A comparative study on the prevalence of enamel defects and dental caries in children and adolescents with and without coeliac disease

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1 A comparative study on the prevalence of enamel defects and dental caries in children and adolescents with and without coeliac disease C.H. PRIOVOLOU, A.P. VANDERAS, L. PAPAGIANNOULIS ABSTRACT. Aim This was to test for differences in the prevalence of enamel defects and dental caries between children and adolescents with and without coeliac disease (CD). Materials and methods The sample consisted of 27 children and adolescents, aged 3 to 18 years with CD, and a control group of 27 healthy subjects matched by age and gender. Enamel defects were diagnosed and classified according to criteria described by Aine [1986], while dental caries was recorded as DMFT(S) and dmft(s) indices [Koch, 1970]. Dental plaque was recorded by the Plaque Control Record Index. Information related to medical history, oral hygiene habits, use of fluoride, history of dental trauma and socioeconomic factors was collected by a structured parental questionnaire. Also, in children with CD the age of initiation and diagnosis of the disease was recorded. Statistics The χ 2 and the paired t-test were used for the statistical analysis of the qualitative and quantitative data respectively. The logistic multiple regression analysis was applied to test whether the time period between the initiation and diagnosis of CD and other related factors had a significant (p 0.05) impact on the presence of enamel defects. Results The prevalence of enamel defects was higher in the CD group. Differences in frequency and symmetrical distribution of the defects were statistically significant between CD and control groups. With respect to dental caries, significant differences in the mean values of DMFS/dmfs were found between the two groups. Higher values of DMFS/dmfs were recorded in the control group. Conclusion CD increases the risk of developing enamel defects in permanent teeth but not of having dental caries. KEYWORDS: Coeliac disease, Enamel defects, Dental caries. Introduction Coeliac disease is a disorder of the mucous membrane of the small intestine which is characterized by a permanent intolerance to gluten found in wheat, rye, barley and oats [European Society of Paediatric Gastroenterology and Nutrition, 1970]. The clinical symptoms of the disease are vomiting, diarrhea, reduction in weight, abdominal distension, anaemia and retarded rate of growth in children and adolescents. The aetiology of coeliac disease is considered multifactorial involving environmental and genetic factors [Davidson and Bridges, 1987]. It has been reported that coeliac disease can influence the mineralization of permanent teeth [Rasmussen and Espelid, 1980; Martelosi and Department of Paediatric Dentistry, School of Dental Medicine, University of Athens, Greece Ventura, 1996]. The results of the studies, however, are contradictory as some reported a significant effect of coeliac disease on the prevalence of enamel defects in children and adolescents [Aine, 1986; Mariani et al., 1994; Ventura and Martelossi, 1997; Aguirre et al., 1997], while others did not find such a relationship [Shmerling et al., 1980; Andersson-Wenckert et al., 1984; Rasmusson and Eriksson, 2001]. In addition, four studies investigated the effect of coeliac disease on dental caries and found no significant differences between children and adolescents with and without the disease [Fulstow, 1979; McLoughlin et al., 1980; Andersson-Wenckert et al., 1984; Aguirre et al., 1997]. In these studies, the ages of the subjects were different between case and control groups and diagnostic criteria of dental caries were not well defined. It is conceivable that the effect of coeliac disease on enamel defects and dental caries needs further investigation. 102 EUROPEAN JOURNAL OF PAEDIATRIC DENTISTRY 2/2004

2 ENAMEL DEFECTS AND DENTAL CARIES IN CHILDREN WITH COELIAC DISEASE The purpose of this study was to test for differences in the prevalence of enamel defects and dental caries between children and adolescents with and without coeliac disease. Materials and methods Study population. The study population consisted of 27 children and adolescents, 10 boys and 17 girls, aged 3 to 18 years with coeliac disease, and a control group of 27 healthy children and adolescents matched by age and gender. The criterion used to match children by age was their date of birth. The control group consisted of children and adolescents who visited postgraduate and undergraduate paediatric dental clinics for prevention and/or dental treatment. Subjects who were present in the clinics during the examination period and met the criteria of age and gender were included in the study. All children were examined by one investigator, calibrated by a qualified paediatric dentist. Coeliac disease was diagnosed according to the criteria of the European Society of Paediatric Gastroenterology and Nutrition [1970]. Table 1 presents the distribution of subjects by age, gender and groups. Eighteen children in both groups had only primary teeth in their mouth. It has been reported that the mineralization of the crowns of the primary teeth is completed at about 6 months of age [Kraus, 1959]. As coeliac disease is manifested after the introduction of gluten in diet it is likely that it could not affect the development of enamel defects in the primary teeth. Concerning the enamel defects, therefore, these children were excluded from the statistical analysis. Thus, the final sample for the enamel defects was 18 subjects in each group, while for the dental caries the original sample was included. Medical and dental history. Information related to each child s medical history (diseases and medications), oral hygiene habits, use of fluoride and history of dental trauma was collected by a structured questionnaire distributed to the parents. Also, in those children with coeliac disease the age of initiation of the clinical symptoms, diagnosis of the disease and the elimination of gluten from the diet were recorded. Dental plaque examination. Dental plaque was recorded by the Plaque Control Record Index [O Leary et al., 1972]. According to this index, dental plaque was identified by its presence or absence on four surfaces of each tooth, namely mesial, distal, buccal and lingual after the use of disclosing solution. The index was calculated by dividing the number of surfaces with dental plaque by the total number of the examined surfaces multiplied by 100. Enamel defects. The teeth were cleaned and dried before the examination. Enamel defects were diagnosed and classified according to the criteria described by Aine [1986] as follows: - Grade 0 - No defect. - Grade I - Single or multiple cream, yellow or brown opacities with clearly defined or diffused margins. - Grade II - Enamel surface rough filled with horizontal grooves or shallow pits. - Grade III - A part or the entire surface of enamel is rough filled with deep horizontal grooves which vary in width or have large vertical pits. - Grade IV - The tips of cusps are sharp-pointed and/or the incisal edges are unevenly thinned and rough; the lesion is well defined and may be strongly discolored. All enamel defects were documented by intraoral photographs which were used to test the reliability of the defects diagnosis. Dental caries. The detection of dental caries was performed by a dental mirror and an explorer, using the criteria of [Koch, 1970]: - loss of tooth substance resulting in cavity formation. - stickiness of the explorer in the tooth substance so that a definite pull for removal is required. Dental caries was calculated by the DMFT(S) and dmft(s) indices. None of the children had been living in a water fluoridation area. Age (years) Groups Boys Girls Boys Girls Boys Girls Total Study Control Total TABLE 1 - Distribution of children with and without coeliac disease by age and gender. EUROPEAN JOURNAL OF PAEDIATRIC DENTISTRY 2/

3 C.H. PRIOVOLOU, A.P. VANDERAS, L. PAPAGIANNOULIS Radiographic examination. Two bite-wing radiographs were performed for each patient. Dental caries was recorded when a defined decrease, penetrating two thirds or more, took place in the density of the enamel [Koch, 1967]. Radiographs were examined in a view-box by one investigator. Socioeconomic factors. The socioeconomic factors such as parental age, education (as primary school, high school and college) and profession were collected by a structured questionnaire. The parents were asked to report any other education not included in the three categories. Using reported profession, the parents were classified as white or blue collar workers. Non-manual workers as well as shop sales assistants were classified as white collar group, while the rest were classified as blue collar group [Pearce, 1986]. Statistical methods. The data were computerized and the statistical package for social sciences (SPSS/PC+) was used for analysis. The χ 2 test was applied to test for differences in the history of diseases and medications, oral hygiene habits, use of fluoride, history of dental trauma, presence of enamel defects and socioeconomic factors between the CD and control groups. The paired t-test was used for differences in the height, weight, parent s age, dental plaque and dental caries. Finally, the logistic multiple regression analysis was carried out in the CD group to test whether prevalence of enamel defects was affected by the time period elapsed between the age of initiation of the symptoms of the disease and its diagnosis, child s age, gender, history of medications and dental trauma. The 95% probability level was used. Results Enamel defects. The prevalence of enamel defects in subjects with and without CD was 83.3% and 50% respectively; prevalence of symmetrical distribution was 44.4% in the study group and 11.1% in the control group. Table 2 presents the frequency of the different grades of enamel defects in children with and without CD. The χ 2 test showed statistically significant differences in the prevalence (χ 2 =4.5, p 0.03) and symmetrical distribution (χ 2 =4.98, p 0.02) of the enamel defects between the two groups. Differences in the frequency of the different grades of enamel defects were not statistically significant. No significant differences were found in the height, weight, parental age, parental education, mother s profession, use of fluoride, health problems and dental trauma between the CD and control groups. The χ 2 test showed significant differences in father s profession (χ 2 =5.10, p 0.02) and frequency of medications (χ 2 =4.43, p 0.03) between groups. The percentage of white collar workers was higher in the fathers of the CD group, but blue collar workers were higher in control group fathers. With respect to medications, subjects with CD disease received them, especially iron, more frequently than those without CD. The logistic multiple regression analysis performed in the study group showed that the time period elapsed between the initiation and diagnosis of the CD, subject s age, gender, medications and dental trauma did not have any significant effect on the presence of enamel defects. Of the total number of intraoral photographs, 85% were readable. Complete agreement was noted in the diagnosis and classification of enamel defects between these intraoral photographs and clinical examination. Dental caries. Table 3 shows mean values and standard deviations of the dental plaque and caries indices. The paired t-test showed statistically significant differences in the mean values of DMFS/dmfs (t=-2.09, p 0.04) between the two groups. The higher value was recorded in the CD group. Statistical differences in the Grade of Study group Control group defect* Number Prevalence Number Prevalence of cases % of cases % I 14** 70 9** II III IV *The criteria of classification are those reported by Aine [1986] **Two subjects in the study group and one in the control group had two grades of defect TABLE 2 - Classification of enamel defects in children with and without coeliac disease. 104 EUROPEAN JOURNAL OF PAEDIATRIC DENTISTRY 2/2004

4 ENAMEL DEFECTS AND DENTAL CARIES IN CHILDREN WITH COELIAC DISEASE Groups Dental DMFT/dmft DMFS/dmfs plaque Mean±SD Mean±SD Mean±SD Study group 73.2± ± ±6.86 (N=27) Control group 76.7± ± ±11.83 (N=27) TABLE 3 - Mean values (±SD) for dental plaque and dental caries indices in a group of children with coeliac disease and a control group matched for age and gender. dental plaque index, oral hygiene habits, use of fluoride, health problems, parental age, parental education and mother s profession were not found between groups. However, a significant difference was revealed in father s profession (χ 2 =5.85, p 0.01) with a higher frequency of blue collar workers in the control group and white collar workers in the CD group. Also, significant difference was found in the frequency of medications (χ 2 =5.59, p 0.01), especially ferric medication, between the two groups; higher value was recorded in the CD group. Discussion In this study the hypothesis tested was that CD does not affect the prevalence of enamel defects and dental caries significantly. With respect to the enamel defects, the χ 2 test rejected the null hypothesis since statistically significant differences in prevalence and symmetrical distribution of the defects were found between the CD and control groups. Besides, no significant differences in the frequency of other factors such as health problems, use of fluoride and dental trauma, which could affect the presence of enamel defects, were found. Regarding the socioeconomic factors, the significant difference found in father s profession should be attributed to chance, as no mechanism associating father s profession and enamel defects is known. Also, despite the fact that a significant difference in the consumption of ferric medication was found between the groups, it has not been shown that this medication has a significant impact on enamel mineralization. In addition, the multiple regression analysis did not reveal any significant effect of the medications on the presence of enamel defects in the CD group. These findings, therefore, imply that CD has a significant impact on the development of enamel defects. The results of this study are in agreement with those reported by other investigations [Aine, 1986; Mariani et al., 1994; Aguirre et al., 1997; Ventura and Martelossi, 1997]. In all these studies but one [Mariani et al., 1994], the same criteria of diagnosis and classification of enamel defects were used. Other studies found CD did not significantly impact the presence of enamel defects [Shmerling et al., 1980; Andersson-Wenckert et al., 1984; Rasmusson et al., 2001]; however, these studies did not use the same criteria for the recording of enamel defects and, therefore, their results are not comparable with those of the present study. The Aine s index used in this study was developed in children with CD. As the enamel defects in these patients form a uniform group and lesions are symmetrical and systematic, Aine [1986] reported that other indices are not suitable for defects found in children with CD. Significant differences in severity of enamel defects were not found between the CD and control groups. An explanation is that it is likely the different aetiologic factors, affecting enamel s mineralization during a particular stage, were of similar intensity and duration resulting in similar severity of enamel defects. In the present study, the great majority of enamel defects were of grade I (Table 2) in the CD group, while in the corresponding group of Aine s study [1986] most defects were of grade II (40%). This difference can be explained by the fact that in this study 73% of the cases with CD were diagnosed and treated before the second year of age, while in Aine s study 45% of the cases were diagnosed after the second year of age, implying a longer and more intense impact of the disease on the enamel mineralization process. Two mechanisms have been suggested to explain the effect of CD on the development of enamel defects. Firstly, hypocalcemia, resulting from calcium malabsorption during the clinical symptoms of the disease, is responsible for the defects [Smith and Miller, 1979; Rasmussen and Espelid, 1980; Andersson-Wenckert et al., 1984; Aine, 1986]. Secondly, that a particular genetic mechanism leads to a specific immune response to gluten [Maki et al., 1991]. According to this mechanism, antigens HLA DR3 and HLA DQW2 bound to major histocompatibility complex class II trigger an immune response to gluten and provoke the symptoms of CD and disturbances in enamel development. As no significant impact of the time between initiation and diagnosis of CD on the presence of enamel defects was found in this study, it is likely that CD and enamel defects are related to the same immunological mechanism. However, the pathogenetic mechanism of EUROPEAN JOURNAL OF PAEDIATRIC DENTISTRY 2/

5 C.H. PRIOVOLOU, A.P. VANDERAS, L. PAPAGIANNOULIS the enamel defects in patients with CD needs further investigation. With respect to dental caries, no significant differences were found in the mean values of DMFT/dmft between the CD and control groups. This finding is in agreement with the results of other investigations [Fulstow, 1979; McLoughlin et al., 1980; Andersson-Wenckert et al., 1984; Aguirre et al., 1997]. However, the paired t-test revealed a significant difference in the mean values of DMFS/dmfs, showing that the severity of dental disease is higher in the control group. An explanation of this is difficult as no differences were found between the groups in dental plaque, oral hygiene habits, use of fluorides and health problems. It is also likely that the significant differences found in father s profession and use of ferric medication are not related to severity of dental disease. In the present investigation, an explorer was used to diagnose dental caries in occlusal surfaces. It has been reported that probing the occlusal surfaces with an explorer can produce irreversible traumatic defects [Ekstrand et al., 1987; van Dorp et al., 1988]. The occurrence and size of the defects are strongly related to the degree of tissue opacity [Ekstrand et al., 1987]. It is believed that these opacities, which show a demineralized process of the tooth enamel, can remineralize. It should be pointed out that oral cavity represents a dynamic environment, and desirable conditions for remineralization may not be always present. In addition, it has been reported [Ripa, 1980] that occlusal surfaces get the least benefit from the exposure to fluoride and the placement of sealants on these surfaces is proposed to prevent the development of dental caries. Within this framework, it is likely that the effect of traumatic defect caused by the explorer is not clinically significant, provided that sealants are placed on these surfaces. Conclusion The present investigation provides evidence that coeliac disease increases the risk of developing enamel defects in permanent teeth. The great majority of the lesions were white opacities, especially on the first permanent molars, which were distributed symmetrically. Coeliac disease does not increase the risk of dental caries. Aknowledgements This study submitted to the graduate faculty of the School of Dental Medicine of the University of Athens in partial fulfillment of the requirements for the degree of Master of Dental Science. References Aguirre JM, Rodriguez R, Oribe D, Vitoria JC. Dental enamel defects in celiac patients. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1997 Dec;84(6): Aine L. Dental enamel defects and dental maturity in children and adolescents with coeliac disease. Proc Finn Dent Soc 1986;82 Suppl 3:1-71. Andersson-Wenckert I, Blomquist HK, Fredrikzon B. Oral health in coeliac disease and cow's milk protein intolerance. Swed Dent J 1984;8(1):9-14. Davidson AG, Bridges MA. Coeliac disease: a critical review of aetiology and pathogenesis. Clin Chim Acta 1987 Feb 27;163(1):1-40. Ekstrand K, Qvist V, Thylstrup A. Light microscope study of the effect of probing in occlusal surfaces. Caries Res 1987;21(4): European Society of Paediatric Gastroenterology and Nutrition. Diagnostic criteria in celiac disease. Acta Paediatr Scand 1970;59: Fulstow ED. Incidence of dental caries in coeliac children. Arch Dis Child 1979 Feb;54(2):166. Koch G. Effect of sodium fluoride in dentifrice and mouth wash on incidence of dental caries in schoolchildren. Odontol Revy 1967; Suppl 12. Koch G. Selection and caries prophylaxis of children with high caries activity. One-year results. Odontol Revy 1970;21(1): Kraus BS. Calcification of the human deciduous teeth. J Amer Dent Assoc 1959;59: Maki M, Aine L, Lipsanen V, Koskimies S. Dental enamel defects in first-degree relatives of coeliac disease patients. Lancet 1991 Mar 30;337(8744): Mariani P, Mazzilli MC, Margutti G, Lionetti P, Triglione P, Petronzelli F et al. Coeliac disease, enamel defects and HLA typing. Acta Paediatr 1994 Dec;83(12): McLoughlin MJ, McNeil S, Egan-Mitchell B. Incidence of dental caries in coeliac children. Arch Dis Child 1980 Jan;55(1):80. O Leary TJ, Drake RB, Naylor JE. The plaque control record. J Periodontol 1972 Jan;43(1):38. Pearce DW. The MIT dictionary of modern economics. 3rd ed. Cambridge, MA: The MIT Press; pp. 43, 455. Rasmussen P, Espelid I. Coeliac disease and dental malformation. ASDC J Dent Child 1980 May-Jun;47(3): Rasmusson CG, Eriksson MA. Celiac disease and mineralisation disturbances of permanent teeth. Int J Paediatr Dent 2001 May;11(3): Ripa LW. Occlusal sealants: rationale and review of clinical trials. Int Dent J 1980 Jun;30(2): Shmerling DH, Sacher M, Widmer B, Zur ED. Incidence of dental caries in coeliac children. Arch Dis Child 1980 Jan;55(1):80-1. Smith DM, Miller J. Gastro-enteritis, coeliac disease and enamel hypoplasia. Br Dent J 1979 Aug 21;147(4):91-5. Van Dorp CS, Exterkate RA, ten Cate JM. The effect of dental probing on subsequent enamel demineralization. ASDC J Dent Child 1988 Sep-Oct;55(5): Ventura A, Martelossi S. Dental enamel defects and coeliac disease. Arch Dis Child 1997 Jul;77(1): EUROPEAN JOURNAL OF PAEDIATRIC DENTISTRY 2/2004

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