Top

Published in:

Open Access 01-12-2012 | Review

Celiac disease in type 1 diabetes mellitus

Authors: Maria Erminia Camarca, Enza Mozzillo, Rosa Nugnes, Eugenio Zito, Mariateresa Falco, Valentina Fattorusso, Sara Mobilia, Pietro Buono, Giuliana Valerio, Riccardo Troncone, Adriana Franzese

Published in: Italian Journal of Pediatrics | Issue 1/2012

Abstract

Celiac Disease (CD) occurs in patients with Type 1 Diabetes (T1D) ranging the prevalence of 4.4-11.1% versus 0.5% of the general population. The mechanism of association of these two diseases involves a shared genetic background: HLA genotype DR3-DQ2 and DR4-DQ8 are strongly associated with T1D, DR3-DQ2 with CD. The classical severe presentation of CD rarely occurs in T1D patients, but more often patients have few/mild symptoms of CD or are completely asymptomatic (silent CD). In fact diagnosis of CD is regularly performed by means of the screening in T1D patients. The effects of gluten-free diet (GFD) on the growth and T1D metabolic control in CD/T1D patient are controversial. Regarding of the GFD composition, there is a debate on the higher glycaemic index of gluten-free foods respect to gluten-containing foods; furthermore GFD could be poorer of fibers and richer of fat. The adherence to GFD by children with CD-T1D has been reported generally below 50%, lower respect to the 73% of CD patients, a lower compliance being more frequent among asymptomatic patients. The more severe problems of GFD adherence usually occur during adolescence when in GFD non compliant subjects the lowest quality of life is reported. A psychological and educational support should be provided for these patients.

Barker JM: Clinical review: type 1 diabetes-associated autoimmunity: natural history, genetic associations and screening. J Clin Endocrinol Metab. 2006, 91 (0021-972X): 1210-1217.CrossRefPubMed

Smyth DJ, Plagnol V, Walker NM, Cooper JD, Downes K, Yang JH, Howson JM, Stevens H, McManus R, Wijmenga C, Heap GA, Dubois PC, Clayton DG, Hunt KA, Heel Van, Todd JA: Shared and distinct genetic variant in Type 1 diabetes and celiac disease. N Eng J Med. 2008, 359 (0028-4793): 2837-2838.

Ide A, Eisenbarth GS: Genetic susceptibility in type 1 diabetes and its associated autoimmune disorders. Rev Endocr Metab Disord. 2003, 4 (3): 243-253. 10.1023/A:1025100328425. 1389-9155CrossRefPubMed

Bao F, Yu L, Babu S, Wang T, Hoffenberg EJ, Rewers M, Eisenbarth GS: One third of HLA DQ2 homozygous patients with type 1 diabetes express celiac disease associated transglutaminase autoantibodies. J Autoimmun. 1999, 13: 143-148. 10.1006/jaut.1999.0303. 0896-8411CrossRefPubMed

Cerruti F, Bruno G, Chiarelli F, Lorini R, Meschi F, Sacchetti C: Diabetes Study Group of the Italian Society of Pediatric Endocrinology and Diabetology. 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: 1294-1298. 10.2337/diacare.27.6.1294.CrossRef

Contreas G, Valletta E, Ulmi D, Cantoni S, Pinelli L: Screening of celiac disease in north Italian children with type 1 diabetes: limited usefulness of HLA-DQ typing. Acta Paediatr. 2004, 93: 628-632. 10.1111/j.1651-2227.2004.tb02987.x.CrossRefPubMed

Sanchez-Albisua I, Wolf J, Neu A, Geiger H, Wascher I, Stern M: Coeliac disease in children with type 1 diabetes mellitus: the effect of the gluten free diet. Diabet Med. 2005, 22: 1079-1082. 10.1111/j.1464-5491.2005.01609.x.CrossRefPubMed

Araujo 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.

Goh C, Banerjee K: Prevalence of celiac disease in children and adolescents with type 1 diabetes mellitus in a clinic based population. Postgrad Med J. 2007, 83: 132-136. 10.1136/pgmj.2006.049189.PubMedCentralCrossRefPubMed

10.

Larsson K, Carlsson A, Cederwall E, Jonsson B, Neiderud J, Jonsson B, Lernmark A, Ivarsson SA, Skane Study Group: Annual screening detects celiac disease in children with type 1 diabetes. Pediatr Diabetes. 2008, 9: 354-354. 10.1111/j.1399-5448.2008.00367.x.CrossRefPubMed

11.

Karavanaki K, Kakleas K, Paschali E, Kefalas N, Konstantopoulos I, Petrou V, Kanariou M, Karayanni C: Screening for associated autoimmunity in children and adolescents with type 1 diabetes mellitus (T1DM). Horm Res. 2009, 71: 201-206. 10.1159/000201108.CrossRefPubMed

12.

Djuric Z, Stamenkovic H, Stankovic T, Milecevic R, Brankovic L, Ciric V, Katic V: Celiac disease prevalence in children and adolescents with type 1 diabetes from Serbia. Pediatr Int. 2010, 52: 579-583. 10.1111/j.1442-200X.2010.03085.x.CrossRefPubMed

13.

Bhadada SK, Kochlar R, Bhansali A, Dutta U, Kumar PR, Poornachandra KS, Vaiphei K, Nain CK, Singh K: Prevalence and clinical profile of celiac disease in type 1 diabetes mellitus in north India. J Gastroenterol Hepatol. 2011, 2: 378-381.CrossRef

14.

Gabriel S, Mihaela I, Angela B, Mariana A, Doru D: Prevalence of IgA antitissue transglutaminase antibodies in children with type 1 diabetes mellitus. J Clin Lab Anal. 2011, 25 (3): 156-161. 10.1002/jcla.20449.CrossRefPubMed

15.

Kaspers S, Kordonouri O, Schober E, Grabert M, Hauffa BP, Holl RW, German Working Group for Pediatric Diabetology: Anthropometry, metabolic control, and thyroid autoimmunity in type 1 diabetes with celiac disease: A multicenter survey. J Pediatr. 2004, 145 (6): 790-795. 10.1016/j.jpeds.2004.07.031. 0022-3476CrossRefPubMed

16.

Cerutti F, Bruno G, Chiarelli F, Lorini R, Meschi F, Sacchetti C: Diabetes study group of the Italian Society of Pediatric Endocrinology and Diabetology. 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. 10.2337/diacare.27.6.1294. 0149-5992CrossRefPubMed

17.

Valerio G, Maiuri L, Troncone R, Buono P, Lombardi F, Palmieri R, Franzese A: Severe clinical onset of diabetes and increased prevalence of other autoimmune diseases in children with coeliac disease diagnosed before diabetes mellitus. Diabetologia. 2002, 45 (12): 1719-1722. 10.1007/s00125-002-0923-5. 0012-186XCrossRefPubMed

18.

Pocecco M, Ventura A: Coeliac disease and insulin-dependent diabetes mellitus: a causal association?. Acta Paediatr. 1995, 84 (12): 1432-1433. 10.1111/j.1651-2227.1995.tb13583.x. 0803-5253CrossRefPubMed

19.

Ventura A, Magazzù G, Greco L: Duration of exposure to gluten and risk for autoimmune disorders in patients with celiac disease. SIGEP Study Group for Autoimmune Disorders in Celiac Disease. Gastroenterology. 1999, 117 (2): 297-303. 10.1053/gast.1999.0029900297. 0016-5085CrossRefPubMed

20.

Ventura A, Neri E, Ughi C, Leopaldi A, Citta A, Not T: Gluten-dependent diabetes-related and thyroid-related autoantibodies in patients with celiac disease. J Pediatr. 2000, 137 (2): 263-265. 10.1067/mpd.2000.107160. 0022-3476CrossRefPubMed

21.

Viljamaa M, Kaukinen K, Huhtala H, Kyronpalo S, Rasmussen M, Collin P: Coeliac disease, autoimmune diseases and gluten exposure. Scand J Gastroenterol. 2005, 40 (4): 437-443. 10.1080/00365520510012181. 0036-5521CrossRefPubMed

22.

Holmes GK: Coeliac disease and Type 1 diabetes mellitus - the case for screening. Diabet Med. 2001, 18 (3): 169-177. 10.1046/j.1464-5491.2001.00498.x. 0742-3071CrossRefPubMed

23.

Holmes GK: Potential and latent coeliac disease. Eur J Gastroenterol Hepatol. 2001, 13 (9): 1057-1060. 10.1097/00042737-200109000-00010. 0954-691XCrossRefPubMed

24.

Paparo F, Petrone E, Tosco A, Maglio M, Borrelli M, Salvati VM, Miele E, Greco L, Auricchio S, Troncone R: Clinical, HLA, and small bowel immunohistochemical features of children with positive serum antiendomysium antibodies and architecturally normal small intestinal mucosa. Am J Gastroenterol. 2005, 100 (10): 2294-2298. 10.1111/j.1572-0241.2005.41134.x. 0002-9270CrossRefPubMed

25.

Troncone R, Greco L, Mayer M, Paparo F, Caputo N, Micillo M, Mugione P, Auricchio S: Latent and potential celiac disease. Acta Paediatr Suppl. 1996, 412: 10-14. 0803-5253CrossRefPubMed

26.

Franzese A, Iafusco D, Spadaro R, Cavaliere O, Prisco F, Auricchio R, Troncone R, Valerio G, The Study-Group on Diabetes of Italian Society of Pediatric Endocrinology and Diabetology: Potential celiac disease in type 1 diabetes: A multicenter study. Diabetes Res Clin Pract. 2011, 92 (1): 53-56. 10.1016/j.diabres.2010.12.028. 0168-8227CrossRefPubMed

27.

Peretti N, Bienvenu F, Bouvet C, Fabien N, Tixier F, Thivolet C, Levy E, Chatelain PG, Lachaux A, Nicolino M: The temporal relationship between the onset of type 1 diabetes and celiac disease: a study based on immunoglobulin A antitransglutaminase screening. Pediatrics. 2004, 113: e418-e422. 10.1542/peds.113.5.e418.CrossRefPubMed

28.

Karavanaki K, Kakleas K, Paschali E, Kefelas N, Konstantopoulos I, Petrou V, Kanariou M, Karayianni C: Screening for associated autoimmunity in children and adolescents with type 1 diabetes mellitus (T1DM). Horm Res. 2009, 71: 201-206. 10.1159/000201108.CrossRefPubMed

29.

Husby S, Koletzko S, Korponay-Szabó IR: The ESPGHAN Working Group on Coeliac Disease Diagnosis. ESPGHAN Guidelines for the Diagnosis of Coeliac Disease in Children and Adolescents. An Evidence-based Approach JPGN. 2012, 54 (1): 136-160.

30.

Collin P, Kaukinen K, Valimaki M, Salmi J: Endocrinological disorders and celiac disease. Endocr Rev. 2002, 23 (4): 464-483. 10.1210/er.2001-0035. 0163-769XCrossRefPubMed

31.

Freemark M, Levitsky LL: Screening for celiac disease in children with type 1 diabetes: two views of the controversy. Diabetes Care. 2003, 26 (6): 1932-1939. 10.2337/diacare.26.6.1932. 0149-5992CrossRefPubMed

32.

Rubio-Tapia A, Kyle RA, Kaplan EL, Johnson DR, Page W, Erdtmann F, Brantner TL, Kim WR, Phelps TK, Lahr BD, Zinsmeister AR, Melton LJ, Murray JA: Increased prevalence and mortality in undiagnosed celiac disease. Gastroenterology. 2009, 137 (1): 88-93. 10.1053/j.gastro.2009.03.059. 0036-5521PubMedCentralCrossRefPubMed

33.

Hansen D, Brock-Jacobsen B, Lund E, Bjorn C, Hansen LP, Nielsen C, Fenger C, Lillevang ST, Husby S: Clinical benefit of a gluten-free diet in type 1 diabetic children with screening-detected celiac disease: a population-based screening study with 2 years' follow-up. Diabetes Care. 2006, 29 (11): 2452-2456. 10.2337/dc06-0990. 0149-5992CrossRefPubMed

34.

Sanchez-Albisua I, Wolf J, Neu A, Geiger H, Wascher I, Stern M: Coeliac disease in children with Type 1 diabetes mellitus: the effect of the gluten-free diet. Diabet Med. 2005, 22 (8): 1079-1082. 10.1111/j.1464-5491.2005.01609.x. 0742-3071CrossRefPubMed

35.

Artz E, Warren-Ulanch J, Becker D, Greenspan S, Freemark M: Seropositivity to celiac antigens in asymptomatic children with type 1 diabetes mellitus: association with weight, height, and bone mineralization. Pediatr Diabetes. 2008, 9 (4): 277-284. 10.1111/j.1399-5448.2008.00386.x. 1399-543XCrossRefPubMed

36.

Rami B, Sumnik Z, Schober E, Waldhor T, Battelino T, Bratanic N, Kurti K, Lebl J, Limbert C, Madacsy L, Odink RJ, Paskova M, Soltesz G: 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 (3): 317-321. 10.1097/01.mpg.0000174846.67797.87. 0277-2116CrossRefPubMed

37.

Simmons JH, Klingensmith GJ, McFann K, Rewers M, Ide LM, Taki I, Liu E, Hoffenberg EJ: Celiac Autoimmunity in Children with Type 1 Diabetes: A Two-Year Follow-up. J Pediatr. 2011, 158 (2): 276-281. 10.1016/j.jpeds.2010.07.025. 0022-3476PubMedCentralCrossRefPubMed

38.

Franzese A, Lombardi F, Valerio G, Spagnuolo MI: Update on Coeliac Disease and Type 1 Diabetes Mellitus in Childhood. J Pediatr Endocrinol Metab. 2007, 20 (12): 1257-1264. 0334-018XCrossRefPubMed

39.

Van Koppen EJ, Schweizer JJ, Csizmadia CG, Krom Y, Hylkema HB, Van Geel AM, Koopman HM, Verloove-Vanhorick SP, Mearin ML: Long-term health and quality-of-life consequences of mass screening for childhood celiac disease: a 10-year follow-up study. Pediatrics. 2009, 123 (4): 582-588. 10.1542/peds.2008-2221. 0031-4005CrossRef

40.

Kurppa K, Ashorn M, Iltanen S, Koskinen LL, Saavalainen P, Koskinen O, Mäki M, Kaukinen K: Celiac disease without villous atrophy in children: a prospective study. J Pediatr. 2010, 157 (3): 373-380. 10.1016/j.jpeds.2010.02.070. 0022-3476CrossRefPubMed

41.

Tosco A, Salvati VM, Auricchio R, Maglio M, Borrelli M, Coruzzo A, Paparo F, Boffardi M, Esposito A, D'Adamo G, Malamisura B, Greco L, Troncone R: Natural history of potential celiac disease in children. Clin Gastroenterol Hepatol. 2011, 9 (4): 320-325. 10.1016/j.cgh.2010.09.006.CrossRefPubMed

42.

Westerholm-Ormio M, Vaarala O, Pihkala P, Ilonen J, Savilahti E: Immunologic Activity in the Small Intestinal Mucosa of Pediatric Patients With Type 1 Diabetes. Diabetes. 2003, 52 (9): 2287-2295. 10.2337/diabetes.52.9.2287. 0012-1797CrossRefPubMed

43.

Maglio M, Florian F, Vecchiet M, Auricchio R, Paparo F, Spadaro R, Zanzi D, Rapacciuolo L, Franzese A, Sblattero D, Marzari R, Troncone R: Majority of children with type 1 diabetes produce and deposit anti-tissue transglutaminase antibodies in the small intestine. Diabetes. 2009, 58 (7): 1578-1584. 10.2337/db08-0962. 0012-1797PubMedCentralCrossRefPubMed

44.

Troncone R, Franzese A, Mazzarella G, Paparo F, Auricchio R, Coto I, Mayer M, Greco L: Gluten sensitivity in a subset of children with insulin dependent diabetes mellitus. Am J Gastroenterol. 2003, 98 (3): 590-595. 10.1111/j.1572-0241.2003.07301.x. 0002-9270CrossRefPubMed

45.

Valerio G, Del Puente A, Buono P, Esposito A, Zanatta M, Mozzillo E, Moretto E, Mastidoro L, Franzese A: Quantitative ultrasound of proximal phalanxes in patients with type 1 diabetes mellitus. Diabetes Res Clin Pract. 2004, 64 (3): 161-166. 10.1016/j.diabres.2003.10.021.CrossRefPubMed

46.

Lombardi F, Franzese A, Iafusco D, Del Puente A, Esposito A, Prisco F, Troncone R, Valerio G: Bone involvement in clusters of autoimmune diseases: Just a complication?. Bone. 2010, 46: 551-555. 10.1016/j.bone.2009.09.034.CrossRefPubMed

47.

Kollet O, Dar A, Lapidot T: The multiple roles of osteoclast in host defence: one remodeling and hematopoietic stem cell mobilization. Annu Rev Immunol. 2007, 25: 51-69. 10.1146/annurev.immunol.25.022106.141631.CrossRefPubMed

48.

Galluzzi F, Stagi S, Salti R, Toni S, Piscitelli E, Simonini G, Falcini F, Chiarelli F: Osteoprotegerin serum levels in children with type 1 diabetes: a potential modulating role in bone status. Eur J Endocrinol. 2005, 153: 879-885. 10.1530/eje.1.02052.CrossRefPubMed

49.

Valerio G, Spadaro R, Iafusco D, Lombardi F, Del Puente A, Esposito A: The influence of gluten free diet on quantitative ultrasound of proximal phalanxes in children and adolescents with Type 1 Diabetes mellitus and celiac disease. Bone. 2008, 43: 322-326. 10.1016/j.bone.2008.04.004.CrossRefPubMed

50.

Foster-Powell Kaye, Susanna Holt, Brand-Miller Janette C: International table of glycaemic index and glycaemic load values. Am J Clin Nutr. 2002, 76 (1): 5-56.PubMed

51.

Parker SC, Dornhost A, Frost GS: The glycaemic index of a range of gluten free foods. Diabetics Medicine. 2000, 17: 657-660. 10.1046/j.1464-5491.2000.00356.x.CrossRef

52.

Berti C, Riso P, Monti L, Porrini M: In vitro starch digestibility and in vivo glucose response of gluten free foods and their gluten counterparts. Eur J Nutr. 2004, 43: 198-204.CrossRefPubMed

53.

Kupper C: Dietary guidelines and implementation for celiac disease. Gastroenterology. 2005, 128: S121-S127. 10.1053/j.gastro.2005.02.024.CrossRefPubMed

54.

Errichiello S, Esposito O, Di Mase R, Camarca ME, Natale C, Limongelli MG, Marano C, Coruzzo A, Lombardo M, Strisciuglio P, Greco L: Celiac disease: predictors of compliance with a gluten-free diet in adolescents and young adults. J Pediatr Gastroenterol Nutr. 2010, 50 (1): 54-60. 10.1097/MPG.0b013e31819de82a.CrossRefPubMed

55.

Franzese A, Valerio G, Spagnuolo MI: Management of diabetes in childhood: are children small adults?. Clin Nutr. 2004, 23 (3): 293-305. 10.1016/j.clnu.2003.07.007.CrossRefPubMed

56.

Rashid M, Cranney A, Zarkadas M, Graham ID, Switzer C, Case S, Molloy M, Warren RE, Burrows V, Butzner JD: Celiac disease: evaluation of the diagnosis and dietary compliance in Canadian children. Pediatrics. 2005, 116 (6): e754-e759. 10.1542/peds.2005-0904.CrossRefPubMed

57.

Van Koppen EJ, Schweizer JJ, Csizmadia CG, Krom Y, Hylkema HB, van Geel AM, Koopman HM, Verloove-Vanhorick SP, Mearin ML: Long-term health and quality-of-life consequences of mass screening for childhood celiac disease: a 10-year follow-up study. Pediatrics. 2009, 123 (4): e582-e588. 10.1542/peds.2008-2221.CrossRefPubMed

58.

Kolsteren MM, Koopman HM, Schalekamp G, Mearin ML: Health-related quality of life in children with celiac disease. J Pediatr. 2001, 138 (4): 593-595. 10.1067/mpd.2001.111504.CrossRefPubMed

59.

Wagner G, Berger G, Sinnreich U, Grylli V, Schober E, Huber WD, Karwautz A: Quality of life in adolescents with treated coeliac disease: influence of compliance and age at diagnosis. J Pediatr Gastroenterol Nutr. 2008, 47 (5): 555-561. 10.1097/MPG.0b013e31817fcb56.CrossRefPubMed

60.

Rubin RR, Peyrot M: Quality of life and diabetes. Diabetes Metab Res Rev. 1999, 15: 205-218. 10.1002/(SICI)1520-7560(199905/06)15:3<205::AID-DMRR29>3.0.CO;2-O.CrossRefPubMed

61.

Sud S, Marcon M, Assor E, Daneman D, Mahmud FH: Quality of life in children with diabetes and celiac disease: minimal impact of the 'double diagnosis'. Pediatric Diabetes. 2011

Title: Celiac disease in type 1 diabetes mellitus
Authors: Maria Erminia Camarca
Enza Mozzillo
Rosa Nugnes
Eugenio Zito
Mariateresa Falco
Valentina Fattorusso
Sara Mobilia
Pietro Buono
Giuliana Valerio
Riccardo Troncone
Adriana Franzese
Publication date: 01-12-2012
Publisher: BioMed Central
Published in: Italian Journal of Pediatrics / Issue 1/2012
Electronic ISSN: 1824-7288
DOI: https://doi.org/10.1186/1824-7288-38-10

ACC 2024 Congress

Springer Medicine

Celiac disease in type 1 diabetes mellitus

Abstract

ACC 2024 Congress

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 1/2012

Progress in pediatrics in 2011. Choices in endocrinology, gastroenterology, hemato-oncology, infectious diseases, otolaryngology, pharmacotherapy and respiratory tract illnesses

Access to food outlets and children's nutritional intake in urban China: a difference-in-difference analysis

Traumatic lingual ulceration in a newborn: Riga-Fede disease

Effect of zinc supplementation on growth Hormone Insulin growth factor axis in short Egyptian children with zinc deficiency

Clinical application of exhaled nitric oxide measurement in pediatric lung diseases

Weight status of adolescents in secondary schools in port Harcourt using Body Mass Index (BMI)