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Periodontology 2000, Vol. 74, 2017, 140–157 © 2017 John Wiley & Sons A/S.

ley & Sons A/S. Published by John Wiley & Sons Ltd
Printed in Singapore. All rights reserved PERIODONTOLOGY 2000

Effect of orthodontic treatment


on the periodontal tissues
J O S E P H S. A N T O U N , L I M E I , K E L S I G I B B S & M A U R O F A R E L L A

An increasing number of adult patients are seeking The envelope of tooth movement
orthodontic treatment, many of whom are likely to
Moving teeth with orthodontic appliances is not with-
have some degree of periodontal disease (21). A
out limits. Several factors may influence the extent
reduction in periodontal support can be associated
(and stability) of orthodontic tooth movement, includ-
with labial flaring, extrusion, rotation, spacing and
ing the anatomy of the alveolar bone, pressures
drifting of the teeth (150). Such changes are believed
exerted by soft tissues, periodontal tissue attachment
to occur when the periodontal ligament is no longer
levels, neuromuscular forces and lip–tooth relation-
able to stabilize the teeth against external forces
ships (2, 110). It is commonly believed that the limits
(110). Maxillary incisors are particularly susceptible to
of tooth movement are defined by strict physiologic
pathological migration and over-eruption (25). These
and anatomic boundaries, which, if violated, can
acquired occlusal changes, along with any underlying
result in reduced periodontal and alveolar bone sup-
skeletal discrepancy, often result in a complex mal-
port. Accordingly, large movements of teeth beyond
occlusion that necessitates an interdisciplinary treat-
this so-called ‘envelope of discrepancy’ (Fig. 1) are
ment approach (30, 63).
only possible if favorable remodeling of the facial
Periodontal disease is not necessarily a contraindi-
skeleton is achieved or by orthognathic surgery (112).
cation to orthodontic treatment provided that the
It is unclear, however, how far these boundaries can
condition has been stabilized; however, loss of alveo-
be pushed before the health of the surrounding tissues
lar bone and soft-tissue architecture may pose con-
becomes adversely affected. This clinical dilemma is
siderable challenges to oral rehabilitation. It has been
particularly evident in borderline extraction cases with
suggested that adjunct orthodontic treatment may
reduced periodontal support. There is some anecdotal
play an important role in developing the optimal base
evidence to suggest that adult patients with severe
needed for re-establishing an esthetic and functional
crowding of the teeth and a reduced periodontium
dentition in these cases (86). Orthodontic extrusion of
may be successfully treated by moving the teeth
unrestorable teeth, for instance, may assist the peri-
beyond the envelope of the alveolar process, albeit
odontist and restorative team in harnessing alveolar
using well-controlled force systems (9). One likely rea-
bone and improving the soft-tissue architecture (150).
son for such favorable outcomes is variability in tissue
This adjunct treatment is particularly useful for
response to different treatment mechanics.
patients who require dental implants in esthetic
zones (71, 78).
Orthodontic therapy may also have detrimental
Tissue response to orthodontic forces
effects, including root resorption (11, 73) and bone
dehiscence (44). The introduction of fixed orthodon- When orthodontic forces are applied to teeth, both
tic appliances into the oral cavity also increases the compressive and tensile stresses develop in the sur-
amount of acidogenic biofilm, thus increasing the risk rounding tissues (134). Areas under tension have clas-
of gingivitis and caries (62, 149, 152). A critical issue in sically been described as sites of bone apposition,
the treatment planning of any patient revolves while those under compression undergo bone resorp-
around how much orthodontic movement the peri- tion. The net effect of this remodeling process is the
odontium can tolerate before it becomes adversely movement of teeth along the direction of the applied
affected. force and into the space created by the recently

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Response of periodontal tissues to orthodontic treatment

directly at the alveolar–periodontal ligament interface


Buccal
Palatal on the compression side, while bone apposition occurs
A TRANSVERSE on the tension side and on the external surface of the
alveolar process (85, 86). The net outcome of this near-
simultaneous process is the movement of a tooth
beyond its original alveolar boundary (84).
Lingual Labial
Orthodontists have long been aware of the relation-
B SAGITTAL
ship between force magnitude and the type of resorp-
tion that occurs on the pressure side ever since Carl
Sandstedt’s classical experiments on dogs in the early
1900s (16, 132, 133). Interestingly, in some experi-
Orthodontics Only
Orthodontics + Orthopedics
ments on Beagle dogs, the use of light forces did not
Orthodontics + Surgery seem to prevent hyalinization of the periodontal liga-
ment in the initial stages (155, 156) or influence the
Fig. 1. Conceptual illustration of the ‘envelope of discrep- rate of tooth movement (106). The use of light force
ancy’. Colored polygons represent the biologic boundaries
systems, however, may still prevent further hyaliniza-
of tooth movement for orthodontic treatment only (green
zone), orthodontic treatment and dentofacial orthopedics tion from occurring after the initial period of tooth
(blue zone) and orthodontic treatment and orthognathic movement (120).
surgery (red zone). (A) Transverse tooth envelope for max- The idea that orthodontic forces may contribute to a
illary posterior teeth. (B) Sagittal tooth envelope for differential tissue response in humans is rather appeal-
mandibular anterior teeth. Modified from Graber et al.
ing. From a clinical point of view, it provides clinicians
(49).
with a useful set of tools for the management of adult
patients with reduced periodontal support. Movement
resorbed bone. It has recently been demonstrated, of teeth through bone, for example, may be desirable in
however, that the distribution of compressive and cases where the clinician is interested in extruding a
tensile strains in the periodontal tissues is more com- root-fractured tooth without the accompanying bone
plex than initially believed (27). Findings from experi- (86). On the other hand, movement of teeth with bone
ments in Beagle dogs indicate that different sections may help augment bone as teeth are moved into sites
of the periodontal ligament on the compression side with atrophic alveolar ridges (86).
may appear either normal or disorganized (156). To The purpose of the present review article was there-
complicate matters further, small patches of hyalin- fore to evaluate the clinical effects of various orthodon-
ization are also reported to occur at tooth surfaces tic tooth movements on the surrounding hard and soft
that are not normally under compression (156). tissues. Another objective was to identify important
The magnitude of the applied force is believed to patient and treatment-related factors that may influ-
play a role in determining the pattern of stresses and ence the response of the periodontal tissue to specific
strains in the dento-alveolar tissues. It has also been orthodontic treatments. Different types of orthodontic
suggested that different force systems may determine movements are discussed, including expansion, extru-
whether a tooth will move ‘through’ bone or ‘with’ sion, intrusion and the movement of teeth into edentu-
bone (84–86). A tooth is thought to move through bone lous sites with limited alveolar bone.
when undermining resorption, rather than frontal
resorption, occurs in response to heavy orthodontic
forces (84). Such forces cause constriction of the Orthodontic space closure
microvasculature and localized necrotic areas within
the periodontal ligament (hyalinization), which are One of the most challenging clinical problems in
then removed by tartrate-resistant acid phosphatase- orthodontics is the closure of large edentulous spaces
positive macrophages and multinucleate giant cells with severely resorbed alveolar ridges. These situa-
migrating from adjacent bone marrow sites (16, 22). tions may arise following the loss of a deciduous
Undermining resorption is typically characterized by a tooth with no permanent successor or after extraction
delay in tooth movement because no bone apposition of an unrestorable tooth. In nongrowing patients, the
can occur on the tension side until the necrotic tissue loss of a permanent molar often leads to progressive
on the compression side has been removed (81, 132, tipping, rotation and lingual rolling of the adjacent
133). Under ideal conditions, it is thought that teeth teeth (48, 96, 147). Over time, these uncontrolled
move with their alveolus when resorption occurs tooth movements can result in scissor bites,

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Antoun et al.

nonworking side interferences, poor gingival con- the extent of bone apposition because large dehis-
tours, deepening of the bite and over-eruption of the cences may have been present. Despite these limita-
opposing teeth (1, 48, 124). Pseudopockets may also tions, two notable findings from these studies were
develop because of the bone’s tendency to follow the the slight loss of crestal bone height mesial to the
inferiorly displaced cemento–enamel junction of tooth being protracted (53) and the age-dependent
the tipped tooth (109). The orthodontic management effect on the amount of increase in alveolar bone
of lone standing molars often requires a combination width (143). With respect to the latter, new bone was
of uprighting and space closure. The uprighting of reported to follow the tooth as it moved through the
tipped teeth usually results in apical migration of the edentulous space in young growing individuals but
gingival margin and a decrease in the depth of the not necessarily in older patients (143).
periodontal pocket, which in turn helps to improve The loss of crestal bone height reported in these
plaque control and access to restorative margins (20, two studies may be related to the tipping movements
113). Once a tooth has been uprighted, space closure that occur when a tooth is moved along an arch-wire
can be carried out to help establish occlusal contacts (52). Tipping movements usually result in an unequal
and/or prepare the space for a prosthetic restoration. distribution of stresses within the periodontal liga-
There are several biomechanical and anatomic ment, with higher active forces (118) and levels of
challenges in closing long-standing edentulous compression found in the marginal tissues (119).
spaces with narrow ridges. Space closure is particu- High levels of stress also normally occur in the mar-
larly problematic in the mandible because of the den- ginal alveolar bone where the periodontal ligament
ser cortical plates (103) and greater susceptibility to inserts (85). The large stresses occurring at the mar-
ridge resorption (7). Prosthetic tooth replacements ginal tissues are likely to cause a negative remodeling
may not always be viable because of the limited process, and thus net bone loss, at these sites. It is
quantity and quality of bone available. Orthodontic noteworthy that the risk of bone loss at the alveolar
space closure may reduce costs for ridge augmenta- crest from excessive tipping movements may be
tion and placement of implant-supported restora- higher in adults (120). The benefits of closing edentu-
tions (131). Despite these potential benefits, most lous spaces in patients with significant vertical bone
orthodontists are often reluctant to close large eden- loss should therefore be considered in light of these
tulous spaces (50, 61) because of the risk of localized potential risks. If space closure is necessary, bodily
gingival dehiscence, poor root parallelism, incom- movement of teeth may help to reduce these
plete space closure, increased treatment duration, unwanted effects at the marginal tissues (119).
and relapse (53, 131). Reopening or incomplete The findings from these two human studies suggest
closure of these spaces can lead to further periodon- that bone apposition is possible under the correct cir-
tal breakdown if they result in open interproximal cumstances. Some factors that may favor bone for-
contacts and food traps. In spite of these concerns, mation include the magnitude of the applied force
only a few case reports and retrospective studies have and, accordingly, the level of strain in the surround-
evaluated the effects of space closure on the adjacent ing tissues. According to Frost’s ‘mechanostat’ theory,
periodontal soft tissues and alveolar bone. Most of both low and excessive bone strains can cause
these case reports have described complete or near- osteopenia and bone loss. On the other hand, strain
complete space closure in the posterior mandible, levels in the range of 1,500–3,000 microstrains tend to
with only limited amounts of gingival recession and favor a modeling process which is associated with
loss of anterior anchorage (31, 131). Case reports, bone deposition (42, 43). The type of bone deposited
however, represent the lowest level of evidence avail- during this modeling process is thought to be depen-
able for making clinical decisions (129). dent on the amount of bone strain, with higher levels
Two retrospective human studies have investigated resulting in the formation of woven bone (23). It is
the effect of space closure and found clinically signifi- noteworthy that those strain thresholds are not uni-
cant reductions in posterior space and moderate form between either individuals or bones (141).
increases in the width of the alveolar ridge (53, 143). Recent advancements in the fields of orthodontics
Both studies used small convenience samples and did and periodontics have had a large impact on the
not report on any quantitative measurements of gin- management of edentulous atrophic ridges. Skeletal
gival recession or attachment loss. In addition, the anchorage has been useful for uprighting tipped teeth
thickness of the buccolingual bone around the test (115), facilitating bodily tooth movements during
teeth was assessed directly from the post-treatment space closure and reinforcing anchorage (57). The risk
study casts, which provided little information about of anchorage loss is particularly high in patients with

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Response of periodontal tissues to orthodontic treatment

reduced periodontal support. The relatively apical four Rhesus monkeys and the effect of tooth move-
position of miniscrews is also useful for applying ment into these defects was investigated (107). Histo-
orthodontic forces closer to a tooth’s center of resis- logic findings from that study showed the potential
tance, thus reducing the likelihood of unwanted tip- for complete resolution of these defects in the pres-
ping movements (57). Despite the potential ence of reduced, but healthy, periodontal tissues.
advantages of skeletal anchorage systems, there is still These results are consistent with the findings of some
a lack of high-quality evidence regarding their clinical studies (95, 154) but not of others (29). Using a rat
efficacy. Another important development has been model, Vardimon et al. (154) performed a histomor-
the application of periodontal regeneration therapies phometric analysis on 62 decalcified hemimaxillary
during orthodontic treatment. The clinical outcomes blocks following the movement of teeth into surgi-
of this combined approach are promising, with cally created bony defects. Although a 6.5-fold
increased connective tissue attachment levels increase in the total area of bone apposition was
reported in selected cases (94). A recent review of the reported in the experimental group, this increase was
literature, however, identified significant method- not statistically significant. Another similar study in
ological heterogeneity and a lack of high-quality stud- dogs found no changes in the level of connective tis-
ies in this area (116). Encouragingly, the use of bone sue attachment and the extent of epithelial migration
substitutes to treat localized periodontal defects and following the movement of roots into surgically cre-
augment atrophied alveolar ridges does not seem to ated defects, although coronal bone apposition was
have an adverse effect on orthodontic tooth move- significantly reduced in the experimental group (29).
ment in animals (136). The potential for those techni- Unfortunately, it is difficult to make meaningful com-
ques to improve the efficacy of orthodontic space parisons between these studies because of method-
closure in patients with reduced alveolar bone sup- ological differences in the type of animals used, the
port requires further investigation. size of surgical defect, the type of tooth movement
performed and retention periods. One common fea-
ture of these studies, however, was the large individ-
Considerations for tipped teeth with
ual variation reported in the experimental group (29,
infrabony defects
154). This increased variability is likely to reflect dif-
Infrabony pockets are often associated with peri- ferences in the regenerative capacity of the periodon-
odontally compromised teeth or severely tipped teeth tal tissues following the movement of teeth into
adjacent to edentulous spans. Some authors have osseous defects. The findings of these studies should
warned that orthodontic movements can aggravate also be interpreted with caution because experimen-
the periodontal issues and lead to widening of the tally induced osseous defects in animals may not
defect (61). An important consideration in these treat- completely resemble those found in humans (154).
ments is therefore the response of infrabony pockets Osseous defects are usually created in animals using
to orthodontic tooth movement. traumatic surgical techniques, whereas those found
The response of periodontal tissues to orthodontic in humans are a result of chronic pathological pro-
tooth movement has been investigated in dogs with cesses. On the other hand, animal models are ideal
poor oral hygiene and experimentally induced infra- for investigating attachment-level changes using his-
bony pockets (163). In contrast to the maxillary tologic techniques (87). For obvious ethical consider-
control teeth, bodily movement of the mandibular ations these ‘gold standard’ analytic techniques are
test teeth resulted in a significant increase in pocket seldom possible in human samples. Interestingly, one
depth and loss of connective tissue attachment, espe- human study involved the removal of teeth in block
cially when the teeth were moved toward the infra- sections following molar uprighting, although no sub-
bony defects. One probable reason for the continued sequent histologic analysis was reported (20). It is
destruction of the periodontal tissues and the persis- noteworthy, however, that uprighted molars in that
tence of infrabony pockets in these situations is the study showed a 2.5 mm clinical reduction in pocket
apical displacement of the adjacent supragingival depth in comparison with controls. This reduction,
plaque into subgingival sites (38). however, may be the result of recession, rather than
Other studies, however, have reported improved gain in attachment. An important clinical implication
healing of infrabony defects when good oral-hygiene from both animal and human studies is the need to
measures were implemented. In a similar study to maintain healthy periodontal tissues throughout the
that of Wennstro € m et al. (160), infrabony pockets process of uprighting and space closure. Regular
were experimentally produced around the incisors of monitoring of oral health should therefore be carried

143
Antoun et al.

out throughout the course of orthodontic treatment molars may result in significant ridge resorption and
(117). vertical bone defects, prohibiting the placement of
dental implants in an optimal position (69). Instead, a
dental implant may be placed at the site of the first
Considerations for dental implants
premolar tooth after it has been distalized into the sec-
Space closure can often be challenging in patients ond premolar space (69, 140). An important considera-
with severe Class II or Class III malocclusions unless tion in these situations is the potential effects of
the underlying skeletal discrepancy is corrected. Sin- moving teeth into areas with reduced alveolar bone.
gle dental implants are useful in these cases provided This is a common scenario in older patients, in whom
there is adequate bone at the recipient site. Unfortu- approximately 25% reduction in the width of the alve-
nately, absence or extraction of teeth can lead to sig- olar ridge has been shown to occur during the first
nificant reductions in the width and height of the 3 years following extraction of a deciduous molar
alveolar ridge over time (145). Several methods have (100). The findings of an experimental study involving
been advocated for preparing future implant sites, Beagle dogs suggest that no change in connective tis-
including bone grafting, guided tissue regeneration sue levels occurs following the movement of teeth into
and the use of prerestorative orthodontics (140). edentulous areas with reduced bone height (75).
Strategic repositioning of teeth in the arch can
result in extensive regeneration of the alveolar bone
Summary
and supporting tissues (Figs 2 and 3). The develop-
ment of the alveolar bone using this technique may The management of large edentulous spaces is an
be particularly useful in patients with congenitally important part of oral rehabilitation. Despite the
missing lateral incisors. In these cases, the alveolar limited evidence available, sagittal movement of
ridge of the lateral incisors can be prepared for receiv- teeth into longstanding edentulous sites seems to be
ing future implants by allowing the canines to erupt a viable method for closing residual spaces and
adjacent to the central incisors and then distalizing redeveloping variable amounts of alveolar bone.
them back to their normal positions within the arch Several treatment factors may also help to reduce
(68, 140). Following treatment, bone deposition the risk of marginal tissue breakdown during space
would be expected to occur on the mesial aspect of closure, including the use of light forces, bodily
the distalized canine because this represents a site of tooth movement, absence of inflammatory peri-
tension. odontal disease and the maintenance of good oral
Use of this particular treatment protocol has been hygiene throughout treatment. Nonetheless, the risk
reported to result in adequate alveolar bone width, of gingival recession and attachment loss should be
which is relatively stable up to 4 years after treatment carefully assessed in individual patients before clos-
(67, 140). Similar findings were recently reported in a ing residual spaces.
larger retrospective study of 80 patients with 128
missing lateral incisors (98). Over the study’s 5-year
retention period, the width and height of the alveolar Orthodontic intrusion
bone were reduced by only 2% and 0.4 mm, respec-
tively. Interestingly, a recent systematic review found Orthodontic intrusion may be a useful treatment
that horizontal and vertical bone loss, 6 months after adjunct in a wide range of cases, including the
tooth extraction, were somewhere in the region of management of elongated incisors and traumatic
29–63% and 11–22%, respectively (145). Despite these deep-bite (88), and the restoration of severely worn
encouraging findings, prospective randomized con- incisors (13).
trolled trials are still needed to compare the efficacy
of this treatment modality with other types of ridge-
Intrusion of flared and elongated teeth
augmentation techniques.
A similar treatment protocol has been recom- Flaring and elongation of the incisor teeth is com-
mended for managing congenitally missing second monly seen in patients with advanced periodontal
premolars (140). Although a healthy primary tooth can disease (114, 150). One consequence of these
be expected to last for a considerable period of time, unwanted occlusal changes is the development of a
these teeth may occasionally be lost as a result of traumatic deep-bite, which can cause significant
extensive root resorption, dental caries or infraocclu- soft-tissue and hard-tissue trauma (93). In adults,
sion (17, 139). The late removal of ankylotic primary severe skeletal deep-bites are often treated using a

144
Response of periodontal tissues to orthodontic treatment

Fig. 2. Large osseous defect associ-


ated with three missing mandibular
B incisors. (A) The alveolar bone level
was at the apical third of the root of
the mandibular right lateral incisor
(tooth 42). Gingival recession was
also pronounced, especially on the
mesiobuccal aspect of that tooth. (B)
Tooth 42 was moved mesially along
the alveolar ridge using fixed appli-
ances. Both the clinical appearance
and periapical radiograph show sig-
C nificant bone formation distal to
tooth 42 (yellow arrows). (C) The
final implant-supported restoration.
Gingival inflammation around tooth
42 has resolved, with no significant
change in connective tissue attach-
ment. Clinical photographs and
intra-oral radiographs courtesy of Dr
Alberto Laino (Naples, Italy).

Fig. 3. Alveolar bone formation fol-


lowing space closure in the posterior
maxilla. (A) The maxillary right sec-
ond molar (tooth 17) was moved
mesially following removal of the
first molar. Note the limited space
available for eruption of the third
B molar and the close proximity of the
second molar roots to the maxillary
sinus. (B) Complete space closure
was accompanied by successful
eruption of the third molar and a
significant amount of bone forma-
tion distal to tooth 17. Note the
extensive remodeling of the maxil-
lary sinus floor – no clinical signs or
symptoms of a sinus perforation
were noted. Clinical photographs
and intra-oral radiographs courtesy
of Dr Alberto Laino (Naples, Italy).

joint surgical–orthodontic approach (12), although intruding elongated incisor teeth are the improve-
intrusion of the anterior teeth is also possible in ment in smile esthetics and reduction in soft-tissue
some cases (24). Two important advantages of trauma.

145
Antoun et al.

The intrusion of teeth has a number of important no change in either bony support or clinical crown
effects on the periodontal tissues (33). Bone deposi- length, although individual variability was high for
tion occurs along the stretched periodontal ligament both clinical parameters. Extrapolation of these
fibers in the middle and coronal thirds of the root results to other periodontal patients should be carried
(18). The intensity and direction of the intrusive force, out with caution, however, as the severity of pretreat-
however, seem to play an important role in influenc- ment bone loss in the sample varied greatly, with
ing the responses of these tissues. Light forces are some patients experiencing up to 60% horizontal
likely to reduce stresses in the marginal part of the bone loss, while others had virtually normal bone
periodontal ligament, while forces directed through levels. Nonetheless, these findings are consistent with
the long axis of a tooth favor bodily intrusion and another human study that used a similar intrusive
limit the extent of hyalinization (87). Force magnitude appliance and found reduced clinical crown heights
also affects the reaction of the tissues at an apical of the mandibular incisors (39). No predictors of tis-
level, with heavy intrusive forces associated with a sue response could be identified, presumably because
higher degree of root resorption (18, 33). of the limited sample size and heterogeneity of the
The clinical effects of intrusion have been exten- malocclusions and treatment effects included. How-
sively investigated in both animals and humans (18, ever, even in larger studies, no associations were
26, 33, 39, 41, 83, 87, 88). In one animal study, the use found between bone-level changes and age, gender,
of light and continuous forces resulted in pure intru- treatment time, amount of intrusion and pretreat-
sion without any loss of marginal bone (87). Follow- ment bone level (13).
ing surgical debridement, the intruded teeth in the Although orthodontic intrusion has been shown
five Macaca fascicularis monkeys had greater attach- to improve periodontal support under optimal con-
ment levels, which were attributed to coronal migra- ditions, careful consideration should still be given to
tion of the periodontal ligament cells. In teeth with some of the adverse side effects that may occur as a
poor oral hygiene, however, osteoclastic activity was result of this tooth movement, especially root
noted at the marginal bone level (87). As mentioned resorption and shortening (33, 34). Findings from
earlier, one plausible cause of the breakdown of mar- both animal models and human samples suggest
ginal tissues is the inflammatory response that occurs that force magnitude plays an important role in the
as a result of the displacement of supragingival pla- extent of tissue loss, with heavier forces associated
que below the gingival margin (38). On the other with a higher degree of root resorption (18, 33, 41,
hand, meticulous periodontal therapy during intru- 142). Interestingly, the magnitude of the intrusive
sion exposes the root surface to the periodontal liga- force seems to play a more important role in the
ment cells and increases the likelihood for connective development of root resorption than does the
tissue regeneration (88). This seems consistent with amount of tooth displacement (33). It is important
the findings of an experimental study, which found to note that other factors, such as genetic suscepti-
that teeth intruded in the presence of good oral bility and history of previous trauma, may also
hygiene had shallower pockets and relatively stable increase the risk of root resorption in some patients
marginal bone levels compared with those exposed to (160). Fortunately, most of the resorption lacunae
poor oral hygiene (83). undergo repair once the intrusive force is termi-
The effects of intrusion are not limited to the mar- nated and healing is permitted (83).
ginal tissues, with bone deposition reported on the
labial and palatal surfaces of the alveolar process and
Intrusion of worn incisors
near the root apices (18, 83). The formation of new
bone in these areas is reported to result in a small Long-term incisal wear is typically associated with
increase in the buccolingual width of the alveolar pro- over-eruption, reduction in clinical crown length,
cess. It has been hypothesized that this new bone uneven gingival margin heights and a ‘gummy’ smile
forms in response to the negative loading created by (13, 66). The gingival tissues of fractured or severely
the intrusive forces on the adjacent structures (18, worn teeth often migrate coronally if these teeth are
83). Similar findings have also been reported in a allowed to continue erupting (70). In addition to clini-
sample of deep-bite adult patients with horizontal cal crown-lengthening surgery, orthodontic intrusion
bone loss (88). In that study, following intrusion, bony may be a viable option for displacing the bone and
support increased and clinical crown length soft tissues in an apical direction. During intrusion,
decreased by approximately 7% and 1.1 mm, respec- the gingival tissues typically follow the path of the
tively. A large number of patients experienced little or teeth, although to a lesser extent (39, 92). Following

146
Response of periodontal tissues to orthodontic treatment

orthodontic treatment, however, mucogingival sur- be particularly useful is in implant site development
gery may still be needed to increase clinical crown (Fig. 4).
heights and eliminate pockets that develop from the
stretching of the gingival fibers (92).
Implant site development
The extrusion of hopeless teeth can help develop the
Summary
investing soft and hard tissues before implant place-
Several animal and human studies have investigated ment (4, 19, 166). The effect of orthodontic extrusion
the effect of orthodontic intrusion on the periodontal on the alveolar bone has been studied using various
soft tissues and alveolar bone, although direct com- animal models. In Rhesus monkeys, significant
parison between studies is generally difficult because amounts of bone apposition were found on the lin-
of differences in appliance design, force levels, oral- gual, interproximal and apical surfaces following
hygiene care and treatment durations. Of these spontaneous extrusion of the mandibular incisors
different treatment factors, the maintenance of (10). Although the distance between the cemento–
healthy gingival tissues throughout intrusion appears enamel junction and alveolar crest had slightly
to reduce the risk of marginal bone breakdown. In decreased at the three sites (by 1 mm or less), this
order to facilitate oral hygiene, surgical periodontal was considered to be minimal given that the teeth
debridement may be needed in some patients to had undergone nearly 5 mm of extrusion. These find-
reduce the depth of existing periodontal pockets. ings are consistent with those of another study in
Orthodontic intrusion may be useful for the intru- which extrusion of premolars in three Beagle dogs
sion of elongated and flared incisors, management resulted in a similar pattern of bone apposition
of traumatic deep-bites and the intrusion of over- within 2 weeks of starting treatment (138). After
erupted worn or fractured incisors. Posterior teeth 7 weeks, mature bone was found at the crestal sur-
may also be successfully intruded for receiving pros- face and the periodontal fibers had assumed a similar
thetic restorations, managing open-bites and cor- orientation to controls.
recting occlusal plane discrepancies. The decision to The effect of orthodontic extrusion on the adjacent
use intrusive forces in patients with advanced peri- tissues has been studied in Beagle dogs with a signifi-
odontal disease should take into account the risk of cantly reduced periodontium and poor oral hygiene
root resorption because this may create an unfavor- (153). Using light forces, ranging from 20 to 25 g,
able crown-to-root ratio. In these cases, light forces hemisected premolar teeth were gradually extruded
should be used in order to reduce this risk. to the point of extraction and then stabilized for a
period of 3 weeks. Following retention, new-bone
formation was radiographically and histologically
Orthodontic extrusion detected coronal to the marginal bone level, as well
as apical to the root apices. Similar findings have also
The extrusion of teeth has been advocated as an been reported in a small sample of patients in whom
effective method for managing one- and two-wall the average ratio of bone-to-tooth displacement was
infra-osseous defects (55). Numerous case reports 70% and soft tissue-to-tooth displacement was 65%
have been published to illustrate the potential bene- (4). By extruding teeth approximately 6 mm (to the
fits of tooth extrusion on the adjacent soft and hard point of extrusion), the authors were able to achieve
tissues (55, 56, 108, 144, 165). Some of these reports nearly 4 mm of bone and soft-tissue augmentation.
have found favorable effects on pre-existing peri- Interestingly, no soft-tissue migration occurred in any
odontal pockets, including a reduction in pocket of the patients with established periodontal pockets.
depth, an increased zone of attached gingiva and cre- Several characteristic soft-tissue responses have
stal bone apposition (56). Although some of these also been described when teeth are extruded to the
changes have been attributed to the regular peridon- point of extraction (77). Initially, the gingival margin
tal maintenance often implemented during treatment exhibits a red-collar appearance; pocket depth also
(55), it seems biologically reasonable that stretching tends to decrease during the extrusion process. With
of the periodontal ligament fibers would induce some continued extrusion, a nonkeratinized red patch may
bone apposition at the alveolar crest (49). Interest- appear coronal to the free gingival margin. This thin
ingly, a similar tissue response has also been tissue, which later becomes keratinized to resemble
observed when teeth are allowed to erupt naturally the surrounding gingival tissues, is formed from ever-
(99). One situation where orthodontic extrusion may sion of the pocket lining (20). It is noteworthy,

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Antoun et al.

Fig. 4. Patient with chronic periodontal disease who pre- edgewise appliance. The tooth was root filled during treat-
sented with an elongated and mobile maxillary right cen- ment, and the occlusal surface was gradually reduced as
tral incisor. A lingual retainer supported the tooth at the the tooth was extruded. (C) Periapical radiographs of tooth
time of presentation. (A) The tooth was deemed to have a 11 before treatment, during orthodontic extrusion and
poor prognosis and a decision was made to replace it with after implant placement. Note the angular bony defects
an implant, following orthodontic extrusion. Esthetics was present before treatment. Some bone apposition can be
compromised by the unfavorable shape of the tooth and seen at the crestal ridge during extrusion (yellow arrows)
gingival recession. (B) Intra-oral photographs showing and following treatment. (D) Extra- and intraoral pho-
stepwise extrusion of the tooth with a preadjusted tographs of the final implant-supported restoration.

148
Response of periodontal tissues to orthodontic treatment

however, that these tissue reactions are subject to and soft tissues. Regardless of the method used, how-
individual variation and to the intensity and extent of ever, extrusion should be carried out using light and
extrusion. controlled forces, and in the absence of deep peri-
Extrusion of teeth has a number of desirable odontal pockets (4, 166). Moreover, a short stabiliza-
effects on the position of the gingival margin, pocket tion period following extrusion is recommended to
depth and width of attached gingiva. The gingival allow the new bone to mineralize and mature (4).
margin normally follows the direction of tooth dis-
placement, but to a variable extent (4). In teeth with
Summary
deep periodontal pockets, for example, the coronal
displacement of the soft tissues lags behind that of Although most orthodontists are aware of the poten-
the hard tissues (77). In general, however, extrusion tial to develop prospective implant sites through
of teeth causes the attached fiber bundle to be dis- tooth extrusion, data on the efficacy of this technique
placed coronal to the epithelial attachment, thereby are lacking. Most of the evidence in this area origi-
inverting the periodontal pocket and reducing its nates from case series and small experimental stud-
depth (20, 77). The width of the attached gingiva also ies. Based on the evidence available, however,
increases because the free gingival margin is dis- orthodontic extrusion seems to be an effective
placed more coronal than the mucogingival margin method for developing the investing soft tissues and
(4). This clinical observation has been confirmed in alveolar bone. During orthodontic extrusion, the alve-
animal studies, which used tattoo marks as an objec- olar bone and soft tissues are displaced coronally,
tive record of the position of the mucogingival along with the cemento–enamel junction. There is
margin (10, 59). some evidence that elimination or reduction of peri-
odontal pockets, before extrusion, increases the likeli-
hood of soft-tissue migration. In general, orthodontic
Considerations for the direction of tooth extrusion may offer an effective and less-invasive
extrusion method for developing prospective implant sites,
There is some controversy regarding the ideal angle especially if orthodontic treatment is already
and direction of extrusion when preparing implant indicated.
sites. In general, teeth may either be extruded along
their long axis (4), or with progressive application of
labial root torque (166). In the presence of an angular Orthodontic expansion and incisor
defect, gradual mesiodistal tipping of the teeth proclination
toward the defect may also be considered (151). Each
method has a number of advantages and disadvan- There is an increasing trend toward nonextraction
tages. When extruding teeth with labial root torque, treatment in orthodontics (111), whereby crowding is
the marginal tissues are believed to follow the root managed by increasing the arch length. Lateral expan-
apex as it moves both buccally and coronally (166). sion of the buccal segments, and labial advancement
This scenario may be particularly useful in cases with of the incisors, can theoretically provide a variable
severely resorbed labial bone plates. On the other amount of additional space for the alignment of dis-
hand, excessive application of root torque in cases placed teeth (64, 65). Proclination and advancement
with reduced, but intact, labial plates is likely to com- of the mandibular incisors has been suggested as a
promise the integrity of the remaining buccal bone viable alternative to extractions and orthognathic
and create unwanted bony dehiscences/fenestra- surgery in adult patients with increased overjets and
tions. In such cases, it would seem more reasonable moderate-to-severe crowding (3, 89). Nonetheless,
and less destructive to extrude teeth along their long there is still some controversy regarding the risks of
axis so that the entire periodontium is displaced coro- nonextraction treatment, especially in patients with
nally. significant arch-length discrepancies. One important
Despite these theoretical considerations, there is concern is the effect of orthodontic expansion on the
still a lack of evidence supporting the use of each gingival tissues and alveolar bone.
method in different clinical situations. Future studies
are needed to evaluate and compare the efficacy of
Transverse expansion
different extrusion techniques. Until then, the deci-
sion to use one of these techniques should be based Both maxillary and mandibular arches undergo a sig-
on the amount and architecture of the existing hard nificant amount of transverse development during

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Antoun et al.

normal growth (14, 72, 76, 79). In addition to these Surgically assisted rapid maxillary expansion is
growth-related changes, arch expansion can be often used to manage transverse skeletal discrepan-
achieved using a number of orthodontic appliances, cies in adult patients. The effect of surgically assisted
including arch-wires, removable plates, fixed expan- rapid maxillary expansion on the periodontal tissues
ders and orthognathic surgery. Several animal and seems less detrimental, with minimal change in
human studies have investigated the relationship attachment levels reported (47). Nonetheless, some
between arch expansion and gingival recession, reduction in buccal alveolar bone thickness and cre-
attachment loss and bony dehiscence. The effect of stal bone level can still be expected in these patients
maxillary expansion on the thickness and height of (47). One reason for the more pronounced effects of
buccal alveolar bone has mostly been investigated conventional rapid maxillary expansion on the peri-
using clinical examination (51), computed tomogra- odontal tissues may be related to the heavy forces
phy and cone-beam computed tomography (46, 47, delivered by these appliances to the supporting peri-
128). Although these studies have mainly been limited odontium. During rapid maxillary expansion, heavy
to young patients with a healthy periodontium, their forces are usually needed to induce hyalinization of
findings provide some useful insights into the effect the periodontal ligament around the anchor teeth
of arch expansion on the periodontal tissues. and thus halt initial tooth movement (46). During this
Rapid maxillary expansion has been shown to rather slow process of undermining resorption, the
cause significant changes in alveolar bone thickness forces acting on the anchor teeth are used to expand
following treatment (46, 128). Recently, a comparison the two maxillae laterally. Once the orthopedic effect
between pre- and post-treatment spiral computed has been attained and the undermining resorption
tomography images in a small sample of adolescents process completed, the residual forces will act to
receiving rapid maxillary expansion identified several move the anchor teeth through the alveolar process
areas of bony dehiscence and a 0.6–0.9 mm reduction (46). The extent to which these teeth move will ulti-
in buccal bone plate thickness of the banded teeth mately depend on the amount of orthopedic expan-
(46). Interestingly, the presence of thinner buccal sion achieved, with more favorable and predictable
bone plates at the onset of treatment was associated outcomes usually found in growing patients (15). The
with greater changes in crestal bone levels and the heavy forces produced by rapid maxillary expansion
occurrence of a bony dehiscence following expansion. appliances, along with the diminished orthopedic
A similar relationship between buccal bone changes response found in some patients, may therefore pre-
and initial buccal bone thickness has been reported dispose to a reduction in buccal bone dimensions.
elsewhere (126). It is noteworthy, however, that these The adverse effects of heavy forces on the support-
findings reflect the status of the alveolar bone shortly ing periodontium have fueled interest into the use of
after treatment and do not necessarily account for light-force appliances, which may theoretically favor
any long-term changes that may occur as a result of the movement of teeth ‘with bone’. Self-ligation
bone remodeling. brackets are reported to produce low friction, which
A few studies have investigated the effects of maxil- permits light forces to be delivered to the teeth (80).
lary expansion on the long-term health of the peri- Although conflicting data exist regarding the light
odontal tissues. In one such study, which included force properties of self-ligating brackets (101, 102),
young patients, the prevalence of gingival recession their role in developing labial and buccal bone has
on one or more teeth in the rapid maxillary expansion recently been investigated (28). Using a well-designed
and fixed appliance groups were 20% and 6%, respec- randomized clinical trial, the changes in buccal bone
tively (49). In contrast, other studies have demon- were assessed following transverse expansion with
strated clinically significant increases in intra-arch self-ligating brackets. Transverse expansion was
width, without any detrimental medium-term/long- found to occur mainly as a result of buccal tipping,
term effects on the periodontal tissues (8, 51). Some rather than by true translation of the teeth ‘with’ buc-
of these findings, however, may be related to the cal bone. Interestingly, the buccal tipping produced
techniques used to measure buccal bone changes fol- by these self-ligating bracket systems was similar to
lowing maxillary expansion. For instance, Ballanti that reported in studies using rapid maxillary expan-
et al. (8) measured bone thickness from computed sion (128). The bone area on the buccal aspect of the
tomography scans at the level of the root furcation second premolar was also reduced following expan-
and did not account for the relatively thinner mar- sion, although similar data were not provided for the
ginal regions in which periodontal breakdown would canine or molar teeth. Unlike the other tooth move-
be expected to occur during tooth movement. ments discussed previously, it is plausible that bone

150
Response of periodontal tissues to orthodontic treatment

apposition does not accompany transverse and sagit- attachment levels following lateral expansion (47).
tal tooth movements to the same extent because the One possible explanation for this finding is the fact
overlying cortical plate in this direction is far too thin that gingival and periodontal tissue changes may not
for the osteogenic progenitor cells to form new bone be detectable at the time of appliance removal or
(5). While a small amount of bone may be formed by even after a short period of retention (51). Indeed,
periosteal apposition, excessive tooth movements are long-term evaluation of the periodontal tissues indi-
likely to cause the periodontal ligament to fuse with cates that adult patients undergoing rapid maxillary
the adjacent periosteum, thus creating a bony dehis- expansion have significantly greater clinical crown
cence (45). This theory seems to be well supported by heights than either controls or those who receive sur-
the unexpected, but highly interesting, work of Baten- gically assisted expansion (97).
horst et al. (10), who found distinctive tissue changes
when teeth were both extruded and advanced labi-
Sagittal expansion
ally. During these tooth movements, the alveolar
bone and epithelial attachment increased at the lin- The ideal position of the mandibular incisors has long
gual, interproximal and apical sides of the experimen- been the subject of intense debate. Significant
tal teeth. On the labial aspect, however, bony changes in the pretreatment position of the mandibu-
dehiscence was noted and the epithelial attachment lar incisors are associated with a greater risk of
was located more apically. relapse (54, 90), which makes it an important factor
An important limitation of these human studies is to consider when planning orthodontic cases. Still, a
that most have not evaluated the long-term response more pressing issue is often the effect of incisor pro-
of the periodontal soft tissues and alveolar bone in clination on the health of the periodontal soft tissues
teeth that have been expanded and retained outside and alveolar bone. Clearly, a significant amount of
the cortical bone. Although some recovery of buccal arch space can be gained by proclining the incisors
bone thickness has been reported after a 6-month (64), but at what expense?
retention period in patients treated with rapid maxil- The effect of incisor position on the adjacent alve-
lary expansion, these changes have been small and olar bone has been studied both in dogs (60, 143)
mostly insignificant (8). The effect of retaining the and in monkeys (10, 37, 141, 162). Nearly all of these
apices of premolar teeth outside the cortical plate has animal studies have found a consistent reduction in
also been studied in a small group of Macaca speciosa the level of the alveolar bone following incisor tip-
monkeys (157). Histologic analysis of the premolar ping or bodily displacement. Interestingly, marginal
teeth, immediately after expansion, revealed thinning bone levels increased and experimentally induced
of the buccal cortical plate, lack of bone over the root fenestrations/dehiscences resolved following the
apex and disorganization of the periodontal ligament. repositioning of previously expanded teeth within
There was also a lack of hyalinization in the speci- the alveolus (37, 143, 154). However, that eruption
mens, although this was attributed to the lag period of the incisors during this repositioning process may
between activation of the appliance and histological also have influenced the level of the marginal bone
analysis. In the other phase of the study, retention in these studies, as the alveolar crest migrates coro-
of the premolar apices outside the bone for a period nally to maintain its relationship with the cemento–
of 4 months resulted in osteogenesis around the enamel junction (125). Buccal bone regeneration
exposed root apices and some improvement in the has also been reported in a patient following the
orientation of the periodontal ligament fibers. Unfor- repositioning of a displaced canine tooth back
tunately, the limited study period did not permit the within the alveolus (104).
authors to determine whether complete bony repair Alveolar bone defects may also occur in the
was possible. absence of any deliberate attempt to protrude the
Given the short follow-up period of most studies, teeth outside the cortical plate. In a rare postmortem
the potential for complete recovery of buccal bone report of a deceased adult patient undergoing
thickness and height following transverse expansion orthodontic treatment, the roots of the mandibular
is unclear. It has been suggested that thinning out of incisors were found to have perforated the lingual
the buccal tissues during expansion may predispose plate (159). It is noteworthy that the mandibular sym-
to long-term gingival recession as a result of mechan- physis in this patient was both narrow and high, with
ical trauma and/or periodontitis (51). Previous stud- only a thin amount of alveolar bone supporting the
ies, however, have not found any clinically significant incisors. The presence of bony dehiscence and fenes-
changes in gingival recession and connective tissue trations were also confirmed in the maxilla of this

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Antoun et al.

patient using histological techniques (158). Although process. Excessive bodily advancement or proclination
these findings must be interpreted with caution, they of the teeth for the purpose of gaining additional arch
suggest that specific morphological features may play space may adversely affect the health of the periodon-
an important role in the development and extent of tal tissues, especially in the presence of specific trig-
bony dehiscence and fenestrations. Patients with gering factors, such as overzealous toothbrushing (86).
hyperdivergent skeletal patterns, for instance, are There may be some cases, such as dentoalveolar retru-
reported to have a thinner alveolus and this may pre- sion, where the incisors can be advanced with less risk
dispose them to a greater risk of developing bony of recession (5). Careful evaluation of the periodontal
dehiscence (130). Interestingly, facial type per se does tissues, oral hygiene, underlying skeletal structures
not seem to be associated with a higher frequency of and magnitude of tooth movement is therefore recom-
bony dehiscence and fenestration in untreated indi- mended for individual patients.
viduals (40). Prospective studies with adequate sam-
ple sizes are clearly needed to investigate the
relationship between morphologic features and the Limitations of current research
occurrence of bony defects during orthodontic treat-
ment. There is considerable heterogeneity in the quality and
In addition to the development of a bony dehis- type of studies investigating the effects of orthodontic
cence or fenestration, labial advancement of the treatment on the periodontal tissues and alveolar
mandibular incisors is reported to cause tension at bone. A large proportion of the research in this area
the free gingival margin, which reduces its apico- has been based on animal models. In comparison
coronal height and buccolingual thickness (161, with human studies, experimental models have a
164). Several predisposing factors have been number of important advantages, including the stan-
reported, including patient age (122), gingival bio- dardization of testing conditions and the use of pow-
type (89, 164) and width of the attached gingiva erful, but invasive, analytic techniques. Nonetheless,
(36). The extent of incisor proclination and the pres- several authors have warned that findings from ani-
ence of visible plaque have also been linked with mal models may not necessarily be valid and/or
gingival recession (6, 89, 164). In particular, a thin reproducible in human populations (82, 86, 105).
gingival biotypes, coupled with excessive proclina- There are a number of important differences in the
tion of the incisors, can render the gingival tissues behavior of human and animal tissue during tooth
less resistant to plaque-induced inflammation and movement. In comparison with humans, the labial
traumatic toothbrushing (164). As indefinite reten- and lingual alveolar walls of dogs and rats are denser
tion of the incisors is often required in patients with and contain fewer marrow spaces (121). Other differ-
severely expanded dental arches, it is likely that the ences have also been noted between species in the
risk of gingival recession would be particularly pro- occurrence of hyalinization zones, structural content
longed in these cases. However, the association of the roots, surface texture of the alveolar bone and
between gingival recession and sagittal expansion/ the porosity of the lamina dura (32, 121). Given these
incisor proclination is not consistent throughout the biologic differences and the inherent variability of
literature (3, 35, 123, 127). treatment responses in humans, it possible that ani-
A recent systematic review in this area described mal models may not fully predict the tissue response
the current level of evidence as low and highlighted a achieved in clinical practice (135). Therefore, it is
number of methodological weaknesses, including the important that findings from experimental models
use of retrospective study designs, inadequate clinical are supported by well-designed human studies when-
records and lack of follow-up data (58). The standard ever possible.
of oral hygiene is often not accounted for in these Even in human studies, however, there are a num-
studies. These limitations highlight the need for ber of methodological issues that deserve some con-
well-designed prospective studies to investigate the sideration. Previous studies, for example, have
factors that predispose to gingival recession during assessed the structure and dimensions of the alveolar
orthodontic treatment. bone using a wide range of imaging modalities,
including conventional two-dimensional radiography
(88) and computed tomography (8, 46, 103). An
Summary
increasing number of studies are also currently using
Based on the data available, it would seem prudent to cone-beam computed tomography for assessing alve-
maintain the position of the teeth within the alveolar olar bone changes following orthodontic treatment

152
Response of periodontal tissues to orthodontic treatment

(28, 47, 128). Although the estimation of bone thick- 3. Allais D, Melsen B. Does labial movement of lower incisors
ness/height using cone-beam computed tomography influence the level of the gingival margin? A case-control
study of adult orthodontic patients. Eur J Orthod 2003: 25:
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and fenestrations using three-dimensional rendering development by orthodontic forced extraction: a prelimi-
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