THE ANATOMICAL RECORD 245~374-393(1996)

Tooth Eruption: Theories and Facts

SANDY C. MARKS, JR.AND HUBERT E. SCHROEDER
Department of Cell Biology, University of Massachusetts Medical School, Worcester
Massachusetts (S.C,M.);Department of Oral Structural Biology, Dental Institute,
University of Zurich, Zurich, Switzerland (H2.S.)
ABSTRACT The mechanisms of tooth eruption (i.e., the answer to the
question of how and why teeth erupt) has been a matter of long historical
debate. This review focuses on human and other mammalian teeth with a
time- and spacewise limited period of eruption and analyzes recent obser-
vations and experimental data on dogs, rats, primates, and humans in a
framework of basic biological parameters to formulate a guiding theory of
tooth eruption. Acknowledging basic parameters Ce., that teeth move in
three-dimensional space, erupt with varying speed, and arrive at a func-
tional position that in inheritable) eliminates a number of previously held
theories and favors those that accommodate basic parameters, such as al-
veolar bone remodeling in association with root elongation, with possible
correction factors in the form of cementum apposition and periodontal
ligament formation. We have critically analyzed, summarized, and inte-
grated recent findings associated with preeruptive movements of develop-
ing teeth, the intraosseous stage of premolar eruption in dogs, molar erup-
tion in rodents, and premolar and molar eruption in primates. The variable
speeds of eruption are particularly important. We conclude with basic prin-
ciples of tooth eruption-that is, the type of signals generated by the dental
follicle proper, the conditions under which teeth are moved and the clinical
understanding to be derived from this knowledge. o 1996 Wiley-Liss, Inc.
Key words: Teeth, Rats, Dogs, Primates, Eruption theories

Tooth eruption is defined as the movement of a tooth
from its site of development within the alveolar process
to its functional position in the oral cavity (Massler and
Schour, 1941). However, developing teeth also move in
three dimensions and increase in size within the alve-
olar process before active eruption (Weinmann, 1944),
and erupted teeth and the alveolar processes grow
slowly coronally during the second to fourth decades of
life, long after occlusal contact has first been attained
(Carlson, 1944). Thus, the process(es1of tooth eruption
can be conveniently, even if arbitrarily, divided into
five stages: preeruptive movements, intraosseous erup-
tion, mucosal penetration, preocclusal eruption, and
postocclusal eruption. Teeth develop in alveolar bone,
and during crown formation there are small preerup-
tive, gyratory movements within the jaws. After crown
formation is completed and the root begins to form, an
active eruption process moves the tooth towards its
functioning position. The first part of this journey, the
intraosseous stage, is through bone and for many teeth
through the space occupied by the roots of the primary
dentition. It ends just prior to mucosal penetration
when the speed of eruption begins to accelerate. When
the occlusal plane is approached, this rapid phase of
eruption comes to a halt. Initial events after first
reaching the occlusal plane include consolidation of
periodontal support for the tooth and closure of the root
apex. Later, eruption and alveolar growth in height
proceed a t a slow rate until the fifth decade of life. This
0 1996 WILEY-LISS, INC.
increases and maintains the vertical dimension of the
face, and may also compensate for occlusal attrition. If
contact is lost with teeth in the opposite arch, alveolar
growth and eruption rate increase again.
These stages of tooth eruption will form the context
in which to review and analyze currently available ex-
perimental and clinical data. While recent reviews
(Steedle and Proffit, 1985; Sutton and Graze, 1985;
Thesleff, 1987b; Marks, 1987; Cahill et al., 1988;
Marks et al., 1988; Gorski and Marks, 1992) have pro-
vided a rather general outline, the purpose of this ar-
ticle is to focus on data critical for man and other mam-
malian species in order to arrive a t a rational, testable,
and, if possible, clinically applicable theory (hypothe-
sis) of eruption for teeth with a timely and spacewise
limited period of eruption.
THEORIES OF TOOTH ERUPTION
In the past, numerous theories of tooth eruption have
been proposed. These involved almost all tissues in or
near an erupting tooth. However, none of them alone
can account for the journey a tooth must make in its
lifetime. In order to be valid for biological and clinical
purposes, a guiding theory of tooth eruption has to ac-
Address reprint requests t~ Sandy C. Marks, Jr., Department of
Cell Biology, University of Massachusetts Medical Center, 55 Lake
Avenue North, Worcester MA 01655.
 TOOTH ERUPTION 375
commodate the following factual observations about theory lie in explanations for the early events of tooth
the process: eruption since part of the follicle is lost after mucosal
penetration. Nevertheless, the periodontal ligament,
1. teeth are moved in three-dimensional space, not cementum, and alveolar bone proper are derivatives in
just along their axis; part of the follicle, so that later events could be con-
2. teeth erupt with varying characteristic, stage- trolled by these and other related tissues.
specific speeds; and The dental follicle proper is the thin, dense, ectomes-
3. teeth arrive at a functional position that is inher- enchymal connective tissue investment of a developing
itable. tooth which surrounds the enamel organ. It is sepa-
rated from the latter internally by a basement mem-
With this in mind and focusing on teeth with limited brane and separated from the bone cells lining the
eruption, the following theories cannot be considered crypt by a loose, vascular connective tissue (Schroeder,
as serious contenders: pulpal pressure, pulpal growth, 1986).
traction by periodontal fibroblasts, vascular pressure, The fact that active eruption begins only after crown
and blood-vessel thrust (Herzberg and Schour, 1941; formation is complete (Carlson, 1944) suggests a role
Bryer, 1957; Sutton and Graze, 1985). Instead, root also for the enamel organ and its proteases in the early
elongation, alveolar bone remodeling, and, possibly, signaling of eruption (Gorski et al., 1988a,b; Gorski
periodontal ligament formation provide the most con- and Marks, 1992). In addition, the proximity of the
vincing data to explain tooth eruption in man and enamel organ and the dental follicle and their tight
other mammalian species. adherence in surgical manipulations indicate that
many effects attributed above to the dental follicle
Root Elongation proper may indeed be events initiated or controlled by
Because roots form a t the time of eruption, they have the enamel organ or the reduced enamel epithelium. If
long been considered the force responsible for eruption this is the case, tooth eruption may be yet another ex-
(reviewed by Massier and Schour, 1941). However, root ample of collaborative epithelial-mesenchymal interac-
elongation cannot be expected to move a tooth in three- tions in development.
dimensional space. Furthermore, rootless teeth do
erupt (Witkop, 1975; Shields et al., 1973; Pietrokovski Periodontal Ligament
and Menczel, 1966; Per1 and Farman, 1977; Gowgiel, Formation and renewal of the periodontal ligament is
1961; Carl and Wood, 1980; Cahill and Marks, 1980). associated with the continuous eruption of permanently
This is most obvious in cases of dentin dysplasia Type growing rodent incisors (Berkovitz and Thomas, 1969;
I and following irradiation. In other words, root forma- Berkovitz, 1971). However, for teeth with a limited pe-
tion per se is not required for tooth eruption. It may, riod of growth the presence of a periodontal ligament
however, accelerate eruption speed. does not assure eruption. In the case of osteopetrotic
Alveolar Bone Remodeling mutations (Marks, 1989) a periodontal ligament is
present, but teeth do not erupt, and in the case of root-
The alveolar process forms during tooth development less teeth, in particular those in dentinal dysplasia Type
and is locally deficient in sites where primary or per- I, by definition without a periodontal ligament, erup-
manent teeth fail to develop (Brash, 1928; Lands- tion occurs (Gowgiel, 1961; Witkop, 1975; Shields et al.,
berger, 1924). Thus, alveolar bone growth, tooth devel- 1973; Cahill and Marks, 1980).Therefore, the periodon-
opment, and eruption are interdependent. Formation of tal ligament cannot be essential for tooth eruption in
bone apical to developing teeth has long been proposed man. Its role has been largely oversold by inappropriate
as one mechanism for eruption (Brash, 1928). There is extrapolation to the human dentition of experiments
no doubt that bone forms in these sites, but bone for- performed in animals such as rodents with teeth that
mation per se is not sufficient for tooth eruption either. erupt continuously throughout life.
A good example to illustrate this is the presence of an
unerupted dentition in osteopetrotic mutations in
which bone formation is nearly normal or elevated and CLINICAL AND EXPERIMENTAL DATA ON
bone resorption greatly reduced (Marks, 1989). The TOOTH ERUPTION
same applies for cases of cleidocranial dysplasia in Developing teeth must erupt through a complicated
which deciduous teeth erupt and persist while perma- maze of different mineralized and unmineralized con-
nent teeth erupt late or ectopically (Jensen and Krei- nective tissues. This movement requires resorption of
borg, 1990). Rather, alveolar bone growth involving bone, and often roots of primary teeth, in the direction
turnover (resorption and formation) is required during of movement and formation of bone and root(s) in the
tooth eruption (Weinmann, 1941; Brodie, 1934). opposite direction. The height of the alveolar process
The relatively recent demonstration that bone re- increases during eruption, and there are regional dif-
sorption and bone formation are polarized around ferences in the rates of growth of the jaws during this
erupting teeth and that these metabolic events depend period.
upon the adjacent parts of the dental follicle (Cahill In 1944 Carlson published a comprehensive radio-
and Marks, 1980; Cahill, 1974; Marks et al., 1983; graphic analysis of the eruption of five different types
Marks and Cahill, 1987) have led to the concept that of permanent teeth. He showed that for the human
tooth eruption is a localized, bilaterally symmetrical permanent premolars, 1) eruption begins only after
event in alveolar bone that is regulated by the dental crown formation is complete, 2) root formation occurs
follicle proper, a derivative of cranial ectomesenchyme initially at the expense of basal bone without move-
(Marks, 1987; Cahill et al., 1988). The strengths of this ment of the crown, 3) most root growth occurs during
376 S.C. MARKS, JR.AND H.E. SCHROEDER

the stage of rapid preocclusal eruption to the occlusal

plane, 4) the completion of the root, like its initial
growth, is at the expense of basal bone, and 5) teeth
continue to erupt slowly or move with growth of the
alveolar process throughout life.
Using metallic implants on facial bones t o serve as
fixed reference points, sequential radiographs by Bjork
and Skieller (1972, 1976) showed that differential
growth of the jaws produced a forward rotation around
a center in their anterior part and that remodeling of
the inferior border of the mandibule obscured much of
this differential growth in jaws without internal stan-
dards. These positional changes of the jaws during the
period of tooth eruption mean that most erupting teeth
must fit into a rotating occlusal plane while moving
between and among their neighbors. With these formi-
dable tasks one is hardly surprised that tooth eruption
is sometimes ectopic (Kurol and Bjerklin, 1982, 1986;
Orton and McDonald, 1986; Rasmussen et al., 1983).
Some of the challenges facing erupting teeth are il-
lustrated in Figure l, osteological preparations of the
right posterior mandibular sextants of 7- (Fig. 1A) and
9-year-old (Fig. 1B) children. Notice that during this 2
year period there has been considerable growth of per-
manent teeth and their roots, resorption of roots of the
first primary molar, and resorption of alveolar bone
overlying the second permanent molar. Teeth without
a primary precursor, such as the examples shown in
Figure 1, must erupt into a precise position behind the
last erupted tooth. Failures of development and erup-
tion or premature loss of an adjacent tooth can compli-
cate eruption for neighboring teeth. Permanent teeth
that develop near the apices of primary precursors
must erupt by slowly undermining the support for this Fig. 1. Preparations of the right posterior sextants of mandibles
tooth while establishing their own by growth of roots from 7- (A) and 9-year-old(B)children prepared to show the relative
and basal bone. Add to this the usual bilateral symme- positions of the crowns and roots of the primary (C,D,E) and perma-
try and precise timing of tooth eruption and one can nent (2,3,4,5,6,7) dentitions. Note the changes in the positions of the
appreciate the remarkable challenges facing an erupt- permanent teeth, including root growth, during this 2 year period.
ing tooth.
PREERUPTIVE MOVEMENTS OF DEVELOPING TEETH primary molars (Logan, 1935; Ooe, 1968; Steedle and
Teeth develop from discrete invaginations of the oral Profit, 1985).
ectoderm which invade the mesenchyme of the jaws. THE INTRAOSSEOUS STAGE OF ERUPTION
The collaborative interactions of these epithelial and
ectomesenchymal cells derived from the neural crest All teeth develop within the alveolar bone of the
form the tooth. The original epithelial strand, the gu- jaws. The challenge of the intraosseous stage of tooth
bernaculum dentis, temporarily connects the tooth eruption is t o escape from the bone surrounding the
germ to the oral mucosa. Formation of alveolar bone crown and to redirect the growth of the alveolar bone
around the developing tooth spares the gubernaculum proper to surround and support a developing root. The
and produces a gubernacular canal between the crypt former involves bone resorption and the latter bone
of the developing tooth germ and the oral cavity (Fig. formation on opposite sides of the erupting tooth. These
2). However, for permanent teeth, this canal is not activities have been shown to depend upon the adjacent
present for canines and premolars. During crown de- parts of the true dental follicle.
velopment small, preeruptive random movements of
the tooth have been described (Weinmann, 1944). Eruption of Premolars in Dogs
Whether they are mediated by the follicular events ac- Experimental studies of the eruption of mandibular
companying eruption (see below) or reflect regional dif- premolars in dogs were pioneered by Cahill, who
ferences in the growth and maturation of the jaws showed that an eruption pathway for each tooth was
(Bjork and Skieller, 1976) is not known. At any rate formed by osteoclasts and that neither the appearance
these small movements of the developing crown are of these cells nor the production of an eruption pathway
local and not in the direction of eruption (Carlson, depended upon pressure from the erupting tooth (Ca-
1944). In addition, the premolar tooth germs develop hill, 1969, 1974). The rate of eruption of these teeth
initially lingual to the crowns of the primary molars, exhibited three phases. Initial eruption through bone
but later, when the primary molars erupt, they move was slow; above the alveolar crest eruption was rapid,
labially to grow and erupt in the interradicular space of and the eruption rate slowed again after reaching the
 TOOTH ERUPTION
Fig. 2. The anterior maxilla (A) and mandible (B) of a 5-year-old
child showing the lingual position of the gubernacular canals of the
permanent incisors (arrows).
occlusal plane. Temporary experimental impaction of
erupting teeth demonstrated upon release a remark-
able catch-up eruption, suggesting that the rate-limit-
ing step of early eruption is formation of an eruption
pathway which formed on schedule in these teeth (Ca-
hill, 1970). Bone resorption can be blocked after admin-
istration of bafilomycin A, which binds irreversibly to
proton pumps in osteoclasts (Sundquist et al., 1990).
Infusion of M bafilomycin into crypts of erupting
premolars for 2 weeks stops eruption without affecting
bone formation or the eruption of adjacent teeth
(Sundquist and Marks, 19941, reinforcing the impor-
tance of local bone resorption in tooth eruption. The
third and fourth permanent mandibular premolars in
dogs have a precise, bilaterally symmetrical eruption
sequence (Cahill and Marks, 1982). The radiographic
hallmarks of eruption are illustrated in Figure 3,
which includes a histological section of the third pre-
molar in mid-to-late eruption. Note the prominent ra-
diographic and histological appearance of the eruption
pathway and basal trabecular bone in these figures.
Premolars a t the beginning of eruption have a distinct
dental follicle tightly applied to the reduced enamel
epithelium and separated from the alveolar bone sur-
face by a vascular, loose connective tissue (Fig. 4). No-
tice that the dental follicle proper is a dense, organized,
vascular connective tissue. Examination of the bony
crypt of an erupting tooth by scanning electron micros-
copy (Fig. 5 ) shows that there is resorption in its coro-
nal aspect and formation of alveolar bone in its apical
aspect early in eruption. Light and electron micro-
scopic studies of the follicle and crypt during eruption
377
(Marks et al., 1983; Marks and Cahill, 1986, 1987;
Wise et al., 1985) show that there are osteoclasts and
osteoblasts on opposite sides of the erupting tooth and
that the coronal part of the follicle becomes infiltrated
by mononuclear cells a few days before eruption begins
(Fig. 6). These mononuclear cells have some ultrastruc-
tural and cytochemical features of preosteoclasts and
may fuse with or influence osteoclasts on crypt sur-
faces (Fig. 7). The apical parts of the dental follicle and
crypt are characterized by cell proliferation and follic-
ular cells which bind epidermal growth factor (EGF)
(Marks et al., 1988).
Surgical manipulations of erupting dog premolars
have shown that the dental follicle (which in these
studies included the enamel organ) but not the crown is
needed for formation of an eruption pathway and
timely exfoliation of the primary premolar (Fig. 8). No-
tice that after removal of the crown, a migrating radio-
lucency can be easily discerned and that this consists of
resorption in the direction of movement and formation
of bone in the basal part of the crypt. These radio-
graphic images (Fig. 8) replicate the metabolic activi-
ties of bone surfaces during eruption, demonstrating
that tooth eruption consists of a local coordination of
alveolar bone resorption and formation on opposite
sides of the erupting tooth (Marks and Cahill, 1987).
That the crown itself does not contribute to the erup-
tion process is shown by the eruption of a metal replica
placed within the dental follicle after removal of the
crown just before eruption begins (Marks and Cahill,
1984) (Fig. 9). Furthermore, surgical ablation of one or
both roots does not interfere with eruption (Fig. 10).
Removal of the dental follicle (and enamel organ), how-
ever, stops eruption, and there is formation of neither
an eruption pathway nor basal bone (Cahill and Marks,
1980). Removal of the coronal half of the follicle pre-
vents eruption by preventing formation of an eruption
pathway, and removal of its basal half prevents erup-
tion by preventing bone formation (Marks and Cahill,
1987). These observations demonstrate a regional con-
trol of alveolar bone metabolism by the surgically de-
fined dental follicle, the dental follicle proper and the
enamel organ. (Surgical manipulations of the dental
follicle of erupting teeth by necessity include the
enamel organ or the reduced enamel epithelium be-
cause these tissue layers cannot be separated clini-
cally.) Thus, most experimental studies to date of the
role of the dental follicle in eruption (Cahill and Marks,
1980; Marks and Cahill, 1984,1987) have included the
adjacent enamel epithelium and need to be interpreted
in that light. The true dental follicle externally and
enamel epithelium internally can be separated me-
chanically, however, after incubation in EDTA (Lau
and Ruch, 1983). Recently this procedure was used on
short-term explants of dog premolars to remove the
dental follicle at the beginning of and several weeks
prior to eruption. Crowns with the enamel organ but
without the true dental follicle were replaced in crypts
but did not erupt (Larson et al., 1994). Crowns from
which the follicle was removed and reapplied before
replacing in the crypt did erupt. These studies suggest
that the enamel organ alone is unable to direct tooth
eruption and that the true dental follicle with the
enamel organ is required for eruption. Testing the abil-
ities of the dental follicle alone (without the enamel
 Fig. 3. Radiographs of the eruption of a sham-operated third man-
dibular permanent premolar (P)at 15, 17,19,20,21,22, and 23 weeks
(a-g, respectively). Notice the progressive occlusal movement of the
permanent premolar into the eruption pathway, a radiolucent area
best seen at the tip of the main cusp (b-e) but present all around the
external surface of the crown. Interradicular bone (asterisks) in-
creased with eruption. The fourth permanent premolar crown seen in
panel a was removed with its dental follicle (b) in another experiment.
x1.9. h: A longitudinal section through the mandible of a sham-
operated animal showing the development and eruption of the third
permanent premolar (P3) at 20 weeks. This section corresponds to the
radiograph in panel d. Notice that trabeculae (T)of interradicular
bone have formed under the permanent crown, but bone is being re-
sorbed beneath the deciduous tooth (D3) to form a n eruption pathway
(EP). Notice resorption of the deciduous tooth, especially its posterior
root. E, enamel space; MC, mandibular canal; 1and 2, anterior and
posterior roots, respectively, of permanent premolar. Haematoxylin
and eosin. x 8. Arrows indicate location of Fig. 4. (Reproduced from
Marks and Cahill, 1984, with permission of the publisher.)
 TOOTH ERUPTION
Fig. 4. A High magnification of the region between arrows in Fig.
3 shows that the interval between alveolar bone (AB) and the enamel
(E)and dentin (D) of the crown of the developing permanent premolar
contains three distinct layers of connective tissues. A dense, organized
layer, the dental follicle (DF),lies just outside the enamel epithelia.
The dental follicle is continuous with a loosely organized layer (stars)
of similar width which has a rich vascular supply (Markset al., 1983).
A thin layer of cells (arrowheads) lines the bone surfaces. ~ 3 6 B: .
organ) is technically difficult in this system because a
clear separation of the enamel and the enamel organ is
not possible with this technique without destroying the
orientation and continuity of the dental follicle proper
but must be done to determine whether eruption is
uniquely a property of the dental follicle or requires the
collaboration of the enamel organ.
These data taken together show that the dental fol-
licle (with the enamel epithelium) is necessary for the
coordinated alveolar bone resorption and formation
that characterize intraosseous tooth eruption. Further-
more, these polarized processes in alveolar bone are
related to events in the adjacent part of the dental fol-
licle-mononuclear precursors of osteoclasts and media-
tors of bone resorption coronally and cell proliferation
and bone formation apically (Marks et al., 1983; Marks
and Cahill, 1984, 1986, 1987; Marks, 1987).
Biochemical analyses of the canine premolar dental
follicle (including the enamel organ) during in-
traosseous eruption have provided new insights into
potential mechanisms. The premolar dental follicle is a
highly hydrated structure which reaches its maximal
weight a t the time eruption begins. Collagen content
increases 250%and proteoglycans 45%during eruption
(Gorski et al., 1988a,b). Of the more than 20 proteins
that can be identified in these preparations of enamel
organ and true dental follicle prior to eruption, the
most prominent is a sialoprotein of 95,000 relative mo-
lecular weight (DF-95). At the onset of eruption (16
weeks) DF-95 content is reduced by exactly the amount
of three new sialoproteins of MW 20-25,000 which ap-
379
Photomicrograph of the dental follicle illustrating characteristic fea-
tures when cut in a vertical plane. In this plane apical parts of the
dental follicle show an organized network of fibroblasts and collage-
nous bundles oriented primarily along the plane of section. The fi-
brocollagenous network is most organized and regular next to the
tooth surface, passing progressively into a loosely organized connec-
tive tissue with vascular channels (arrowhead)laterally. x 340. (Re-
produced from Marks et al., 1983, with permission of the publisher.)
pear a t this time. This has been interpreted to mean
that fragmentation of DF-95 is a biochemical marker of
the beginning of tooth eruption. Additional studies
have shown that dental follicles contain collagenolytic
activity (Woessner and Cahill, 1974) and that the fol-
licular content of the metalloproteinases (collagenase
and stromelysin) is reduced during eruption (Gorski
and Marks, 1992), suggesting a role for these enzymes
in tissue turnover. The recent demonstration that in
these preparations DF-95 is localized to the reduced
enamel epithelium (Fig. 11) (Gorski et al., 1994) is bio-
chemical evidence that this epithelium is involved in
and may initiate eruption. Proteases have been identi-
fied in the enamel organ during tooth development
(Nanci et al., 1989; Smith et al., 1989; Den Besten et
al., 1989). Activation of these proteases at the comple-
tion of crown formation could cause fragmentation of
DF-95 and initiate eruption by release of metallopro-
teinases from the dental follicle.
Eruption of Molars in Rodents
Rodent molars develop in troughs of alveolar bone
(Park, 19731, and studies of their eruption have pro-
vided additional insights into the mechanisms of tooth
eruption.
The role of bone, dentin, and root formation in tooth
eruption was studied in the rat molar by O'Brien et al.
(1958), who concluded that changes in the follicle sim-
ilar to sutural growth caused eruption. Later studies of
rat and hamster molar eruption showed that the alve-
olar crest and interdental areas (not the fundus) were
380 S.C. MARKS, JR. AND H.E. SCHROEDER
Fig. 5. Scanning electron micrograph of an anorganic preparationof
the medial crypt surface of an erupting mandibular fourth permanent
premolar in a 19-week-old dog. Three distinct regions are identified
by surface topology and reveal the metabolic state of the bone at this
time: a scalloped superior surface (1) indicative of bone resorption, a
smooth middle area (2) reflecting a restinghnactive bone surface, and
(3) a trabeculated inferior portion consisting of newly formed bone.
MC, mandibular canal; arrow, direction of tooth eruption. x 20. (Re-
produced from Marks et al., in press, with permission of the copyright
holder.)
areas of bone apposition (Kameyama, 1973; Gregg and
Avery, 1964). Immobilization of erupting hamster mo-
lars prevented root growth but not alveolar bone for-
mation, and released molars resumed normal root
growth and erupted rapidly (Gregg, 1965). These de-
velopments were interpreted to mean that root elonga-
tion is a consequence, not a cause, of eruption and that
alveolar bone formation is an important factor in erup-
tion. Analyses of the crypts and follicles of rat molars
has shown that mononuclear cells and osteoclasts are
present early in eruption to form its eruption pathway
(Wise and Fan, 1989) in a manner similar to that
shown earlier for dog premolars (Marks et al., 1983;
Wise et al., 1985). Collagen synthesis by dental follicle
cells of murine molars is high before eruption but
ceases in the coronal part of the follicle after eruption
begins (Shroff et al., 1994). Transforming growth fac-
tor-beta (TGF-P),a chemoattractant for monocytes, has
been localized in the stellate reticulum and follicle of
the first molar in the neonatal period just prior to the
follicular influx of monocytes (Wise and Fan, 1991).
Epidermal growth factor (EGF), which causes prema-
ture eruption of rat incisors (Cohen, 19621, has been
localized in the apical part of the follicle of erupting
teeth in several species (Topham et al., 1987; Thesleff,
1987a; Marks et al., 1988). Around erupting rat mo-
lars, the receptor for EGF is present in the follicle early
in eruption, and EGF itself is present in the follicle
later (Wise et al., 1992a,b). The potential relationship
between EGF and TGF-P has been clarified by the dem-
onstration that EGF can increase TGF-P mRNA levels
in cultured stellate reticulum from erupting rat molars
(Lin and Wise, 1993). Cells from the rat molar follicle
and stellate reticulum contain large, electron-dense
granules (Wise et al., 1990) which have been isolated
and shown to consist primarily of two proteins of 167
and 200 kDa (Lin et al., 1992a). Injection of these pro-
teins into young rats delays eruption of incisors and
molars (Lin et al., 1992b). These studies together show
that the tissues surrounding an erupting tooth contain
both inhibitors and accelerators of the process.
Experiments with colony-stimulating factor-1 (CSF-
11, a growth factor promoting the differentiation and
survival of monocytes, macrophages, and osteoclasts
(Stanley et al., 1983), have shown that it accelerates
molar eruption in rats by increasing monocytes in the
follicle and osteoclasts on crypt surfaces (Cielinski et
al., 1994). CSF-1 treatment of the osteopetrotic rat mu-
tation toothless ( t l )improves tooth eruption (Marks et
al., 19921, and its effect on eruption of a particular
tooth depends upon when CSF-1 administration be-
gins (Iizuka et al., 1992). CSF-1 treatment begun a t
birth results in incisor eruption 15 days later. Delay-
ing treatment for 36-48 h severely restricts incisor
eruption. Similarly, first molars erupt when treatment
begins on the third day but do not erupt when treat-
ment is delayed beyond the eleventh day. These data
indicate that each tooth has a characteristic window
of eruption during which eruption is possible. If an
eruption pathway cannot be provided during this time,
eruption is compromised because ankylosis develops
(Iizuka et al., 1992). This suggests that bone resorp-
tion is the rate-limiting step of intraosseous erup-
tion (Marks et al., 1994). Recent work by Wise and
Lin (1994) has shown that the rat molar follicle pro-
duces and translates CSF-1 mRNA and that CSF-1 it-
self has an autocrine effect to increase CSF-1 mRNA.
Furthermore, interleukin-1-alpha (IL-la), a potent
promoter of bone resorption, is produced in the enamel
organ in response to EGF and causes follicular cells
to produce CSF-1 (Wise and Lin, 1994; Wise et al.,
1994).
Taken together these studies of rodent molar erup-
tion show that localized bone formation and resorption
are major events in eruption, that root formation is a
consequence not a cause of eruption, and that the
timely availability of an eruption pathway is a require-
ment for successful eruption. They also suggest that
the enamel organ plays a role in eruption and that
CSF-1, EGF, TGF-p, and IL-1 are likely candidates for
the local molecular regulation of eruption. This hy-
pothesis is summarized in Figure 12.
 TOOTH ERUPTION 381

Fig. 6. Transmission electron micrograph of a monocyte in the dental follicle showing its typical
morphology of round shape, indented nucleus, Golgi apparatus, and dense-core, membrane-bound gran-
ules (arrowheads). x 17,000. (Reproduced from Wise et al., 1985, with permission of the publisher.)

Tooth Eruption in Primates
Studies in nonhuman primates have shown that
rootless teeth can erupt (Gowgiel, 1961) and that the
follicle is important in eruption. Damage to the follicle
was the most reliable predictor of failed eruption in a
transplantation study (Kristerson and Andreasen,
1984). Formation of bone below erupting teeth was
noted in an autoradiographic study of tooth eruption in
two rhesus monkeys by Kenney and Ramfiord
(1969a,b). Schroeder et al. (1992) have recently de-
scribed tooth eruption in four monkeys that received
fluorescent and/or radioactive labels. This study corre-
lated radiographic, microradiographic, autoradio-
graphic, and histologic perspectives on root and bone
growth of erupting multirooted molars and premolars
in these animals. Among their key observations are the
high levels of bone formation around erupting teeth,
seen most prominently in interradicular areas and a t
the alveolar crest (Fig. 131, and the reciprocal interac-
tions of root formation and bone formation at the root
apex (Fig. 14). In periods of rapid root growth, bone
formation occurs primarily in furcation areas. Bone
growth in the apical region occurs only if root growth is
not fast enough to keep up with eruption. Most teeth in
primates exhibit changes in orientation of their long
axis. This is established during development and main-
tained in eruption by a flexible asymmetry of bone
formation, most prominent in furcations (Fig. 15).
These studies show that a plastic asymmetry of bone
formation occurs during tooth eruption and suggest
that the primary determinant of both the direction and
rate of tooth eruption is the rate of formation of the
eruption pathway and its coordination with bone for-
mation in selected areas of the crypt and the alveolar
crest.
Root Growth
Roots begin to form early in eruption, and, as Carl-
son (1944) has demonstrated for human premolars,
their initial projection from the crown can cause re-
sorption of bone a t the base of the crypt. Much has been
published about root growth and the high rate of peri-
odontal ligament turnover during incisor and molar
eruption in rodents (Melcher and Correia, 1971; Ten
Cate, 1971; Beertsen et al., 1974; Pitaru et al., 1976;
Sodek, 1978; Perera and Tonge, 1981a,b; Beertsen and
382 S.C. MARKS, JR.AND H.E. SCHROEDER

Fig. 7. Electron micrograph of osteoclasts (0)on the bony (B)crypt surface of an erupting dog premolar.
The largest osteoclast is surrounded by five (numbered)mononuclear cells, each of which has the dense-
core vesicles found in osteoclasts and their precursors. OC, osteocyte. x 4500. (Reproducedfrom Wise et
al., 1985, with permission of the publisher.)

Hoeben, 1987). We suggest that these activities are
likely related more to providing support for and accom-
modating root growth of a rapidly erupting, functional
tooth, in the case of the incisor, and to occlusal pres-
sures on the molar ridge prior to eruption than to the
mechanisms of eruption per se. While the demonstra-
tions that rootless teeth erupt (Gowgiel, 1961; Marks
and Cahill, 1984; Carl and Wood, 1980) mean that root
formation doesnt cause eruption, formation of the root
during the intraosseous stage is an energetically expe-
dient effect of eruption. The recent quantitation of root
growth in a fluorochrome-labelled monkey (Bosshardt
et al., 1989) has shown that roots grow faster in pri-
mary than in permanent teeth, that growth is greatest
early in root formation, and that the dentin formation
rate varies considerably in different regions of a tooth
during root formation. Thus, the space for an erupting
tooth is accomplished by bone resorption, and move-
ment into that space is produced by a reciprocating
collaboration of root growth and adjacent bone forma-
tion. When root growth equals the rate of formation of
the eruption pathway (EP) and that of interradicular
bone apposition, no bone is formed in the fundus of the
crypt (example: molars). When root growth exceeds EP
formation, basal bone is resorbed accommodatingly,
and when root growth is less than EP formation bone is
formed in the fundus (example: canines). These scenar-
ios can occur episodically during eruption of a single
 TOOTH ERUPTION 383

Fig. 8. Radiographsof alveolar bone before (a)and after (b)removal
of the third premolar (P)crown with preservation of the dental follicle
at 15 (pre-and postoperativein panels a and b, respectively),17 (c),19
(d), and 21 (e) weeks. Formation of an eruption pathway occurred
even without a crown, and a radiolucent space (asterisks) moved oc-
clusalward with resorption of the roots of the overlying deciduous
premolar. x 1.9. f: A histologic section of the mandible at 19 weeks
after removal of the third permanent premolar crown but retention of
the dental follicle. Notice formation of an eruption pathway (EP) be-
tween the mots (1,2) of the deciduous precursor and the projection of
new alveolar bone trabeculae (T)from the base of the crypt. Remnants
of the dental follicle have proliferated to form cords and cysts (arrow-
heads) in the area formerly occupied by the crown. MC, mandibular
canal. Haematoxylin and eosin. x8. (Reproduced from Marks and
Cahill, 1984, with permission of the publisher.)

tooth, or they can characterize the interplay of root are continued and coordinated by the dental follicle
growth and basal bone during eruption. These recipro- through local signals which involve proteins and
cal variabilities of bone resorption, bone formation, and growth factors made in the follicle or adjacent tissues.
root growth provide for different rates of eruption for a
MUCOSAL PENETRATION AND
single tooth. PREOCCLUSAL ERUPTION
These studies of the intraosseous stage of tooth erup-
tion show that this phase is characterized by a trans- Formation of the eruption pathway is completed soon
location of the tooth through the developing alveolus after the cusps reach the alveolar crest, and at this
by a coordinated resorption and formation of bone, that point the rate of eruption accelerates. As an erupting
this process can be plastic and asymmetrical to accom- tooth approaches the surface epithelium, there is thick-
modate root growth and tooth drift, and that these met- ening and transformation of the enamel epithelium
abolic events likely begin in the enamel epithelia and and fusion with the oral epithelium. These processes
384 S.C. MARKS, JR.AND H.E. SCHROEDER

Fig. 9. Radiographs of the eruption and loss of a metal replica of a third permanent premolar crown
placed within a dental follicle at 15 weeks (a) and followed for 1 (b),2 (c), 4 (d), 5 (e), 6 (n, and 7 (g)
weeks. Notice formation of the eruption pathway (asterisk) and occlusal movement of the metal replica
with time. x 1.9. h A clinical photograph of the erupting metal crown replica (arrowhead)at 21 weeks,
corresponding to panel f. x 1.9. (Reproduced from Marks and Cahill, 1984, with permission of the pub-
lisher.)

are accomplished by proliferation of the outer enamel
epithelium and via local proteolytic activity (Toto and
Sicher, 1966). Release of enamel matrix proteins just
prior to and during the period of mucosal penetration is
believed to be the basis for a local hypersensitivity re-
action which underlies the frequent clinical signs (local
erythema, rhinitis, fever) of eruption (Pierce et al.,
1986). A major accomplishment of mucosal penetration
is formation of the junctional epithelium on the tooth
surface. This unique epithelial attachment to a miner-
alized surface is initially a derivative of the enamel
epithelia (Schroeder and Listgarten, 1977), and it is
continually renewed apically over the tooth surface
during eruption (Marks et al., 1994). Otherwise, very
little is known about this stage.
Preocclusal eruption from gingival emergence to the
occlusal plane is accomplished by root growth and for-
mation of bone at the base of the crypt and/or the in-
terradicular septa. Because the alveolar process is still
growing and the alveolar crest extends in height dur-
ing this phase, an erupting tooth eventually has to
overtake this alveolar growth to continue its eruption.
Proffit and colleagues (1991) have used a high resolu-
tion video microscope to show that human premolars
move from gingival emergence to the occlusal plane at
rates up to 75 p,m per day.
ERUPTION AT THE OCCLUSAL PLANE
Once the occlusal plane is approached, tooth eruption
slows dramatically but continues a t a slow pace
through the fifth decade of life (Carlson, 1944; Darling
and Levers, 1976; Ainamo and Talari, 1976). Initial
events after reaching the occlusal plane are directed at
increasing support for this new position. These include
formation of circumferential buttressing bone (i.e., al-
veolar bone proper), producing the lamina dura of
dental radiographs, and maturation of fibers of the
periodontal ligament. During this period root forma-
tion is completed a t the expense of basal bone for those
teeth with a relatively short eruption distance. How-
ever, we lack information on the mechanisms of final
shifting and drift in the horizontal plane by which an
incisor or molar is brought into its position within the
dental arch. Possibly resorption and formation of bone
on opposite sites of the apical walls of the alveolus and
rapid deposition of cellular cementum at respective
sites of the apical root could act synergistically to move
the crown in the vesibulo-oral direction.
Teeth continue to erupt through later decades, and
occlusal wear may be in part compensated for by ce-
mental apposition. The position of the alveolar crest in
relation to the tooth appears to remain constant, al-
 TOOTH ERUPTION
Fig. 10. A An anteroposterior section of an erupted premolar in
which both root growth zones were destroyed surgically at the begin-
ning of root elongation (16 weeks). ES, enamel space; ODB, odonto-
blast; OSD, osteodentin;T, trabecular bone; 3P, third premolar. B: An
anteroposterior section of an erupting premolar in which the posterior
root growth zone was destroyed surgically 5 weeks earlier. The unop-
erated anterior root developed normally. The area between the broken
though the occurrence of the periodontal diseases has
made extrapolations from modern and ancient skeletal
remains difficult (Whittaker, 1985; Levers and Dar-
ling, 1983; Murphy, 1959; Danenberg et al., 1991).
Even when occlusal wear is limited, continued bodily,
occlusal movement of teeth occurs as a result of an
increase in height of the alveolar process causing an
increase in anterior facial height (Mazeland, 1980a,b;
Ainamo and Talari, 1976) through the fifth decade.
Loss of antagonists increases the eruption rate of a
tooth, and this is believed to result largely from appo-
sition of apical cementum and bodily movements of the
tooth and adjacent periodontium (Compagnon and
Woda, 1991; Anneroth and Ericsson, 1967).
SPEEDS OF TOOTH ERUPTION
The speed of tooth eruption has several characteris-
tics (see Table 1). First, eruption itself has to proceed a t
a certain speed overall to move a tooth into its func-
tional position on schedule. Prolonged delays can pre-
vent eruption and result in ankylosis of tooth to bone.
Second, the eruption speed is not uniform. Erupting
teeth move a t different speeds a t different times. Ini-
tially, eruption is slow within bone; it increases there-
385
lines, the usual position of the posterior root, is almost completely
occupied by trabecular bone. Eruption rate was unaltered. These pho-
tographs demonstrate that growth of one or both roots is not needed
for timely tooth eruption and that their place is taken by expansions
of the newly formed interradicular bone which keeps the crown on its
eruption schedule (large arrows). x 10. (Reproduced from Cahill and
Marks, 1980, with permission of the publisher.)
after but becomes very slow as the tooth approaches the
occlusal plane. These remarkable shifts in speed are
also seen in root formation, which is fast at first, slows
as the apical foramen narrows, and is very slow there-
after. Third, this implies that bone resorption and for-
mation like root growth must occur a t a variety of
speeds depending upon the stage of eruption. Fourth,
during intraosseous eruption the rate of bone (and root)
resorption determines the rate of eruption. Once the
tooth leaves the intraosseous stage, the speed of erup-
tion depends upon the rate of bone apposition and/or
root elongation. Intraosseous eruption proceeds at a
rate of 1-10 pmlday depending upon the tooth, and this
represents the maximal rate of resorption of bone
(Parfitt, 1984). Thereafter the rate can increase up to
75 p d d a y (Proffit et al., 1991). But there are discrep-
ancies between these data and documented ectopic
eruptions of mandibular premolars-that is, migra-
tions (Sutton, 1968; Orton and McDonald, 1986; Loh,
1988) which can move within bone a t up to 19 pdday.
This elevated rate might be explained by the fact that
these migrating teeth moved largely through cancel-
lous bone, not denser cortical bone or tooth roots.
While it is not clear what specifically causes eruption
386 S.C. MARKS, JR.AND H.E. SCHROEDER

t bone resorption

t recruitment

, - CSF-1

, positive
feedback

TGF- p Upregulates

Upregulates

Fig. 11. A Antibodies to the sialoprotein of 95,000 relative molec-

ular weight (DF-95)in the dog premolar follicle are localized in the EGF IL- la
enamel organ (EO),not the true dental follicle (DF), of this tooth.
Production,characterization,and use of antibodiesto DF-95 havebeen
described (Gorski et al., 1994). B Lack of staining of an adjacent
8 I
section of the dental follicle treated with preimmune serum indicates
specificity of the localization in A. X 65. Fig. 12.Hypothetical diagram of the potential interactions of some
cellular and molecular events known to be related to formation of the
eruption pathway during tooth eruption. The accuracy of these as-
sumptions is presently being tested in vivo.
to begin, rates to change, and eruption to slow dramat-
ically a t the occlusal plane, there is considerable infor-
mation about parts of these processes derived from
studies in a number of species. We believe that a syn- developing tooth through bone by a coordinated bone
thesis of these data into working hypotheses about metabolism, resorption in the direction of eruption, and
eruption can be of biological and clinical benefit, stim- formation in the opposite direction. Root growth starts
ulating further investigations. before active eruption. Teeth are moved into the erup-
tion pathway by bone formation which is most easily
BASIC PRINCIPLES OF TOOTH ERUPTION seen in the furcation areas of multirooted teeth. Bone
Active tooth eruption begins in an intraosseous en- formation in the alveolar fundus next to growing root
vironment. It requires formation of an eruption path- tips occurs only when root growth does not keep pace
way by osteoclasts, and the direction in which this with eruption. Like bone resorption, alveolar bone for-
pathway is formed will determine the direction of mation associated with tooth eruption depends upon
crown eruption, a t least initially. Single-rooted ante- the dental follicle and is associated with high cell pro-
rior teeth erupt along the path of the gubernacular liferation. Bone resorption and bone and root formation
canal, the small channel that connects the bony crypt during eruption are coordinated but are not necessarily
surrounding the tooth to the oral surface of the alveo- tightly synchronized. Because the alveolar process it-
lus. Eruption pathway formation requires bone resorp- self grows during tooth eruption, bone formation a t the
tion which is regulated by the dental follicle, and suc- alveolar crest is generally equalled and eventually sur-
cessful tooth eruption depends upon its timely, passed by that in the alveolar fundus and/or between
bilateral occurrence. The cellular events in the follicle the roots.
related to resorption occur after the crown is formed Thus, the intraosseous stage of tooth eruption in-
and involve some signal(s) from the enamel epithe- volves bone resorption to form an eruption pathway
lium. Likely mediators include matrix metalloprotein- and interradicular bone formation, root growth, and
ases, interleukin-1, epidermal growth factor-1, and un- fundic bone apposition which move the erupting tooth
defined proteins in the enamel organ and the dental into the eruption pathway. These events are regulated
follicle. by the dental follicle which develops regions to initiate
Tooth eruption is essentially the translocation of a and control bone formation, regions to initiate and con-
 Fig. 13. Microradiographs (a,c) of bucco-lingual (a,b) and mesio-
distal (c,d) ground sections of the right (a,b)and leR (c,d)maxillary
jaws of a 13-month-old M. fasciculuris monkey, with the plane of
sectioning running bucco-lingually through the palatine root (a,b)
and, mesio-distally,through the center of the first permanent molar
(MI) (c,d). The furcational area, the bottom wall of the alveolus, and
the mesial (upperinset) and palatal (lower inset) walls of the alve-
olus are shown as fluorescent micrographs in the insets. The first
permanent molar is still largely intraosseous, and its roots are devel-
oped to about one-third of their final length. Note major bone appo-
sition in the furcational septum (arrowheads), distally to the first
permanent molar and a t the crest of the alveolar process (arrows). a , b
x9. c,d x7. Insets: x 13. (Reproduced from Schroeder et al., 1992,
with permission of the redactory board.)
388 S.C. MARKS. JR. AND H.E. SCHROEDER

Fig. 14. Microradiographs (a,d,D of bucco-lingual (b)and mesio-
distal (e) ground sections and correspondingradioautographs (c,g)of
the right (a-d) and left (e-g) second mandibular premolar (PJ, of a 45-
(a-d) and a 44- (e-g) month-old M.fasciculuris monkey, respectively,
with the plane of sectioning running bucco-lingually through the fur-
cation (a,b) and the distal root (d) and, mesio-distally, through the
center (e-g) of these premolars. The latter are still intraosseous, with
roots developed to about one-third ( a 4 or 90% (e-g) of their final
length. Note that bone apposition and the respective 3H-proline in-
corporation(arrowheads) is mainly in the furcational region (a-c, e-g)
and less equator (f). mz, second deciduous molar. a,b,d x 7.5.e,E x 6.
g: x 4. (Reproducedfrom Schroeder et al., 1992, with permission of the
redactory board.)
 TOOTH ERUPTION 389

Fig. 15. Mesio-distal (a)and bucco-oral (d)ground sections and cor-
responding microradiographs (b,e) and autoradiographs (c,O of the
right maxillary first (PI)and second premolars (P,) ( a 4 of the right
second premolar (P2, d-f) of a 45- (d-f) and a 44- ( a 4 month-old M.
fascicularis monkey, respectively, with the plane of sectioning run-
ning through the center of these teeth. The latter are still in-
traosseous, with roots developed to 50-90% of their final length. Note
that bone apposition and the respective 3H-proline activity (arrow-
heads) occur mainly at the distal ( a 4 and furcational (d-e) aspects of
the premolar roots and less so or none a t the alveolar fundus. a,b: x 6.
d,e: x 7.5. c,E x 4. (Reproducedfrom Schroeder et al., 1992, with per-
mission of the redactory board.)
390 S.C. MARKS, JR.AND H.E. SCHROEDER

TABLE 1. Daily rate of tooth eruption and of intraosseous migration of human teeth in comparison to that of
bone remodeling and root growth elogation'
Intraosseous Extraalveolar Postocclusion
Literature Year Method used Type of teeth rate (pdday) rate (pdday) rate
Carison ~ 1944 Radiographs 31/41 1.0-3.1 10.0-17.5
33/43 2.6-4.3 14.5-20.5
34/44 3.3-5.6 9.7-12.3
35/45 2.6-3.3 12.4-41.6
36/46 6.0-10.0 6.0-10.0
Burke 1954 Radiographs 21 - 17-39
Burke and Newel1 1958 Clinical photography 11/21 40-73
Burke 1963 Clinical plaster models 11/21 28-34
Siersbaek-Nielsen 1971 Radiographs 11/21 -
(Implants) 31/41 -
Berkovitz and Bass 1976 Clinical plaster models 18/28 8-17
Smith 1980 Clinical plaster models 13/23 11.4
33/43 14.3
34/44 15.7
35/45 - 24.3
Profit et al. 1991 Video imaging system 15/25 - 25-75
Sutton 1968 Radiographs 35 15 (migration) -
Orton and McDonald 1986 Radiographs 45 12-19 (migration) -
Loh 1988 Radiographs 45 7 (migration) -
Sissons 1971 Bone apposition 1.4-2.1 -
Parfitt 1984 Bone apposition 1.0-3.0 -
Bone resorption 5.0-10.0 -
Schroeder et al. 1992 Fluorochrome Bone apposition - 15-22
(M. fascicularis) (Interradicular)
Bosshardt et al. 1989 Fluorochrome Root growth, 10-36
elongation
( M . fascicularisl
'Taken from Schroeder (1991).

trol bone resorption, and areas which remain neutral.
Where these regions develop in a particular follicle will
determine the direction of tooth eruption, when they
develop will determine the time of eruption, and how
they are synchronized will determine whether there
will be complications.
In conclusion, we suggest that the basic principles of
tooth eruption are as follows:
1. Any region of a dental follicle has the potential for
initiating and regulating bone resorption and bone for-
mation or for not influencing bone metabolism. Thus,
ectopic eruption is easily explained by aberrant activa-
tion in the follicle. We know little about these regional
properties of the dental follicle, and they hold the key
to changing the direction and rates of eruption, clini-
cally. Most experimental data about the role of the den-
tal follicle have come from studies of dog premolars.
These teeth move in a single direction with little me-
sial drift and are surrounded by a unidirectional polar-
ization of bone resorption and formation that depend
upon adjacent parts of the dental follicle. The rather
uncomplicated movement of these teeth should not un-
necessarily restrict the application of data derived from
them.
2. Movement of teeth during eruption consists of
preparing a path through bone or soft tissues and mov-
ing them along this path. The pathway is prepared by
resorption of bone and roots of primary teeth and re-
moval of soft tissues including epithelial penetration.
Teeth are moved into these spaces by bone formation
which occurs apical to an erupting crown and can ac-
commodate the growth of roots. Formation of the erup-
tion pathway is the rate-limiting step as revealed by
rapid catch-up eruption of temporarily impacted teeth,
accelerated eruption with early formation of a pathway
following CSF-1 administration, and failure of erup-
tion when an eruption pathway is not formed.
3. Root formation is accommodated during tooth
eruption and is a consequence, not a cause, of the pro-
cess.
4. Bone formation and root formation move an
erupting tooth through the oral epithelium and into its
position within the dental arch a t the occlusal plane. In
the latter part of and after eruption, the periodontal
ligament forms and is reorganized. This accounts for its
high turnover rate. It is unlikely that the periodontal
ligament contributes substantially to eruption but may
have a role late in the process. It certainly contributes
to the stability of the functioning tooth. Bone formation
and possibly formation of apical cementum maintain a
slow eruptive movement throughout the life of the
tooth.
In summary, the key to the successful clinical man-
agement of tooth eruption consists of understanding
that this process consists largely of the local regulation
of alveolar bone metabolism to produce resorption in
the direction of eruption and shift and formation of
bone a t the opposite site. Our ability to selectively and
discretely affect these processes a t present is limited
and includes the local stimulation of resorption by ex-
traction of a primary tooth or surgical removal of bone
and assisting mucosal penetration by incising the gin-
 TOOTH ERUPTION 391
giva. More comprehensive analyses of the molecular Carl, W., and R. Wood 1980 Effects of radiation on the developing
mediators of eruption will certainly increase clinical dentition and supporting bone. J. Am. Dent. Assoc., 101:646-648.
Carlson, H. 1944 Studies on the rate and amount of eruption of certain
options in the near future. human teeth. Am. J. Orthodont. Oral Surg., 30.575-588.
Cielinski, M., M. Jolie, G. Wise, and S.C. Marks, Jr. 1994 Colony-
ACKNOWLEDGMENTS stimulating factor-1 (CSF-1)is a potent stimulator of tooth erup-
tion in the rat. In: Proceedings of the International Conferenceon
The authors work reported in this review has been Biological Mechanisms of Tooth Eruption, Resorption and Re-
supported by grants from the National Institutes of placement by Implants. 2. Davidovitch, ed., EBSCO Press, Bir-
Health (DE05996 and DE07444). It is a pleasure to Cohen, mingham, AL. pp. 429-436.
S. 1962 Isolation of a mouse submaxillary gland protein ac-
thank Drs. D. Bosshardt, D. Cahill, M. Cielinski, J. celerating incisor eruption and eyelid opening in the newborn
Gorski, H.-U. Luder, and G. Wise for their significant animal. J. Biol. Chem., 237:1555-1562.
contributions to this work. Compagnon, D., and A. Woda 1991 Supraeruption of the unopposed
maxillary first molar. J. Prosthet. Dent., 66:29-34.
Danenberg, P.J., R.S. Hirsch, N.G. Clarke, P.I. Leppard, and L.C.
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Beertsen, W., V. Everts, and A. Van Den Hooff 1974 Fine structure of Den Besten, P.K., L.M. Hefferman, B.V. Treadwell, and B.J. Awbrey
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Bosshardt. D.. H.U. Luder. and H.E. Schroeder 1989 Rate and growth follicle during tooth eruption. Connect. Tissue Res., 18:175-190.
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