Celiac disease: extraintestinal manifestations and concomitant diseases

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription or Fee Access

Abstract

Celiac disease is a systemic autoimmune disease caused by gluten consumption, which is characterized not only by damage to the small intestine, but also by a wide range of extra-intestinal manifestations. The article discusses the main extra-intestinal manifestations and concomitant autoimmune diseases, such as neurological disorders, dermatological and endocrinological diseases, reproductive disorders (infertility, miscarriage) and liver diseases.

About the authors

E. A. Sabelnikova

Moscow Clinical Scientific and Practical Center named after A.S. Loginov of the Department of Health of Moscow; Russian University of Medicine of the Ministry of Health of Russia

Email: sabelnikova_e_a@mail.ru
Moscow, Russia; Moscow, Russia

S. V. Bykova

Moscow Clinical Scientific and Practical Center named after A.S. Loginov of the Department of Health of Moscow

Email: s.bykova@mknc.ru
Moscow, Russia

D. A. Degtyarev

Moscow Clinical Scientific and Practical Center named after A.S. Loginov of the Department of Health of Moscow

Email: daniil_degterev@mail.ru
Moscow, Russia

References

  1. Rubio-Tapia A., Hill I.D., Semrad C. et al. American College of Gastroenterology Guidelines Update: Diagnosis and Management of Celiac Disease // Am. J. Gastroenterol. 2023. Jan. 1;118(1):59–76. doi: 10.14309/ajg.0000000000002075
  2. Husby S., Koletzko S., Korponay-Szabó I. et al. European Society Paediatric Gastroenterology, Hepatology and Nutrition Guidelines for Diagnosing Coeliac Disease 2020 // J. Pediatr. Gastroenterol. Nutr. 2020. Jan;70(1):141–156. doi: 10.1097/MPG.0000000000002497. PMID: 31568151
  3. Therrien A., Kelly C.P., Silvester J.A. Celiac Disease: Extraintestinal Manifestations and Associated Conditions // J Clin Gastroenterol. 2020, vol. 54, no. 1, pp. 8–21. doi: 10.1097/MCG.0000000000001267
  4. Парфёнов А.И., Быкова С.В., Сабельникова Е.А. и др. Всероссийский консенсус по диагностике и лечению целиакии у детей и взрослых // Терапевтический архив. 2017. № 89(3). С. 94–107.
  5. Parfenov A.I., Bykova S.V., Sabelnikova E.A. et al. All-Russian consensus on the diagnosis and treatment of celiac disease in children and adults // Therapeutic archive. 2017, no. 89(3), pp. 94–107.
  6. Talarico V., Giancotti L, Mazza G.A. et al. Iron Deficiency Anemia in Celiac Disease // Nutrients. 2021, May, 17;13(5):1695. doi: 10.3390/nu13051695
  7. Montoro-Huguet M.A., Santolaria-Piedrafita S., Cañamares-Orbis P., García-Erce J.A. Iron Deficiency in Celiac Disease: Prevalence, Health Impact, and Clinical Management // Nutrients. 2021, Sep., 28;13(10):3437. doi: 10.3390/nu13103437
  8. Mahadev S., Laszkowska M., Sundström J. et al. Prevalence of Celiac Disease in Patients With Iron Deficiency Anemia-A Systematic Review With Meta-analysis // Gastroenterology, 2018, Aug.,155(2):374-382.e1. doi: 10.1053/j.gastro.2018.04.016
  9. Kochhar R., Jain K., Thapa B.R. et al. Clinical presentation of celiac disease among pediatric compared to adolescent and adult patients // Indian J. Gastroenterol. 2012, 31:116–120. doi: 10.1007/s12664-012-0198-9
  10. Bottaro G., Cataldo F., Rotolo N. et al. The clinical pattern of subclinical/silent celiac disease: Analyses is on 1026 consecutive cases // Am. J. Gastroenterol. 1999, 94:691–696. doi: 10.1016/S0002-9270(98)00819-3
  11. Mahadev S., Laszkowska M., Sundström J. et al. Prevalence of Celiac Disease in Patients with Iron Deficiency Anemia – a Systematic Review with Meta-analysis // Gastroenterology. 2018, 155:374–382. doi: 10.1053/j.gastro.2018.04.016
  12. 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:S57–S67. doi: 10.1053/j.gastro.2005.02.014
  13. Smukalla S., Lebwohl B., Mears J.G. et al. How Often Do Hematologists Consider Celiac Disease in Iron-Deficiency Anemia? Results of a National Survey // Clin. Adv. Hematol. Oncol. 2014, 12:100–105.
  14. Chin R.L., Latov N., Green P.H. et al. Neurologic complications of celiac disease // J. Clin. Neuromuscul Dis. 2004, vol. 5, no. 3, pp. 129–137. PMID: 19078744.
  15. Hadjivassiliou M., Croall I.D., Zis P. et al. Neurologic Deficits in Patients With Newly Diagnosed Celiac Disease Are Frequent and Linked With Autoantibodies to Transglutaminase 6 // Clin. Gastroenterol. Hepatol. 2019, vol. 17, no. 13, pp. 2678–2686. doi: 10.1016/j.cgh.2019.03.014
  16. Thawani S.P., Brannagan T.H. 3rd, Lebwohl B. et al. Risk of Neuropathy Among 28,232 Patients With Biopsy-Verified Celiac Disease // JAMA Neurol. 2015, vol. 72, no. 6, pp. 806–811. doi: 10.1001/jamaneurol.2015.0475
  17. Zis P., Sarrigiannis P.G., Rao D.G. et al. Quality of Life in Patients with Gluten Neuropathy: A Case-Controlled Study // Nutrients. 2018, vol. 10, no. 10, p. 1366. doi: 10.3390/nu10101366
  18. Dimitrova A.K., Ungaro R.C., Lebwohl B. et al. Prevalence of migraine in patients with celiac disease and inflammatory bowel disease // Headache. 2013, vol. 53, no. 2, pp. 344–355. doi: 10.1111/j.1526-4610.2012.02260.x
  19. Lebwohl B., Roy A., Alaedini A. et al. Risk of Headache-Related Healthcare Visits in Patients with Celiac Disease: A Population-Based Observational Study // Headache. 2016, vol. 56, no. 5, pp. 849–858. doi: 10.1111/head.12806
  20. Zis P., Julian T., Hadjivassiliou M. Headache Associated with Coeliac Disease: A Systematic Review and Meta-Analysis // Nutrients. 2018, vol. 10, no. 10, p. 1445. doi: 10.3390/nu10101445
  21. Jericho H., Sansotta N., Guandalini S. Extraintestinal Manifestations of Celiac Disease: Effectiveness of the Gluten-Free Diet // J. Pediatr. Gastroenterol. Nutr. 2017, vol. 65, no. 1, pp. 75–79. doi: 10.1097/MPG.0000000000001420
  22. Lichtwark I.T., Newnham E.D., Robinson S.R. et al. Cognitive impairment in coeliac disease improves on a gluten-free diet and correlates with histological and serological indices of disease severity // Aliment Pharmacol. Ther. 2014, vol. 40, no. 2, pp. 160–170. doi: 10.1111/apt.12809
  23. Yelland G.W. Gluten-induced cognitive impairment (“brain fog”) in coeliac disease // J. Gastroenterol. Hepatol. 2017, vol. 32, suppl. 1, pp. 90–93. doi: 10.1111/jgh.13706
  24. Aljulifi M.Z., Mahzari M., Alkhalifa L. et al. The prevalence of celiac disease in Saudi patients with type 1 diabetes mellitus // Ann. Saudi Med. 2021, Mar–Apr, 41(2):71–77. doi: 10.5144/0256-4947.2021.71
  25. Eland I., Klieverik L., Mansour A.A., Al-Toma A. Gluten-Free Diet in Co-Existent Celiac Disease and Type 1 Diabetes Mellitus: Is It Detrimental or Beneficial to Glycemic Control, Vascular Complications, and Quality of Life? // Nutrients. 2022, Dec. 30;15(1):199. doi: 10.3390/nu15010199
  26. Tersigni C., Castellani R., de Waure C. et al. Celiac disease and reproductive disorders: meta-analysis of epidemiologic associations and potential pathogenic mechanisms // Hum. Reprod. Update. 2014, Jul.–Aug.; 20(4):582-93. doi: 10.1093/humupd/dmu007
  27. Tersigni C., Castellani R., de Waure C. et al. Celiac disease and reproductive disorders: meta-analysis of epidemiologic associations and potential pathogenic mechanisms // Hum. Reprod. Update. 2014, Jul.–Aug.; 20(4):582-93. doi: 10.1093/humupd/dmu007
  28. Быкова С.В., Сабельникова Е.А., Парфёнов А.И. и др. Reproductive disorders in women with celiac disease. Effect of the etiotropic therapy // Экспериментальная и клиническая гастроэнтерология. 2011. № 3. С. 12–8.
  29. Bykova S.V., Sabelnikova E.A., Parfenov A.I., et al. Reproductive disorders in women with celiac disease. Effect of the etiotropic therapy // Experimental and Clinical Gastroenterology. 2011, no. 3, pp. 12–8.
  30. Silvester J.A., Graff L.A., Rigaux L. et al. Symptomatic suspected gluten exposure is common among patients with coeliac disease on a gluten-free diet // Aliment Pharmacol Ther., 2016; 44:612.
  31. Graziano M., Rossi M. An update on the cutaneous manifestations of coeliac disease and non-coeliac gluten sensitivity // Int. Rev. Immunol. 2018:1–10.
  32. Lungaro L., Manza F., Costanzini A. et al. Osteoporosis and Celiac Disease: Updates and Hidden Pitfalls // Nutrients. 2023, vol. 15, no. 5, p. 1089. doi: 10.3390/nu15051089
  33. Абдулова Е.А., Дроздов В.Н., Парфёнов А.И. Минеральная плотность костной ткани у больных целиакией и медикаментозная коррекция её нарушений // Экспериментальная и клиническая гастроэнтерология. 2011. № 3. С. 78–83.
  34. Abdulova E.A., Drozdov V.N., Parfenov A.I. Bone mineral density in patients with celiac disease and drug correction of its disorders // Experimental and clinical gastroenterology. 2011, no. 3, pp. 78–83.
  35. Stenson W.F., Newberry R., Lorenz R. et al. Increased Prevalence of Celiac Disease and Need for Routine Screening Among Patients With Osteoporosis // Arch. Intern. Med. 2005; 165:393–399. doi: 10.1001/archinte.165.4.393
  36. Hoffmanova I., Sanchez D., Tuckova L. et al. Celiac Disease and Liver Disorders: From Putative Pathogenesis to Clinical Implications // Nutrients. 2018, vol. 10, no. 7, p. 892. doi: 10.3390/nu10070892
  37. Pelaez-Luna M., Schmulson M., Robles-Diaz G. Intestinal involvement is not sufficient to explain hypertransaminasemia in celiac disease? // Med. Hypotheses. 2005, vol. 65, no. 5, pp. 937–941. doi: 10.1016/j.mehy.2005.05.016
  38. Rubio-Tapia A., Murray J.A. The Liver and Celiac Disease // Clin. Liver Dis. 2019, vol. 23, no. 2, pp. 167–176. doi: 10.1016/j.cld.2018.12.001
  39. Первичный склерозирующий холангит. Взгляд терапевта и хирурга / Под ред. И.Е. Хатькова, Е.В. Винницкой. М.: Литтерра, 2019.
  40. Primary sclerosing cholangitis. A therapist’s and surgeon’s view / Edited by I.E. Khatkov, E.V. Vinnitskaya. Moscow: Litterra, 2019.
  41. Boberg K.M., Spurkland A., Rocca G. et al. The HLA-DR3,DQ2 heterozygous genotype is associated with an accelerated progression of primary sclerosing cholangitis // Scand. J. Gastroenterol. 2001, vol. 36, no. 8, pp. 886–890. doi: 10.1080/003655201750313441
  42. Murray J.A., Moore S.B., Van Dyke C.T. et al. HLA DQ gene dosage and risk and severity of celiac disease // Clin. Gastroenterol. Hepatol. 2007, vol. 5, no. 12, pp. 1406–1412. doi: 10.1016/j.cgh.2007.08.013

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2025 Russian Academy of Sciences