Relationship Between Celiac Disease and Dental Caries in Children and Adolescents: A Systematic Review and Meta-Analysis

Albuquerque, Sylvia Amélia Vasconcelos de; Moreira, Kelly Maria Silva; Araújo, Djairo Vinícius Alves de; França, Glória Maria de; Nóbrega, Diego Figueiredo; Costa, Marcelo de Almeida; Santos, Natanael Barbosa dos; Imparato, José Carlos Pettorossi

doi:10.1590/pboci.2024.045

Sylvia Amélia Vasconcelos de Albuquerque

Conceptualization

Formal Analysis

Data Curation

Supervision

Department of Child Dental Health, Faculty of Dentistry, São Leopoldo Mandic College, Campinas, SP, Brazil

https://orcid.org/0000-0002-6449-1625

Kelly Maria Silva Moreira

Software

Formal Analysis

Resources

Department of Child Dental Health, Faculty of Dentistry, São Leopoldo Mandic College, Campinas, SP, Brazil

https://orcid.org/0000-0002-1137-3908

Djairo Vinícius Alves de Araújo

Methodology

Validation Investigation

Project Administration

Professional Master's Degree in Health Research, CESMAC University Center, Maceió, AL, Brazil

https://orcid.org/0009-0004-0199-5406

Glória Maria de França Corresponding author: Glória Maria de França E-mail:gloriafracam@gmail.com

Conceptualization

Methodology

Investigation

Professional Master's Degree in Health Research, CESMAC University Center, Maceió, AL, Brazil

https://orcid.org/0000-0002-0483-6601

Diego Figueiredo Nóbrega

Validation

Writing - Review

Editing

Visualization

and Project Administration.

Professional Master's Degree in Health Research, CESMAC University Center, Maceió, AL, Brazil

https://orcid.org/0000-0003-2288-4102

Marcelo de Almeida Costa

Validation

Funding Acquisition.

Faculty of Dentistry, Federal University of Alagoas, Maceió, AL, Brazil

https://orcid.org/0009-0008-1130-3564

Natanael Barbosa dos Santos

Software

Investigation

Writing - Original Draft

Supervision

Professional Master's Degree in Health Research, CESMAC University Center, Maceió, AL, Brazil

https://orcid.org/0000-0003-1811-2927

José Carlos Pettorossi Imparato

Validation

Writing - Review

Editing

Visualization

Supervision.

Department of Child Dental Health, Faculty of Dentistry, São Leopoldo Mandic College, Campinas, SP, Brazil

https://orcid.org/0000-0002-1990-2851

Corresponding author: Glória Maria de França E-mail:gloriafracam@gmail.com

Academic Editor: Alessandro Leite Cavalcanti

Conflict of Interest

The authors declare no conflicts of interest.

	Caries in the Permanent Dentition			Caries in the Primary Dentition
Authors	Index	Control	Celiac	Index	Control	Celiac
		Mean±SD	Mean±SD		Mean±SD	Mean±SD
Zoumpoulakis et al. [⁷[7] Zoumpoulakis M, Fotoulaki M, Topitsoglou V, Lazidou P, Zouloumis L, Kotsanos N. Prevalence of dental enamel defects, aphthous-like ulcers and other oral manifestations in celiac children and adolescents: A comparative study. J Clin Pediatr Dent 2019; 43(4):274-280. https://doi.org/10.17796/1053-4625-43.4.9 https://doi.org/10.17796/1053-4625-43.4.... ]	DMFT DMFS	NR p=0.788		dmft dmfs	NR
Cantekin et al. [¹⁰[10] Cantekin K, Arslan D, Delikan E. Presence and distribution of dental enamel defects, recurrent aphthous lesions and dental caries in children with celiac disease. Pak J Med Sci 2015; 31(3):606-609. https://doi.org/10.12669/pjms.313.6960 https://doi.org/10.12669/pjms.313.6960... ]	DMFT	1.83±1.78	3.75±2.62	dmft	4.56±2.87	3.25±3.25
Biçak et al. [¹²[12] Bıçak DA, Urgancı N, Akyüz S, Usta M, Kızılkan NU, Alev B, et al. Clinical evaluation of dental enamel defects and oral findings in coeliac children. Eur Oral Res 2018; 52(3):150-156. https://doi.org/10.26650/eor.2018.525 https://doi.org/10.26650/eor.2018.525... ]	DMFT / DMFS	6.77±4.43 / 8.96±8.75	4.48±3.67 / 6.20±6.74	dmft / dmfs	2.33±2.83 / 4.08±5.59	2.88±1.99 / 5.76±5.19
Acar et al. [¹³[13] Acar S, Yetkıner AA, Ersın N, Oncag O, Aydogdu S, Arıkan C. Oral findings and salivary parameters in children with celiac disease: A preliminary study. Med Princ Pract 2012; 21:129-133. https://doi.org/10.1159/000331794 https://doi.org/10.1159/000331794... ]	DMFS	2.60±5.3	2.74±5.70	dmfs	2.60±5.3	2.74± .70
Ortega Páez et al. [¹⁴[14] Ortega-Páez E, Lafuente PJ, García PB, Lozano JM, Calvo JCL. Prevalence of dental enamel defects in celiac patients with deciduous dentition: A pilot study. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2008; 106(1):74-78. https://doi.org/10.1016/j.tripleo.2008.01.022 https://doi.org/10.1016/j.tripleo.2008.0... ]				dmft / dmfs	0.70±1 / 0.73±1.57	0.17±0.64 / 0.23±0.97
Cruz et al. [¹⁵[15] Cruz ITSA, Fraiz FC, Celli A, Amenabar JM, Assunção LRS. Dental and oral manifestations of celiac disease. Med Oral Patol Oral Cir Bucal 2018; 23(6):e639-645. https://doi.org/10.4317/medoral.22506 https://doi.org/10.4317/medoral.22506... ]		n=9 [untreated caries]	n=12 [untreated caries]
Bramanti et al. [¹⁶[16] Bramanti E, Cicciù M, Matacena G, Costa S, Magazzù G. Clinical evaluation of specific oral manifestations in pediatric patients with ascertained versus potential coeliac disease: A cross-sectional study. Gastroenterol Res Pract 2014; 2014:934159. https://doi.org/10.1155/2014/934159 https://doi.org/10.1155/2014/934159... ]^ Potential celiac patients (mean DMFT: 1.57±1.87; mean dmft: 1.60±2.67); NR = Not Reported.	DMFT	2.41±1.63	2.52±3.22	dmft	1.86±1.98	1.07±1.63
Mina et al. [¹⁷[17] Mina S, Riga C, Azcurra AI, Brunotto M. Oral ecosystem alterations in celiac children: A follow-up study. Arch Oral Biol 2012; 57(2):154-160. https://doi.org/10.1016/j.archoralbio.2011.08.017 https://doi.org/10.1016/j.archoralbio.20... ]	DMFT	Baseline: 52% DMFT=0 18 months: 57% DMFT=0	Baseline: 76% DMFT=0 18 months: 87% DMFT=0	dmft	Baseline: 39% DMFT=0 18 months: 57% DMFT=0	Baseline: 35% DMFT=0 18 months: 87% DMFT=0
Alsadat et al. [²⁴[24] Alsadat FA, Alamoudi NM, El-Housseiny AA, Felemban OM, Dardeer FM, Saadah OI. Oral and dental manifestations of celiac disease in children: A case-control study. BMC Oral Health 2021; 21(1):669. https://doi.org/10.1186/s12903-021-01976-4 https://doi.org/10.1186/s12903-021-01976... ]	DMFT	1.90±2.18	2.81±3.21	dmft	6.56±4.20	5.01±4.0
Farmakis et al. [²⁵[25] Farmakis E, Puntis JWL, Toumba KJ. Enamel defects in children with coeliac disease. Eur J Paediatr Dent 2005; 6(3):129-132.]	DMFT / DMFS	0.71±0.52 / 2.14±1.83	0.13±0.12 / 0.13±0.12	dmft / dmfs	3.43±1.03 / 8.00±3.02	0.50±0.31 / 0.76±0.38
Shahraki et al. [²⁶[26] Shahraki T, Mehr SO, Hill ID, Shahraki M. A comparison of the prevalence of dental enamel defects and other oral findings in children with and without celiac disease. Iran J Pediatr 2019; 29(1):e64353. https://doi.org/10.5812/ijp.64353 https://doi.org/10.5812/ijp.64353... ]	DMFT	0.6±1.2	0.7±1.5	dmft	2.4±2.6	5.1±4.6
Saraceno et al. [²⁷[27] Saraceno R, Perugia C, Ventura A, Lore B, Chimenti S, Docimo R. Aphthous, coeliac disease and other dental disorders in childhood. G Ital Dermatol Venereol 2016; 151(3):239-243.]	NR	n=38 had caries (45%)	n=38 had caries (45%)
Shteyer et al. [²⁹[29] Shteyer E, Berson T, Lachmanovitz O, Hidas A, Wilschanski M, Menachem M, et al. Oral health status and salivary properties in relation to gluten-free diet in children with celiac disease. J Pediatr Gastroenterol Nutr 2013; 57(1):49-52. https://doi.org/10.1097/MPG.0b013e31828b3705 https://doi.org/10.1097/MPG.0b013e31828b... ]	Mean DMFT / dmft	DMFT / dmft (mean 3.4±3.7)	Recently diagnosed celiac: DMFT/dmft (mean 1.5±2.2) Celiac without gluten + 6 months: DMFT/dmft (mean 2.0±2.6)
Bolgül et al. [³⁰[30] Bolgül BS, Arslanoğlu Z, Tumen EC, Yavuz I, Çelenk S, Atakul F. Significance of oral symptoms in early diagnosis and treatment of celiac disease. Turkiye Klinikleri J Med Sci 2009; 29(3):599-604.]	DMFT	6.9±1.7	2.4± 1.3
Avşar and Kalayci [³⁴[34] Avşar A, Kalayci AG. The presence and distribution of dental enamel defects and caries in children with celiac disease. Turk J Pediatr 2008; 50(1):45-50.]	DMFT	6.4±4.32^* * Mean of the group without gluten restriction;	6.1±4.28
de Carvalho et al. [³⁵[35] de Carvalho FK, Queiroz AM, Silva RAB, Sawamura R, Bachmann L, Silva LAB, et al. Oral aspects in celiac disease children: Clinical and dental enamel chemical evaluation. Oral Surg Oral Med Oral Pathol Oral Radiol 2015; 119(6):636-643. https://doi.org/10.1016/j.oooo.2015.02.483 https://doi.org/10.1016/j.oooo.2015.02.4... ]	DMFT	3.90±5.2	2.11±3.2
Dane and Gürbüz [³⁶[36] Dane A, Gürbüz T. Clinical evaluation of specific oral and salivary findings of coeliac disease in eastern Turkish paediatric patients. Eur J Paediatr Dent 2016; 17(1):53-56.]	DMFT	4.71±1.9	4.74±3.46	dmft	2.3±2.0	2.63±3

	Study Design	Selection			Comparability	Outcome		Total^# # Maximum = 9 Stars; Selection: (1) (a) truly representative of the mean of the target population or (b) poorly representative of the mean of the target population (1 star), (c) selected group of users, (d) no description; (2) (a) justified and satisfactory (1 star), (b) not justified; (3) (a) biopsy diagnosis (2 stars), (b) no description of the diagnostic method (1 star); Comparability: (1) (a) study controlled for the most critical factor (age matching) (1 star), (b) study controlled for any additional factor (serological test for two groups) (2 stars); Outcome: (1) (a) independent blind assessment of dental caries or (b) record linkage (2 stars), (c) no description; (2) (a) the statistical test used to analyze the data is clearly described and appropriate, and the measurement of the association is present (1 star), (b) the statistical test is not appropriate, not described, or incomplete.
Authors		Representativeness of the Sample	Sample Size	Ascertainment of Exposure	Based on Design and Analysis	Assessment of Outcome	Statistical Test
Zoumpoulakis et al. [⁷[7] Zoumpoulakis M, Fotoulaki M, Topitsoglou V, Lazidou P, Zouloumis L, Kotsanos N. Prevalence of dental enamel defects, aphthous-like ulcers and other oral manifestations in celiac children and adolescents: A comparative study. J Clin Pediatr Dent 2019; 43(4):274-280. https://doi.org/10.17796/1053-4625-43.4.9 https://doi.org/10.17796/1053-4625-43.4.... ]	Cross-sectional	★	-	★★	★★	-	★	6
Cantekin et al. [¹⁰[10] Cantekin K, Arslan D, Delikan E. Presence and distribution of dental enamel defects, recurrent aphthous lesions and dental caries in children with celiac disease. Pak J Med Sci 2015; 31(3):606-609. https://doi.org/10.12669/pjms.313.6960 https://doi.org/10.12669/pjms.313.6960... ]	Cross-sectional	★	-	★	★	-	★	4
Biçak et al. [¹²[12] Bıçak DA, Urgancı N, Akyüz S, Usta M, Kızılkan NU, Alev B, et al. Clinical evaluation of dental enamel defects and oral findings in coeliac children. Eur Oral Res 2018; 52(3):150-156. https://doi.org/10.26650/eor.2018.525 https://doi.org/10.26650/eor.2018.525... ]	Cross-sectional	★	★	★★	★★	★★	★	9
Acar et al. [¹³[13] Acar S, Yetkıner AA, Ersın N, Oncag O, Aydogdu S, Arıkan C. Oral findings and salivary parameters in children with celiac disease: A preliminary study. Med Princ Pract 2012; 21:129-133. https://doi.org/10.1159/000331794 https://doi.org/10.1159/000331794... ]	Cross-sectional	★	-	★★	★	-	★	5
Ortega Páez et al. [¹⁴[14] Ortega-Páez E, Lafuente PJ, García PB, Lozano JM, Calvo JCL. Prevalence of dental enamel defects in celiac patients with deciduous dentition: A pilot study. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2008; 106(1):74-78. https://doi.org/10.1016/j.tripleo.2008.01.022 https://doi.org/10.1016/j.tripleo.2008.0... ]	Cross-sectional	★	-	★★	★★	-	★	6
Cruz et al. [¹⁵[15] Cruz ITSA, Fraiz FC, Celli A, Amenabar JM, Assunção LRS. Dental and oral manifestations of celiac disease. Med Oral Patol Oral Cir Bucal 2018; 23(6):e639-645. https://doi.org/10.4317/medoral.22506 https://doi.org/10.4317/medoral.22506... ]	Cross-sectional	★	-	★★	★	-	★	5
Bramanti et al. [¹⁶[16] Bramanti E, Cicciù M, Matacena G, Costa S, Magazzù G. Clinical evaluation of specific oral manifestations in pediatric patients with ascertained versus potential coeliac disease: A cross-sectional study. Gastroenterol Res Pract 2014; 2014:934159. https://doi.org/10.1155/2014/934159 https://doi.org/10.1155/2014/934159... ]	Cross-sectional	★	-	★★	★	★★	★	7
Mina et al. [¹⁷[17] Mina S, Riga C, Azcurra AI, Brunotto M. Oral ecosystem alterations in celiac children: A follow-up study. Arch Oral Biol 2012; 57(2):154-160. https://doi.org/10.1016/j.archoralbio.2011.08.017 https://doi.org/10.1016/j.archoralbio.20... ]	Longitudinal	★	-	★★	★	-	★	5
Alsadat et al. [²⁴[24] Alsadat FA, Alamoudi NM, El-Housseiny AA, Felemban OM, Dardeer FM, Saadah OI. Oral and dental manifestations of celiac disease in children: A case-control study. BMC Oral Health 2021; 21(1):669. https://doi.org/10.1186/s12903-021-01976-4 https://doi.org/10.1186/s12903-021-01976... ]	Cross-sectional	★	★	★★	★	-	★	6
Farmakis et al. [²⁵[25] Farmakis E, Puntis JWL, Toumba KJ. Enamel defects in children with coeliac disease. Eur J Paediatr Dent 2005; 6(3):129-132.]	Cross-sectional	-	-	★	★	-	★	3
Shahraki et al. [²⁶[26] Shahraki T, Mehr SO, Hill ID, Shahraki M. A comparison of the prevalence of dental enamel defects and other oral findings in children with and without celiac disease. Iran J Pediatr 2019; 29(1):e64353. https://doi.org/10.5812/ijp.64353 https://doi.org/10.5812/ijp.64353... ]	Cross-sectional	★	-	★★	★	★★	★	7
Saraceno et al. [²⁷[27] Saraceno R, Perugia C, Ventura A, Lore B, Chimenti S, Docimo R. Aphthous, coeliac disease and other dental disorders in childhood. G Ital Dermatol Venereol 2016; 151(3):239-243.]	Cross-sectional	★	-	★	★	-	★	4
Shteyer et al. [²⁹[29] Shteyer E, Berson T, Lachmanovitz O, Hidas A, Wilschanski M, Menachem M, et al. Oral health status and salivary properties in relation to gluten-free diet in children with celiac disease. J Pediatr Gastroenterol Nutr 2013; 57(1):49-52. https://doi.org/10.1097/MPG.0b013e31828b3705 https://doi.org/10.1097/MPG.0b013e31828b... ]	Cross-sectional	★	-	★★		★★	★	6
Bolgül et al. [³⁰[30] Bolgül BS, Arslanoğlu Z, Tumen EC, Yavuz I, Çelenk S, Atakul F. Significance of oral symptoms in early diagnosis and treatment of celiac disease. Turkiye Klinikleri J Med Sci 2009; 29(3):599-604.]	Cross-sectional	★	-	★★	★	-	★	5
Avşar and Kalayci [³⁴[34] Avşar A, Kalayci AG. The presence and distribution of dental enamel defects and caries in children with celiac disease. Turk J Pediatr 2008; 50(1):45-50.]	Cross-sectional	★	-	★★	★	-	★	5
de Carvalho et al. [³⁵[35] de Carvalho FK, Queiroz AM, Silva RAB, Sawamura R, Bachmann L, Silva LAB, et al. Oral aspects in celiac disease children: Clinical and dental enamel chemical evaluation. Oral Surg Oral Med Oral Pathol Oral Radiol 2015; 119(6):636-643. https://doi.org/10.1016/j.oooo.2015.02.483 https://doi.org/10.1016/j.oooo.2015.02.4... ]	Cross-sectional	★	-	★	★	-	★	4
Dane and Gürbüz [³⁶[36] Dane A, Gürbüz T. Clinical evaluation of specific oral and salivary findings of coeliac disease in eastern Turkish paediatric patients. Eur J Paediatr Dent 2016; 17(1):53-56.]	Cross-sectional	★	-	★★	★	-	★	5

[1] Corresponding author: Glória Maria de França E-mail:gloriafracam@gmail.com

Brasil

Brasil

Relationship Between Celiac Disease and Dental Caries in Children and Adolescents: A Systematic Review and Meta-Analysis

ABSTRACT

Objective:

Material and Methods:

Results:

Conclusion: