C H A P T E R 3
and Function of the
Joseph P. Fiorellini, David Kim, Yu-Cheng Chang
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:
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
This chapter first discusses the structural components of the
normal periodontium; it then describes their development,
vascularization, innervation, and functions.
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
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.
words, the specific structure of different types of gingiva reflects
each one's effectiveness as a barrier to the penetration by microbes
and noxious agents into the deeper tissue.
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).
In about 50% of cases, it is demarcated from the
adjacent attached gingiva by a shallow linear depression called the
free gingival groove.
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.
FIG. 3.1 Normal gingiva in a young adult. Note the
demarcation (mucogingival line) (arrows) between the
attached gingiva and the darker alveolar mucosa.
FIG. 3.2 Diagram showing the anatomic landmarks of
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
These strict conditions of normalcy can be produced
experimentally only in germ-free animals or after intense and
prolonged plaque control.
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
; other studies have reported 1.5 mm
and 0.69 mm.
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
probe diameter, probing force, and level of inflammation.
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
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
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.
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
FIG. 3.3 Mean width of the attached gingiva in the
human permanent dentition.
Because the mucogingival junction remains stationary
throughout adult life,
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.
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.
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
(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,
and the presence
or absence of some degree of recession. Fig. 3.6 depicts the
variations in normal interdental gingiva.
FIG. 3.4 Site of extraction showing the facial and
palatal interdental papillae and the intervening col
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
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
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
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.
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
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
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.
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).
Functions and Features of Gingival
Mechanical, chemical, water, and microbial barrier
Major Cell Type
Other Cell Types
Replacement of damaged cells
Synthesis of basal lamina components
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
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
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
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
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
considered to be at intermediate stages of keratinization. These
areas can progress to maturity or dedifferentiate under different
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,
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,
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.
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
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.
Electron microscopy reveals that keratinocytes are interconnected
by structures on the cell periphery called desmosomes.
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
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.
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
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
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.
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.
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
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
FIG. 3.11 Pigmented gingiva of dog showing
melanocytes (M) in the basal epithelial layer and
melanophores (C) in the connective tissue (Glucksman
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
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.
FIG. 3.12 Human gingival epithelium, oral aspect.
Immunoperoxidase technique showing Langerhans
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.
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.
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
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 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
3.13). The basal lamina is permeable to fluids, but it acts as a barrier
to particulate matter.
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.
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.
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.
The degree of gingival keratinization diminishes with age and the
onset of menopause,
but it is not necessarily related to the
different phases of the menstrual cycle.
Keratinization of the oral
mucosa varies in different areas in the following order: palate (most
keratinized), gingiva, ventral aspect of the tongue, and cheek (least
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.
In keeping with the complete or almost-complete maturation,
histoenzyme reactions for acid phosphatase and pentose-shunt
enzymes are very strong.
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
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.
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).
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).
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.
FIG. 3.15 Scanning electron microscopic view of the
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.)
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.
phosphatase staining is negative,
although lysosomes have been
described in exfoliated cells.
Despite these morphologic and chemical characteristics, the
sulcular epithelium has the potential to keratinize if it is reflected
and exposed to the oral cavity
or if the bacterial flora of the
sulcus is totally eliminated.
Conversely, the outer epithelium loses
its keratinization when it is placed in contact with the tooth.
findings suggest that the local irritation of the sulcus prevents
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.
Unlike the junctional
epithelium, however, the sulcular epithelium is not heavily
infiltrated by polymorphonuclear neutrophil leukocytes, and it
appears to be less permeable.
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
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.
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
routinely in the junctional epithelium of both conventional rats and
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
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.
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
Similar to sulcular epithelium, junctional epithelium exhibits
lower glycolytic enzyme activity than outer epithelium, and it also
lacks acid phosphatase activity.
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.
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
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
Organic strands from the enamel appear to extend
into the lamina densa.
The junctional epithelium attaches to
afibrillar cementum that is present on the crown (usually restricted
to an area within 1 mm of the cementoenamel junction)
cementum in a similar manner.
Histochemical evidence for the presence of neutral
polysaccharides in the zone of the epithelial attachment has been
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.
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.
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.
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.
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.
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
into a junctional epithelium proceeds in an apical direction without
interrupting the attachment to the tooth. According to Schroeder
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.
regenerating epithelial cells move toward the tooth surface and
along it in a coronal direction to the gingival sulcus, where they are
(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
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.
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
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.
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.
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.
The rapid shedding of
cells effectively removes bacteria that adhere to the epithelial cells
and therefore is an important part of the antimicrobial defense
mechanisms at the dentogingival junction.
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.
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
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,
and it may be an accumulation of tissue
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
diagnostic or prognostic biomarker of the biologic state of the
periodontium in health and disease
(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).
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
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.
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
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.
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
Fibronectin binds fibroblasts to the fibers and many
other components of the intercellular matrix, thereby helping to
mediate cell adhesion and migration. Laminin, which is another
glycoprotein found in the basal lamina, serves to attach it to
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.
The elastic fiber system is composed of oxytalan, elaunin, and
elastin fibers distributed among collagen fibers.
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.
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
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
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.
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
(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.)
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
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
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
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.
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
Fibroblast heterogeneity is now a well-established feature of
fibroblasts in the periodontium.
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.
Mast cells, which are distributed throughout the body, are
numerous in the connective tissue of the oral mucosa and the
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.
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,
but they are practically
constant in healthy, normal gingiva, even before complete tooth
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)
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.
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
architecture of the tissues.
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.
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.
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.
The periodic acid–Schiff reaction also
outlines vascular walls by revealing a positive line in the basal
Endothelial cells express 5-nucleotidase activity as
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.
In addition, laser
Doppler flow measurement provides a noninvasive means for the
observation of blood flow modifications related to disease.
Three sources of blood supply to the gingiva are as follows (Figs.
3.22 and 3.23):
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
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
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
: 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
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
(Fig. 3.24; also see Fig.
3.23). The loops are sometimes linked by cross-communications,
and flattened capillaries serve as reserve vessels when the
circulation is increased in response to irritation.
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,
anastomosing plexus that extends parallel to the enamel from the
base of the sulcus to the gingival margin.
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
By contrast, the inflamed gingival vasculature
exhibits an irregular vascular plexus pattern, with the microvessels
exhibiting a looped, dilated, and convoluted appearance.
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
The lymphatic drainage of the gingiva
brings in the lymphatics of the connective tissue papillae.
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
Gingival innervation is derived from fibers that arise from
nerves in the periodontal ligament and from the labial, buccal, and
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.
Correlation of Clinical and Microscopic
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.
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
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
Physiologic Pigmentation (Melanin)
Melanin is a non–hemoglobin-derived brown pigment with the
• 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
clinically), but it is absent or severely diminished
• 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.
According to Dummett,
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.
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.
Information about the
repigmentation of oral tissues after surgical procedures is extremely
limited, and no definitive treatment is offered at this time.
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.
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
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.
FIG. 3.27 A thickened, shelflike contour of gingiva on a
tooth in lingual version aggravated by local irritation
caused by plaque accumulation.
The shape of the interdental gingiva is governed by the contour of
the proximal tooth surfaces and the location and shape of the
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
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
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.
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.
Stippling is less
prominent on lingual than facial surfaces and may be absent in
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
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.
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
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.
suggests a connective-tissue–based genetic determination of the
type of epithelial surface.
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,
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.
Gottlieb and Orban
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
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
Stage 1: The teeth reach the line of occlusion. The junctional
epithelium and the base of the gingival sulcus are on the
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).
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).
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.
It is continuous
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.
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
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.
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.
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,
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,
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.
There are at least 19 recognized
collagen species encoded by at least 25 separate genes dispersed
among 12 chromosomes.
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.
FIG. 3.33 Collagen microfibrils, fibrils, fibers, and
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.
The principal fibers are composed
mainly of collagen type I,
whereas reticular fibers are composed
of collagen type III. Collagen type IV is found in the basal
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.
Type VI collagen has also been
immunolocalized in the periodontal ligament and the gingiva.
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.
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).
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
FIG. 3.35 Transseptal fibers (F) at the crest of the
Alveolar crest fibers extend obliquely from the cementum just
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
resist lateral tooth movements. The incision of these fibers during
periodontal surgery does not increase tooth mobility unless
significant attachment loss has occurred.
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.
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
run parallel to the root surface in a
vertical direction and bend to attach to the cementum
cervical third of the root. They are thought to regulate vascular
An elastic meshwork has been described in the periodontal
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
The principal fibers are remodeled by the periodontal ligament
cells to adapt to physiologic needs
and in response to different
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.
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.
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-
These cells synthesize collagen and possess the
capacity to phagocytose “old” collagen fibers and degrade them
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.
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,
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
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.
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
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
and the cervical area.
They diminish in
number with age
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.
Although their functional properties are still considered to be
the epithelial rests are reported to contain keratinocyte
growth factors, and they have been shown to be positive for
tyrosine kinase A neurotrophin receptor.
epithelial rests proliferate when stimulated,
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.
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.,
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
For example, fibromodulin (a small proteoglycan rich
in keratan sulfate and leucine) has been identified in bovine
The most comprehensive study of the
proteoglycans in periodontal ligament was performed with the use
of fibroblast cultures of human ligament.
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
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
Functions of Periodontal Ligament
The functions of the periodontal ligament are categorized as
physical, formative and remodeling, nutritional, and sensory.
The physical functions of the periodontal ligament entail the
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
Resistance to Impact of Occlusal Forces (Shock
Two theories pertaining to the mechanism of tooth support have
been considered: the tensional theory and the viscoelastic system
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.
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).
FIG. 3.39 Foramina perforating the lamina dura of a
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.
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.
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.
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
and the coronal half of the clinical root have been
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
(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.
Thickness of the Periodontal Ligaments of 172 Teeth From 15
Average of Alveolar
0.23 0.17 0.24 0.21
83 teeth from 4
0.20 0.14 0.19 0.18
36 teeth from 5
0.17 0.12 0.16 0.15
35 teeth from 5
Age 24 years (1
0.16 0.09 0.15 0.13
18 teeth from 1
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
Periodontal ligament and alveolar bone cells are exposed to
physical forces in response to mastication, parafunction, speech,
and orthodontic tooth movement.
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
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
Cartilage formation in the periodontal ligament, although
unusual, may represent a metaplastic phenomenon in the repair of
this ligament after injury.
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
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.
A rapid turnover of sulfated
glycosaminoglycans in the cells and amorphous ground substance
of the periodontal ligament also occurs.
It should be noted that
most of these studies have been performed in rodents and that
information about primates and humans is scarce.
Nutritional and Sensory Functions
The periodontal ligament supplies nutrients to the cementum, bone,
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
This relatively high blood vessel content may
provide hydrodynamic damping to applied forces as well as high
perfusion rates to the periodontal ligament.
The periodontal ligament is abundantly supplied with sensory
nerve fibers that are capable of transmitting tactile, pressure, and
pain sensations via the trigeminal pathways.
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.
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.
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
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)
Both consist of a calcified interfibrillar matrix and
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
and which are formed by the
fibroblasts, and fibers that belong to the cementum matrix
(intrinsic), which are produced by the cementoblasts.
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
In addition, immunohistochemical studies have
shown that the distribution of proteoglycans is closely associated
with the cementoblasts and the cementocytes.
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.
III collagen appears to coat the type I collagen of the Sharpey
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
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.
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
cementum tend to be more calcified than the interior regions,
according to evidence obtained by scanning electron microscopy.
Acellular cementum also contains intrinsic collagen fibrils that are
calcified and irregularly arranged or parallel to the surface.
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.
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
they may have a central, uncalcified core surrounded by a calcified
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,
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.
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.
On the basis of these findings, Schroeder
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
• 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
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%).
Opinions differ with regard
to whether the microhardness increases
or decreases with age,
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
Studies of cementum have identified adhesion proteins with
arginyl–glycyl–aspartic acid sequences: bone sialoprotein,
osteopontin, and osteonectin.
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
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.
Ikezawa and colleagues
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.
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.
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.
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.
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.
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.
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
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).
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.
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.
Radiographically, the radiolucent shadow of the periodontal
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.
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
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.
systemic disturbances that may lead to or may be associated with
hypercementosis include acromegaly, arthritis, calcinosis,
rheumatic fever, and thyroid goiter.
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.
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%).
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.
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
(Fig. 3.45); orthodontic movement
; pressure from
malaligned erupting teeth, cysts, and tumors
; teeth without
functional antagonists; embedded teeth; replanted and transplanted
; periapical disease; and periodontal disease. Systemic
conditions that are cited as predisposing an individual to or
inducing cemental resorption include calcium deficiency,
hereditary fibrous osteodystrophy,
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
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.
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.)
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,
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
In other words, a variety of macromolecules
present in the extracellular matrix of the periodontium are likely to
play a regulatory role in cementogenesis.
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
regeneration under specific conditions.
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
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,
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
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
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.
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
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
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
Exposure of Cementum to the Oral
Cementum becomes exposed to the oral environment in cases of
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
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
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.
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).
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 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,
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
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.
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
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
consists mainly of collagen type I (90%),
with small amounts of noncollagenous proteins such as osteocalcin,
osteonectin, bone morphogenetic protein, phosphoproteins, and
Osteopontin and bone sialoprotein are cell-
adhesion proteins that appear to be important for the adhesion of
both osteoclasts and osteoblasts.
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.
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.
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.
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
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
formed by the fusion of mononuclear cells of asynchronous
When osteoclasts are active rather than resting,
they possess an elaborately developed ruffled border from which
hydrolytic enzymes are thought to be secreted.
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.
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,
bone tumors, and
translated through the secretory activity of the
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
4. Sequestering of mineral ions and amino acids within the
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.
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.
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
(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.
Bundle bone is not unique to the
jaws; it occurs throughout the skeletal system wherever ligaments
and muscles are attached.
FIG. 3.54 Deep penetration of Sharpey fibers into
bundle bone of a rat molar.
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,
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.
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.
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
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.
Moreover, the nature and impact of
periosteal bone resorption are virtually unexplored.
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
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%.
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.)
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.
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.
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.
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.
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.
The cervical portion
of the alveolar plate is sometimes considerably thickened on the
facial surface, apparently as reinforcement against occlusal forces
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).
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
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
The remodeling of the alveolar bone affects its height, contour,
and density and is manifested in the following three areas: adjacent
to the periodontal ligament, in relation to the periosteum of the
facial and lingual plates, and along the endosteal surface of the
Development of the Attachment
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
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.
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
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.
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
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,
and it consists of undifferentiated
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.
Studies of the squirrel monkey have shown that, during eruption,
cemental Sharpey fibers appear first, followed by Sharpey fibers
emerging from the bone.
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
or in actively erupting human
and monkey teeth
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.
The existence of such a
plexus, however, has not been confirmed by radioautographic data
and other studies, and it is considered a microscopic artifact.
The developing periodontal ligament and the mature periodontal
ligament contain undifferentiated stem cells that retain the potential
to differentiate into osteoblasts, cementoblasts, and fibroblasts.
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
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
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
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
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.
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
(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.
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
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
(see Chapter 26).
Comparison of Periodontal Width of Functioning and Functionless
Teeth in a 38-Year-Old Man
AVERAGE WIDTH OF PERIODONTAL SPACE
Entrance of Alveolus
Middle of Alveolus
Fundus of Alveolus
Heavy Function 0.35 0.28 0.30
Left upper second
Light Function 0.14 0.10 0.12
Left lower first
Functionless 0.10 0.06 0.06
Left upper third
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.
The periodontal ligament also
atrophies and appears thinned; the fibers are reduced in number
and density, disoriented,
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
or thickened, and the distance from the cementoenamel
junction to the alveolar crest is increased.
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.
For example, Murrell
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
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
Vascularization of the Supporting
The blood supply to the supporting structures of the tooth is
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.
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
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
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.
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.)
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
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.
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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