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J Clin Periodontol 2008; 35: 501–506 doi: 10.1111/j.1600-051X.2008.01211.

Periodontal parameters and Catherine Giannopoulou1, Alexander


Dudic2, Xavier Montet3, Stavros
Kiliaridis2 and Andrea Mombelli1

cervical root resorption during 1


2
3
Department of Periodontology;
Department of Orthodontics and
Department of Cell Physiology and

orthodontic tooth movement Metabolism, University of Geneva, Geneva


Switzerland

Giannopoulou C, Dudic A, Montet X, Kiliaridis S, Mombelli A. Periodontal


parameters and cervical root resorption during orthodontic tooth movement. J Clin
Periodontol 2008; 35: 501–506. doi: 10.1111/j.1600-051X.2008.01211.x.

Abstract
Objectives: To assess the relationship between periodontal parameters and cervical
root resorption in orthodontically moved teeth.
Material and Methods: In a standardized experimental tooth movement in 16
periodontally healthy subjects, 29 pre-molars were tipped buccally for 8 weeks.
Eighteen contralateral pre-molars not subjected to orthodontic movement served as
controls. Plaque Index (PI), Gingival Index (GI), probing depth and bleeding on
probing were assessed three times before and six times during the experimental phase.
Teeth were extracted and scanned in a micro-computed tomography scanner. The
presence or absence, and the severity of cervical root resorption were evaluated on the
three-dimensional reconstruction of the scans by two calibrated examiners.
Results: Overall, periodontal parameters were not different between the test and the
control teeth. Clear signs of buccal cervical resorption were detected on 27 of 29
orthodontically moved teeth and on one control tooth. Ten subjects had perfect oral
hygiene and no gingivitis, whereas six subjects showed a moderate level of plaque and
gingivitis (420% occurrences of PI or GI with 40). No relationship could be
demonstrated between resorption and periodontal parameters. Key words: cervical root resorption;
Conclusions: Nearly all orthodontically moved teeth showed signs of cervical orthodontic movement; periodontal parameters
resorption. Periodontal parameters were unrelated to this important side effect of
orthodontic treatment. Accepted for publication 13 January 2008

It has been shown that orthodontic forces extensively investigated (for a review, Root resorption is an undesirable side
represent a physical agent capable of see Krishnan & Davidovitch 2006). How- effect of orthodontic treatment. When a
inducing an inflammatory reaction in the ever, the effect of orthodontic movement tooth is tipped buccally, pressure is
periodontium. This reaction is necessary on the gingiva has been studied to a lesser created on the cervical part of the buccal
for orthodontic tooth movement. The dif- extent. Unlike bone and periodontal liga- side of the tooth and on the apical part of
ferent phases of tooth movement invol- ment, gingival tissue is not resorbed after the palatin/lingual side. These pressure
ving the recruitment of different cells such orthodontic treatment but is compressed areas are the ones where root resorption
as osteoclast and osteoblast progenitors as and consequently retracted. The fact that is mostly expected (Hollender et al.
well as inflammatory cells have been orthodontic force does not induce gingival 1980, Linge & Linge 1991, Davidovitch
resorption prevents the formation of perio- 1996, Kurol et al. 1996). While apical
dontal pockets and the detachment of the root resorptions can be seen in radio-
Conflict of interest and source of tooth from the gingiva. However, ortho- graphs (McFadden et al. 1989, Mirabella
funding statement dontic treatment produces a local change & Artun 1995a, b), to diagnose root
The authors declare that they have no in the oral ecosystem, with changes in the resorption on the buccal and palatal
conflict of interests. composition of bacterial plaque and con- surfaces of the root, the radiograph is
The present study was supported by the sequently the development of gingivitis an inadequate tool (Andreasen et al.
Swiss National Science Foundation (Grant (Huser et al. 1990, Alexander 1991, 1987, Chapnick 1989). Therefore, the
No. 3200-112296).
Paolantonio et al. 1999). inflammatory changes underlying the
r 2008 The Authors 501
Journal compilation r 2008 Blackwell Munksgaard
502 Giannopoulou et al.

remodelling processes necessary for assessed at the first (day 0) and all Belgium). This system is based on a
tooth movement have to be investigated following visits at the buccal, mesial, cone-beam X-ray source and a charge-
in a wider context. distal and palatal sites of all pre-molars coupled device camera, and allows
This study explores one aspect of this scheduled for extraction: Plaque Index acquiring images with resolutions ran-
phenomenon by assessing the potential (PI) (Silness & Loe 1964), Gingival ging from 35 to 9 mm. All scans were
relationship between clinical perio- Index (GI) (Löe 1967), periodontal acquired at a 9 mm resolution using the
dontal parameters obtained during probing depth (PPD) and presence or following parameters: 65 kV anode vol-
orthodontically induced tooth move- absence of bleeding on probing (BOP). tage, 100 mA, 0.451 rotation step and
ment and cervical root resorption 589 ms exposure time per view. For
observed after treatment. each mode, a 0.5 mm aluminium filter
Standardized orthodontic tooth
movement
was installed in the beam path to cut off
the softest X-rays in order to increase
Material and Methods The study was divided into three phases: the accuracy of the beam-hardening
Subjects
baseline (day 0, day 7, day 21), the early correction (BHC). These settings
experimental period (day 28, day 35, allowed to scan a tooth in 90 min.
Sixteen patients (12 females and four day 49) and late experimental period Cross-sectional images were recon-
males) were selected among patients (day 56, day 63, day 77). The outline structed using a classical Feldkamp
attending the Orthodontic Department of the study is shown in Fig. 1. cone-beam algorithm (Feldkamp et al.
in Geneva for orthodontic treatment. Each patient contributed with at least 1984). The corrected image data were
The mean age of the patients was 17.7 one experimental and one control pre- calibrated in the conventional linear
years with a range of 11.3–43.0 years. molar. During the baseline period, only scale of CT number, known as Houns-
The patients had to meet the following periodontal examinations were performed. field units (HU), defined so that water
criteria: (i) good general health, (ii) In the beginning of the early experimental and air have values of 0 and
healthy periodontium, i.e., probing period (day 21), 29 pre-molars randomly 1000 HU, respectively.
depth 43 mm and no radiographic evi- assigned to the experimental group were The three-dimensional (3D) recon-
dence of bone loss, (iii) no radiographic tipped buccally. For this movement, a structions of the micro-CT scans were
evidence of idiopathic root resorption, sectional archwire (0.019  0.025 TMA, analysed by two calibrated examiners
(iv) no previous orthodontic treatment, Ormco, Glendora, CA, USA) was acti- (A. D. and C. G.). The amount of root
(v) no history of previous dental trauma, vated buccally and attached with a ligature resorption on the cervical part of the
(vi) severe crowding in both jaws and to the bracket of the experimental tooth in buccal side was assessed semi-quantita-
(vii) scheduled to begin orthodontic order to exert a 1N force. At day 49 tively on randomly sequenced movies
treatment comprising extractions of at (beginning of the late experimental peri- and categorized into three groups: (i)
least the two or four first or second pre- od), the amount of force was controlled those without any resorption, including
molars. Informed consent in written and adjusted. A transpalatal and lingual not more than one barely visible shallow
form was obtained from the patients arch were placed as anchorage. Eighteen resorption up to an 80 mm depth, (ii)
(and the parents) before the beginning contralateral pre-molars bonded with those with moderate resorption, includ-
of the study. The protocol was approved brackets but not subjected to orthodontic ing a few small and shallow craters of
by the Medical Ethics Committee of the tooth movement served as controls. At the 80–120 mm depth and (iii) those with
University of Geneva. end of the whole experimental period severe resorption, including several
(day 77), all pre-molars were carefully large and deep craters of 4120 mm
extracted, placed in 4% formaldehyde depth (Fig. 2).
Clinical examination
solution and scanned in a micro-computed
Before the beginning of the study, sub- tomography (CT) scanner.
Statistics
jects received oral hygiene instructions
and all tooth surfaces were cleaned and Micro-CT acquisition and reconstruction
The following subject-based parameters
polished. Motivation for good plaque were generated separately for the
control was given to all patients. The All images were acquired on a Skyscan- experimental teeth and control teeth
following clinical parameters were 1076 micro-CT (Skyscan, Aartselaar, for the three baseline examinations, the

Baseline Early experimental period Late experimental period


Day 0 Day 7 Day 21 Day 28 Day 35 Day 49 Day 56 Day 63 Day 77
1 week 2 weeks 1 week 2 weeks 4 weeks
Start of
after after Reactivation after after after
activation
activation activation reactivation reactivation reactivation
Oral
hygiene x x x x x x x x
instructions
Periodontal
x x x x x x x x x
examination
Extractions x

Fig. 1. Outline of the study.


r 2008 The Authors
Journal compilation r 2008 Blackwell Munksgaard
Cervical root resorption and periodontal parameters 503

The statistical analysis was per-


formed using SPSS for Windows
(Release 13.0.0., standard version,
SPSS Inc., Chicago, IL, USA).

Interrater agreement

The interrater agreement on the micro-


CT scans was assessed using Cohen’s k.
The frequencies for the presence or
absence of root resorption on the cervi-
cal part of the buccal side of the root
assessed by both observers are shown in
Table 1. The bold figures along the
diagonal show the observed frequencies
of agreement when evaluating root
resorption on the 3D micro-CT scan
images; the corresponding expected fre-
quencies are shown just below. The
calculated Cohen’s k is 0.77. There
appears to be a substantial agreement
between the two observers in the coding
No resorption Moderate resorption Severe resorption
of cervical root resorption on the 3D
Fig. 2. Presence or absence and severity of cervical root resorption evaluated by two micro-CT scans.
calibrated examiners in one experimental and two control pre-molars of one patient: the
first control pre-molar shows no resorption; the second control pre-molar shows moderate
resorption; and the third experimental pre-molar shows severe resorption.
Results
Table 2 shows the mean values of prob-
Table 1. Observed (in bold) and expected frequencies of buccal cervical root resorption ing depth, the percentage of buccal sites
assessment on three-dimensional micro-computed tomography (CT) images with PI and GI scores 40 and the
First observer Second observer percentage of buccal sites that bled
upon probing for the experimental and
no moderate severe total control teeth at baseline (day 0, day 7
resorption resorption resorption and day 21), the early experimental
period (day 28, day 35 and day 49)
No resorption
and during the late experimental period
Observed 11 1 1 13
Expected 3.3 7.7 (day 56, day 65 and day 77). No sig-
Moderate resorption nificant differences were observed for
Observed 1 5 2 8 any of the clinical parameters between
Expected 1.2 experimental and control teeth through-
Severe resorption out the study; both showed relatively
Observed 0 1 25 26 good periodontal status with a mean
Expected 15.5 PPD below 3 mm, a percentage of scores
Total 12 7 28 47
of PI and GI40 not exceeding 26.6%
and 19.8%, respectively, and no more
than 10% sites with a positive BOP.
three examinations in the early experi- experimental period using the Fisher During the late experimental period,
mental period and the three examina- exact test for PI, GI and BOP and the an increase in the number of buccal sites
tions of the late experimental period: the t-test for PPD. The w2 test was used to with plaque and/or gingival inflamma-
percentage of sites per subject with a study the relationship between the tion was observed for both experimental
PI40, the percentage of sites per sub- patient’s hygiene level and the degree and control teeth. However, the differ-
ject with a GI40 and the percentage of of cervical root resorption. p values ences from the baseline and/or the
sites per subject with BOP40. In addi- o0.05 were accepted for statistical early experimental period were not
tion, the mean PPD ( standard devia- significance. significant.
tion) was calculated for each subject The relationship between resorption Figure 3 shows the presence or
in each experimental phase by summing and clinical parameters was further absence and the severity of cervical
the scores and dividing by the number tested using logistic regression, with root resorption in the experimental and
of sites graded. The same parameters the presence or absence of resorption control teeth evaluated in the 3-D recon-
were assessed separately for the buccal as the dependent variable and treatment structions of the micro-CT scans. The
sites. or no treatment and the clinical para- presence or absence and the severity of
The differences between test and con- meters in the three experimental phases apical root resorption are reported in a
trol teeth were determined for each as independent variables. companion paper. As explained under
r 2008 The Authors
Journal compilation r 2008 Blackwell Munksgaard
504 Giannopoulou et al.

Table 2. Percentage of buccal sites with PI and GI40, BOP positive and PPD (mean  SD) in experimental (n 5 29) and control teeth (n 5 18)
Baseline Early experimental period Late experimental period

experimental control experimental control experimental control

PI (40) 17.7% 17.5% NS 21.5% 20.0% NS 24.7% 26.6% NS


GI (40) 8.0% 9.1% NS 11.8% 6.6% NS 19.8% 17.5% NS
BOP (positive) 3.2% 10.0% NS 3.7% 4.1% NS 6.5% 9.1% NS
PPD (mm) 2.20  0.31 2.05  0.27 NS 2.35  0.38 2.30  0.38 NS 2.36  0.44 2.39  0.38 NS
NS, not significant (p40.05); PI, Plaque Index; GI, Gingival Index; BOP, bleeding on probing; PPD, pocket probing depth; SD, standard deviation.

100% P < .001 however, in several undesirable side


effects. These effects include mainly
the development of gingivitis, root
resorption, gingival recession, caries,
No resorption
marginal bone loss and pulpal reactions.
50% Moderate resorption For many years, the extent and depth
Severe resorption of a resorbed area on the root surface of
an orthodontically moved and then ex-
tracted tooth was evaluated by histology
(Owman-Moll et al. 1995, Kurol &
Owman-Moll 1998). However, root
0% resorption is a 3D phenomenon and its
Experimental teeth Control teeth
extent needs to be quantified with pre-
Fig. 3. Severity of cervical root resorption on the reconstructed micro-computed tomography cision. The micro-CT scanner is a rapid
images. and accurate method with high resolu-
tion, providing enhanced visual and
perspective assessment of root surfaces,
Table 3. Relationship between degree of cer- relationship could be demonstrated thus offering a 3D analysis of the cra-
vical resorption and patients’ hygiene level between resorption and periodontal ters. Thus, this method may serve as a
Hygiene Buccal cervical resorption on parameters (Table 3). Logistic regres- gold standard. Hence, due to the high
level reconstructed micro-computed sion analysis confirmed these findings as precision we may obtain, histology
tomography (CT) images treatment or no treatment was the only would not offer any further information.
significant predictor for the presence or Concerning the gingival response
severe moderate or no absence of resorption; the clinical para- to tooth movement, wide variations in
resorption resorption meter had no further significant effect. the clinical appearance have been
Moderate 11 (39%) 11 (58%) described, depending on the type of
(n 5 6) tooth movement (rotation, labial move-
Good 17 (61%) 8 (42%) ment), the force, the patient’s hygiene
(n 5 10) Discussion level, etc. (for a review, see Redlich
The present study was designed to eval- et al. 1999). Gingivitis has been de-
uate the relationship between perio- scribed as the most common side effect
‘‘Material and Methods’’, the amount of dontal parameters and cervical root of orthodontic movement due to plaque
root resorption was categorized into resorption in orthodontically moved accumulation. Several studies have
three groups: no resorption, moderate teeth. Signs of buccal cervical resorp- shown that fixed orthodontic therapy is
resorption and severe resorption. Clear tion were obvious on almost all ortho- almost always related to inflammation
signs of buccal cervical resorption were dontically moved teeth, as evaluated in of gingival tissues (Zachrisson &
detected in 27 out of 29 (93%) of the the reconstructed images of the micro- Zachrisson 1972, Kloehn & Pfeifer
experimental teeth and one out of CT scanner. However, as no significant 1974, Huser et al. 1990, Alexander
18 (5%) of the control teeth. Moderate differences were observed for any of the 1991). This situation is mostly related
resorption was observed in one pre- periodontal parameters between experi- to hampered oral hygiene and conse-
molar of the experimental group mental and control teeth, it was con- quently to the accumulation of bacterial
(3.4%) and in six pre-molars (33%) of cluded that periodontal parameters are plaque. Furthermore, the composition of
the control group. unrelated to cervical root resorption. bacterial plaque following placement of
Finally, we assessed whether the Cellular and tissue reactions start orthodontic appliances changes to a
degree of cervical root resorption is immediately after force application: the more pathogenic flora (Diamanti-Kipioti
correlated to the patient’s level of oral early phase of orthodontic tooth move- et al. 1987, Paolantonio et al. 1996). An
hygiene. Ten subjects had perfect oral ment involves an acute inflammatory orthodontic appliance modifies locally
hygiene and no signs of gingivitis, response characterized by periodontal the supragingival environment, thus
whereas six subjects showed a moderate vasodilation and migration of leucocytes affecting the colonization and occur-
level of plaque and gingivitis (420% out of the capillaries. Inflammation is rence of specific microorganisms. For
occurrences of PI and GI). However, no essential to tooth movement, resulting, example, Paolantonio et al. (1996)
r 2008 The Authors
Journal compilation r 2008 Blackwell Munksgaard
Cervical root resorption and periodontal parameters 505

reported a remarkable frequency of movement, which should be distinct Brezniak, N. & Wasserstein, A. (2002a) Ortho-
detection of Actinobacillus actinomyce- from the other type of root resorption. dontically induced inflammatory root resorp-
temcomitans (A.a) in young individuals Often, there are no obvious clinical tion. Part I: the basic science aspects. The
wearing orthodontic appliances. The signs and the condition is only detected Angle Orthodontist 72, 175–179.
presence of A.a was related to the gin- radiographically. However, where the Brezniak, N. & Wasserstein, A. (2002b) Ortho-
gival bleeding index but not to the lesion is visible, the clinical features dontically induced inflammatory root resorp-
tion. Part II: the clinical aspects. The Angle
plaque levels. Other pathogenic bacteria may vary from a small defect at the
Orthodontist 72, 180–184.
such as Porphyromonas gingivalis, Pre- gingival margin to a pink discoloration Chapnick, L. (1989) External root resorption: an
votella intermedia, Tannerella forsythia of the tooth crown (Heithersay 1999b). experimental radiographic evaluation. Oral
and Fusobacterium have been detected Furthermore, this condition is associated Surgery, Oral Medicine and Oral Pathology
after bracket placement, resulting in with inflammation of the periodontal 67, 578–582.
more gingival inflammation and bleed- tissues and does not involve the pulp Davidovitch, Z. (1996) Etiologic factors in
ing (Naranjo et al. 2006). However, of the tooth. In our study, even if force-induced root resorption. In: Davido-
these pathogens could be significantly patients were highly motivated, cervical vitch, Z. & Norton, L. A. (eds). Biological
reduced when the orthodontic appliance root resorption was present. We cannot, Mechanisms of Tooth Movement and Cranio-
was removed and professional prophy- however, rule out the possibility that facial Adaptation, pp. 349–355. Boston: Har-
laxis was given to the patient (Sallum resorption would have been more severe vard Society for the Advancement of
et al. 2004). if patients showed a poor hygiene level. Orthodontics.
Diamanti-Kipioti, A., Gusberti, F. A. & Lang,
The subjects in our study showed Because no differences in the perio-
N. P. (1987) Clinical and microbiological
almost similar gingival conditions for dontal parameters were found between
effects of fixed orthodontic appliances. Jour-
the experimental and control teeth. This experimental and control teeth, we may nal of Clinical Periodontology 14, 326–333.
is mainly due to the oral hygiene assume that plaque, BOP and PPD have Feldkamp, L. A., Davis, L. C. & Kress, J. W.
instructions given to each patient before no prognostic effect on cervical root (1984) Practical cone-beam algorithm. Jour-
and during the whole experimental treat- resorption as a consequence of ortho- nal of the Optical Society of America A 1,
ment. Several studies have shown that it dontic tooth movement. Although teeth 612–619.
is possible to achieve and maintain a were selected to exclude any external or Heithersay, G. S. (1999a) Invasive cervical
high standard of gingival health during predisposition to resorption and were resorption: an analysis of potential predispos-
orthodontic treatment (Lundstrom & carefully extracted using forceps, ing factors. Quintessence International 30,
Hamp 1980a, Lundstrom et al. 1980b). resorption craters were evident in seven 83–95.
The slight deterioration of the gingival pre-molars of the control group (six pre- Heithersay, G. S. (1999b) Clinical, radiologic
and histopathologic features of invasive cer-
status observed after 3 months in ortho- molars with moderate resorption and
vical resorption. Quintessence International
dontically treated children was mainly one pre-molar with severe resorption).
30, 27–37.
due to the sub-gingivally located ortho- This demonstrates that resorption could Hollender, L., Ronnerman, A. & Thilander, B.
dontic bands. In fact, banded teeth may be a naturally occurring physiologic (1980) Root resorption, marginal bone sup-
give higher PI and bleeding scores as phenomenon. Other studies involving port and clinical crown length in orthodonti-
compared with control teeth (Huser the identification of molecules asso- cally treated patients. European Journal of
et al. 1990), especially in patients with ciated with and/or responsible for root Orthodontics 2, 197–205.
established gingivitis (Sallum et al. resorption during orthodontic tooth Huser, M. C., Baehni, P. C. & Lang, R. (1990)
2004). movement may be necessary. Effects of orthodontic bands on microbiolo-
Cervical resorption has been de- In conclusion, cervical root resorp- gic and clinical parameters. American
scribed as an aggressively destructive tion is a common sequela of orthodontic Journal of Orthodontics and Dentofacial
form of external root resorption, classi- treatment. All the orthodontically Orthopedics 97, 213–218.
Kloehn, J. S. & Pfeifer, J. S. (1974) The effect
fied in the group of inflammatory moved teeth showed moderate and/or
of orthodontic treatment on the periodontium.
resorptions and starting sub-gingivally severe resorption on the cervical part
The Angle Orthodontist 44, 127–134.
at the cervical root surface of the tooth. of the buccal side. Periodontal para- Krishnan, V. & Davidovitch, Z. (2006) Cellular,
Although the aetiology remains uncer- meters did not seem to be associated molecular, and tissue-level reactions to ortho-
tain, several predisposing factors have with root resorption, as no changes were dontic force. American Journal of Orthodon-
been assessed, such as trauma, intra-oral observed clinically during the experi- tics and Dentofacial Orthopedics 129,
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Heithersay (1999a) identified that of all tion and root resorption during early ortho-
potential predisposing factors, ortho- dontic tooth movement in adolescents. The
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17, 93–99. Gingival response to orthodontic force. unige

Clinical Relevance prediction and prevention are still between resorption and periodontal
Scientific rationale for the study: impossible. parameters.
Cervical root resorption is a common Principal findings: All orthodonti- Practical implications: Routine
sequela of orthodontic treatment cally moved teeth showed signs of periodontal parameters are unrelated
associated with inflammation of the cervical resorption. However, no to cervical root resorption resulting
periodontal tissues. Nevertheless, relationship could be demonstrated from orthodontic tooth movement.

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Journal compilation r 2008 Blackwell Munksgaard

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