Prevalence of celiac disease and celiac-related antibody status in pediatric patients with type 1 diabetes in Jordan

Rasha Odeh, Abeer Alassaf, Lubna Gharaibeh, Sarah Ibrahim, Fareed Khdair Ahmad, Kamel Ajlouni, Rasha Odeh, Abeer Alassaf, Lubna Gharaibeh, Sarah Ibrahim, Fareed Khdair Ahmad, Kamel Ajlouni

Abstract

Objective: Scientific findings regarding the prevalence of celiac disease (CD) in pediatric patients with type 1 diabetes (T1D) in the Arab world are scarce. We aimed to determine the prevalence of biopsy-proven celiac disease (BPCD) among pediatric patients with T1D from Jordan. We also assessed the possible predictors for developing CD in this cohort of patients and we compared T1D patients who developed BPCD with those who had positive CD serology but negative histology and/or fluctuating CD serology.

Methods: Celiac serology and duodenal biopsy results from 2012 to 2017 were collected from patients with T1D. The outcome of positive celiac serology and the risk factors for CD in T1D patients were investigated.

Results: A total of 538 children of which 278 boys (51.7%) were included in the study. The prevalence of positive serology and the diagnosis of BPCD in this cohort of T1D patients were 16.6 and 9.1% respectively. Eighty percent of those with BPCD were asymptomatic and 47% were diagnosed with CD at onset of T1D. Spontaneous normalization of celiac serology occurred in 23.6% of those with positive serology.

Conclusion: CD is prevalent in T1D pediatric patients from Jordan (9.1%). It is often asymptomatic and the majority of cases were diagnosed at onset or within 5 years of T1D diagnosis. Spontaneous normalization of CD serology occurred in some patients with T1D. Hence, a watchful follow-up is recommended in such patients.

Figures

Figure 1
Figure 1
Study participants flow chart. *This patient was found to have BPCD (Marsh ≥3). **These two patients had infiltrative disease (Marsh 1) and were added to the group of patients with T1D and fluctuating CD serology. BPCD, biopsy-proven celiac disease; CD, celiac disease; T1D, type 1 diabetes; tTG IgA, anti-tissue transglutaminase immunoglobulin A.

References

    1. Bai JC, Fried M, Corazza GR, Schuppan D, Farthing M, Catassi C, Greco L, Cohen H, Ciacci C, Eliakim R, et al. World Gastroenterology Organisation global guidelines on celiac disease. Journal of Clinical Gastroenterology 2013. 47 . (10.1097/MCG.0b013e31827a6f83)
    1. Camarca ME, Mozzillo E, Nugnes R, Zito E, Falco M, Fattorusso V, Mobilia S, Buono P, Valerio G, Troncone R, et al. Celiac disease in type1 diabetes mellitus. Italian Journal of Pediatrics 2012. 38 10 (10.1186/1824-7288-38-10)
    1. Larsson K, Carlsson A, Cederwall E, Jönsson B, Neiderud J, Jonsson B, Lernmark A, Ivarsson SA. & Skåne Study Group. Annual screening detects celiac disease in children with type 1 diabetes. Pediatric Diabetes 2008. 9 . (10.1111/j.1399-5448.2008.00367.x)
    1. Salardi S, Volta U, Zucchini S, Fiorini E, Maltoni G, Vaira B, Cicognani A. Prevalence of celiac disease in children with type 1 diabetes mellitus increased in the mid-1990s: an 18-year longitudinal study based on anti-endomysial antibodies. Journal of Pediatric Gastroenterology and Nutrition 2008. 46 . (10.1097/MPG.0b013e31815d697e)
    1. Pham-Short A, Donaghue KC, Ambler G, Chan AK, Craig ME. Coeliac disease in Type 1 diabetes from 1990 to 2009: higher incidence in young children after longer diabetes duration. Diabetic Medicine 2012. 29 e286–e289. (10.1111/j.1464-5491.2012.03720.x)
    1. Fröhlich-Reiterer EE, Huber J, Katz H, Suppan E, Obermayer-Pietsch B, Deutschmann A, Demel U, Acham-Roschitz B, Weinhandl G, Ambros-Rudolph CM, et al. Do children and adolescents with type 1 diabetes mellitus have a higher frequency of parietal cell antibodies than healthy controls? Journal of Pediatric Gastroenterology and Nutrition 2011. 52 . (10.1097/MPG.0b013e3181fedb2a)
    1. Craig ME, Prinz N, Boyle CT, Campbell FM, Jones TW, Hofer SE, Simmons JH, Holman N, Tham E, Fröhlich-Reiterer E, et al. Prevalence of celiac disease in 52,721 youth with type 1 diabetes: international comparison across three continents. Diabetes Care 2017. 40 . (10.2337/dc16-2508)
    1. 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 Medical Journal 2012. 33 .
    1. Al-Hussaini A, Sulaiman N, Al-Zahrani M, Alenizi A, El Haj I. High prevalence of celiac disease among Saudi children with type 1 diabetes: a prospective cross-sectional study. BMC Gastroenterology 2012. 12 180 (10.1186/1471-230X-12-180)
    1. Al-Ashwal AA, Shabib SM, Sakati NA, Attia NA. Prevalence and characteristics of celiac disease in type 1 diabetes mellitus in Saudi Arabia. Saudi Medical Journal 2003. 24 .
    1. Mankaï A, Ben Hamouda H, Amri F, Ghedira-Besbes L, Harbi A, Tahar Sfar M, Sahloul Essoussi A, Jeddi M, Ghedira I. Screening by anti-endomysium antibodies for celiac disease in Tunisian children with type 1 diabetes mellitus. Gastroenterologie Clinique et Biologique 2007. 31 . (10.1016/S0399-8320(07)89413-9)
    1. 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 Paediatrica 1996. 412 . (10.1111/j.1651-2227.1996.tb14254.x)
    1. 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/Metabolism Research and Reviews 2003. 19 . (10.1002/dmrr.333)
    1. Al-Sinani S, Sharef SW, Al-Yaarubi S, Al-Zakwani I, Al-Naamani K, Al-Hajri A, Al-Hasani S. Prevalence of celiac disease in Omani children with type 1 diabetes mellitus: a cross sectional study. Oman Medical Journal 2013. 28 . (10.5001/omj.2013.73)
    1. Sun S, Puttha R, Ghezaiel S, Skae M, Cooper C, Amin R. & North West England Paediatric Diabetes Network. The effect of biopsy-positive silent coeliac disease and treatment with a gluten-free diet on growth and glycaemic control in children with type 1 diabetes. Diabetic Medicine 2009. 26 . (10.1111/j.1464-5491.2009.02859.x)
    1. Sud S, Marcon M, Assor E, Palmert MR, Daneman D, Mahmud FH. Celiac disease and pediatric type 1 diabetes: diagnostic and treatment dilemmas. International Journal of Pediatric Endocrinology 2010. 2010 161285 (10.1155/2010/161285)
    1. Mahmud FH, Elbarbary NS, Fröhlich-Reiterer E, Holl RW, Kordonouri O, Knip M, Simmons K, Craig ME. ISPAD Clinical Practice Consensus Guidelines 2018: other complications and associated conditions in children and adolescents with type 1 diabetes. Pediatric Diabetes 2018. 19 . (10.1111/pedi.12740)
    1. American Diabetes Association. 12. Children and adolescents: standards of medical care in diabetes—2018. Diabetes Care 2018. 41 S126–S136. (10.2337/dc18-S012)
    1. Castellaneta S, Piccinno E, Oliva M, Cristofori F, Vendemiale M, Ortolani F, Papadia F, Catassi C, Cavallo L, Francavilla R. High rate of spontaneous normalization of celiac serology in a cohort of 446 children with type 1 diabetes: a prospective study. Diabetes Care 2015. 38 . (10.2337/dc14-2890)
    1. Marsh MN, Crowe PT. Morphology of the mucosal lesion in gluten sensitivity. Baillière’s Clinical Gastroenterology 1995. 9 . (10.1016/0950-3528(95)90032-2)
    1. Nusier MK, Brodtkorb HK, Rein SE, Odeh A, Radaideh AM, Klungland H. Serological screening for celiac disease in schoolchildren in Jordan. Is height and weight affected when seropositive? Italian Journal of Pediatrics 2010. 36 16 (10.1186/1824-7288-36-16)
    1. Albatayneh EM, Alnawaiseh NA, Al-Sarayreh SA, Al-saraireh YM, Al-Zayadneh EM, Abu-lobbad MA. Serologic screening of celiac disease in patients with Type 1 diabetes. Journal of Endocrinology and Metabolism 2018. 8 . (10.14740/jem507w)
    1. Barera G, Bonfanti R, Viscardi M, Bazzigaluppi E, Calori G, Meschi F, Bianchi C, Chiumello G. Occurrence of celiac disease after onset of type 1 diabetes: a 6-year prospective longitudinal study. Pediatrics 2002. 109 . (10.1542/peds.109.5.833)
    1. Smyth DJ, Plagnol V, Walker NM, Cooper JD, Downes K, Yang JH, Howson JM, Stevens H, McManus R, Wijmenga C, et al. Shared and distinct genetic variants in type 1 diabetes and celiac disease. New England Journal of Medicine 2008. 359 . (10.1056/NEJMoa0807917)
    1. Kozhakhmetova A, Wyatt RC, Caygill C, Williams C, Long AE, Chandler K, Aitken RJ, Wenzlau JM, Davidson HW, Gillespie KM, et al. A quarter of patients with type 1 diabetes have co-existing non-islet autoimmunity: the findings of a UK population-based family study. Clinical and Experimental Immunology 2018. 192 . (10.1111/cei.13115)
    1. Simell S, Hoppu S, Simell T, Ståhlberg MR, Viander M, Routi T, Simell V, Veijola R, Ilonen J, Hyöty H, et al. Age at development of type 1 diabetes- and celiac disease-associated antibodies and clinical disease in genetically susceptible children observed from birth. Diabetes Care 2010. 33 . (10.2337/dc09-1217)
    1. Cerutti F, Bruno G, Chiarelli F, Lorini R, Meschi F, Sacchetti C. & Diabetes Study Group of the Italian. 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 . (10.2337/diacare.27.6.1294)
    1. Glastras SJ, Craig ME, Verge CF, Chan AK, Cusumano JM, Donaghue KC. The role of autoimmunity at diagnosis of type 1 diabetes in the development of thyroid and celiac disease and microvascular complications. Diabetes Care 2005. 28 . (10.2337/diacare.28.9.2170)
    1. Uibo O, Heilman K, Rägo T, Shor R, Paal M, Metsküla K, Tillmann V, Uibo R. Symptomless celiac disease in type 1diabetes: 12-year experience in Estonia. Pediatrics International 2010. 52 . (10.1111/j.1442-200X.2009.02955.x)
    1. Pocecco M, Ventura A. Coeliac disease and insulin-dependent diabetes mellitus: a causal association? Acta Paediatrica 1995. 84 . (10.1111/j.1651-2227.1995.tb13583.x)
    1. Viljamaa M, Kaukinen K, Huhtala H, Kyronpalo S, Rasmussen M, Collin P. Coeliac disease, autoimmune diseases and gluten exposure. Scandinavian Journal of Gastroenterology 2005. 40 . (10.1080/00365520510012181)
    1. Guariso G, Conte S, Presotto F, Basso D, Brotto F, Visonà Dalla Pozza L, Pedini B, Betterle C. Clinical, subclinical and potential autoimmune diseases in an Italian population of children with coeliac disease. Alimentary Pharmacology and Therapeutics 2007. 26 . (10.1111/j.1365-2036.2007.03526.x)
    1. Poulain C, Johanet C, Delcroix C, Lévy-Marchal C, Tubiana-Rufi N. Prevalence and clinical features of celiac disease in 950 children with type 1 diabetes in France. Diabetes and Metabolism 2007. 33 . (10.1016/j.diabet.2007.06.004)
    1. Crone J, Rami B, Huber WD, Granditsch G, Schober E. Prevalence of celiac disease and follow-up of EMA in children and adolescents with type 1 diabetes mellitus. Journal of Pediatric Gastroenterology and Nutrition 2003. 37 . (10.1097/00005176-200307000-00011)
    1. Telega G, Bennet TR, Werlin S. Emerging new clinical patterns in the presentation of celiac disease. Archives of Pediatrics and Adolescent Medicine 2008. 162 . (10.1001/archpediatrics.2007.38)
    1. McGowan KE, Castiglione DA, Butzner JD. The changing face of childhood celiac disease in North America: impact of serological testing. Pediatrics 2009. 124 . (10.1542/peds.2008-2373)
    1. Waisbourd-Zinman O, Hojsak I, Rosenbach Y, Mozer-Glassberg Y, Shalitin S, Phillip M, Shamir R. Spontaneous normalization of anti tissue transglutaminase antibody levels is common in children with type 1 diabetes mellitus. Digestive Diseases and Sciences 2012. 57 . (10.1007/s10620-011-2016-0)

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