Periodontology 2000, Vol.

13, 1997, 76-90 Copyright 0 M u n k s g a a r d 1997

Printed in Denmark . All rights reserved PERIODONTOLOGY 2000
ISSN 0906-6713

Alveolar bone and the

alveolar process:
the socket that is never stable
JEAN-LOUIS SAFFAR, & MARCCHERRUAU
JEAN- JACQUES LASFARGUES

Evolution has complicated the relationship between occlusion between antagonistic teeth. It is a complex
teeth and jaws. In mammals a complex tissue, the motion including vertical and horizontal compon-
periodontal ligament, joins the two organs. This has ents that results in an oblique movement, often
led to the differentiation of specialized structures at complicated by oral tilt of the teeth. The vertical
the periodontal ligament interfaces with the root component consists of an eruption, and the direc-
(the cementum) and the jaw (the alveolar wall or al- tion of the horizontal component varies: teeth mi-
veolar bone proper) in which the fiber bundles of the grate mesially in humans and primates but bucco-
periodontal ligament are anchored. Once inserted, distally in rodents. Sicher & Weimann (57) suggested
these fibers are called Sharpey’s fibers. that the continuous growth of rat jaws and their pos-
The alveolar wall is surrounded by the supporting teriorly oriented lengthening is responsible for distal
bone with which it forms an anatomical unit. The movement. If so, the movement may be regarded as
supporting bone includes the buccal and oral cor- one of the adaptive mechanisms maintaining the
tical plates and the septa. The cortical plates are in interrelationships of the various components of the
continuity with the cortices of the body of the jaws. masticatory apparatus during growth. In humans,
Cancellous bone is interposed between the alveolar the anteriorly oriented lengthening of the jaws may
wall and the cortical plates. In some locations, the induce mesial migration. With anthropological
amount of cancellous bone is minimal, and some- studies having shown that some facial growth per-
times there is none (Fig. la). The alveolar wall and sists throughout life (9, 141, the mesial migration
the cortical plates merge at the alveolar bone crest. may compensate for this growth. The dependence of
The buccal and oral plates are united by the inter- tooth migration on growth is suggested by the rather
dental and interradicular septa which are formed by rapid decrease in the rate of tooth migration with
cancellous bone. The interdental septa are covered age in the rat (Table l), while growth declines. On
by compact cortical bone (Fig. lb). the other hand, the intensity of occlusal wear is
After the eruption period, the relationship be-
tween the teeth and their supporting structures re-
mains dynamic, as the former migrate spon-
taneously within the alveolar process. This implies Table 1. Variation in the rate of molar migration
adaptation mechanisms preserving the anchorage to with age in rats. These values were obtained after
bone and the integrity of the periodontal ligament, injections of fluorescent dyes. The calculations
which is a source of progenitor cells renewing the were based on the distance and time intervals be-
tween the labeling
tissues (24, 3 3 ) .
1 Aee (weeks1
- - -
Migration rate
(urnldavl
__ _ _
Reference
__
7 7.1 30
Biomechanical considerations 8 6.7 64
10 5.5 27
12 3.9 27
Migration starts as soon as the functional period of 3.5 27
the teeth begins, that is, after the establishment of
__ ~ __

76
 Alveolar bone and alveolar process

Fig. 1. Human mandible. A. Bucco-oral section through alveolar bone cortices are in continuity with the external
a first bicuspid. The alveolar plates are so thin that no envelope of the body of the jaw. B. Bucco-oral section
cancellous bone is interposed between the cortices and through an interdental septum. The bone crest is cortical
the alveolar wall. Cancellous bone is only present in the in nature. The medullary spaces are wide with a progress-
apical third of the root where the medullary spaces are ive enlargement towards the basal bone.
small compared with those present in the basal bone. The

maximal during their first 100 days of life, that is, studies, as the dental arches progressively shorten as
when the movement is at its maximum, and slows a consequence of proximal wear. A reduction of
down thereafter (28). As crown wear proceeds about 1 cm per arch before third-molar eruption was
throughout life (13, 56) provoking a crown height re- reported in Australian aborigines (8). Lysell (32)
duction of about 40-50% in older animals, teeth found in medieval skulls an average shortening of 5-
probably continue to migrate, even if at a slower 6 mm; in contrast, in modern Swedish adults the rate
pace. However, McCulloch & Melcher (35) observed of proximal wear was far less extensive: about 1 mm
no sign of alveolar wall activity in 6-month-old mice, per arch in a 9-year period (29). These data suggest
which was interpreted as an arrest of migration with that the intensity of tooth movement in humans may
increasing age. Similar data are not available in other depend on the degree of tooth wear and ultimately
animal species. Nevertheless, information on on the type of diet.
humans can be inferred from anthropological As crown wear appears to be a primary determi-

77
Saffar et al.

nant of tooth migration, the latter can be regarded

as an adaptation to maintain tooth contact. This is
evident in populations with pronounced tooth at-
trition (that is, wearing away of both occlusal and
proximal surfaces), without loss of tooth contact (8,
14).
Studies designed to characterize the mechanical
factors governing tooth movement in the horizontal
direction have found that the contraction of the
transseptal fibers appeared to be of paramount im-
portance (41,42,48,55).The role of the forces gener-
ated during mastication (51, 63) and the general di-
rection of occlusal wear (50, 51) have also been rec-
ognized. In contrast, an anterior component of
occlusal forces, forces from the cheeks and tongue
and angulation of the roots do not influence tooth Fig. 3.Human periodontium. Buccal plate of a lower bicus-
pid (non decalcified material, 4-pm-thick bucco-oral
movement (39, 40, 49, 51). Attrition may also allow (frontal) section, toluidine blue staining). A. The alveolar
positioning of antagonistic teeth in relatively more wall is well delimited by a network of cement lines (arrows)
stable occlusal relationships: once the occlusal sur- separating it from the compact supporting bone. The bor-
faces are adapted, migration would slow down. Ac- derline between the two types of bone is apparent in the po-
cordingly, cusp interdigitation during normal func- larized light view of the same area (B). The fibrillar orien-
tation of the 2 types of bone is strikingly different: the ex-
tion tends to regulate proximal migration (50). trinsic fibrillar network is almost perpendicular to the
alveolar wall surface and in continuity with the periodontal
ligament fiber bundles. It extends up to the cement lines
(compare A and B). However at this magnification it is not
possible to discriminate the successive layers of bundle
bone clearly visible in A. The supporting bone exhibits the
typical fibrillar organization of haversian bone.

The alveolar wall: anatomical and

histological characteristics
The alveolar wall is perforated by channels through
which blood vessels and nerve fibers connect the
marrow spaces to the periodontal ligament (Fig. 2).
Because of the inserting Sharpey’s fibers, the al-
veolar wall reveals a double fibrillar orientation.
Sharpey’s fibers form the extrinsic component, run-
ning perpendicular to the bone surface. Their colla-
gen is produced by periodontal ligament fibroblasts.
No cell is entrapped in these fibers ( 3 ) .At their inser-
tion in bone, they become mineralized, with their
periphery being hypermineralized and their core hy-
Fig. 2. Microradiograph of the periodontium of the buccal
root of the first lower molar (rat, horizontal section). The
pomineralized (10). The intrinsic fibrillar network,l
polarization of the socket in relation to the migration of laid down by osteoblasts between Sharpey’s fibers, is
the tooth is easily discernible: one side of the socket (the irregularly arranged and less dense ( 3 ) .This specific
resorbing side) is scalloped and irregularly excavated by type of bone with its double fiber orientation is
many juxtaposed lacunae, whereas the other side (the ap- known as bundle bone.
position side) is smooth and regular. Note the openings of
vascular channels (white arrows), for which this wall was
also designated as cribriform plate. The thick black arrow This term, formerly used for cementum (311, was
points to the direction of tooth migration. chosen as it is well suited for the alveolar wall situation.

78
 Alveolar bone and alveolar process

emergence of the Sharpey's fibers to the evolving

tooth position, as proposed for cementum (25).
Because of tooth movement, the socket is spatially

gration,
oriented:that
theis,
side
opposite
of the socket
the migrating
in the direction of mi-
root, is irregu-
I -b
I '
lar and scalloped by numerous lacunae of various
I '

L
+I '' lengths and depths (=the resorbing side) while the
opposite side is regular and smooth (=the apposition
side) (Fig. 2, 6A). The overall activity in the alveolar

~~,
/
I

'L
I

-
I
\

~
'\
wall is assimilable to modeling (Fig. 41, a process en-
suring the shaping of bones during growth (19, 47).
Modeling also allows the adaptations to mechanical
usage and overloading, as it results in bone architec-
A 6 C ture changes that reduce strains under a given load

D
Fig. 4. Modeling is a process allowing shaping during
growth or restoration of the shape of a bone (as an organ).
In adults modeling ensures shape transformation of a
bone to minimize repetitive, uniformly oriented dynamic
strains applied to it. A. Changes of a long bone in length
at its ends and in width during growth. B. Restoration in
young individuals of the shape of a long bone after frac-
ture malunion. C. Migration of a tooth under the influ-
ence of occlusal forces. These adaptive changes are
achieved through oriented surface activities (D) involving
osteoclastic removal on one side of a bone and compensa-
tory osteoblastic formation on the other. Over time the
bone mass is maintained but the bone drifts through a
modification of its external and internal architecture.
Source: adapted from Frost (17, 19).

As cementum surrounds the root, so a layer of

bundle bone covers the whole socket. As a conse-
quence, the supporting bone is never in anatomical
contact and functional relationship with the peri-
odontal ligament (Fig. 3). The layer of functional
bundle bone is thin: it ranges between 100 and 200
Fm in humans (26). The bundle bone may appear
thicker on one side of the socket (the apposition Fig. 5. Histological illustration analogous to Fig. 4D. Ham-
one), but only its outer layer is likely functional (2, ster mandible, interdental septum between m l and m2
4) as suggested by the presence of regularly spaced (decalcified material, Cajal-Gallego trichrome staining).
cement lines. These cement lines act like boundaries One side of the septum is subjected to osteoclastic resorp-
tion (open arrows) and the other is in formation. This de-
between the bone formed on both sides, interrupt-
vice permits the drift of the septum in front of a migrating
ing (or modifymg) the course of the extrinsic fibers. tooth. Note the presence of a continuous cement line (thin
This results in the formation of successive functional arrows) delimiting the functional bundle bone along the
layers. This layering probably adapts the angle of apposition side.

79
Saffar et al.

Fig. 6. Events effecting the deformation of the socket. The clast lineage, which is released in the resorbing compart-
thick arrow points to the general direction of tooth mi- ment of the cell. As seen in C, the enzyme is evenly distrib-
gration. A. General view of the socket of the buccal root uted in the cytoplasm. After osteoclast withdrawal, the
of the first mandibular molar (horizontal section, tol- bone surface is coated with tartrate-resistant acid phos-
uidine blue staining). Along the resorbing side, multi- phatase (arrows), which is incorporated in the reversal
nucleated osteoclasts (B) excavate the alveolar wall. The line. In D, the reversal line is already formed in the lower
resorbing apparatus of the cell (ruffled border) is clearly part of the lacuna (open arrows), where large cells are en-
visible (arrow) contrasting with the finely vacuolated cyto- gaged in synthetic activities, whereas at the top of the la-
plasm. These vacuoles contain an enzyme (tartrate-resis- cuna the line is not yet present (thin arrows), indicating a
tant acid phosphatase), considered specific to the osteo- less mature reversal stage. E. Typical osteoblasts

80
 Alveolar bone and alveolar process

lay down bone matrix over a densely stained reversal line. Along the apposition side, a row of osteoblasts (H) covers
F shows localized fluorescent labeling in a lacuna under- a layer of mineralizing osteoid tissue that lines the al-
going bone formation at the time of incorporation of calc- veolar wall. The progressive accumulation of bone is evi-
ein, a fluorescent dye, in the mineralization front. At the denced by 2 fluorescent labeling (I). At high magnification
completion of bone formation, a resting phase of variable (J), plump osteoblasts appear between the Sharpey’s fibers
duration takes place. G. Resting phase. The less mineral- (arrows). At the interface between the osteoid matrix and
ized new bone (arrows) contrasts with the darker support- the mineralized bone, a granular layer marks the mineral-
ing bone. Reversal lines buried at the interface with the 2 ization front in which the fluorescent dj7e has been incor-
types of bone indicate previous episodes of resorption. porated.

81
Saffur et al.

(19, 21). During modeling, one side of a bony struc-

ture is subjected to apposition while the other is sub-
jected to resorption (Fig. 4-45). These activities occur
for long periods of time without interruption (tooth
attrition is a lifelong process), as long as required by
mechanical usage (47).

Kinetics of the deformation

of the alveolar wall accompanying
migration
When the teeth migrate, the bone surrounding
them does not migrate but is re-arranged (or pref-
erably deformed2) in front of and behind the mi-
grating root. The deformation of the alveolar wall
is achieved through the removal of bone along the
resorbing side and the concomitant deposition of
bone along the apposition side (Fig. 5-7). However,
although this deformation preserves periodontal
ligament width, it is complicated by the necessary Fig. 7. Human periodontium (undecalcified material, 4-
pm-thick horizontal section, toluidine blue staining). Re-
conservation of an effective periodontal ligament sorbing and apposition sides of the socket of a lower in-
anchorage to bone without functional disturbance, cisor. A.Resorbing side. A large lacuna (arrowheads)occu-
so that the principles of modeling as defined pies the center of the field, revealing a recent episode of
above are somewhat modified along the resorbing resorption. A n osteoclast without contact with the bone
side. surface (inactive cell) is still present (thin arrow). B. Appo-
sition side. A row of cells lines the bone surface. In some
areas, these cells are separated from the bone by a layer
Cellular dynamics on the resorbing side of nonmineraked matrix (thin arrows). The cell density
is higher near the bone surface than elsewhere in the peri-
The succession of events occurring in each lacuna odontal ligament (in contrast to the inactive side seen in
(or focus) implies the coordinated recruitment and Fig. 3A). C cementum.
activity of a team of different cells performing pre-
cise tasks in an unalterable sequence. These include
osteoclasts removing a local packet of bone (resorp- jacent foci are asynchronous, that is, at different
tion phase) and osteoblasts laying down bone in the stages of activity.
resorption bay (formation phase). Baron (2, 5) inte- During resorption the osteoclasts excavate the
grated an intermediate step, the reversal phase, dur- layer of bundle bone (Fig. 6B,C), pass through the
ing which the coupling of the sequence occurs (47). cement line and resorb the supporting bone. They
During coupling, the bone surface is prepared to re- remove aU the mineralized material without distinc-
ceive osteoblasts whose precursors are recruited tion between extrinsic and intrinsic components so
simultaneously As everywhere in the skeleton, ad- that the periodontal ligament fiber bundles become
detached at their point of insertion in bone: the peri-
odontal ligament anchorage is locally lost.
At the end of the resorption phase, the osteoclasts
z Deformation is relevant to the terminology of bio-
materials and biomechanics. It refers to the modulus of
elasticity of bone tissue and thus to its property to have
its shape modified when a mechanical strain is applied
(17, 19). Depending on the intensity of the strain the Fig. 8. Reconstitution of the attachment apparatus after
deformation is elastic, without permanent modifi- an episode of resorption. A. In this lacuna the fiber
cation, or adaptive. In the latter case, the architecture bundles (snows) appear disconnected at the level of the
is modified through modeling (Fig. 4). Beyond a certain former bone surface (the arrowheads point to the edge of
threshold, the strain exceeds the adaptive potential and the lacuna). and thus end in a distance from the bottom
a rupture (=fracture) OCCUTS. of the lacuna. B. Early re-attachment stage: some fibers

82
 Alveolar bone and alveolar process

are anchored to the reversal line (arrows),but the conti- (same lacuna as in Fig. 6E). The continuity of the fiber
nuity of the Sharpey’s fibers has not yet been restored. attachment is now restored. D. In this partially bone-filled
The cells near the reversal line may be engaged in fiber lacuna the attachment is fully functional: the fibers are
synthesis. C. Sharpey’s fibers are anchored onto the ce- continuous from the periodontal ligament to the reversal
menting line and become embedded in bone matrix line.

83
Saffar et al.

tion and deepen the lacunae (18). The next step is

the formation of a cement line (Fig. 6D),here termed
reversal line, that records the exact limit reached by
resorption. Morphologically, globular accretions are
deposited over the bone surface demineralized dur-
ing resorption. The confluence of these accretions
forms a regular layer of mineralized material
smoothing the resorbed surface (67). Its constitutive
material is partly of osteoclast and of phagocyte ori-
gin, such as acid phosphatase (Fig. 6C) and polysac-
charides (7, 44). Growth factors released during re-
sorption from the bone matrix and by the phago-
cytes are likely to be incorporated in the cement line
to attract and induce differentiation of competent
cells (47). It is from this boundary and onto it that
anchorage is reconstituted (Fig. 8). Fibroblastic cells
attracted to the lacuna during reversal line formation
secrete thin collagen fibrils in contact with it. Their
Fig. 9. A new cycle of resorptionhas started an osteoclast development restores the continuity of the peri-
(arrow) resorbs a zone of bone subjected to a previous odontal ligament fiber bundles which become an-
episode of resorption as shown by the reversal line (small chored to the bottom of the lacuna (Fig. 8C,D). Os-
thin arrows) buried in bone. (Rat periodontiurn, demin- teoblasts align between the reconstituted fiber
eralized material, Cajal-Gallego trichrome staining).
bundles and secrete bone matrix (Fig. 6E) that em-
beds these fibers. Mineralization (Fig. 6F) firmly an-
chors the peripheral part of Sharpey’s fibers in the
withdraw. The reversal phase then begins. Mononuc- new bone. Thereafter, a resting phase follows (Fig.
leated phagocyte-like cells come in contact with the 6G) until the functional conditions locally activate a
bone surface (62); these cells may complete resorp- new cycle (Fig. 91, during which more bone is re-

Fig. 10. Periosteal bone formation (arrows) compensating wall aspect. Rat periodontium (nondemineralized4-pm-
for the ongoing resorption of the cortex b m its alveolar thick horizontal section, toluidine blue staining).

84
 Alveolar bone and alveolar process

moved to accommodate further migration of the

tooth.
Only minute amounts of bone are formed per
cycle in the lacunae (Fig. 6EG) so that the bone bal-
ance remains markedly negative. Tooth movement
results from the summation of these localized defi-
cits at a given time (5, 64).
The asynchronicity of the foci allows a high level
of anchorage to be maintained. In fact, the attach-
ment is lost within resorption lacunae and in parts
of the reversal foci (Fig. 8 ) for only small periods of
time. About 10% of the resorbing side is in active
resorption in young rats (30, 64); the cycle duration
averages 11 days, with resorption lasting 1.5 days
and reversal 3.5 days. Such loss of attachment is of
no significance for the clinical behavior of the tooth,
in particular its mobility. The morphological appear-
ance of the mesial side of the sockets indicates that
the same events accompany the migration of human
teeth (Fig. 7A). However, morphometric data are not
available in humans.

The apposition side

The apposition side is characterized by the presence
of a continuous row of osteoblastic cells that lie be-
tween the Sharpey’s fibers over a layer of osteoid
tissue (Fig. 6H,J). Confirming their osteoblast pheno-
type, these cells express osteocalcin and osteonectin
messenger RNA (59). A granular material at the bor-
derline of the mineralized tissue represents the min-
eralization front (Fig. 6J).At some distance, a cement
line is buried in bone (Fig. 5). Other lines are seen
Fig. 11. Top of an interdental septum. The periodontal
deeper within bone, when the layer of bundle bone ligament fiber bundles of one root (R) seem to run
is thick (2). As indicated above, only the outer layer through the septal bone and emerge in the periodontal
of bundle bone is functional. Under physiological ligament of the adjacent root. However an episode of re-
conditions, no resorption occurs on the apposition sorption evidenced by a scalloped bone surface (arrows)
has interrupted a possible fiber continuity that is now
side.
definitely lost, if it ever existed. Demineralized rat ma-
Due to the ongoing deposition of bone, the bone terial, 4-pm-thick horizontal section, Cajal-Gallego tri-
balance is highly positive (Fig. 61) and the amount chrome staining.
of bone deposited along the apposition side equal-
izes the net deficit at the resorbing side. Conse-
quently the bone balance is equilibrated around the
socket (5,64),in line with the principles of modeling. placed by haversian remodeling. In no case does this
The deformation of the socket (external architec- remodeling reach the periodontal ligament, since a
ture) is accompanied by a re-arrangement of the layer of bundle bone is always present and a cement
supporting bone (internal architecture). The removal line separates the endosteal bone from the func-
of bone on the resorbing side is compensated by la- tional bundle bone. The spatial arrangement of these
mellar bone formation on the endosteal aspect of activities along the endosteal surfaces, occurring
the alveolar wall. On the apposition side the no mostly in the apical half of the septa, was confirmed
longer functional bundle bone is resorbed from the by in situ hybridization for various markers of the
endosteum and replaced by lamellar bone. In osteoblast and osteoclast phenotypes (59). The outer
humans, accumulation of bundle bone can be re- periosteal envelope is also involved in the re-ar-
Saffaret al.

Fig. 12. Nonspecific esterase reaction showing the pres- odontal ligament. They are never seen in contact with the
ence near the bone surface of cells expressing the enzyme bone surface. These cells may be osteoclast precursors (6).
(arrows),generally assigned to the monocyte-macrophage Rat periodontiurn (undecalcified material, 4-pm-thick
lineage. These cells are always associated with the vascu- horizontal section).
lar network located in the bone-related part of the peri-

rangement of the supporting bone. In the rat, perios- 20, 2211. They may act in a viscous manner at low
teal formation maintains the thickness of the buccal strain rates and as an elastic material at higher
cortex (Fig. 10). strain rates. Moreover, they may permit energy
The cement lines that completely surround the transfer in loading situations (12). These data may
socket give evidence of the ongoing deformation. be of paramount importance for the dissipation of
Their presence does not support the assumption the functional andlor parafunctional forces in the
that Sharpey’s fibers unite the ligaments of ad- supporting bone and the entire jaws.
jacent roots through the septa (15, 16, 52). This
might occur at the top of the septa at an early
stage of their formation, but as soon as tooth mi-
gration starts, these connections are lost (Fig. ll). Origin of the bone cells carrying
Cement lines are hypomineralized: they contain out the deformation of the socket
less calcium and phosphorus and more sulfur
(likely to be associated with glycoproteins) than During the development of the tooth organ, the cells
bone matrix (12). Their Ca:P ratio is higher than in forming the alveolar wall originate from the fibrous
bone, suggesting that the mineral is in the form of dental follicle as demonstrated by transplantation
calcium carbonate instead of hydroxyapatite (12). studies (61, 66). These cells arise from cells having
Their organic and mineral composition suggests migrated from the neural crests during embryogen-
striking mechanical properties. Cement lines would esis (reviewed by Ten Cate (60) and in this volume),
be more ductile than the surrounding bone matrix so that the primary alveolar wall is an ectomesen-
and this could increase resistance to fatigue failure chymal derivative. Whether cells of this lineage still
by preventing crack growth within the mineralized reside in the mature periodontal ligament and inter-
bone substance [crack generation is a frequent vene in the local homeostasis is unknown but seems
event in bone resulting from mechanical usage (11, likely, as suggested by the differentiation of bundle

86
 Alveolar bone and alveolar process

Fig. 13. The bone-relatedpart of the periodontal ligament phatase-positive cells are preosteoclasts. Cells positive for
contains mononucleated tartrate-resistant acid phospha- this enzyme sometimes seen near the root surface might
tase-positive cells (arrows) that are either associated with be preodontoclasts (arrowhead). Rat periodontium (non-
the vascular network (usually these cells are small) or demineralized material, 4-pm-thick horizontal section,
located between the vessels and the bone surface (where light toluidine blue counterstaining).
they tend to be larger). These tartrate-resistant acid phos-

bone around mature teeth transplanted into the oral they become osteoblasts. Bone may contain chemo-
mucosa (1). tactic factors for periodontal ligament cells different
In the mature periodontium, the renewal of the from the chemoattractants bound in cementum (46).
alveolar wall is effected by periodontal ligament A contribution of the endosteal spaces of the sup-
cells. These cells are positive for bone-type alkaline porting bone to the alveolar wall osteoblast popula-
phosphatase (45, 58, 65) and they express mRNA for tion has also been proposed (38).
this isoenzyme (23). Bovine periodontal ligament Far fewer data exist on the origin and location of
cells respond to PTH by producing CAMP and to osteoclast precursors. In a kinetic study on osteo-
1,25-(OH)2D3 by synthesizing osteocalcin, two clast differentiation in a synchronized model of bone
characteristic features of the osteoblast phenotype remodeling, Baron et al. (6) showed that nonspecific
(45). Isolated rat periodontal ligament cells can form esterase-positive cells (nonspecific esterase is a spe-
bone nodules under appropriate culture conditions cific marker of the phagocyte phenotype) differen-
(43). tiate into tartrate-resistant acid phosphatase-posi-
The osteoprogenitor cells reside in the environ- tive cells which fuse to form osteoclasts. In the peri-
ment of the blood vessel network located in the odontal ligament, we have localized nonspecific
bone-related part of periodontal ligament (36, 37, esterase-positive cells close to the blood vessels (Fig.
54). Based on the analysis of nuclear size as a marker 12), mostly at the resorbing side of the socket (Saffar
of osteoblast differentiation (53), Roberts et al. (54) et al., unpublished data). Mononucleated tartrate-re-
observed in rats that perivascular cells move away sistant acid phosphatase-positive cells (preosteo-
from these vessels towards the root. During mi- clasts) are found between the vascular network and
gration, they increase in size and differentiate into the bone surface (Fig. 13). These data strongly sug-
preosteoblasts. After mitosis, upon an adequate sig- gest that these blood vessel-associated nonspecific
nal, they migrate towards the bone surface, where esterase-positive cells are osteoclast precursors.

87
Saffar et al. ~

McCulloch et al. (34) reported the presence of 3. Baron R. Ultrastructure de l’os fascicule et des fibres de
macrophages in the rat periodontal ligament close Sharpey de la lame cribriforme. J Biol Buccale 1973: 1: 201-
213.
to blood vessels, these may contribute to this non- 4. Baron R. Histologie et physiologie de la lame cribriforme.
specific esterase-positive osteoclast precursor popu- In: Entretiens de Bichat, Odonto-Stomatologie. Paris, Ex-
lation. pansion Scientifique, 1973: 7-15.
5. Baron R. Le remaniement de 1’0s alveolaire au cours du
deplacement spontank et provoquk des dents. Rev Orthop
Dent Fac 1975: 9: 309-325.
Conclusion 6. Baron R, Tran Van E: Nefussi JR, Vignery A. Kinetic and
cytochemical identification of osteoclast precursors and
Teeth migrate adaptively to crown attrition. The mi- their differentiation into multinucleated osteoclasts. Am J
gration rate seems to peak during growth and de- Pathol 1986: 122: 363-378.
clines afterwards without ceasing completely. To ac- 7. Baron R, Vignery A, Horowitz M. Lymphocyte, macro-
phages and the regulation of bone. In: Peck WA, ed. Bone
commodate the movement, the surrounding bone
and mineral research annual 2. Amsterdam: Elsevier, 1984:
has to deform in front of and behind the migrating 175-243.
teeth. This deformation is quite assimilable to the 8. Begg PR, Kesling PC. Begg orthodontic. Theory and prac-
process known as modeling in bone physiology. Dur- tice. Philadelphia: Saunders, 1971.
ing modeling one side of a bone is resorbed by os- 9. Behrents RG. Growth in the aging craniofacial skeleton.
Ann Arbor: Center for Human Growth and Development,
teoclasts while bone is deposited by osteoblasts on
University of Michigan, 1985.
the opposite side. This permits progressive drift of 10. Boyde A, Jones SJ. S.E.M. of cementum and Sharpey fibre
the bone surfaces and ultimately the gross modifi- bone. Z Zellforsch 1968: 92: 536-548.
cation of the organ shape. During tooth migration 11. Burr DB. Remodeling and the repair of fatigue damage. Cal-
this process is complicated by the necessary preser- cif Tissue Int 1993: 53: S755S81.
vation of the periodontal ligament anchorage to 12. Burr DB, Schaffler MB, Frederickson RG. Composition of
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