Original Article

Tooth movement, orofacial pain, and leptin, interleukin-1b, and tumor

necrosis factor–a levels in obese adolescents
Rafaela Carolina Soares Bonatoa; Marta Artemisa Abel Mapengoa; Lucas José de Azevedo-Silvab;
Guilherme Jansonc; Silvia Helena de Carvalho Sales-Peresd

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ABSTRACT
Objectives: To evaluate tooth movement, orofacial pain, and leptin, interleukin (IL)–1b, and tumor
necrosis factor (TNF)–a cytokine levels in the gingival crevicular fluid (GCF) during orthodontic
treatment in obese adolescents.
Materials and Methods: Participants included adolescent patients aged 12–18 years: group 1,
obese (n ¼ 30), and group 2, nonobese controls (n ¼ 30). They were evaluated before (T0) and after
1 hour (T1), 24 hours (T2), and 1 week (T3) of fixed appliance bonding. Periodontal examination (T0),
collection of GCF (T1, T2, T3), and evaluation of Little’s irregularity index (T0, T3) were performed, and
a visual analog scale was used to measure pain (T1, T2, T3). Evaluation of IL-1b, TNF-a, and leptin
cytokines was performed using a Luminex assay. Mann-Whitney and t-tests were used for
intergroup comparisons, and a generalized estimating equation and cluster analyses were used for
comparisons among observation times (P , .05).
Results: The obese group had a higher prevalence of probing depth of 4 mm and bleeding on
probing. Orthodontic tooth movement was similar in both groups. Peak of pain was at T2 in both
groups and was higher in the obese patients. TNF-a showed a slight increase at T1, followed by a
gradual decrease at T2 and T3 in both groups. The obese group had a higher concentration of IL-1b
before and during orthodontic treatment. There was no difference in tooth movement between
obese and control patients during the first week of orthodontic treatment.
Conclusions: Obese adolescents had a greater subjective report of orofacial pain after 24 hours of
orthodontic treatment and higher concentrations of IL-1b proinflammatory cytokine before and
during tooth movement as compared with nonobese control adolescents. (Angle Orthod.
2022;92:95–100.)
KEY WORDS: Obesity; Tooth movement; Inflammation; Interleukin-1b; Tumor necrosis factor–a

INTRODUCTION
a
Postgraduate Student, Department of Pediatric Dentistry,
Orthodontics and Public Health, Bauru School of Dentistry, Obesity and its associated comorbidities are in-
University of São Paulo, Bauru, São Paulo, Brazil. creasingly prevalent among adolescents. Childhood
b
Postgraduate Student, Department of Prosthodontics and
Periodontology, Bauru School of Dentistry, University of São and adolescent obesity are associated with health
Paulo, Bauru, São Paulo, Brazil. consequences later in life, including adult overweight/
c
Professor, Department of Orthodontics, Bauru School of obesity1 and cardiovascular, musculoskeletal, and
Dentistry, University of São Paulo, Bauru, São Paulo, Brazil.
d
Associate Professor, Department of Pediatric Dentistry, endocrine diseases.2
Orthodontics and Public Health, Bauru School of Dentistry, Patients with obesity suffer from chronic inflamma-
University of São Paulo, Bauru, São Paulo, Brazil. tion accompanied by elevated inflammatory cytokines,
Corresponding author: Silvia Helena de Carvalho Sales
suggesting that these individuals display a dysfunc-
Peres, Department of Pediatric Dentistry, Orthodontics and
Public Health, Bauru Dental School, University of São Paulo, tional immune response. Elevated inflammatory cyto-
Alameda Octávio Pinheiro Brisolla, 9-75, Bauru, SP 17012-901, kines interleukin (IL)–1b, IL-6, and tumor necrosis
Brazil. factor (TNF)–a are primarily produced by an increased
(e-mail: [email protected])
number of macrophages in obese adipose tissue, and
Accepted: May 2021. Submitted: January 2021.
Published Online: August 2, 2021
their altered circulating levels have been reported in
Ó 2022 by The EH Angle Education and Research Foundation, patients with obesity, contributing to local as well as
Inc. systemic chronic inflammation.3

DOI: 10.2319/011321-44.1 95 Angle Orthodontist, Vol 92, No 1, 2022

96 BONATO, MAPENGO, DE AZEVEDO-SILVA, JANSON, DE CARVALHO SALES-PERES

Encountering obese patients who undergo ortho- treated with antibiotics in the past 6 months, smoker,
dontic treatment is becoming more common, as the and pregnant or breast-feeding.
incidence of individuals who are obese and overweight
is increasing worldwide.4 The effect of oral habits on Anthropometric Evaluation
cranial and maxillofacial growth and development is
Measurements of body mass and body composition
dependent on the nature, onset, and duration of the
were performed using Inbody 230 Multifrequency
habits. Orofacial pain may negatively affect adoles-
Tetrapolar Bioimpedanciometer (Biospace, Rio de
cents. Widespread pain may indicate changes related
to central sensitization, partially explaining the rela- Janeiro, Brazil), with 100 g of precision and a
tionship between obesity and comorbidities with painful maximum capacity of 250 kg.9 Height was measured
conditions.5 using a stadiometer attached to the wall with an

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The tooth movement induced by fixed orthodontic accuracy of 0.1 cm. The diagnosis of nutritional status
appliances causes a change of the microbiome and through body mass index (BMI) was performed using
subsequent infections, such as an inflammatory the BMI percentile, obtained through growth curves
response in the periodontium. Orthodontic appliances according to sex and age,10 using the World Health
make it more difficult to keep teeth clean and induce Organization AnthroPlus software 1.0.4 (https://pt.
plaque accumulation. The events leading to tooth freedownloadmanager.org/Windows-PC/WHO-
movement are complex and include interactions AnthroPlus-GRATUITO.html).
between cells in the alveolar bone and the periodontal
ligament. Tooth displacement and bone-remodeling Clinical Evaluation
activity are consequences of an inflammatory process Clinical evaluations were performed at four time
induced by mechanical stimulus.6 points: before fixed appliance bonding (T0) and at 1
Therefore, both adipose tissue and the inflammation hour (T1), 24 hours (T2), and 1 week (T3) after bonding
generated by orthodontic tooth movement alter the of appliances. At T0, evaluation of Little’s irregularity
levels of TNF-a, IL-1b, and leptin, which are simulta- index, collection of gingival crevicular fluid (GCF), and
neously related to obesity and tooth movement.7,8 a periodontal examination (probing depth, gingival
However, there are no reports about the relationship bleeding index, and presence of calculus) were
between orthodontic treatment and inflammatory cyto- performed. The fixed appliance consisted of 0.022 3
kines, periodontal status, and orofacial pain in obese 0.028-inch Roth prescription metal brackets (Morelli,
adolescents. Thus, this study aimed to prospectively Sorocaba, Brazil). After bonding, 0.014-inch NiTi arch
investigate the impact of obesity on orthodontic tooth wires were inserted and tied with elastomeric or metal
movement regarding the changes in inflammatory ligatures, when necessary.
cytokines, periodontal conditions, and orofacial pain. To assess probing depth, the distance from the
gingival margin to the most apical point of the gingival
MATERIALS AND METHODS
sulcus/pocket was considered. The periodontal probe
Design and Participants was introduced with light pressure, parallel to the tooth
axis. The probing depth and blooding on probing were
This was a prospective cohort study in which data evaluated at three sites: mesial, central, and distal on
were collected before and after bonding of the fixed the buccal and palatal/lingual surfaces of all teeth,
orthodontic appliances (1 hour, 24 hours, and 1 except the third molars.11
week). The study was approved by the Committee At T1, T2, and T3, the visual analog scale (VAS) was
of the Faculty of Dentistry of Bauru (CAAE used to evaluate pain, and GCF was collected. In
68559617.8.0000.5417). addition, at T3, Little’s irregularity index was measured.
The sample consisted of 60 adolescent patients
aged 12 to 18 years, divided into two groups: group 1, Little’s Irregularity Index
obese (n ¼ 30; 16 female, 14 male), and group 2,
nonobese control (n ¼ 30; 17 female, 13 male). Little’s irregularity index was measured on the
Recruitment and clinical evaluations were carried out mandibular dental model with a digital caliper (model/
at the Orthodontic Clinic of the Faculty of Dentistry of code 500-144B, Mitutoyo, Suzano, Brazil) with an
Bauru. Eligibility criteria were orthodontic records accuracy of 0.01 mm, parallel to the occlusal plane.
indicating the use of fixed orthodontic appliances, Little’s irregularity index consisted of measuring the
between 12 and 18 years of age at the beginning of linear displacement of the anatomical contact points
orthodontic treatment, permanent dentition, and Little’s between adjacent mandibular incisors, and the sum of
irregularity index between 3 and 12 mm. Exclusion the five measurements is the irregularity index. This
criteria were regular use of anti-inflammatory drugs, measure represented the distance by which the

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TOOTH MOVEMENT IN OBESE ADOLESCENTS 97

Table 1. Anthropometric Characteristics of Participants Stratified by Groupa

G1 Obese, Mean 6 SD (Min–Max) G2 Eutrophic, Mean 6 SD (Min–Max) P
Age, y 14.06 6 2.24 (12–18) 14.56 6 1.73 (12–18) .14
Weight, kg 74.98 6 20.08 (47.9–127.4) 53.33 6 9.10 (40.5–76.6) .00*
Height, m 1.63 6 9.13 (1.45–1.84) 1.65 6 8.30 (1.85–1.50) .83
BMI, kg/m2 25.05 6 3.13 (20.72–28.04) 19.90 6 2.00 (18.30–22.72) .00*
WHR 0.93 6 0.07 (0.80–1.08) 0.81 6 0.04 (0.75–0.90) .00*
SMM 26.35 6 7.22 (15.9–42.8) 23.94 6 5.28 (16.8–35.5) .19
Fat mass 29.74 6 12.17 (10.8–59.0) 10.93 6 4.42 (10.8–23.0) .00*
Body fat, % 37.0 6 6.9 (15.6–52.3) 20.17 6 7.3 (7.8–33.8) .00*
Protein mass 9.4 6 2.4 (6.0–14.9) 8.6 6 1.8 (6.2–12.5) .18
Mineral mass 3.3 (2.1–5.0) 6 0.8 3.0 (2.3–4.4) 6 0.6 .06

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Total body water 34.9 (22.1–54.5) 6 8.9 32.0 (23.2–46.0) 6 6.5 .24
a
BMI indicates body mass index; SMM, skeletal muscular mass; WHR, waist-to-hip ratio.
* Statistically significant at P , .05.

contact points must be moved to achieve alignment12 reading of the plates by MagPix equipment (Luminex
and was used in this study indirectly to measure the Corporation, Austin, Tex), following the protocol
amount of tooth movement in the groups. Similar indicated by the manufacturer.
intergroup changes in the index would indicate similar Mann-Whitney and t-tests were used for intergroup
amounts of tooth movement. comparisons, and a generalized estimating equation
and cluster analyses were used for interphase com-
VAS for Orofacial Pain parisons (P , .05).
Pain sensitivity was evaluated after 1 hour, 24 hours,
and 1 week of fixed appliance bonding (T1, T2, T3) using RESULTS
a VAS in which the patient scored the intensity of pain
The obese group (G1) showed significantly higher
experienced from 0 to 10.13 The volunteers were
values for weight, BMI, waist-to-hip ratio, fat mass, and
instructed not to use any analgesic medications within
percentage body fat as compared with the controls
1 week of fixed appliance bonding.
(G2; Table 1). The participants were stratified accord-
GCF Collection ing to their periodontal status. G1 had a significantly
smaller percentage of 0- to 3-mm probing depths and a
GCF was collected with sterile absorbent paper significantly greater percentage of 4- to 5-mm probing
cones. For collection, supragingival plaque removal depths and bleeding sites than G2 did (Table 2).
was performed, followed by isolation with cotton rolls Crowding was similar in the groups, both initially and
and drying with an air syringe for 5 seconds. After
after 1 week of treatment (Table 3). There were
preparation, absorbent paper cones (#30, Tanari, AM,
significant decreases in crowding after 1 week of
Brazil) were inserted into the gingival sulcus at a 1 mm
treatment in both groups.
depth for 30 seconds, distal to the six mandibular
anterior teeth (central and lateral incisors, and canine). Pain intensity was greater at all time points for the
If the paper ends were contaminated with blood or obese group; however, the difference between groups
saliva, they were discarded. was significant only at T2 (Table 4).
Immediately after collection, the paper cones were The obese group had significantly higher concentra-
transferred to Eppendorf tubes containing 200 lL of tions of IL-1b cytokine than the control group did. The
buffered saline (phosphate-buffered saline) with 0.1% concentration varied significantly with time (Table 5).
Tween 20 solution (USB Corp, Cleveland, Ohio) and 1 TNF-a cytokine varied significantly with time.
lL of protease inhibitor cocktail (Sigma-Aldrich, St
Louis, Mo). The tubes were shaken for 30 minutes and Table 2. Periodontal Parameters by Groupa
centrifuged at 10,000 rpm for 5 minutes and then G1 (n ¼ 30) G2 (n ¼ 30)
stored at 808C for further laboratory analysis. Obese Eutrophic P
PD, mm 2.13 6 0.34 2.07 6 0.25 .39
Laboratory Stage PD 0–3 mm, % sites 97.44 6 4.35 98.05 6 3.45 .00*
PD 4–5 mm, % sites 0.53 6 1.00 0.21 6 0.52 .00*
Evaluation of IL-1b, TNF-a, and leptin in the GCF % Calculus, teeth 7.97 6 8.64 5.90 6 6.78 .48
was performed using Luminex xMAP for multiple % BOP, sites 11.27 6 5.92 6.50 6 3.76 .00*
assays, using the appropriate kit (Cat. No. HADK2- a
BOP indicates bleeding on probing; PD, probing depth.
MAG-61K, Millipore Corporation, Billerica, Mass), with * Statistically significant at P , .05.

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98 BONATO, MAPENGO, DE AZEVEDO-SILVA, JANSON, DE CARVALHO SALES-PERES

Table 3. Little’s Irregularity Index: Initial (T0) and After 1 wk of Orthodontic Treatment (T3)
T0 T3 Group Time Group 3 Time
Dental crowding, mm
G1 4.90a (4.01–5.79) 3.50b (2.67–4.33) .43 .00* .72
G2 4.50a (3.75–5.25) 3.03b (2.38–3.68)
a,b
Indicates statistically significant differences
* Statistically significant at P , .05.

DISCUSSION a previous study19 that demonstrated that 32.1% of

obese patients had a prevalence of sites with BOP
This longitudinal study showed that tooth movement
greater than 25%, compared with only 7.6% of

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triggered greater orofacial pain after 24 hours of
nonobese patients; however, there was no evaluation
orthodontic treatment in obese adolescents.
of the probing depth in that study. The prevalence of
Obesity is a pathologic condition associated with
BOP was higher compared with the present study
excess adipose accumulation and the production of
because of methodological differences. The current
systemic proinflammatory factors, which lead to chron-
study investigated BOP at six sites per tooth, in
ic subclinical inflammation.14 In this study, BMI15 and
addition to two additional sites.
body composition (fat mass, skeletal muscle mass, The periodontal condition can be aggravated by the
water)16 were assessed using bioimpedance tests. The presence of dental crowding due to the difficulty in
BMI of the group of obese adolescents was signif- cleaning. The present study included patients who
icantly higher than the nonobese control group (Table needed orthodontic treatment because of the presence
1), with an average of 37.6% fat in body composition of mandibular crowding, regardless of the anteropos-
and 20.17%, respectively. Therefore, it is highly terior relationship of the basal bones. The groups had
recommended to assess not only the BMI but also similar initial crowding (Table 3). These results were in
the percentage of fat mass.16 agreement with the findings of a previous study20 in
In the present study, the periodontal condition was which there was no significant difference in maxillary
evaluated before bonding the orthodontic appliances. and mandibular dental crowding in obese and non-
The probing depths and the number of sites with 4- to obese adolescents aged 13 years. According to that
5-mm pockets were significantly higher in obese study, obese and nonobese patients had similar needs
individuals (Table 2). A recent systematic review for orthodontic treatment.
reported there was a tendency for greater probing Obese patients perceived greater pain at all of the
depths in obese adolescents and found an association times evaluated, with a peak and significantly greater
between obesity and periodontitis.17 The adverse effect intensity than the control group after 24 hours (Table
of obesity on the periodontium can be mediated by 4). A previous, prospective cohort study21 assessed the
proinflammatory cytokines, such as interleukins, adi- influence of obesity on perceived orofacial pain in
pokines, and numerous other bioactive substances adolescents undergoing orthodontic therapy using
that are produced by adipose tissue, which are fixed appliances and showed that obesity was associ-
involved in the pathophysiology of obesity and peri- ated with higher pain levels and consumption of
odontitis.7 Therefore, the differences in periodontal analgesics compared with controls. These studies
parameters at baseline of the obese group were suggest that obesity influenced tooth movement by
already expected and were difficult to eliminate. affecting bone remodeling and also affected orthodon-
Obese adolescents had a higher prevalence of sites tic therapy–related parameters such as pain percep-
with bleeding on probing (BOP) (Table 2). BOP has tion.
been widely used as a sign of gingival inflammation In addition, obesity was associated with changes in
and active periodontal disease and is used for the adipokine, leptin, and resistin levels22 in the GCF, all of
purpose of determining periodontal health.18 The which have been reported to influence bone remodel-
findings of the present study were in agreement with ing and the function of osteoblasts/osteoclasts.23 Leptin
had numerically higher concentrations in the obese
Table 4. Comparison of the Mean Visual Analog Scale Scores for group at the four time points evaluated (Table 3). This
Perceived Pain, by Group and Time higher concentration in obese people can be explained
G1 G2 P by the fact that leptin is synthesized from adipose
T1 0.53 6 0.25 0.10 6 0.98 .110 tissue.24 One hypothesis would be a possible adapta-
T2 6.57 6 0.26 5.13 6 0.44 .006* tion with a change in the response of obese people to
T3 1.07 6 0.32 0.43 6 0.14 .074 the obesogenic environment based on a previous
* Statistically significant at P , .05. study in which rats were the experimental model.25

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TOOTH MOVEMENT IN OBESE ADOLESCENTS 99

Table 5. Comparisons of Leptin, IL-1b, and TNF-a Cytokine Concentrations Over Time, Within and Between Groups
T0 T1 T2 T3 Group Time Group 3 Time
Leptin, pg/mL
G1 14.9 (10.6–19.2) 14.8 (11.5–18.0) 12.0 (11.4–12.5) 13.0 (11.5–14.4) .08 .30 .41
G2 11.9 (11.3–12.4) 11.8 (11.4–12.0) 11.5 (11.3–11.7) 11.7 (11.4–12.0)
IL-1b, pg/mL
G1 10.3 (5.0–15.6) 12.8 (6.9–18.7) 20.1 (12.4–27.7) 17.9 (7.5–28.2) .01* .00* .61
G2 4.47 (2.9–6.0) 3.4 (1.7–5.0) 11.5 (3.9–19.0) 12.2 (5.6–18.8)
TNF-a, pg/mL
G1 0.47 (0.29–0.65) 0.90 (0.73–1.07) 0.80 (0.55–1.05) 0.40 (0.15–0.65) .28 .00* .34
G2 0.37 (0.19–0.54) 0.63 (0.44–0.83) 0.60 (0.33–0.87) 0.50 (0.26–0.74)

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* Statistically significant at P , .05.

There were decreases in leptin concentrations in supports the role of inflammation in initial tooth
relation to baseline at T1 and T2, with a slight increase movement.30 On the other hand, leptin levels de-
at T3 in both groups. A decrease IN leptin concentration creased in the first week. The hypothesis would be
in the GCF after 1 hour and 24 hours after bonding of that this was caused by leptin’s inhibition of bone
fixed appliances suggested that leptin may be one of resorption, which is desirable at the beginning of tooth
the mediators responsible for tooth movement.26 movement.
The decrease in leptin levels at the beginning of Despite the limitations of this investigation, the
tooth movement might possibly be explained by the results contribute to the scientific literature, since there
fact that leptin inhibits genesis and action of osteo- are few studies associating excess weight, pain, and
clasts.27 This decrease in GCF leptin concentration orthodontic tooth movement. The relationship between
might be consequent to tissue resorption in the obesity and orthodontic treatment, especially in relation
compressed and tension sites or even secondary to to tooth movement, remains unexplained because of
possible cell necrosis in the periodontal ligament the scarcity of studies in this area. Therefore, clinical
during orthodontic treatment.28 protocols should not yet be changed, and tooth
The correlation between salivary leptin and the slow resorption should not be considered to be associated
tooth movement rate in obese individuals was present- with obesity, as scientific data are insufficient.
ed previously.29 However, the current results demon-
strated that the tooth movement was similar in both CONCLUSIONS
groups (Table 3). The obese group had the highest
concentration of IL-1b cytokine 24 hours after bonding,  Obese adolescents displayed higher orofacial pain
while this occurred at 7 days in the control group. after 24 hours of orthodontic treatment and higher
According to a systematic review,7 the IL-1b cytokine concentrations of IL-1b proinflammatory cytokine
level peaked after 24 hours. On the other hand, before and during tooth movement than nonobese
another study reported that the peak was reached in adolescents did.
7 days.30 However, IL-1b is one of the chemical  There was no difference in tooth movement between
inflammatory mediators that induces secretion of obese and nonobese patients during the first week of
substances that cause pain.31 This fact can be orthodontic treatment.
confirmed by the intergroup difference in the levels of
cytokine and pain since obese individuals in the ACKNOWLEDGMENTS
present study reported peak pain after 24 hours,
coinciding with the peak concentration of IL-1b. This work was supported by the São Paulo Research
Foundation (FAPESP grant 2018/25934-0) and the
In both groups, there was an increase in the
Coordination of Superior Level Staff Improvement (CAPES
concentration of TNF-a cytokine at T1 and T2 in relation
financial code 001).
to baseline, with a decline at T3. This behavior followed
the pattern described in a systematic review,8 in which
DISCLOSURE
all evaluated studies showed an increase in the first 24
hours after bonding of fixed appliances, with a decline The authors declare no conflict of interest.
after 1 week. As was found in the current study, the
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Angle Orthodontist, Vol 92, No 1, 2022