Skip to main content

Advertisement

Log in

Prevalence and Clinical Features of Celiac Disease in Healthy School-Aged Children

  • Original Article
  • Published:
Digestive Diseases and Sciences Aims and scope Submit manuscript

Abstract

Background/Aims

The aim of this study was to determine the prevalence of celiac disease (CD) in healthy school-aged children in the northern region of Cyprus and to investigate the existence of potential markers that may accompany CD. This is the first study to measure the prevalence of CD in the northern region of Cyprus.

Methods

This study included 3792 school-aged children who were between the ages of 6 and 10 years between January 2015 and October 2016. CD was screened using total serum IgA, IgA anti-tissue transglutaminase (tTG), and IgA antiendomysial (EMA) antibodies. Subjects with selective IgA deficiency were further tested for IgG-tTG. Small intestinal biopsies were performed on all subjects with tTG antibody positivity. Risk factors and symptoms related to CD were evaluated using questionnaires in both the CD and control groups.

Results

Of the 3792 subjects, 39 were antibody positive (IgA-tTG was positive only in 14 subjects, IgA-tTG plus IgA-EMA in 21 subjects, and IgG-tTG in 4 subjects). IgA deficiency was detected in 11 subjects (0.29%). IgG-tTG was positive in 4 subjects with IgA deficiency (36.3%). Intestinal biopsies were performed on 28 of the 39 seropositive subjects. The biopsy findings of 15 children were consistent with CD (IgA-tTG positive in 3, IgA-tTG and IgA-EMA positive in 10, and IgG-tTG positive in 2). Thus, biopsies confirmed CD in 1:256 children (0.39%).

Conclusions

Our study, which is the first study of school-aged children from the northern region of Cyprus, revealed that CD is a prevalent disease in this region.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. Ludvigsson JF, Leffler DA, Bai JC, et al. The Oslo definitions for coeliac disease and related terms. Gut. 2013;62:43–52.

    Article  Google Scholar 

  2. Sollid LM, Jabri B. Triggers and drivers of autoimmunity: lessons from coeliac disease. Nat Rev Immunol. 2013;13:294–302.

    Article  CAS  Google Scholar 

  3. Mishra A, Prakash S, Sreenivas V, et al. Structural and functional changes in the tight junctions of asymptomatic and serology-negative first-degree relatives of patients with celiac disease. J Clin Gastroenterol. 2016;50:551–560.

    Article  CAS  Google Scholar 

  4. Maglio M, Tosco A, Auricchio R, et al. Intestinal deposits of anti-tissue transglutaminase IgA in childhood celiac disease. Dig Liver Dis. 2011;43:604–608.

    Article  CAS  Google Scholar 

  5. Di Niro R, Mesin L, Zheng NY, et al. High abundance of plasma cells secreting transglutaminase 2-specific IgA autoantibodies with limited somatic hypermutation in celiac disease intestinal lesions. Nat Med. 2012;18:441–445.

    Article  Google Scholar 

  6. Wolf J, Petroff D, Richter T, et al. Validation of antibody-based strategies for diagnosis of pediatric celiac disease without biopsy. Gastroenterology. 2017;153:410–419.

    Article  CAS  Google Scholar 

  7. Pitman M, Sanders DS, Green PHR, Lebwohl B. Rates of Duodenal Biopsy During Upper Endoscopy Differ Widely Between Providers: Implications for Diagnosis of Celiac Disease. J Clin Gastroenterol 2017 Oct 31. https://doi.org/10.1097/mcg.0000000000000957. [Epub ahead of print]. https://www.ncbi.nlm.nih.gov/pubmed/29095420

  8. Mustalahti K, Catassi C, Reunanen A, et al. The prevalence of celiac disease in Europe: results of a centralized, international mass screening project. Ann Med. 2010;42:587–595.

    Article  Google Scholar 

  9. Husby S, Koletzko S, Korponay-Szabó IR, et al. European society for pediatric gastroenterology, hepatology, and nutrition guidelines for the diagnosis of coeliac disease. J Pediatr Gastroenterol Nutr. 2012;54:136–160.

    Article  CAS  Google Scholar 

  10. Tio M, Cox MR, Eslick GD. Meta-analysis: coeliac disease and the risk of all-cause mortality, any malignancy and lymphoid malignancy. Aliment Pharmacol Ther. 2012;35:540–551.

    Article  CAS  Google Scholar 

  11. 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;128:57–67.

    Article  Google Scholar 

  12. World Health Organisation. Physical status: the use and interpretation of anthropometry. In: Report of a WHO Expert Committee. TRS No. 854. Geneva: World Health Organization; 1995.

  13. 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.

    Article  CAS  Google Scholar 

  14. Catassi C, Gatti S, Fasano A. The new epidemiology of celiac disease. J Pediatr Gastroenterol Nutr. 2014;59:7–9.

    Article  Google Scholar 

  15. White LE, Merrick VM, Bannerman E, et al. The rising incidence of celiac disease in Scotland. Pediatrics. 2013;132:924–931.

    Article  Google Scholar 

  16. Dalgic B, Sari S, Basturk B, et al. Prevalence of celiac disease in healthy Turkish school children. Am J Gastroenterol. 2011;106:1512–1517.

    Article  CAS  Google Scholar 

  17. Ertekin V, Selimoğlu MA, Kardaş F, Aktaş E. Prevalence of celiac disease in Turkish children. J Clin Gastroenterol. 2005;39:689–691.

    Article  Google Scholar 

  18. Korponay-Szabó IR, Kovács JB, Czinner A, Gorácz G, Vámos A, Szabó T. High prevalence of silent celiac disease in preschool children screened with IgA/IgG antiendomysium antibodies. J Pediatr Gastroenterol Nutr. 1999;28:26–30.

    Article  Google Scholar 

  19. Castaño L, Blarduni E, Ortiz L, et al. Prospective population screening for celiac disease: high prevalence in the first 3 years of life. J Pediatr Gastroenterol Nutr. 2004;39:80–84.

    Article  Google Scholar 

  20. Hill ID, Dirks MH, Liptak GS, et al. Guideline for the diagnosis and treatment of celiac disease in children: recommendations of the North American Society for pediatric gastroenterology, hepatology and nutrition. J Pediatr Gastroenterol Nutr. 2005;40:1–19.

    Article  Google Scholar 

  21. Stern M. Comparative evaluation of serologic tests for celiac disease: a European initiative toward standardization. J Pediatr Gastroenterol Nutr. 2000;31:513–519.

    Article  CAS  Google Scholar 

  22. Wong RC, Wilson RJ, Steele RH, Radford-Smith G, Adelstein S. A comparison of 13 guinea pig and human anti-tissue transglutaminase antibody ELISA kits. J Clin Pathol. 2002;55:488–494.

    Article  CAS  Google Scholar 

  23. Toftedal P, Nielsen C, Madsen JT, Titlestad K, Husby S, Lillevang ST. Positive predictive value of serological diagnostic measures in celiac disease. Clin Chem Lab Med. 2010;48:685–691.

    Article  CAS  Google Scholar 

  24. Donaldson MR, Book LS, Leiferman KM, Zone JJ, Neuhausen SL. Strongly positive tissue transglutaminase antibodies are associated with Marsh 3 histopathology in adult and pediatric celiac disease. J Clin Gastroenterol. 2008;42:256–260.

    CAS  PubMed  Google Scholar 

  25. Fasano A, Berti I, Gerarduzzi T, et al. Prevalence of celiac disease in at-risk and not-at-risk groups in the United States: a large multicenter study. Arch Int Med. 2003;163:286–292.

    Article  Google Scholar 

  26. Ivarsson A, Myléus A, Norström F, et al. Prevalence of childhood celiac disease and changes in infant feeding. Pediatrics. 2013;131:687–694.

    Article  Google Scholar 

  27. Roka V, Potamianos SP, Kapsoritakis AN, et al. Prevalence of coeliac disease in the adult population of central Greece. Eur J Gastroenterol Hepatol. 2007;19:982–987.

    Article  Google Scholar 

  28. Karagiozoglou-Lampoudi T, Zellos A, Vlahavas G, et al. Screening for coeliac disease in preschool greek children: the feasibility study of a community-based project. Acta Paediatr. 2013;102:749–754.

    Article  Google Scholar 

  29. Green PH, Cellier C. Celiac disease. N Engl J Med. 2007;357:1731–1743.

    Article  CAS  Google Scholar 

  30. Bardella MT, Fredella C, Saladino V, et al. Gluten intolerance: gender- and age-related differences in symptoms. Scand J Gastroenterol. 2005;40:15–19.

    Article  Google Scholar 

  31. Szajewska H, Shamir R, Mearin L, et al. Gluten introduction and the risk of coeliac disease: a position paper by the European Society for pediatric gastroenterology, hepatology, and nutrition. J Pediatr Gastroenterol Nutr. 2016;62:507–513.

    Article  CAS  Google Scholar 

  32. Saukkonen J, Kaukinen K, Koivisto AM, et al. Clinical Characteristics and the Dietary Response in Celiac Disease Patients Presenting With or Without Anemia. J Clin Gastroenterol. 2016 Jun 15. [Epub ahead of print]. https://www.ncbi.nlm.nih.gov/pubmed/27306936

  33. Cannings-John R, Butler CC, Prout H, et al. A case-control study of presentations in general practice before diagnosis of coeliac disease. Br J Gen Pract. 2007;57:636–642.

    PubMed  PubMed Central  Google Scholar 

  34. Toftedal P, Hansen DG, Nielsen C, Lillevang ST, Hansen TP, Husby S. Questionnaire-based case finding of celiac disease in a population of 8- to 9-year-old children. Pediatrics. 2010;125:518–524.

    Article  Google Scholar 

  35. Jansen M, van Zelm M, Groeneweg M, et al. The identification of celiac disease in asymptomatic children: the Generation R Study. J Gastroenterol. 2018;53:377–386.

    Article  Google Scholar 

  36. Rosen A, Sandstrom O, Carlsson A, et al. Usefulness of symptoms to screen for celiac disease. Pediatrics. 2014;133:211–218.

    Article  Google Scholar 

  37. Türkiye Beslenme ve Sağlık Araştırması 2010: Beslenme Durumu ve Alışkanlıklarının Değerlendirilmesi Sonuç Raporu. Ankara: Sağlık Bakanlığı Yayın; 2014;e466-72. Sağlık Bakanlığı Sağlık Araştırmaları Genel Müdürlüğü, Hacettepe Üniversitesi Sağlık Bilimleri Fakültesi Beslenme ve Diyetetik Bölümü, Ankara Numune Eğitim ve Araştırma Hastanesi. http://www.sagem.gov.tr/tbsa_beslenme_yayini.pdf

  38. Wijnhoven TM, van Raaij JM, Spinelli A, et al. WHO European childhood obesity surveillance initiative: body mass index and level of overweight among 6-9-year-old children from school year 2007/2008 to school year 2009/2010. BMC Public Health. 2014;14:806.

    Article  Google Scholar 

  39. Vivas S, de Morales JMR, Fernandez M, et al. Age-related clinical, serological, and histopathological features of celiac disease. Am. J. Gastroenterol. 2008;103:2360–2365.

    Article  Google Scholar 

  40. McGowan KE, Castiglione DA, Butzner JD. The changing face of childhood celiac disease in North America: impact of serological testing. Pediatrics. 2009;124:1572–1578.

    Article  Google Scholar 

  41. Agardh D, Lee HS, Kurppa K, et al. Clinical features of celiac disease: a prospective birth cohort. Pediatrics. 2015;135:627–634.

    Article  Google Scholar 

  42. van Dommelen P, Grote FK, Oostdijk W, et al. Screening rules for growth to detect celiac disease: a case-control simulation study. BMC Pediatr. 2008;8:35.

    Article  Google Scholar 

  43. Saari A, Harju S, Makitie O, et al. Systematic growth monitoring for the early detection of celiac disease in children. JAMA Pediatr. 2015;169:e1525.

    Article  Google Scholar 

Download references

Acknowledgments

This study was conducted under the leadership and with financial support of the Turkish Pediatric Association. We thank the Cyprus Turkish Pediatric Association, and Turkish Pediatric Association for all their support. We also thank Figen Ince, Hasret Ayyıldız Civan, Mine Ozdil Cirkinoglu, Bircan Kavaz, Hulya Madi, Sevgi Oksuz, Nazife Oner, Kamuran Arıbuka, Saziye Guçlu, Remzi Gardiyanoglu, Nurcin Incirli, Ayten Beyar, Raşit Kayra, Halil Hızal, Hasan Garabli, Cemal Mert, Şenel Dalınç, Nesibe Kocaman, Ayşen Yücel Varol, Cengiz Elyeli, Havva Duran, Pembe Akgöl, Emine Ertekin, Şenay Koşar, Rağbet Tosun, Osman Kılınç, Saniye Yıldırım, Arife Tek, Şengül Uçak, Nevin Çınar, Esma Karaca, Emine Zurnalı, Ayşe Çürük, Hatice Turan, Mahmude Erdevir, Havva Uçar, Suna Sağır, Cemile Şener, and Selçuk Çağsın for both blood sampling in the schools and informing parents of the study group.

Northern Cyprus Celiac Study Group: Adem Karbuz, Serhat Guler, Alper Kacar, Soner Sazak, Figen Ince, Mine Ozdil Cirkinoglu, Bircan Kavaz, Hulya Madi, Sevgi Oksuz, Bekir Yigit Develi, Nazife Oner, Kamuran Arıbuka, Saziye Guçlu, Remzi Gardiyanoglu, Nurcin Incirli.

Author information

Authors and Affiliations

Authors

Consortia

Corresponding author

Correspondence to Omer Faruk Beser.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

A list of the Northern Cyprus Celiac Study Group is given in Acknowledgements section.

This research project was funded by the Turkish Pediatric Association without charge. The study protocol was approved by the Ethics Committee of Istanbul University Cerrahpasa Medical Faculty (B.30.2.İST.0.30.90.00).

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 41 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Beser, O.F., Gulluelli, E., Cullu Cokugras, F. et al. Prevalence and Clinical Features of Celiac Disease in Healthy School-Aged Children. Dig Dis Sci 64, 173–181 (2019). https://doi.org/10.1007/s10620-018-5320-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10620-018-5320-0

Keywords

Navigation