P E D IA T R IC D E N T IS T R Y V 38 / NO 1 JAN / FEB 16

CASE-CONTROL STUDY

Caries Experience in Individuals with Moebius Syndrome

Talita Castro, DDS, MSc' • Adriana 0 1 . Ortega, DDS, PhD2 • Maria Carolina Mussi, DDS, PhD3 • Mariana M, Braga, DDS, PhD4 • Marina Gallottini, DMD, PhD5

A b stract: Purpose: M o e b iu s s y n d ro m e (M S ) is a ra re c o n g e n ita l fa c ia l d ip le g ia c h a ra c te riz e d b y p a r tia l o r c o m p le te s ix th a n d s e v e n th c ra n ia l

n e rv e palsy. O ro fa c ia l m a n ife s ta tio n s in c lu d e m ic ro g n a th ia , in c re a s e d o v e rb ite , h ig h a rc h e d p a la te , m o r p h o lo g ic a l c h a n g e s in th e to n g u e , a n d
d e n ta l c ro w d in g . Case re p o rts a n d s m a ll case series h a v e s h o w n a h ig h p re v a le n c e o f caries in M S p a tie n ts . The p u rp o s e o f th is s tu d y was
to c o m p a re th e p re v a le n c e o f caries b e tw e e n in d iv id u a ls w ith M o e b iu s s y n d ro m e a n d c o n tro ls u sin g th e In te rn a tio n a l Caries D e te c tio n a n d
A s s e s s m e n t S ys te m (ICDAS). M eth o d s : A t o ta l o f 9 0 p a rtic ip a n ts w ere d iv id e d in to tw o g ro u p s : (1) th e s tu d y g ro u p , c o m p ris in g 3 4 in d iv id u a ls
w ith M S ; a n d (Z) th e c o n tro l g ro u p , c o m p ris in g 5 6 a g e - a n d g e n d e r-m a tc h e d h e a lth y s u b je c ts w ith o u t MS. A ll in d iv id u a ls w e re e v a lu a te d f o r
th e p re s e n ce o f caries u sin g th e ICDAS. F o r s ta tis tic a l analysis, d iffe re n t IC D AS scores w e re u s e d as c u to ff p o in ts . Results: The n u m b e r o f
ca rio u s le sio n s in th e M S g ro u p was h ig h e r o n ly f o r e a rly -s ta g e ca ries (i.e., ICDAS scores o f I a n d 2 ; Z 7.0 ± 2 3 .0 versus 16.0±14.1 a n d 2 6 3 ± 2 3 .2
versus 15.2+13.6, re s p e ctive ly). Conclusion: M o e b iu s s y n d ro m e p a tie n ts h a v e m o r e e a rly ca rio u s le s io n s th a n c o n tro ls w ith o u t th e s y n d ro m e .
(P e d ia tr D e n t 2016;38(1):68-71) R eceived M a y 2 8 ,2 0 1 5 I L a st R evision O c to b e r 2 7 ,2 0 1 5 I A c c e p te d O c to b e r 2 7 ,2 0 1 5

KEYW ORDS: M O E B IU S S Y N D R O M E , D EN TAL C AR IES, FACIAL PARALYSIS

Moebius syndrome (MS) is a rare congenital facial diplegia (i.e., whether MS patients most commonly have mild, moder­
characterized by partial or complete sixth and seventh cranial ate, or severe caries).
nerve palsy. Other cranial nerves can also be affected, such as The International Caries Detection and Assessment System
the fifth, ninth, and 12th. MS is nonprogressive and is gener­ (ICDAS) is based on visual inspection for analysis and quan­
ally associated with limb reduction defects,1'2 and its etiology tification of carious lesions. It was developed to promote the
is multifactorial.3 The most widely accepted theory to explain current understanding of the initiation and progression of
the etiopathogenesis of MS is the interruption of blood supply carious lesions to the field of epidemiological and clinical
to the subclavian arteries during embryogenesis. It has been research.12
suggested that this interruption is due to exposure to terato­
genic agents during the first trimester of embryogenesis and
induces malformation of the hindbrain, resulting in the MS
phenotype.4
MS patients present with hypomimia (mask-like facies)
and convergent strabismus,5 with varying degrees of involve­
ment (Figure).6,7 In addition, they can have difficulty speaking
and chewing because of involvement of the tongue, lips, palate,
and, occasionally, larynx.8 Motor and morphological changes
in the tongue have frequently been reported, including impaired
tongue movements and unilateral lingual paresis.3 It is specu­
lated that MS patients are at increased risk for dental caries.9,10
A previous study11 examined oral motor performance in
the same group of MS patients and found a significant lack of
lip closure and dysphagia. This means that MS patients can be
considered a natural model of the lack of muscle activity and
the role of soft tissue (lip, cheek, and tongue) motion in the
etiopathogenesis of caries.11
To the best of our knowledge, no previous scientific stu­
dies have evaluated the prevalence of caries in MS patients or
characterized them based on the pattern of caries occurrence

1Dr. Castro is a PhD student, 3Dr. Mussi is a visiting professor, and 5Dr. G allottini is a
professor. Department o f Oral Pathology' and Special Patients. Special Care Dentistry-
Center, and 4Dr. Braga is an associate professor. D epartment o f Orthodontics an d Pedi­
atric Dentistry, all in the School o f Dentistry, University o f Sao Paulo, Sdo Paulo, Brazil.
2Dr. Ortega is an assistant professor. D epartment o f Pediatric Dentistry. Cruzeiro do Sul
University, Sao Paulo. Brazil.
Correspond w ith Dr. G allottini at mhcgmaga@usp. br
Figure. Oro-facial characteristics of individuals with Moebius syn­
drome. A) Front picture of a seven-year-old male patient showing
the mask-like face and the absence of lip closure. B) Lateral picture
o f a seven-year-old female p a tie n t show ing m icrognathia.
C) Picture of a 14-year-old female patient showing whitespots
on the teeth (arrows) indicative of initial caries. D) Picture of a
eight-year-old male patient showing malformation of the tongue.

68 C A R IE S E X P E R IE N C E IN M O E B IU S S Y N D R O M E
 PEDIATRIC DENTISTRY V 3 8 IN 0 1 JAN / FEB 16

This study’s hypothesis was that MS patients have more (2) the control group, comprising 56 age- and gender-matched
caries than those without MS. Therefore, the purpose of this healthy subjects without MS.
study was to compare the prevalence of caries between indivi­ All participants answered questions regarding their dietary
duals with Moebius syndrome and controls using the Inter­ and oral hygiene habits (Table 1). The questionnaire was based
national Caries Detection and Assessment System (ICDAS). on studies that evaluated caries risk based on dietary and hy­
giene habits.13,14 The subjects were subsequently evaluated for
Methods the presence of caries by means of the World Health Organi­
This research project was approved by the Research Ethics zation’s (W H O ) decayed, missing, and filled perm anent
Committee of the School of Dentistry, University of Sao Paulo, tooth surfaces (DMFS) index and the ICDAS. All evaluations
Sao Paulo, Brazil. All participants were recruited during their were performed in a single session by the same examiner who
dental visits, and inform ed consent was provided by their was not blinded to the patient’s condition. The examiner was
parents. A total of 90 participants were divided into two trained and calibrated in the use of the DMFS index and the
groups: (1) the study group, comprising 34 MS patients; and ICDAS, and the intraobserver reproducibility was 0.87. The
teeth were examined under artificial light and in relative isola­
tion after prophylaxis with a prophy brush and prophylaxis
Table 1. QUESTIONNAIRE ABOUT DIETARY AND paste. All tooth surfaces were evaluated using a W H O probe.
HYGIENE HABITS ANSWERED BY ALL MOEBIUS Univariate regression analysis was performed to deter­
SYNDROME PATIENTS AND CONTROLS mine whether having MS was associated with having at least
one carious lesion and with the number of decayed, missing,
Q u estio n S tudy C ontrol and filled tooth surfaces. Given that the present study included
group group subjects with primary, mixed, or permanent dentition, we chose
N (% ) N (% )
to use the sum of decayed, missing, and filled tooth surfaces
How many times do you eat daily?* for all teeth and decayed, missing, and filled primary tooth
surfaces. The values of decayed, missing, and filled primary
<3x 5(16.1) 0 (0 )
tooth surfaces (d m fs ) and decayed, missing, and filled primary
4-5x 10 (32.2) 23 (41.0) teeth ( d m f t ) were calculated using data obtained by the
6-7x 16(51.6) 33 (58.9) W H O criteria and ICDAS. To perform the statistical analysis,
>7x 0(0 ) 0 (0 ) we used five different cutoffs (Table 2) as follow: (1) Cut off
one— inclusion of all carious lesions, scores one to six for the
Do you breastfeed?
ICDAS indicated dental caries; (2) cutoff two— ICDAS scores
Yes 9 (26.5) 50 (89.2) zero and one were classified as sound, and scores two to six
W ho handles oral hygiene? were classified as decayed; (3) cutoff three— ICDAS scores
M other and/or father
zero to two were classified as sound, and three to six were
16 (47.0) 15 (26.7)
classified decayed; (4) cutoff four— ICDAS scores zero to three
The child 15 (44.1) 39 (69.6) were considered sound, and scores four to six were considered
Other 3 (8.8) 2 (3.5) decayed; and (5) cutoff five— ICDAS scores zero to four were
W hat is your toothbrushing frequen cy with fluoridated classified as sound, and scores five and six were considered
toothpaste per day? decayed.
The numbers of missing and filled teeth were also used
0 1 (2.9) 0 (0 )
as outcome measures. An ICDAS score of five (distinct cavity
lx 0(0 ) 7(12.5) with visible dentin) is equivalent to the W H O definition of
2x 12 (35.2) 24 (42.8) caries. For all analyses, the level of significance was set at five
3x 14 (71.1)
percent.
23 (41.0)
>4x 7 (20.5) 2 (3.5)
Do you floss?
Table 2. DIFFERENT INTERNATIONAL CARIES DETECTION
Never 20 (58.8) 34 (60.7)
AND ASSESSMENT SYSTEM (ICDAS) SCORES USED
lx/w k 7 (20.5) 16 (28.5) AS CUTOFF POINTS IN ORDER TO PERFORM
>2x/wk 2 (5.8) 0 (0 ) THE STATISTICAL ANALYSIS AND CLASSIFY CARIES
lx/day 4(11.7) 5 (8.9)
STATUS OF TOOTH SURFACES

>2x/day 1 (2.9) 1 (1-7) ICD A S Sound surface D ecayed surface

cutoff p oints
Do you use mouthwash with fluoride?
Never 28 (82.3) 43 (76.8) 1 ICDAS score 0 ICDAS scores 1-6
lx/w k 2 (5.8) 4(7.1) 2 ICDAS scores 0 and 1 ICDAS scores 2-6
>2x/wk 1 (2.9) 0 (0 ) ICDAS scores 0-2
3 ICDAS scores 3-6
lx/day 2 (5.8) 8 (14.2) 4 ICDAS scores 0-3 ICDAS scores 4-6
>2x/day 1 (2.9) 1 (1.7) ICDAS scores 0-4
5 ICDAS scores 5 and 6

* Three study group subjects used a nasogastric tube.

CARIES EXPERIENCE IN M O E B IU S S YNDROME 69

PEDIATRIC DENTISTRY V 38 / NO 1 JAN / FEB 16

Results versus 15.2± 13.6, respectively; Table 4). There were no signifi­
O f the 34 individuals in the study group, 17 (50 percent) were cant differences between the two groups when cutoff points
female and 17 (50 percent) were male. The mean age was 9.73 three, four, and five were used (Table 4). Considering the
years old +5.7 (standard deviation) years old. Among the 56 WHO DMFS index, there were no significant differences be­
individuals in the control group, 28 (50 percent) were female tween the two groups in terms of the number of teeth filled
and 28 (50 percent) were male. The mean age was 8.16±3.2 and missing due to caries.
years old. There were no statistically significant differences be­
tween the two groups in terms of gender or age. Discussion
The dietary habits of the individuals of both groups In the present study, the number of carious lesions was found
were similar (/U0.05) and consisted of meats, vegetables, and to be higher in MS participants than in age- and gender-
carbohydrates. O f the 34 MS participants, 26.4 percent had matched controls. Although a higher occurrence of carious
been breastfed. The oral hygiene habits of all participants were lesions had previously been reported in MS patients,6 this
similar and characterized by toothbrushing two or three times had never been systematically demonstrated before. Another
a day with fluoride toothpaste (Table 1). finding of the present study was that the number of carious le­
The two groups were similar in terms of the number of sions in the MS group was higher only for early-stage caries
individuals with caries in all cutoffs (/^D.05; Table 3). How­ (cutoff points one and two). To the best of our knowledge,
ever, caries experience of the MS patients was found to be the present study is the first to use a system that assesses the
higher than that of the controls when cutoff points one and various stages of carious lesions in order to diagnose caries in
two were used (27.0±23.0 versus 16.0±l4.1, and 26.3±23.2 special needs patients.
W hen we employed the W H O DMFS
index, we found no significant differences be­
tween the study and control groups in terms of
T a b le 3. N U M BE R OF M O EBIU S SYN D R O M E (M S) PATIENTS A N D CONTROLS (C)
the number of carious lesions. This finding
W H O H A D AT LEAST O NE CARIOUS LESION, AC CO RDING TO THE
reveals a limitation of using the W HO caries
INTERNATIO NAL CARIES DETECTION A N D ASSESSMENT SYSTEM (IC D AS)*
classification system in specific populations. If
ICDAS C u toff C u to ff C u to ff C u to ff C u to ff we had used the WHO system only, the results of
p o in t 1 p o in t 2 p o in t 3 p o in t 4 p o in t 5 the present study would have shown that MS
patients do not have more caries than do con­
Groups (total MS C MS C MS C MS C MS C trols. However, the ICDAS allowed us to detect
no. o f subjects) n =34 n =56 n =34 n =56 n =34 n =56 n =34 n =56 n =34 n =56
early-stage lesions, which were more common in
No. o f participants
33 51 33 51 27 44 24 37 22 36
the MS group.
with at least 1 The MS subjects who participated in the
(97) (91) (97) (91) (79.4) (78.6) (70.6) (66) (64.7) (64.3)
carious lesion n ( % )
present study make regular visits (no more than
P-value 0.50 0.50 0.86 0.83 0.85 six months apart) to the Special Care Dentistry
Center at the School of Dentistry, University of
* C u to ff point 1: ICDAS score o f 0=sound; ICDAS scores o f 1—6=decayed; cutoff point 2: Sao Paulo. These patients are part of a caries pre­
ICDAS scores o f 0 and l=sound; ICDAS scores o f 2—6=decayed; cutoff p o in t 3: ICDAS vention protocol that includes dental prophylaxis,
scores o f 0—2=sound; ICDAS scores o f 3—6=decayed; cu to ff p o in t 4: ICDAS scores o f instructions on oral hygiene, encouragement of
0-3 = so u n d ; ICDAS scores o f 4-6=decayed; cutoff point 5: ICDAS scores o f 0-4=sound;
ICDAS scores of 5 and 6=decayed.
proper oral hygiene, and fluoride varnish applied
to active carious lesions. The frequency of these
procedures might explain why the proportion of
advanced caries in these MS patients was not
T a b le 4 . M EAN S A N D STANDARD DEVIATIONS (SD) OF TH E NUM BERS OF CARIOUS higher. Nevertheless, the fact that early carious le­
LESIONS IN M O EBIU S SYN D R O M E (M S ) PATIENTS A N D CONTROLS (C) sions were detected in those participants shows
ACCO RDING TO THE INTERNATIO NAL CARIES DETECTION A N D that they remain at risk for caries and regular visits
ASSESSMENT SYSTEM (IC D AS)* to the clinic and a caries prevention protocol are
ICDAS C u to ff C u to ff C u to ff C u to ff C u to ff
important. We believe that close monitoring plays
p o in t 1 p o in t 2 p o in t 3 p o in t 4 p o in t 5 an important role in maintaining the oral health
of MS patients.
Groups MS C MS C MS C MS C MS C A reduction in the prevalence of caries in the
Mean of general population and the subsequent need for
27.0 16.0 26.3 15.2 13.3 10.4 11.9 9.1 11.3 8.5 evaluating enamel lesions—an evaluation that is
no. of
±23.0 +14.1 ±23.2 ±13.6 ±18.4 ±12.3 + 18.2 ±11.5 ±18.3 ±11.2
caries ±SD essential for preventing restorative procedures and
A-value 0.0013t 0.0012f 0.277 0.288 0.292
reducing associated costs12,15—resulted in the use
of tools and systems for assessing the various sta­
ges of caries, such as the ICDAS.15 In addition to
* C u to ff point 1: ICDAS score o f 0=sound; ICDAS scores o f l-6=decayed; cutoff point 2:
ICDAS scores o f 0 and l=sound; ICDAS scores o f 2—6=decayed; cutoff point 3: ICDAS
providing information on noncavitated carious
scores o f 0 -2 = so u n d ; ICDAS scores o f 3-6=decayed; c u to ff p o in t 4: ICDAS scores of lesions, the ICDAS can generate data that can be
0—3=sound; ICDAS scores o f 4-6=decayed; cutoff point 5: ICDAS scores o f 0-4=sound; compared with those from previous studies using
ICDAS scores of 5 and 6=decayed. the W HO caries classification system, which
t Statistically significant differences (P<0.001). assesses cavitated carious lesions only and has been

70 CARIES EXPERIENCE IN M O EBIU S SYN D R O M E


used in epidemiological studies since 1939.16 Furthermore,
the ICDAS has been found to have discriminatory validity in
analyses of social, behavioral, and dietary factors associated
with dental caries.17
This study’s limitation is that our sample size was derived
as a convenience sample. Both MS and control groups were
recruited during their dental visits to the University of Sao
Paulo. These subjects were already receiving preventive dental
care on a regular basis; therefore, their caries experience may
not be representative of the general population.
This study does not allow us to determine the responsible
factors for higher caries prevalence in MS patients. We assume
that impaired masticatory function and quantitative and qua­
litative salivary alterations may be present in this unique group
of individuals; thus, the potential impact of factors needs to
be studied further.
Conclusion
Based on this study’s results, the following conclusion can
be made:
1. Moebius syndrome patients have more early carious
lesions than controls without the syndrome.
References
1. Kumar D. Moebius syndrome. J Med Genet 1990;27:
122- 6 .
2. Stromland K, Sjogreen L, Miller M, et al. Mobius se­
quence: a Swedish multidiscipline study. Eur J Paediatr
Neurol 2002;6:35-45.
3. Verzijl HT, van der Zwaag B, Cruysberg JR, Padberg GW.
Mobius syndrome redefined: a syndrome of rhombence-
phalic maldevelopment. Neurology 2003;61:327-33.
4. Briegel W. Neuropsychiatric findings of Mobius se­
quence: a review. Clin Genet 2006;70:91-7.
5. MacKinnon S, Oystreck DT, Andrews C, Chan WM,
et al. Diagnostic distinctions and genetic analysis of
patients diagnosed with Moebius syndrome. Ophthal­
mology 2014;121:1461-8.
6. Jacob FD, Kanigan A, Richer L, El Hakim H. Unilateral
Mobius syndrome: two cases and a review of the litera­
ture. Int J Pediatr Otorhinolaryngol 2014;78:1228-31.
PED IA TR IC D E N T IS TR Y V 3 8 / NO 1 JAN / FEB 16
7. Matsui K, Kataoka A, Yamamoto A, et al. Clinical charac­
teristics and outcomes of Mobius syndrome in a chil­
dren’s hospital. Pediatr Neurol 2014;51:781-9.
8. Sjogreen L, Andersson-Norinder J, Jacobsson C. Develop­
ment of speech, feeding, eating, and facial expression in
Mobius sequence. Int J Pediatr Otorhinolaryngol 2001;
60:197-204.
9. De Serpa Pinto MV, De Magalhaes MH, Nunes FD.
Moebius syndrome with oral involvement. Int J Paediatr
Dent 2002;12:446-9.
10. Pradhan A, Gryst M. Atraumatic restorative technique:
case report on dental management of a patient with
Moebius syndrome. Aust Dent J 2015;60:255-9.
11. Ortega Ade O, Marques-Dias MJ, Santos MT, Castro T,
Gallottini M. Oral motor assessment in individuals with
Moebius syndrome. J Oral Pathol Med 2014;43:157-61.
12. Pitts N. “ICDAS”: an international system for caries de­
tection and assessment being developed to facilitate caries
epidemiology, research and appropriate clinical manage­
ment. Community Dent Health 2004;21:193-8.
13. Punitha VC, Amudhan A, Sivaprakasam P, Rathanaprabu
V. Role of dietary habits and diet in caries occurrence and
severity among urban adolescent school children. J Pharm
Bioallied Sci 2015;7(suppl 1):S296-S300.
14. Llena C, Leyda A, Forner L, Garcet S. Association between
the number of early carious lesions and diet in children
with high prevalence of caries. Eur J Paediatric Dent
2015;16:7-12.
15. Assaf AV, Zanin L, Meneghim Mde C, Pereira AC, Ambro-
sano GM. Comparison of reproducibility measurements
for calibration of dental caries epidemiological surveys.
Cad Saude Publica 2006;22(9): 1901-7.
16. Braga MM, Oliveira LB, Bonini GA, Bonecker M, Mendes
FM. Feasibility of the International Caries Detection and
Assessment System (ICDAS-II) in epidemiological sur­
veys and comparability with standard World Health Or­
ganization criteria. Caries Res 2009;43:245-9.
17. Ismail Al, Sohn W, Tellez M, et al. The International Ca­
ries Detection and Assessment System (ICDAS): an inte­
grated system for measuring dental caries. Community
Dent Oral Epidemiol 2007;35:170-8.
CARIES EXPERIEN C E IN M O E B IU S S Y N D R O M E 71
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