportion or sufficiently extensive to present a radiographicallydetectable alteration in the root contour.Microscopic cementum resorption is extremely common; in onestudy, it occurred in 236 of 261 teeth (90.5%).118 The average numberof resorption areas per tooth was 3.5. Of the 922 areas of resorption,708 (76.8%) were located in the apical third of the root, 177 (19.2%)in the middle third, and 37 (4.0%) in the gingival third.252 Approximately 70% of all resorption areas were confined to thecementum without involving the dentin.Cementum resorption may be caused by local or systemic factors,or it may occur without apparent etiology (i.e., idiopathic). Localconditions that cause cementum resorption include trauma fromocclusion194 (Fig. 3.45); orthodontic movement117,193,217; pressure frommalaligned erupting teeth, cysts, and tumors144; teeth withoutfunctional antagonists; embedded teeth; replanted and transplantedteeth3,135; periapical disease; and periodontal disease. Systemicconditions that are cited as predisposing an individual to orinducing cemental resorption include calcium deficiency,136hypothyroidism,23 hereditary fibrous osteodystrophy,269 and Pagetdisease.218FIG. 3.45 Cemental resorption associated withexcessive occlusal forces. (A) Low-power histologicsection of the mandibular anterior teeth. (B) High-power micrograph of the apex of the left central incisorshortened by the resorption of cementum and dentin.Note the partial repair of the eroded areas (arrows)and the cementicle at the upper right.Cementum resorption appears microscopically as baylike253 concavities in the root surface. (Fig. 3.46) Multinucleated giant cellsand large mononuclear macrophages are generally found adjacentto cementum that is undergoing active resorption (Fig. 3.47).Several sites of resorption may coalesce to form a large area ofdestruction. The resorptive process may extend into the underlyingdentin and even into the pulp, but it is usually painless. Cementumresorption is not necessarily continuous and may alternate withperiods of repair and the deposition of new cementum. The newlyformed cementum is demarcated from the root by a deeply stainingirregular line termed a reversal line, which delineates the border ofthe previous resorption. One study showed that the reversal lines ofhuman teeth contain a few collagen fibrils and highly accumulatedproteoglycans with mucopolysaccharides (glycosaminoglycans)and that fibril intermingling occurs only in some places betweenreparative cementum and resorbed dentin or cementum.293,294Embedded fibers of the periodontal ligament reestablish afunctional relationship in the new cementum.FIG. 3.46 Scanning electron micrograph of a rootexposed by periodontal disease showing a largeresorption bay (R). Remnants of the periodontalligament (P) and calculus (C) are visible. Cracking ofthe tooth surface occurs as a result of the preparationtechnique. (×160.) (Courtesy Dr. John Sottosanti, La Jolla, California.)254 FIG. 3.47 Resorption of cementum and dentin. Amultinuclear osteoclast in seen (X). The direction ofresorption is indicated by the arrow. Note the scallopedresorption front in the dentin (D). The cementum is thedarkly stained band at the upper and lower right. P,Periodontal ligament.Cementum repair requires the presence of viable connectivetissue. If epithelium proliferates into an area of resorption, repairwill not take place. Cementum repair can occur in devitalized aswell as vital teeth.Histologic evidence demonstrates that cementum formation iscritical for the appropriate maturation of the periodontium, bothduring development and during the regeneration of lostperiodontal tissues.225 In other words, a variety of macromoleculespresent in the extracellular matrix of the periodontium are likely toplay a regulatory role in cementogenesis.169The regeneration of cementum requires cementoblasts, but theorigin of the cementoblasts and the molecular factors that regulatetheir recruitment and differentiation are not fully understood.However, research provides a better understanding; for example,the epithelial cell rests of Malassez are the only odontogenicepithelial cells that remain in the periodontium after the eruption ofteeth, and they may have some function in cementum repair and255 regeneration under specific conditions.114 The rests of Malassez maybe related to cementum repair by activating their potential tosecrete matrix proteins that have been expressed in toothdevelopment, such as amelogenins, enamelins, and sheath proteins.Several growth factors have been shown to be effective incementum regeneration, including members of the transforminggrowth factor superfamily (i.e., bone morphogenetic proteins),platelet-derived growth factor, insulin-like growth factor, andenamel matrix derivatives139,225 (Fig. 3.48).FIG. 3.48 A clinical human histology shows that newcementum and new periodontal ligament fiber formedat a previous periodontal defect treated withrecombinant human platelet-derived growth factor-BBwith β-tricalcium phosphate. (Courtesy Dr. Daniel WK Kao,Philadelphia, Pennsylvania.)AnkylosisFusion of the cementum and the alveolar bone with obliteration ofthe periodontal ligament is termed ankylosis. Ankylosis occurs inteeth with cemental resorption, which suggests that it mayrepresent a form of abnormal repair. Ankylosis may also developafter chronic periapical inflammation, tooth replantation, andocclusal trauma and around embedded teeth. This condition isrelatively uncommon, and it occurs most frequently in the primary256 dentition.176Ankylosis results in the resorption of the root and its gradualreplacement by bone tissue. For this reason, reimplanted teeth thatankylose will lose their roots after 4 to 5 years and will beexfoliated. Clinically, ankylosed teeth lack the physiologic mobilityof normal teeth, which is one diagnostic sign for ankyloticresorption. In addition, these teeth usually have a special metallicpercussion sound; if the ankylotic process continues, they will be ininfraocclusion.90 However, the clinical diagnosis of ankylosis bymobility and percussion tests alone is only reliable when at least20% of the root surface is affected.10As the periodontal ligament is replaced with bone duringankylosis, proprioception is lost, because pressure receptors in theperiodontal ligament are deleted or do not function correctly.Furthermore, the physiologic drifting and eruption of teeth can nolonger occur, and thus the ability of the teeth and periodontium toadapt to altered force levels or directions of force is greatlyreduced.173 Radiographically, resorption lacunae are filled withbone, and the periodontal ligament space is missing.Because no definitive causes can be found in ankylotic rootresorption, no predictable treatment can be suggested. Treatmentmodalities range from a conservative approach, such as restorativeintervention, to surgical, such as the extraction of the affectedtooth.186When titanium implants are placed in the jaw, healing results inbone that is formed in direct apposition to the implant withoutintervening connective tissue. This may be interpreted as a form ofankylosis. Because resorption of the metallic implant cannot occur,the implant remains indefinitely “ankylosed” to the bone. Inaddition, a true periodontal pocket will not form; the apicalproliferation of the epithelium along the root, which is a keyelement of pocket formation, is not possible because of theankylosis.Exposure of Cementum to the OralEnvironmentCementum becomes exposed to the oral environment in cases of257 gingival recession and as a result of the loss of attachment in pocketformation. The cementum is sufficiently permeable to be penetratedin these cases by organic substances, inorganic ions, and bacteria.Bacterial invasion of the cementum occurs frequently in individualswith periodontal disease, and cementum caries can develop (seeChapter 23).Alveolar ProcessThe alveolar process is the portion of the maxilla and mandible thatforms and supports the tooth sockets (alveoli). It forms when thetooth erupts to provide the osseous attachment to the formingperiodontal ligament; it disappears gradually after the tooth is lost.Because the alveolar processes develop and undergo remodelingwith tooth formation and eruption, they are tooth-dependent bonystructures.227 Therefore the size, shape, location, and function of theteeth determine their morphology. Interestingly, although thegrowth and development of the bones of the jaw determine theposition of the teeth, a certain degree of repositioning of the teethcan be accomplished through occlusal forces and in response toorthodontic procedures that rely on the adaptability of the alveolarbone and the associated periodontal tissues.251The alveolar process consists of the following:1. An external plate of cortical bone is formed by haversianbone and compacted bone lamellae.2. The inner socket wall of thin, compact bone called thealveolar bone proper is seen as the lamina dura in radiographs.Histologically, it contains a series of openings (i.e., thecribriform plate) through which neurovascular bundles linkthe periodontal ligament with the central component of thealveolar bone: the cancellous bone.3. Cancellous trabeculae between these two compact layers actas supporting alveolar bone. The interdental septum consistsof cancellous supporting bone enclosed within a compactborder (Fig. 3.49).258 FIG. 3.49 Mesiodistal section through the mandibularmolars of a 17-year-old girl obtained at autopsy. Note theinterdental bony septa between the first and secondmolars. The dense cortical bony plates represent thealveolar bone proper (i.e., the cribriform plates) and aresupported by cancellous bony trabeculae. The third molaris still in the early stages of root formation and eruption.In addition, the bones of the jaw include the basal bone, which isthe portion of the jaw located apically but unrelated to the teeth(Fig. 3.50).259 FIG. 3.50 Section through a human jaw with a tooth insitu. The dotted line indicates the separation betweenthe basal bone and the alveolar bone. (Redrawn from Ten CateAR: Oral histology: development, structure, and function, ed 4, St Louis, 1994,Mosby.)The alveolar process is divisible into separate areas on ananatomic basis, but it functions as a unit, with all parts interrelatedin the support of the teeth. Figs. 3.51 and 3.52 show the relativeproportions of cancellous bone and compact bone that form thealveolar process. Most of the facial and lingual portions of thesockets are formed by compact bone alone; cancellous bonesurrounds the lamina dura in apical, apicolingual, andinterradicular areas.260 FIG. 3.51 Relative proportions of cancellous bone andcompact bone in a longitudinal faciolingual section of(A) mandibular molars, (B) lateral incisors, (C) canines,(D) first premolars, (E) second premolars, (F) firstmolars, (G) second molars, and (H) third molars.261 FIG. 3.52 The shape of the roots and the surroundingbone distribution in a transverse section of maxilla andmandible at the midroot level.Bone consists of two-thirds inorganic matter and one-thirdorganic matrix. The inorganic matter is composed principally of theminerals calcium and phosphate, along with hydroxyl, carbonate,citrate, and trace amounts of other ions101,102 such as sodium,magnesium, and fluorine. The mineral salts are in the form ofhydroxyapatite crystals of ultramicroscopic size and constituteapproximately two-thirds of the bone structure.The organic matrix75 consists mainly of collagen type I (90%),185with small amounts of noncollagenous proteins such as osteocalcin,osteonectin, bone morphogenetic protein, phosphoproteins, andproteoglycans.209 Osteopontin and bone sialoprotein are cell-adhesion proteins that appear to be important for the adhesion ofboth osteoclasts and osteoblasts.163 In addition, paracrine factors,including cytokines, chemokines, and growth factors, have beenimplicated in the local control of mesenchymal condensations thatoccur at the onset of organogenesis. These factors probably play aprominent role in the development of the alveolar processes.251Although the alveolar bone tissue is constantly changing itsinternal organization, it retains approximately the same form fromchildhood through adult life. Bone deposition by osteoblasts isbalanced by resorption by osteoclasts during tissue remodeling andrenewal. It is well known that the number of osteoblasts decreaseswith aging; however, no remarkable change in the number ofosteoclasts has ever been reported.191Remodeling is the major pathway of bony changes in shape,resistance to forces, repair of wounds, and calcium and phosphatehomeostasis in the body. Indeed, the coupling of bone resorptionwith bone formation constitutes one of the fundamental principlesby which bone is necessarily remodeled throughout its life. Boneremodeling involves the coordination of activities of cells from twodistinct lineages, the osteoblasts and the osteoclasts, which formand resorb the mineralized connective tissues of bone.251The regulation of bone remodeling is a complex process thatinvolves hormones and local factors acting in an autocrine and aparacrine manner on the generation and activity of differentiated262 bone cells.251 Bone contains 99% of the body's calcium ions andtherefore is the major source for calcium release when the calciumblood levels decrease; this is monitored by the parathyroid gland. Adecrease in blood calcium is mediated by receptors on the chief cellsof the parathyroid glands, which then release parathyroid hormone.Parathyroid hormone stimulates osteoblasts to release interleukin-1and interleukin-6, which stimulate monocytes to migrate into thebone area. Leukemia-inhibiting factor, which is secreted byosteoblasts, coalesces monocytes into multinucleated osteoclasts,which then resorb bone, thereby releasing calcium ions fromhydroxyapatite into the blood. This release normalizes the bloodlevel of calcium. A feedback mechanism of normal blood levels ofcalcium turns off the secretion of parathyroid hormone. Meanwhile,osteoclasts have resorbed organic matrix along withhydroxyapatite. The breakdown of collagen from the organic matrixreleases various osteogenic substrates, which are covalently boundto collagen. This in turn stimulates the differentiation of osteoblasts,which ultimately deposit bone. This interdependency of osteoblastsand osteoclasts in remodeling is called coupling.The bone matrix that is laid down by osteoblasts isnonmineralized osteoid. While new osteoid is being deposited, theolder osteoid located below the surface becomes mineralized as themineralization front advances.Bone resorption is a complex process that is morphologicallyrelated to the appearance of eroded bone surfaces (i.e., Howshiplacunae) and large, multinucleated cells (osteoclasts) (Fig. 3.53).Osteoclasts originate from hematopoietic tissue55,110,197 and areformed by the fusion of mononuclear cells of asynchronouspopulations.141,201,264 When osteoclasts are active rather than resting,they possess an elaborately developed ruffled border from whichhydrolytic enzymes are thought to be secreted.278 These enzymesdigest the organic portion of bone. The activity of osteoclasts andthe morphology of the ruffled border can be modified andregulated by hormones such as parathyroid hormone (indirectly)and calcitonin, which has receptors on the osteoclast membrane.263 FIG. 3.53 Rat alveolar bone. This histologic view showtwo multinucleated osteoclasts in the Howship lacuna.Another mechanism of bone resorption involves the creation ofan acidic environment on the bone surface, thereby leading to thedissolution of the mineral component of bone. This event can beproduced by different conditions, including a proton pumpthrough the cell membrane of the osteoclast,34 bone tumors, andlocal pressure197 translated through the secretory activity of theosteoclast.Ten Cate264 described the sequence of events in the resorptiveprocess as follows:1. Attachment of osteoclasts to the mineralized surface of bone2. Creation of a sealed acidic environment through the actionof the proton pump, which demineralizes bone and exposesthe organic matrix3. Degradation of the exposed organic matrix to its constituentamino acids via the action of released enzymes (e.g., acidphosphatase, cathepsin)4. Sequestering of mineral ions and amino acids within theosteoclast264 Notably, the cellular and molecular events involved in boneremodeling have a strong similarity to many aspects ofinflammation and repair. The relationships among matrixmolecules (e.g., osteopontin, bone sialoprotein, SPARC [secretedprotein, acidic, rich in cysteine], osteocalcin), blood clotting, andwound healing are clearly evident.251Cells and Intercellular MatrixOsteoblasts, which are the cells that produce the organic matrix ofbone, are differentiated from pluripotent follicle cells. Alveolarbone is formed during fetal growth by intramembranousossification, and it consists of a calcified matrix with osteocytesenclosed within spaces called lacunae. The osteocytes extendprocesses into canaliculi that radiate from the lacunae. The canaliculiform an anastomosing system through the intercellular matrix ofthe bone, which brings oxygen and nutrients to the osteocytesthrough the blood and removes metabolic waste products. Bloodvessels branch extensively and travel through the periosteum. Theendosteum lies adjacent to the marrow vasculature. Bone growthoccurs via the apposition of an organic matrix that is deposited byosteoblasts. Haversian systems (i.e., osteons) are the internalmechanisms that bring a vascular supply to bones that are too thickto be supplied only by surface vessels. These are found primarily inthe outer cortical plates and the alveolar bone proper.Socket WallThe socket wall consists of dense, lamellated bone, some of which isarranged in haversian systems and bundle bone. Bundle bone is theterm given to bone adjacent to the periodontal ligament thatcontains a great number of Sharpey fibers286 (Fig. 3.54). It ischaracterized by thin lamellae arranged in layers parallel to theroot, with intervening appositional lines (Fig. 3.55). Bundle bone islocalized within the alveolar bone proper. Some Sharpey fibers arecompletely calcified, but most contain an uncalcified central corewithin a calcified outer layer.240 Bundle bone is not unique to thejaws; it occurs throughout the skeletal system wherever ligamentsand muscles are attached.265 FIG. 3.54 Deep penetration of Sharpey fibers intobundle bone of a rat molar.266 FIG. 3.55 Bundle bone associated with the physiologicmesial migration of the teeth. (A) Horizontal sectionthrough the molar roots during the process of mesialmigration (left, mesial; right, distal). (B) Mesial rootsurface showing osteoclasis of bone (arrows). (C)Distal root surface showing bundle bone that has beenpartially replaced with dense bone on the marrow side.PL, Periodontal ligament.The cancellous portion of the alveolar bone consists of trabeculaethat enclose irregularly shaped marrow spaces lined with a layer ofthin, flattened endosteal cells. Wide variation occurs in thetrabecular pattern of cancellous bone,200 which is affected byocclusal forces. The matrix of the cancellous trabeculae consists ofirregularly arranged lamellae separated by deeply stainingincremental and resorption lines indicative of previous boneactivity, with an occasional haversian system.Cancellous bone is found predominantly in the interradicularand interdental spaces and in limited amounts facially or lingually,except in the palate. In the adult human, more cancellous boneexists in the maxilla than in the mandible.Bone MarrowIn the embryo and the newborn, the cavities of all bones areoccupied by red hematopoietic marrow. The red marrow graduallyundergoes a physiologic change to the fatty or yellow inactive typeof marrow. In the adult, the marrow of the jaw is normally of thelatter type, and red marrow is found only in the ribs, sternum,vertebrae, skull, and humerus. However, foci of the red bonemarrow are occasionally seen in the jaws, often accompanied by theresorption of bony trabeculae.41 Common locations are themaxillary tuberosity, the maxillary and mandibular molar andpremolar areas, and the mandibular symphysis and ramus angle,which may be visible radiographically as zones of radiolucency.Periosteum and EndosteumLayers of differentiated osteogenic connective tissue cover all of thebone surfaces. The tissue that covers the outer surface of bone is267 termed periosteum, whereas the tissue that lines the internal bonecavities is called endosteum.The periosteum consists of an inner layer composed of osteoblastssurrounded by osteoprogenitor cells, which have the potential todifferentiate into osteoblasts, and an outer layer rich in blood vesselsand nerves and composed of collagen fibers and fibroblasts.Bundles of periosteal collagen fibers penetrate the bone, therebybinding the periosteum to the bone. The endosteum is composed ofa single layer of osteoblasts and sometimes a small amount ofconnective tissue. The inner layer is the osteogenic layer, and theouter layer is the fibrous layer.Cellular events at the periosteum modulate bone size throughoutan individual's life span, and a change in bone size is probably theresult of the balance between periosteal osteoblastic and osteoclasticactivities. Little is currently known about the control of periostealosteoblastic activity or the clinical importance of variations inperiosteal bone formation.196 Moreover, the nature and impact ofperiosteal bone resorption are virtually unexplored.Interdental SeptumThe interdental septum consists of cancellous bone that is borderedby the socket wall cribriform plates (i.e., lamina dura or alveolarbone proper) of approximating teeth and the facial and lingualcortical plates (Fig. 3.56). If the interdental space is narrow, theseptum may consist of only the cribriform plate. In one study, forexample, the space between the mandibular second premolars andfirst molars consisted of cribriform plate and cancellous bone in85% of the cases and of only cribriform plate in the remaining15%.116 If the roots are too close together, an irregular “window”can appear in the bone between adjacent roots (Fig. 3.57). Betweenmaxillary molars, the septum consisted of cribriform plate andcancellous bone in 66.6% of cases; it was composed of onlycribriform plate in 20.8%, and it had a fenestration in 12.5%.116268 FIG. 3.56 Interdental septa. (A) Radiograph of themandibular incisor area. Note the prominent laminadura. (B) Interdental septa between the mandibularanterior teeth shown in A. There is a slight reduction inbone height with widening of the periodontal ligamentin the coronal areas. The central cancellous portion isbordered by the dense bony cribriform plates of thesocket, which form the lamina dura around the teeth inthe radiograph. Attachments for the mentalis muscleare seen between the canine and lateral incisors. (FromGlickman I, Smulow J: Periodontal disease: clinical, radiographic, andhistopathologic features, Philadelphia, 1974, Saunders.)269 FIG. 3.57 Boneless “window” between adjoining closeroots of molars.Determining root proximity radiographically is important (seeChapters 33 and 35). The mesiodistal angulation of the crest of theinterdental septum usually parallels a line drawn between thecementoenamel junctions of the approximating teeth.209 Thedistance between the crest of the alveolar bone and thecementoenamel junction in young adults varies between 0.75 and1.49 mm (average, 1.08 mm). This distance increases with age to anaverage of 2.81 mm.93 However, this phenomenon may not be asmuch a function of age as of periodontal disease.The mesiodistal and faciolingual dimensions and shape of theinterdental septum are governed by the size and convexity of thecrowns of the two approximating teeth as well as by the position ofthe teeth in the jaw and their degree of eruption.209Osseous TopographyThe bone contour normally conforms to the prominence of theroots, with intervening vertical depressions that taper toward themargin (Fig. 3.58). Alveolar bone anatomy varies among patientsand has important clinical implications. The height and thickness ofthe facial and lingual bony plates are affected by the alignment ofthe teeth, the angulation of the root to the bone, and occlusal forces.FIG. 3.58 Normal that the bone contour conforms tothe prominence of the roots.270 On teeth in labial version, the margin of the labial bone is locatedfarther apically than it is on teeth that are in proper alignment. Thebone margin is thinned to a knife edge, and it presents anaccentuated arc in the direction of the apex. On teeth in lingualversion, the facial bony plate is thicker than normal. The margin isblunt, rounded, and horizontal rather than arcuate. The effect of theroot-to-bone angulation on the height of alveolar bone is mostnoticeable on the palatal roots of the maxillary molars. The bonemargin is located farther apically on the roots, and it formsrelatively acute angles with the palatal bone.120 The cervical portionof the alveolar plate is sometimes considerably thickened on thefacial surface, apparently as reinforcement against occlusal forces(Fig. 3.59).FIG. 3.59 Variations in the cervical portion of thebuccal alveolar plate. (A) Shelflike conformation. (B)Comparatively thin buccal plate.Fenestration and DehiscenceIsolated areas in which the root is denuded of bone and the rootsurface is covered only by periosteum and overlying gingiva aretermed fenestrations. In these areas, the marginal bone is intact.When the denuded areas extend through the marginal bone, thedefect is called a dehiscence (Fig. 3.60).271 FIG. 3.60 Dehiscence on the canine and fenestrationof the first premolar.Such defects occur on approximately 20% of the teeth; they occurmore often on the facial bone than on the lingual bone, they aremore common on anterior teeth than on posterior teeth, and theyare frequently bilateral. Microscopic evidence of lacunar resorptionmay be present at the margins. The cause of these defects is notclear. Prominent root contours, malposition, and labial protrusionof the root in combination with a thin bony plate are predisposingfactors.78 Fenestration and dehiscence are important because theymay complicate the outcome of periodontal surgery.Remodeling of Alveolar BoneIn contrast with its apparent rigidity, alveolar bone is the leaststable of the periodontal tissues, because its structure is in aconstant state of flux. A considerable amount of internalremodeling takes place by means of resorption and formation, andthis is regulated by local and systemic influences. Local influencesinclude functional requirements on the tooth and age-relatedchanges in bone cells. Systemic influences are probably hormonal(e.g., parathyroid hormone, calcitonin, vitamin D3).The remodeling of the alveolar bone affects its height, contour,and density and is manifested in the following three areas: adjacent272 to the periodontal ligament, in relation to the periosteum of thefacial and lingual plates, and along the endosteal surface of themarrow spaces.Development of the AttachmentApparatusAfter the crown has formed, the stratum intermedium and thestellate reticulum of the enamel organ disappear. The outer andinner epithelia of the enamel organ remain and form REE. Theapical portion of this constitutes the Hertwig epithelial root sheath,which will continue to grow apically and which determines theshape of the root. Before the beginning of root formation, the rootsheath bends horizontally at the future cementoenamel junction,thereby narrowing the cervical opening and forming the epithelialdiaphragm. The epithelial diaphragm separates the dental folliclefrom the dental papilla.After root dentin formation begins, the Hertwig root sheathbreaks up and partially disappears; the remaining cells form theepithelial clusters or strands known as the epithelial rests of Malassez(see Fig. 3.37A). In multirooted teeth, the epithelial diaphragmgrows in such a way that tonguelike extensions develophorizontally, thereby leaving spaces for each of the future roots toform.The role of the Hertwig epithelial root sheath in rootdevelopment, especially as it relates to the initiation ofcementogenesis, has become a focus of research.271 On the basis ofvarious studies, it is now generally accepted that there is a transientperiod of the secretion of proteins (e.g., bone sialoprotein,osteopontin, amelin) by the cells of the Hertwig epithelial rootsheath.38,85 In addition, research shows that growth anddifferentiation factors may play roles in the development of theattachment apparatus of periodontal tissues. Pluripotent dentalfollicle cells have been shown to differentiate into osteoblasts,cementoblasts, and periodontal fibroblasts.241Cementum273 The rupture of the Hertwig root sheath allows the mesenchymalcells of the dental follicle to contact the dentin, where they startforming a continuous layer of cementoblasts. On the basis ofimmunochemical and ultrastructural studies, Thomas270 andothers35,165 have speculated that cementoblasts can be of epithelialorigin (i.e., the Hertwig root sheath), having undergone anepithelial mesenchymal transformation.Cementum formation begins with the deposition of a meshworkof irregularly arranged collagen fibrils sparsely distributed in aground substance or matrix called precementum or cementoid. This isfollowed by a phase of matrix maturation, which subsequentlymineralizes to form cementum. Cementoblasts, which are initiallyseparated from the cementum by uncalcified cementoid, sometimesbecome enclosed within the matrix and are trapped. After they areenclosed, they are referred to as cementocytes, and they will remainviable in a manner similar to that of osteocytes.A layer of connective tissue known as the dental sac surrounds theenamel organ and includes the epithelial root sheath as it develops.The zone that is immediately in contact with the dental organ andcontinuous with the ectomesenchyme of the dental papilla is calledthe dental follicle,262,263,266 and it consists of undifferentiatedfibroblasts.Periodontal LigamentAs the crown approaches the oral mucosa during tooth eruption,these fibroblasts become active and start producing collagen fibrils.They initially lack orientation, but they soon acquire an orientationthat is oblique to the tooth. The first collagen bundles then appearin the region immediately apical to the cementoenamel junction andgive rise to the gingivodental fiber groups. As tooth eruptionprogresses, additional oblique fibers appear and become attached tothe newly formed cementum and bone. The transseptal andalveolar crest fibers develop when the tooth merges into the oralcavity. Alveolar bone deposition occurs simultaneously withperiodontal ligament organization.250Studies of the squirrel monkey have shown that, during eruption,cemental Sharpey fibers appear first, followed by Sharpey fibers274 emerging from the bone.107 Sharpey fibers are fewer in number andmore widely spaced than those that emerge from the cementum. Ata later stage, alveolar fibers extend into the middle zone to join thelengthening cemental fibers and to attain their classic orientation,thickness, and strength when occlusal function is established.Early investigators suggested that the individual fibers, ratherthan being continuous, consisted of two separate parts splicedtogether midway between the cementum and the bone in a zonecalled the intermediate plexus. The plexus has been reported in theperiodontal ligament of continuously growing incisors but not inthe posterior teeth of rodents119,177,300 or in actively erupting humanand monkey teeth107 and not after teeth reach occlusal contact. Therearrangement of the fiber ends in the plexus is supposed toaccommodate tooth eruption without necessitating the embeddingof new fibers into the tooth and the bone.177 The existence of such aplexus, however, has not been confirmed by radioautographic dataand other studies, and it is considered a microscopic artifact.232The developing periodontal ligament and the mature periodontalligament contain undifferentiated stem cells that retain the potentialto differentiate into osteoblasts, cementoblasts, and fibroblasts.172Alveolar BoneJust before mineralization, osteoblasts start producing matrixvesicles. These vesicles contain enzymes (e.g., alkaline phosphatase)that help to jump-start the nucleation of hydroxyapatite crystals. Asthese crystals grow and develop, they form coalescing bonenodules, which, with fast-growing nonoriented collagen fibers, arethe substructure of woven bone and the first bone formed in thealveolus. Later, through bone deposition, remodeling, and thesecretion of oriented collagen fibers in sheets, mature lamellar boneis formed.28,29The hydroxyapatite crystals are generally aligned with their longaxes parallel to the collagen fibers, and they appear to be depositedon and within the collagen fibers in mature lamellar bone. In thisway, bone matrix is able to withstand the heavy mechanical stressesapplied to it during function.The alveolar bone develops around each tooth follicle during275 odontogenesis. When a deciduous tooth is shed, its alveolar bone isresorbed. The succedaneous permanent tooth moves into place anddevelops its own alveolar bone from its own dental follicle. As thetooth root forms and the surrounding tissues develop and mature,alveolar bone merges with the separately developing basal bone,and the two become one continuous structure. Although alveolarbone and basal bone have different intermediate origins, both areultimately derived from neural crest ectomesenchyme.Mandibular basal bone begins mineralization at the exit of themental nerve from the mental foramen, whereas the maxillary basalbone begins at the exit of the infraorbital nerve from the infraorbitalforamen.Physiologic Migration of the TeethTooth movement does not end when active eruption is completedand the tooth is in functional occlusion. With time and wear, theproximal contact areas of the teeth are flattened, and the teeth tendto move mesially. This is referred to as physiologic mesial migration.By the age of 40 years, this process results in a reduction of about0.5 cm in the length of the dental arch from the midline to the thirdmolars. Alveolar bone is reconstructed in compliance with thephysiologic mesial migration of the teeth. Bone resorption isincreased in areas of pressure along the mesial surfaces of the teeth,and new layers of bundle bone are formed in areas of tension on thedistal surfaces (see Fig. 3.55).External Forces and the PeriodontiumThe periodontium exists for the purpose of supporting teeth duringfunction, and it depends on the stimulation that it receives fromfunction for the preservation of its structure. Therefore a constantand sensitive balance is present between external forces and theperiodontal structures.Alveolar bone undergoes constant physiologic remodeling inresponse to external forces, particularly occlusal forces. Bone isremoved from areas where it is no longer needed and added toareas where it is presently needed.276 The socket wall reflects the responsiveness of alveolar bone toexternal forces. Osteoblasts and newly formed osteoid line thesocket in areas of tension; osteoclasts and bone resorption occur inareas of pressure. Forces exerted on the tooth also influence thenumber, density, and alignment of cancellous trabeculae. The bonytrabeculae are aligned in the path of the tensile and compressivestresses to provide maximal resistance to the occlusal force with aminimum of bone substance100,247 (Fig. 3.61). When forces areincreased, the cancellous bony trabeculae increase in number andthickness, and bone may be added to the external surface of thelabial and lingual plates.FIG. 3.61 Bony trabeculae realigned perpendicular tothe mesial root of a tilted molar.A study has shown that the presence of antagonists of occlusalforce and the severity of periodontal disease increase the extensionof periodontal tissue resorption.66The periodontal ligament also depends on the stimulationprovided by function to preserve its structure. Within physiologiclimits, the periodontal ligament can accommodate increasedfunction with an increase in width (Table 3.2), a thickening of itsfiber bundles, and an increase in the diameter and number ofSharpey fibers. Forces that exceed the adaptive capacity of theperiodontium produce injury called trauma from occlusion. Because277 trauma from occlusion can only be confirmed histologically, theclinician is challenged to use clinical and radiographic surrogateindicators in an attempt to facilitate and assist with its diagnosis111(see Chapter 26).TABLE 3.2Comparison of Periodontal Width of Functioning and FunctionlessTeeth in a 38-Year-Old ManAVERAGE WIDTH OF PERIODONTAL SPACEEntrance of Alveolus(mm)Middle of Alveolus(mm)Fundus of Alveolus(mm)Heavy Function 0.35 0.28 0.30Left upper secondbicuspidLight Function 0.14 0.10 0.12Left lower firstbicuspidFunctionless 0.10 0.06 0.06Left upper thirdmolarModified from Kronfeld R: Histologic study of the influence of function on the humanperiodontal membrane. J Am Dent Assoc 18:1242, 1931.When occlusal forces are reduced, the number and thickness ofthe trabeculae are reduced.64 The periodontal ligament alsoatrophies and appears thinned; the fibers are reduced in numberand density, disoriented,11,208 and ultimately arranged parallel to theroot surface (Fig. 3.62). This phenomenon is termed disuse atrophy orafunctional atrophy. With this condition, the cementum is eitherunaffected64 or thickened, and the distance from the cementoenameljunction to the alveolar crest is increased.204278 FIG. 3.62 Atrophic periodontal ligament (P) of a toothdevoid of function. Note the scalloped edge of thealveolar bone (B), which indicates that resorption hasoccurred. C, Cementum.Decreased occlusal function causes changes in the periodontalmicrovasculature, such as the occlusion of blood vessels and adecrease in the number of blood vessels.121 For example, Murrelland colleagues187 reported that the application and removal oforthodontic force produced significant changes in blood vesselnumber and density; however, no evidence-based explanationexists for why the force stimulated such changes in the number ofblood vessels.Orthodontic tooth movement is thought to result from site-specific bone remodeling in the absence of inflammation. It is wellrecognized that tensional forces will stimulate the formation andactivity of osteoblastic cells, whereas compressive forces promoteosteoclastic activity.251Vascularization of the SupportingStructuresThe blood supply to the supporting structures of the tooth is279 derived from the inferior and superior alveolar arteries to themandible and maxilla, and it reaches the periodontal ligament fromthree sources: apical vessels, penetrating vessels from the alveolarbone, and anastomosing vessels from the gingiva.63The branches of the apical vessels supply the apical region of theperiodontal ligament before the vessels enter the dental pulp. Thetransalveolar vessels are branches of the intraseptal vessels thatperforate the lamina dura and enter the ligament. The intraseptalvessels continue to vascularize the gingiva; these gingival vessels inturn anastomose with the periodontal ligament vessels of thecervical region.84The vessels within the periodontal ligament are contained in theinterstitial spaces of loose connective tissue between the principalfibers, and they are connected in a netlike plexus that runslongitudinally and closer to the bone than the cementum54 (Figs.3.63 and 3.64). The blood supply increases from the incisors to themolars; it is greatest in the gingival third of single-rooted teeth, lessin the apical third, and least in the middle; it is equal in the apicaland middle thirds of multirooted teeth; it is slightly greater on themesial and distal surfaces than on the facial and lingual surfaces;and it is greater on the mesial surfaces of the mandibular molarsthan on the distal surfaces.33280 FIG. 3.63 Vascular supply of a monkey periodontiumperfused with India ink. Note the longitudinal vessels inthe periodontal ligament and the alveolar arteriespassing through channels between the bone marrow(M) and the periodontal ligament. D, Dentin. (Courtesy Dr.Sol Bernick, Los Angeles, California.)281 FIG. 3.64 Vascular supply to the periodontal ligamentin a rat molar as viewed by scanning electronmicroscopy after perfusion with plastic and tissuecorrosion. Middle and apical areas of the periodontalligament are shown with longitudinal blood vesselsfrom the apex (below) to the gingiva (above),perforating vessels entering the bone (b), and manytransverse connections (arrowheads). Apical vessels(a) form a cap that connects with the pulpal vessels.(Courtesy NJ Selliseth and K Selvig, University of Bergen, Norway.)The vascular supply to the bone enters the interdental septathrough nutrient canals together with veins, nerves, andlymphatics. Dental arterioles, which also branch off the alveolararteries, send tributaries through the periodontal ligament, andsome small branches enter the marrow spaces of the bone throughthe perforations in the cribriform plate. Small vessels that emanatefrom the facial and lingual compact bone also enter the marrow andspongy bone.The venous drainage of the periodontal ligament accompanies thearterial supply. Venules receive the blood through the abundantcapillary network. In addition, arteriovenous anastomoses bypassthe capillaries and are seen more frequently in apical andinterradicular regions; their significance is unknown.Lymphatics supplement the venous drainage system. 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