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Vol 10, No 6 (2021)
Research paper
Published online: 2021-12-28

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Prevalence of celiac disease in patients with type 1 diabetes: a systematic review and meta-analysis

Ahmed Albatineh1, Fazel Dehvan2, Hossein Shariari2, Yousef Moradi2, Borhan Moradveisi2, Reza Ghanei Gheshlagh2
DOI: 10.5603/DK.2021.0055
Clin Diabetol 2021;10(6):447-461.

Abstract

Background. Celiac disease (CD) is more prevalent among

type 1 diabetes (T1D) patients compared to the general

population and can be accompanied by hypoglycemia

episodes in T1D patients. Studies worldwide have reported

CD prevalence with large variability. This study aimed

to estimate the pooled prevalence of CD in T1D patients.

Methods. PubMed, Web of Science, Science Direct, and

Scopus were searched without time limitation using

the keywords: Celiac Disease, Gluten Enteropathy, Gluten-

Sensitive Enteropathy, Wheat Hypersensitivity, Tissue

Transglutaminase Antibody, Endomysial Antibody

Disease, Diabetes Mellitus, and IDDM. Random-effects

inverse variance-weighted model, subgroup analysis,

and meta-regression were implemented. Heterogeneity

was examined using Cochran’s Q test and I2 statistics.

Results. A pooled analysis of 55 articles with total

sample size 71,853 revealed that the CD prevalence in

patients with T1D was 5.08% (95% CI: 4.44%, 5.73%)

with large heterogeneity (I2 = 84%). To account for

publication bias, using trim-and-fill method, the

pooled prevalence was 4.0% (95% CI: 3.38%, 4.73%).

The prevalence of CD was higher in Asia (6.53%, 95%

CI: 4.89%, 8.16%) compared to USA (4.89%, 95% CI:

3.85%, 5.93%) and Europe (4.76%, 95% CI: 3.78%,

5.74%). In addition, studies conducted after 2008

reported pooled prevalence (6.37%, 95% CI: 5.25%,

7.49%) significantly higher than those conducted before

2008 (4.14%, 95% CI: 3.19%, 5.09%). Studies with

quality score 10 had significantly higher prevalence

(7.0%, 95% CI: 5.04%, 8.96%) compared with quality

score 7 (3.66%, 95% CI: 2.61%, 4.70%).

Conclusion. CD is highly prevalent in T1D patients.

Studies from Asia, those published after the year 2008,

and studies with quality score 10 had higher pooled

CD prevalence. Therefore, early screening for CD in T1D

patients is important to prevent complications of CD.

Keywords: type 1 diabetesceliac diseaseprevalencemeta-analysis

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References

  1. Akar HH, Patiroglu T, Sevinc E, et al. Contribution of KIR genes, HLA class I ligands, and KIR/HLA class I ligand combinations on the genetic predisposition to celiac disease and coexisting celiac disease and type 1 diabetes mellitus. Rev Esp Enferm Dig. 2015; 107(9): 547–553.
    CrossRefPubMed
  2. Bhadada SK, Kochhar R, Bhansali A, et al. Prevalence and clinical profile of celiac disease in type 1 diabetes mellitus in north India. J Gastroenterol Hepatol. 2011; 26(2): 378–381.
    CrossRefPubMed
  3. Akirov A, Pinhas-Hamiel O. Co-occurrence of type 1 diabetes mellitus and celiac disease. World J Diabetes. 2015; 6(5): 707–714.
    CrossRefPubMed
  4. Crone J, Rami B, Huber WD, et al. Prevalence of celiac disease and follow-up of EMA in children and adolescents with type 1 diabetes mellitus. J Pediatr Gastroenterol Nutr. 2003; 37(1): 67–71.
    CrossRefPubMed
  5. Djurić Z, Stamenković H, Stanković T, et al. Celiac disease prevalence in children and adolescents with type 1 diabetes from Serbia. Pediatr Int. 2010; 52(4): 579–583.
    CrossRefPubMed
  6. Amin R, Murphy N, Edge J, et al. Coeliac disease in children and adolescents with IDDM: clinical characteristics and response to gluten-free diet. Diabet Med. 1998; 15(1): 38–44, doi: 10.1002/(SICI)1096-9136(199801)15:1<38::AID-DIA520>3.0.CO;2-L.
    PubMed
  7. Gillett PM, Gillett HR, Israel DM, et al. High prevalence of celiac disease in patients with type 1 diabetes detected by antibodies to endomysium and tissue transglutaminase. Can J Gastroenterol. 2001; 15(5): 297–301.
    CrossRefPubMed
  8. Picarelli A, Di Tola M, D'Amico T, et al. Type 1 diabetes mellitus and celiac disease: endothelial dysfunction. Acta Diabetol. 2013; 50(4): 497–503.
    CrossRefPubMed
  9. Kasiri K, Rostampour N, Lotfizadeh M, et al. Frequency of celiac disease in children with type 1 diabetes. Journal of Shahrekord University of Medical Sciences. 2018; 20(3): 72–81.
  10. Doğan B, Oner C, Bayramicli OU, et al. Prevalence of celiac disease in adult type 1 patients with diabetes. Pakistan Journal of Medical Sciences. 1969; 31(4).
    CrossRef
  11. Baptista ML, Koda YuK, Mitsunori R, et al. Prevalence of celiac disease in Brazilian children and adolescents with type 1 diabetes mellitus. J Pediatr Gastroenterol Nutr. 2005; 41(5): 621–624.
    CrossRefPubMed
  12. Nowier SR, Eldeen NS, Farid MM, et al. Prevalence of celiac disease among type 1 diabetic Egyptian patients and the association with autoimmune thyroid disease. Bratisl Lek Listy. 2009; 110(4): 258–262.
    PubMed
  13. Moher D, Liberati A, Tetzlaff J, et al. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA Statement. Open Med. 2009; 3(3): e123–e130.
    PubMed
  14. Farrugia MK, Kirsch AJ. Application of the strengthening the reporting of observational studies in epidemiology (STROBE) statement to publications on endoscopic treatment for vesicoureteral reflux. J Pediatr Urol. 2017; 13(3): 320–325.
    CrossRefPubMed
  15. Knapp G, Hartung J. Improved tests for a random effects meta-regression with a single covariate. Stat Med. 2003; 22(17): 2693–2710.
    CrossRefPubMed
  16. DerSimonian R, Laird N, DerSimonian R, et al. Meta-analysis in clinical trials. Control Clin Trials. 1986; 7(3): 177–188.
    CrossRefPubMed
  17. Higgins JPT, Thompson SG, Deeks JJ, et al. Measuring inconsistency in meta-analyses. BMJ. 2003; 327(7414): 557–560.
    CrossRefPubMed
  18. Agresti A, Coull B. Approximate is better than "exact" for interval estimation of binomial proportions. The American Statistician. 1998; 52(2): 119.
    CrossRef
  19. Newcombe RG. Two-sided confidence intervals for the single proportion: comparison of seven methods. Stat Med. 1998; 17(8): 857–872, doi: 10.1002/(sici)1097-0258(19980430)17:8<857::aid-sim777>3.0.co;2-e.
    PubMed
  20. Begg C, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics. 1994; 50(4): 1088.
    CrossRef
  21. Egger M, Davey Smith G, Schneider M, et al. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997; 315(7109): 629–634.
    CrossRefPubMed
  22. Duval S, Tweedie R. A Nonparametric "Trim and Fill" Method of Accounting for Publication Bias in Meta-Analysis. Journal of the American Statistical Association. 2000; 95(449): 89.
    CrossRef
  23. Duval S, Tweedie R. Trim and fill: A simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics. 2000; 56(2): 455–463.
    CrossRefPubMed
  24. R Core Team (2018). R: A language and environment for statistical computing. R Foundation for Statistical Computing V, Austria. URL: https://www.R-project.org/. [Last accessed at: 11.02.2021].
  25. Schwarzer G. An R package for meta-analysis. R news. 2007; 7(3): 40–45.
  26. Viechtbauer W. Conducting meta-analyses in R with the metafor package. Journal of statistical software. 2010; 36(3): 1–48.
  27. Sahin Y, Cakir M, Isakoca M, et al. Prevalence of celiac disease in children with type 1 diabetes mellitus in the south of turkey. Iranian Journal of Pediatrics. 2019; 30(1).
    CrossRef
  28. Odeh R, Alassaf A, Gharaibeh L, et al. Prevalence of celiac disease and celiac-related antibody status in pediatric patients with type 1 diabetes in Jordan. Endocr Connect. 2019; 8(6): 780–787.
    CrossRefPubMed
  29. Puñales M, Bastos MD, Ramos AR, et al. Prevalence of celiac disease in a large cohort of young patients with type 1 diabetes. Pediatr Diabetes. 2019; 20(4): 414–420.
    CrossRefPubMed
  30. Slae M, Romem A, Edri S, et al. Celiac disease and celiac antibodies in DM1 patients: when are screening and biopsy recommended? Dig Dis Sci. 2019; 64(2): 487–492.
    CrossRefPubMed
  31. Paruk IM, Naidoo VG, Pirie FJ, et al. Prevalence and characteristics of celiac disease in South African patients with type 1 diabetes mellitus: Results from the Durban Diabetes and Celiac Disease Study. J Gastroenterol Hepatol. 2019; 34(4): 673–678.
    CrossRefPubMed
  32. Velasco-Benítez CA, Ruíz-Extremera Á, Matallana-Rhoades AM, et al. Prevalence of markers of celiac disease in Colombian children with diabetes mellitus type 1. Colomb Med (Cali). 2018; 49(4): 273–279.
    CrossRefPubMed
  33. Singh P, Seth A, Kumar P, et al. Coexistence of celiac disease & type 1 diabetes mellitus in children. Indian J Med Res. 2017; 145(1): 28–32.
    CrossRefPubMed
  34. Craig ME, Prinz N, Boyle CT, et al. Prevalence of celiac disease in 52,721 youth with type 1 diabetes: international comparison across three continents. Diabetes Care. 2017; 40(8): 1034–1040.
    CrossRefPubMed
  35. Bianchi M, Cartabia M, Clavenna A, et al. Serological screening for celiac disease in a northern Italian child and adolescent population after the onset of type 1 diabetes: a retrospective longitudinal study of a 7-year period. Eur J Gastroenterol Hepatol. 2016; 28(6): 696–701.
    CrossRefPubMed
  36. Srivastava A, Chaturvedi S, Dabadghao P, et al. Prevalence of celiac disease in Indian children with type 1 diabetes. Indian J Gastroenterol. 2016; 35(5): 372–378.
    CrossRefPubMed
  37. Dogan B, Oner C, Bayramicli OU, et al. Prevalence of celiac disease in adult type 1 patients with diabetes. Pak J Med Sci. 2015; 31(4): 865–868.
    CrossRefPubMed
  38. Joshi R, Madvariya M. Prevalence and clinical profile of celiac disease in children with type 1 diabetes mellitus. Indian J Endocrinol Metab. 2015; 19(6): 797–803.
    CrossRefPubMed
  39. Honar N, Karamizadeh Z, Saki F. Prevalence of celiac disease in patients with type 1 diabetes mellitus in the south of Iran. Turk J Gastroenterol. 2013; 24(2): 122–126.
    CrossRefPubMed
  40. Bybrant MC, Örtqvist E, Lantz S, et al. High prevalence of celiac disease in Swedish children and adolescents with type 1 diabetes and the relation to the Swedish epidemic of celiac disease: a cohort study. Scand J Gastroenterol. 2014; 49(1): 52–58.
    CrossRefPubMed
  41. Al-Sinani S, Sharef SW, Al-Yaarubi S, et al. Prevalence of celiac disease in omani children with type 1 diabetes mellitus: a cross sectional study. Oman Med J. 2013; 28(4): 260–263.
    CrossRefPubMed
  42. Saadah OI, Al-Agha AE, Al Nahdi HM, et al. Prevalence of celiac disease in children with type 1 diabetes mellitus screened by anti-tissue transglutaminase antibody from Western Saudi Arabia. Saudi Med J. 2012; 33(5): 541–546.
    PubMed
  43. Al-Hussaini A, Sulaiman N, Al-Zahrani M, et al. High prevalence of celiac disease among Saudi children with type 1 diabetes: a prospective cross-sectional study. BMC Gastroenterol. 2012; 12: 180.
    CrossRefPubMed
  44. Mansour AA, Najeeb AA. Coeliac disease in Iraqi type 1 diabetic patients. Arab J Gastroenterol. 2011; 12(2): 103–105.
    CrossRefPubMed
  45. Uibo O, Heilman K, Rägo T, et al. Symptomless celiac disease in type 1 diabetes: 12-year experience in Estonia. Pediatr Int. 2010; 52(2): 230–233.
    CrossRefPubMed
  46. Fallahi GH, Ahmadian JH, Rabbani A, et al. Screening for celiac disease in diabetic children from Iran. Indian Pediatr. 2010; 47(3): 268–270.
    CrossRefPubMed
  47. Sari S, Yeşilkaya E, Eğritaş O, et al. Prevalence of celiac disease in Turkish children with type 1 diabetes mellitus and their non-diabetic first-degree relatives. Turk J Gastroenterol. 2010; 21(1): 34–38.
    CrossRefPubMed
  48. Ergür AT, Oçal G, Berberoğlu M, et al. Celiac disease and autoimmune thyroid disease in children with type 1 diabetes mellitus: clinical and HLA-genotyping results. J Clin Res Pediatr Endocrinol. 2010; 2(4): 151–154.
    CrossRefPubMed
  49. Narula P, Porter L, Langton J, et al. Gastrointestinal symptoms in children with type 1 diabetes screened for celiac disease. Pediatrics. 2009; 124(3): e489–e495.
    CrossRefPubMed
  50. Salardi S, Volta U, Zucchini S, et al. Prevalence of celiac disease in children with type 1 diabetes mellitus increased in the mid-1990 s: an 18-year longitudinal study based on anti-endomysial antibodies. J Pediatr Gastroenterol Nutr. 2008; 46(5): 612–614.
    CrossRefPubMed
  51. Remes-Troche JM, Rios-Vaca A, Ramírez-Iglesias MT, et al. High prevalence of celiac disease in Mexican Mestizo adults with type 1 diabetes mellitus. J Clin Gastroenterol. 2008; 42(5): 460–465.
    CrossRefPubMed
  52. Poulain C, Johanet C, Delcroix C, et al. Prevalence and clinical features of celiac disease in 950 children with type 1 diabetes in France. Diabetes Metab. 2007; 33(6): 453–458.
    CrossRefPubMed
  53. Goh C, Banerjee K. Prevalence of coeliac disease in children and adolescents with type 1 diabetes mellitus in a clinic based population. Postgrad Med J. 2007; 83(976): 132–136.
    CrossRefPubMed
  54. Tanure MG, Silva IN, Bahia M, et al. Prevalence of celiac disease in Brazilian children with type 1 diabetes mellitus. J Pediatr Gastroenterol Nutr. 2006; 42(2): 155–159.
    CrossRefPubMed
  55. Aygun C, Uraz S, Damci T, et al. Celiac disease in an adult Turkish population with type 1 diabetes mellitus. Dig Dis Sci. 2005; 50(8): 1462–1466.
    CrossRefPubMed
  56. Sanchez-Albisua I, Wolf J, Neu A, et al. Coeliac disease in children with Type 1 diabetes mellitus: the effect of the gluten-free diet. Diabet Med. 2005; 22(8): 1079–1082.
    CrossRefPubMed
  57. Mahmud FH, Murray JA, Kudva YC, et al. Celiac disease in type 1 diabetes mellitus in a North American community: prevalence, serologic screening, and clinical features. Mayo Clinic proceedings. 2005; 80(11): 1429–34.
  58. Laadhar L, Zitouni M, Kallel-Sellami M, et al. Celiac disease in adult patients with type 1 diabetes mellitus in Tunisia. Diabetes Metab. 2005; 31(1): 83–86.
    CrossRefPubMed
  59. Cerutti F, Bruno G, Chiarelli F, et al. Younger age at onset and sex predict celiac disease in children and adolescents with type 1 diabetes: an Italian multicenter study. Diabetes Care. 2004; 27(6): 1294–1298.
    CrossRefPubMed
  60. Crone J, Rami B, Huber WD, et al. Prevalence of celiac disease and follow-up of EMA in children and adolescents with type 1 diabetes mellitus. J Pediatr Gastroenterol Nutr. 2003; 37(1): 67–71.
    CrossRefPubMed
  61. Körner A, Tóth-Heyn P, Dezsofi A, et al. Frequency of coeliac disease in Hungarian children with type 1 diabetes mellitus. Eur J Pediatr. 2003; 162(1): 1–5.
    CrossRefPubMed
  62. Al-Ashwal AA, Shabib SM, Sakati NA, et al. Prevalence and characteristics of celiac disease in type I diabetes mellitus in Saudi Arabia. Saudi Med J. 2003; 24(10): 1113–1115.
    PubMed
  63. Güvenç S, Kaymakoğlu S, Gürel N, et al. The prevalence of manifest and latent celiac disease in type 1 diabetes mellitus. Turk J Gastroenterol. 2002; 13(2): 103–107.
    PubMed
  64. Spiekerkoetter U, Seissler J, Wendel U. General screening for celiac disease is advisable in children with type 1 diabetes. Horm Metab Res. 2002; 34(4): 192–195.
    CrossRefPubMed
  65. Barera G, Bonfanti R, Viscardi M, et al. Occurrence of celiac disease after onset of type 1 diabetes: a 6-year prospective longitudinal study. Pediatrics. 2002; 109(5): 833–838.
    CrossRefPubMed
  66. Hansen D, Bennedbaek FN, Hansen LK, et al. High prevalence of coeliac disease in Danish children with type I diabetes mellitus. Acta Paediatr. 2001; 90(11): 1238–1243.
    PubMed
  67. Aktay AN, Lee PC, Kumar V, et al. The prevalence and clinical characteristics of celiac disease in juvenile diabetes in Wisconsin. J Pediatr Gastroenterol Nutr. 2001; 33(4): 462–465.
    CrossRefPubMed
  68. Schober E, Bittmann B, Granditsch G, et al. Screening by anti-endomysium antibody for celiac disease in diabetic children and adolescents in Austria. J Pediatr Gastroenterol Nutr. 2000; 30(4): 391–396.
    CrossRefPubMed
  69. Vitoria JC, Castaño L, Rica I, et al. Association of insulin-dependent diabetes mellitus and celiac disease: a study based on serologic markers. J Pediatr Gastroenterol Nutr. 1998; 27(1): 47–52.
    CrossRefPubMed
  70. Roldan MB, Barrio R, Roy G, et al. Diagnostic value of serological markers for celiac disease in diabetic children and adolescents. J Pediatr Endocrinol Metab. 1998; 11(6): 751–756.
    CrossRefPubMed
  71. Fraser-Reynolds KA, Butzner JD, Stephure DK, et al. Use of immunoglobulin A-antiendomysial antibody to screen for celiac disease in North American children with type 1 diabetes. Diabetes Care. 1998; 21(11): 1985–1989.
    CrossRefPubMed
  72. Talal AH, Murray JA, Goeken JA, et al. Celiac disease in an adult population with insulin-dependent diabetes mellitus: Use of endomysial antibody testing. American Journal of Gastroenterology. 1997; 92(8): 1280–1284.
  73. Rensch MJ, Merenich JA, Lieberman M, et al. Gluten-sensitive enteropathy in patients with insulin-dependent diabetes mellitus. Ann Intern Med. 1996; 124(6): 564–567.
    CrossRefPubMed
  74. Saukkonen T, Savilahti E, Reijonen H, et al. Coeliac disease: frequent occurrence after clinical onset of insulin-dependent diabetes mellitus. Childhood Diabetes in Finland Study Group. Diabet Med. 1996; 13(5): 464–470, doi: 10.1002/(SICI)1096-9136(199605)13:5<464::AID-DIA101>3.0.CO;2-R.
    PubMed
  75. Sigurs N, Johansson C, Elfstrand PO, et al. Prevalence of coeliac disease in diabetic children and adolescents in Sweden. Acta Paediatr. 1993; 82(9): 748–751.
    CrossRefPubMed
  76. Baujat B, Mahé C, Pignon JP, et al. A graphical method for exploring heterogeneity in meta-analyses: application to a meta-analysis of 65 trials. Stat Med. 2002; 21(18): 2641–2652.
    CrossRefPubMed
  77. Singh P, Arora A, Strand TA, et al. Global prevalence of celiac disease: systematic review and Meta-analysis. Clin Gastroenterol Hepatol. 2018; 16(6): 823–836.e2.
    CrossRefPubMed
  78. Sharifi N, Khoshbaten M, Aliasgarzade A, et al. Celiac disease in patients with type-1 diabetes mellitus screened by tissue transglutaminase antibodies in northwest of Iran. Int J Diabetes Dev Ctries. 2008; 28(3): 95–99.
    CrossRefPubMed
  79. Uibo R, Sullivan EP, Uibo O, et al. Comparison of the prevalence of glutamic acid decarboxylase (GAD65) and gliadin antibodies (AGA) in a randomly selected adult estonian population. Horm Metab Res. 2001; 33(9): 564–567.
    CrossRefPubMed
  80. Singh P, Arora S, Singh A, et al. Prevalence of celiac disease in Asia: A systematic review and meta-analysis. J Gastroenterol Hepatol. 2016; 31(6): 1095–1101.
    CrossRefPubMed
  81. Makharia GK. Celiac disease screening in southern and East Asia. Dig Dis. 2015; 33(2): 167–174.
    CrossRefPubMed
  82. Cummins AG, Roberts-Thomson IC. Prevalence of celiac disease in the Asia-Pacific region. J Gastroenterol Hepatol. 2009; 24(8): 1347–1351.
    CrossRefPubMed
  83. Dubé C, Rostom A, Sy R, et al. The prevalence of celiac disease in average-risk and at-risk Western European populations: a systematic review. Gastroenterology. 2005; 128(4 Suppl 1): S57–S67.
    CrossRefPubMed
  84. Jameson JL. Harrison's principles of internal medicine. McGraw-Hill Education 2018.

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