Skip to main content
Top
Published in: BMC Gastroenterology 1/2012

Open Access 01-12-2012 | Research article

High prevalence of celiac disease among Saudi children with type 1 diabetes: a prospective cross-sectional study

Authors: Abdulrahman Al-Hussaini, Nimer Sulaiman, Musa Al-Zahrani, Ahmed Alenizi, Imad El Haj

Published in: BMC Gastroenterology | Issue 1/2012

Login to get access

Abstract

Background

There is lack of data on prevalence of celiac disease (CD) in children with type 1 diabetes (T1D) in Arabs in the Middle East. The present investigation aims to study the prevalence rate and clinical characteristics of CD among Saudi children with T1D using a combination of the most sensitive and specific screening serologic tests (anti- tissue transglutaminase antibodies IgA [anti-TTG] and ednomyseal antibodies [EMA]) and to determine the lower cut-off value of anti- anti-TTG level that best predicts CD in children with T1D.

Methods

Children with T1D following in diabetic clinic have been prospectively screened for presence of CD, over a two-year period (2008–2010), by doing anti-TTG, EMA, and total IgA. Children with positive anti-TTG titres (>50 U/ml) and/or EMA and children with persistently low positive anti-TTG titres (two readings 20–50 U/ml; within 6 months intervals) had upper endoscopy and 6 duodenal biopsies.

Results

One hundred and six children with T1D have been screened for CD: age ranged between 8 months to 15.5 years (62 females). Nineteen children had positive anti-TTG and/or EMA, however only 12 children had biopsy proven CD (11.3%). Five of 12 had gastrointestinal symptoms (42%). Children with T1D and CD had significantly lower serum iron than children with T1D alone (8.5 μgm/L Vs 12.5 μgm/L; P = 0.014). The sensitivity and specificity of anti-TTG were 91.6% and 93.6%, with a positive and negative predictive value of 64.7% and 98.8%, respectively. Receiver operated characteristics analysis for the best cut-off value of anti-TTG level for diagnosis of CD was 63 units (sensitivity 100% and specificity 98.8%).

Conclusion

CD is highly prevalent among Saudi children with T1D. Anti-TTG titres more than 3 times the upper limit of normal has very high sensitivity and specificity for diagnosis of CD in T1D children.
Appendix
Available only for authorised users
Literature
1.
go back to reference Tanure MG, Silva IN, Bahia M, Penna FJ: Prevalence of celiac disease in Brasilian children with type 1 diabetes mellitus. J Pediatr Gastroenterol Nutr. 2006, 42: 155-159. 10.1097/01.mpg.0000189338.15763.4a.CrossRefPubMed Tanure MG, Silva IN, Bahia M, Penna FJ: Prevalence of celiac disease in Brasilian children with type 1 diabetes mellitus. J Pediatr Gastroenterol Nutr. 2006, 42: 155-159. 10.1097/01.mpg.0000189338.15763.4a.CrossRefPubMed
2.
go back to reference Sakly W, Bienvenu F, Peretti N, Lachaux A, Morel S, Bouvier R, Nicolino M, Bienvenu J, Spiteri A, Fabien N: IgA anti-transglutaminase antibodies as a tool for screening atypical forms of coeliac disease in a French at-risk paediatric population. Eur J Gastroenterol Hepatol. 2005, 17: 235-239. 10.1097/00042737-200502000-00016.CrossRefPubMed Sakly W, Bienvenu F, Peretti N, Lachaux A, Morel S, Bouvier R, Nicolino M, Bienvenu J, Spiteri A, Fabien N: IgA anti-transglutaminase antibodies as a tool for screening atypical forms of coeliac disease in a French at-risk paediatric population. Eur J Gastroenterol Hepatol. 2005, 17: 235-239. 10.1097/00042737-200502000-00016.CrossRefPubMed
3.
go back to reference Boudraa G, Hachelaf W, Benbouabdellah M, Belkadi M, Benmansour FZ, Touhami M: Prevalence of coeliac disease in diabetic children and their first-degree relatives in west Algeria: screening with serological markers. Acta Paediatr. 1996, 412 (suppl): 58-60.CrossRef Boudraa G, Hachelaf W, Benbouabdellah M, Belkadi M, Benmansour FZ, Touhami M: Prevalence of coeliac disease in diabetic children and their first-degree relatives in west Algeria: screening with serological markers. Acta Paediatr. 1996, 412 (suppl): 58-60.CrossRef
4.
go back to reference Fraser-Reynolds KA, Butzner JD, Stephure DK, Trussell RA, Scott RB: Use of immunoglobulin A-antiendomysial antibody to screen for celiac disease in North American children with type 1 diabetes. Diabetes Care. 1998, 21: 1985-1989. 10.2337/diacare.21.11.1985.CrossRefPubMed Fraser-Reynolds KA, Butzner JD, Stephure DK, Trussell RA, Scott RB: Use of immunoglobulin A-antiendomysial antibody to screen for celiac disease in North American children with type 1 diabetes. Diabetes Care. 1998, 21: 1985-1989. 10.2337/diacare.21.11.1985.CrossRefPubMed
5.
go back to reference Hansen D, Bennedbaek FN, Hansen LK, Høier-Madsen M, Hegedü LS, Jacobsen BB, Husby S: High prevalence of coeliac disease in Danish children with type I diabetes mellitus. Acta Paediatr. 2001, 90: 1238-1243. 10.1111/j.1651-2227.2001.tb01568.x.CrossRefPubMed Hansen D, Bennedbaek FN, Hansen LK, Høier-Madsen M, Hegedü LS, Jacobsen BB, Husby S: High prevalence of coeliac disease in Danish children with type I diabetes mellitus. Acta Paediatr. 2001, 90: 1238-1243. 10.1111/j.1651-2227.2001.tb01568.x.CrossRefPubMed
6.
go back to reference Mankaï A, Ben Hamouda H, Amri F, Ghedira-Besbes L, Harbi A, TaharSfar M, SahloulEssoussi A, Jeddi M, Ghedira I: Screening by anti-endomysium antibodies for celiac disease in Tunisian children with type 1 diabetes mellitus. Gastroenterol Clin Biol. 2007, 31: 462-466. 10.1016/S0399-8320(07)89413-9.CrossRefPubMed Mankaï A, Ben Hamouda H, Amri F, Ghedira-Besbes L, Harbi A, TaharSfar M, SahloulEssoussi A, Jeddi M, Ghedira I: Screening by anti-endomysium antibodies for celiac disease in Tunisian children with type 1 diabetes mellitus. Gastroenterol Clin Biol. 2007, 31: 462-466. 10.1016/S0399-8320(07)89413-9.CrossRefPubMed
7.
go back to reference Ashabani A, Abushofa U, Abusrewill S, Abdelazez M, Tucková L, Tlaskalová-Hogenová H: The prevalence of coeliac disease in Libyan children with type 1 diabetes mellitus. Diabetes Metab Res Rev. 2003, 19: 69-75. 10.1002/dmrr.333.CrossRefPubMed Ashabani A, Abushofa U, Abusrewill S, Abdelazez M, Tucková L, Tlaskalová-Hogenová H: The prevalence of coeliac disease in Libyan children with type 1 diabetes mellitus. Diabetes Metab Res Rev. 2003, 19: 69-75. 10.1002/dmrr.333.CrossRefPubMed
8.
go back to reference Al-Ashwal A, Shabib S, Sakati N, Attia N: Prevalence and characterstics of celiac disease in type 1 diabetes mellitus in Saudi Arabia. Saudi Med J. 2003, 24: 1113-1115.PubMed Al-Ashwal A, Shabib S, Sakati N, Attia N: Prevalence and characterstics of celiac disease in type 1 diabetes mellitus in Saudi Arabia. Saudi Med J. 2003, 24: 1113-1115.PubMed
9.
go back to reference Rostom A, Dubé C, Cranney A, Saloojee N, Sy R, Garritty C, Sampson M, Zhang L, Yazdi F, Mamaladze V, Pan I, McNeil J, Moher D, Mack D, Patel D: Celiac disease. Evid Rep Technol Assess (Summ). 2004, 104: 1-6. Rostom A, Dubé C, Cranney A, Saloojee N, Sy R, Garritty C, Sampson M, Zhang L, Yazdi F, Mamaladze V, Pan I, McNeil J, Moher D, Mack D, Patel D: Celiac disease. Evid Rep Technol Assess (Summ). 2004, 104: 1-6.
10.
go back to reference Saadah OI, Al-Agha AE, Al Nahdi HM, Bokhary RY, Bin Talib YY, Al-Mughales JA, Al Bokhari SM: 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: 541-546.PubMed Saadah OI, Al-Agha AE, Al Nahdi HM, Bokhary RY, Bin Talib YY, Al-Mughales JA, Al Bokhari SM: 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: 541-546.PubMed
11.
go back to reference Dahlbom I, Korponay-Szabo IR, Kovacs JB, Szalai Z, Maki M, Hansson T: Prediction ofclinical and mucosal severity of coeliac disease and dermatitis herpetiformis by quantification of IgA/IgG serum antibodies to tissue transglutaminase. J Pediatr Gastroenterol Nutr. 2010, 50: 140-146. 10.1097/MPG.0b013e3181a81384.CrossRefPubMed Dahlbom I, Korponay-Szabo IR, Kovacs JB, Szalai Z, Maki M, Hansson T: Prediction ofclinical and mucosal severity of coeliac disease and dermatitis herpetiformis by quantification of IgA/IgG serum antibodies to tissue transglutaminase. J Pediatr Gastroenterol Nutr. 2010, 50: 140-146. 10.1097/MPG.0b013e3181a81384.CrossRefPubMed
12.
go back to reference Hill PG, Holmes GK: Coeliac disease: a biopsy is not always necessary for diagnosis. Aliment Pharmacol Ther. 2008, 27: 572-577. 10.1111/j.1365-2036.2008.03609.x.CrossRefPubMed Hill PG, Holmes GK: Coeliac disease: a biopsy is not always necessary for diagnosis. Aliment Pharmacol Ther. 2008, 27: 572-577. 10.1111/j.1365-2036.2008.03609.x.CrossRefPubMed
13.
go back to reference Vivas S, de Morales JG R, Riestra S, Arias L, Fuentes D, Alvarez N, Calleja S, Hernando M, Herrero B, Casqueiro J, Rodrigo L: Duodenal biopsy may be avoided when high transglutaminase antibody titers are present. World J Gastroenterol. 2009, 15: 4775-4780. 10.3748/wjg.15.4775.CrossRefPubMedPubMedCentral Vivas S, de Morales JG R, Riestra S, Arias L, Fuentes D, Alvarez N, Calleja S, Hernando M, Herrero B, Casqueiro J, Rodrigo L: Duodenal biopsy may be avoided when high transglutaminase antibody titers are present. World J Gastroenterol. 2009, 15: 4775-4780. 10.3748/wjg.15.4775.CrossRefPubMedPubMedCentral
14.
go back to reference Bizzaro N, Tampoia M, Villalta D, Platzgummer S, Liguori M, Tozzoli R, Tonutti E: Low specificity of anti-tissue transglutaminase antibodies in patients with primary biliary cirrhosis. J Clin Lab Anal. 2006, 20: 184-189. 10.1002/jcla.20130.CrossRefPubMed Bizzaro N, Tampoia M, Villalta D, Platzgummer S, Liguori M, Tozzoli R, Tonutti E: Low specificity of anti-tissue transglutaminase antibodies in patients with primary biliary cirrhosis. J Clin Lab Anal. 2006, 20: 184-189. 10.1002/jcla.20130.CrossRefPubMed
15.
go back to reference Villalta D, Bizzaro N, Tonutti E, Tozzoli R: IgG anti-transglutaminase autoantibodies in systemic lupus erythematosus and Sjogren syndrome. Clin Chem. 2002, 48: 1133-PubMed Villalta D, Bizzaro N, Tonutti E, Tozzoli R: IgG anti-transglutaminase autoantibodies in systemic lupus erythematosus and Sjogren syndrome. Clin Chem. 2002, 48: 1133-PubMed
16.
go back to reference Vecsei A, Arenz T, Heilig G, Arenz S, Bufler P, Koletzko S: Influence of age and geneticrisk on anti-tissue transglutaminase IgA titers. J Pediatr Gastroenterol Nutr. 2009, 48: 544-549. 10.1097/MPG.0b013e31818c5ff6.CrossRefPubMed Vecsei A, Arenz T, Heilig G, Arenz S, Bufler P, Koletzko S: Influence of age and geneticrisk on anti-tissue transglutaminase IgA titers. J Pediatr Gastroenterol Nutr. 2009, 48: 544-549. 10.1097/MPG.0b013e31818c5ff6.CrossRefPubMed
17.
go back to reference Marsh MN: Gluten, major histocompatibility complex, and the small intestine. A molecular and immunobiologic approach to the spectrum of gluten sensitivity ('celiac sprue'). Gastroenterology. 1992, 102: 330-354.CrossRefPubMed Marsh MN: Gluten, major histocompatibility complex, and the small intestine. A molecular and immunobiologic approach to the spectrum of gluten sensitivity ('celiac sprue'). Gastroenterology. 1992, 102: 330-354.CrossRefPubMed
18.
go back to reference Rostami K, Kerckhaert J, Tiemessen R, von Blomberg BM, Meijer JW, Mulder CJ: Sensitivity of antiendomysium and antigliadin antibodies in untreated celiac disease: disappointing in clinical practice. Am J Gastroenterol. 1999, 94: 888-894. 10.1111/j.1572-0241.1999.983_f.x.CrossRefPubMed Rostami K, Kerckhaert J, Tiemessen R, von Blomberg BM, Meijer JW, Mulder CJ: Sensitivity of antiendomysium and antigliadin antibodies in untreated celiac disease: disappointing in clinical practice. Am J Gastroenterol. 1999, 94: 888-894. 10.1111/j.1572-0241.1999.983_f.x.CrossRefPubMed
19.
go back to reference Boudras G, Hachdef W, Benbouadbellah M, Belkadi M, Benmansour FZ, Touchami M: Prevalence of celiac disease in diabetic children and their first degree relatives in west Algeria—screening with serological markers. Acta Pediatr. 1996, 412: 58-60.CrossRef Boudras G, Hachdef W, Benbouadbellah M, Belkadi M, Benmansour FZ, Touchami M: Prevalence of celiac disease in diabetic children and their first degree relatives in west Algeria—screening with serological markers. Acta Pediatr. 1996, 412: 58-60.CrossRef
20.
go back to reference Wasertreguer S, Litwin N, Mora M: Enfermedad celı’aca asociada com diabetes mellitus insulinodependiente. Arch Arg Pediatr. 1996, 94: 10-13. Wasertreguer S, Litwin N, Mora M: Enfermedad celı’aca asociada com diabetes mellitus insulinodependiente. Arch Arg Pediatr. 1996, 94: 10-13.
21.
go back to reference Amin R, Murphy N, Edge J, Ahmed ML, Acerini CL, Dunger DB: A longitudinal study of the effects of a gluten-free diet on glycemic control and weight gain in subjects with Type 1 diabetes and celiac disease. Diabetes Care. 2002, 25: 1117-1122. 10.2337/diacare.25.7.1117.CrossRefPubMed Amin R, Murphy N, Edge J, Ahmed ML, Acerini CL, Dunger DB: A longitudinal study of the effects of a gluten-free diet on glycemic control and weight gain in subjects with Type 1 diabetes and celiac disease. Diabetes Care. 2002, 25: 1117-1122. 10.2337/diacare.25.7.1117.CrossRefPubMed
22.
go back to reference Kaspers S, Kordonouri O, Schober E, Krause U, Schimmel U, Hauffa BP, Holl RW: Anthropometric parameters, metabolic control and thyroid autoimmunity in 127 biopsy-positive children and adolescents with Type 1 diabetes and celiac disease compared to 18,470 diabetic subjects without celiac disease. A multicenter survey. Diabetologia. 2003, 44 (Suppl): A232-A233. Kaspers S, Kordonouri O, Schober E, Krause U, Schimmel U, Hauffa BP, Holl RW: Anthropometric parameters, metabolic control and thyroid autoimmunity in 127 biopsy-positive children and adolescents with Type 1 diabetes and celiac disease compared to 18,470 diabetic subjects without celiac disease. A multicenter survey. Diabetologia. 2003, 44 (Suppl): A232-A233.
23.
go back to reference Birgit R, Zdenek S, Edith S, Thomas W, Tadej B, Nina B, Kalman K, Jan L, Catarina L, Laszlo M, Roetloef J, Magdalena P, Gyula S: Screening Detected Celiac Disease in Children with Type 1 Diabetes Mellitus: Effect on the Clinical Course (A Case Control Study). J Pediatr Gastroenterol Nutr. 2005, 41: 317-321. 10.1097/01.mpg.0000174846.67797.87.CrossRef Birgit R, Zdenek S, Edith S, Thomas W, Tadej B, Nina B, Kalman K, Jan L, Catarina L, Laszlo M, Roetloef J, Magdalena P, Gyula S: Screening Detected Celiac Disease in Children with Type 1 Diabetes Mellitus: Effect on the Clinical Course (A Case Control Study). J Pediatr Gastroenterol Nutr. 2005, 41: 317-321. 10.1097/01.mpg.0000174846.67797.87.CrossRef
24.
go back to reference Buysschaert M, Tomasi JP, Hermans MP: Prospective screening for biopsy proven coeliac disease, autoimmunity and malabsorption markers in Belgian subjects with Type 1 diabetes. Diabet Med. 2005, 22: 889-892.CrossRefPubMed Buysschaert M, Tomasi JP, Hermans MP: Prospective screening for biopsy proven coeliac disease, autoimmunity and malabsorption markers in Belgian subjects with Type 1 diabetes. Diabet Med. 2005, 22: 889-892.CrossRefPubMed
25.
go back to reference Fallahi GH, Ahmadian JH, Rabbani A, Yousefnezhad A, Reaei N: Screening for celiac disease in diabetic children from Iran. Ind Pediatr. 2010, 47: 268-270. 10.1007/s13312-010-0048-8.CrossRef Fallahi GH, Ahmadian JH, Rabbani A, Yousefnezhad A, Reaei N: Screening for celiac disease in diabetic children from Iran. Ind Pediatr. 2010, 47: 268-270. 10.1007/s13312-010-0048-8.CrossRef
26.
go back to reference Shahbazkhani B, Faezi T, Akbari MR, Mohamadnejad M, Sotoudeh M, Rajab A, Tahaghoghi S, Malekzadeh R: Coeliac disease in Iranian type I diabetic patients. Dig Liver Dis. 2004, 36: 191-194. 10.1016/j.dld.2003.10.015.CrossRefPubMed Shahbazkhani B, Faezi T, Akbari MR, Mohamadnejad M, Sotoudeh M, Rajab A, Tahaghoghi S, Malekzadeh R: Coeliac disease in Iranian type I diabetic patients. Dig Liver Dis. 2004, 36: 191-194. 10.1016/j.dld.2003.10.015.CrossRefPubMed
27.
go back to reference Araújo J, da Silva GA, de Melo FM: Serum prevalence of celiac disease in children and adolescents with type 1 diabetes mellitus. J Pediatr (Rio J). 2006, 82: 210-214. Araújo J, da Silva GA, de Melo FM: Serum prevalence of celiac disease in children and adolescents with type 1 diabetes mellitus. J Pediatr (Rio J). 2006, 82: 210-214.
28.
go back to reference Agrawal RP, Rathore A, Joshi A, Changal H, Kochar DK: Prevalence of celiac disease in type 1 diabetes mellitus in North West Rajasthan. India Diabet Res Clin Pract. 2008, 79: e15-e16.CrossRef Agrawal RP, Rathore A, Joshi A, Changal H, Kochar DK: Prevalence of celiac disease in type 1 diabetes mellitus in North West Rajasthan. India Diabet Res Clin Pract. 2008, 79: e15-e16.CrossRef
29.
go back to reference Holmes GKT: Coeliac disease and type 1 diabetes mellitus: the case for screening. Diabet Med. 2001, 18: 169-177. 10.1046/j.1464-5491.2001.00498.x.CrossRefPubMed Holmes GKT: Coeliac disease and type 1 diabetes mellitus: the case for screening. Diabet Med. 2001, 18: 169-177. 10.1046/j.1464-5491.2001.00498.x.CrossRefPubMed
30.
go back to reference Koletzko S, Burgin-Wolff A, Koletzko B, Knapp M, Burger W, Griineklee D, Herz G, Ruch W, Thon A, Wendel U, Zuppinger K: Prevalence of coeliac disease in diabetic children and adolescents. A multicenter study. Eur J Pediatr. 1988, 148: 113-117. 10.1007/BF00445915.CrossRefPubMed Koletzko S, Burgin-Wolff A, Koletzko B, Knapp M, Burger W, Griineklee D, Herz G, Ruch W, Thon A, Wendel U, Zuppinger K: Prevalence of coeliac disease in diabetic children and adolescents. A multicenter study. Eur J Pediatr. 1988, 148: 113-117. 10.1007/BF00445915.CrossRefPubMed
31.
go back to reference Crone J, Rami B, Huber W, Granditsch G, Schober E: Prevalence of Celiac Disease and Follow-up of EMA in Children and Adolescents with Type 1 Diabetes Mellitus. J Pediatr Gastroenterol Nutr. 2003, 37: 67-71. 10.1097/00005176-200307000-00011.CrossRefPubMed Crone J, Rami B, Huber W, Granditsch G, Schober E: Prevalence of Celiac Disease and Follow-up of EMA in Children and Adolescents with Type 1 Diabetes Mellitus. J Pediatr Gastroenterol Nutr. 2003, 37: 67-71. 10.1097/00005176-200307000-00011.CrossRefPubMed
32.
go back to reference Husby S, Koletzko S, Korponay-Szabó IR, Mearin ML, Phillips A, Shamir R, Troncone R, Giersiepen K, Branski D, Catassi C, Lelgeman M, Mäki M, Ribes-Koninckx C, Ventura A, Zimmer KP, ESPGHAN Working Group on Coeliac Disease Diagnosis; ESPGHAN Gastroenterology Committee: European Society for Pediatric Gastroenterology, Hepatology, and Nutrition guidelines for the diagnosis of coeliac disease. J Pediatr Gastroenterol Nutr. 2012, 54: 136-160. 10.1097/MPG.0b013e31821a23d0.CrossRefPubMed Husby S, Koletzko S, Korponay-Szabó IR, Mearin ML, Phillips A, Shamir R, Troncone R, Giersiepen K, Branski D, Catassi C, Lelgeman M, Mäki M, Ribes-Koninckx C, Ventura A, Zimmer KP, ESPGHAN Working Group on Coeliac Disease Diagnosis; ESPGHAN Gastroenterology Committee: European Society for Pediatric Gastroenterology, Hepatology, and Nutrition guidelines for the diagnosis of coeliac disease. J Pediatr Gastroenterol Nutr. 2012, 54: 136-160. 10.1097/MPG.0b013e31821a23d0.CrossRefPubMed
Metadata
Title
High prevalence of celiac disease among Saudi children with type 1 diabetes: a prospective cross-sectional study
Authors
Abdulrahman Al-Hussaini
Nimer Sulaiman
Musa Al-Zahrani
Ahmed Alenizi
Imad El Haj
Publication date
01-12-2012
Publisher
BioMed Central
Published in
BMC Gastroenterology / Issue 1/2012
Electronic ISSN: 1471-230X
DOI
https://doi.org/10.1186/1471-230X-12-180

Other articles of this Issue 1/2012

BMC Gastroenterology 1/2012 Go to the issue