Skip to main content

Advertisement

Log in

Thromboembolic complications and cardiovascular events associated with celiac disease

  • Review Article
  • Published:
Irish Journal of Medical Science (1971 -) Aims and scope Submit manuscript

Abstract

Celiac disease (CD) is a chronic intestinal immune-mediated disease occurring in genetically susceptible individuals who are exposed to gluten. Although it primarily affects the small intestine, CD has been associated with a wide spectrum of extraintestinal manifestations, including thromboembolism and cardiovascular events. The risk of ischemic stroke, myocardial infarction, and thromboembolism, such as deep vein thrombosis and pulmonary embolism, is higher in patients with CD, while there is accumulating evidence that gluten-free diet in CD patients decreases the risk of these complications. The pathogenetic mechanism of increasing hypercoagulability in CD is multifactorial and involves hyperhomocysteinemia due to malabsorption of vitamins B12, B6, and folic acid; endothelial dysfunction; acceleration of atherosclerosis; chronic inflammation; thrombocytosis; and thrombophilia. Therefore, in cases of thromboembolic complications and cardiovascular disease of obscure etiology, clinicians’ awareness of possible celiac disease is warranted.

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.

Similar content being viewed by others

References

  1. Al-Toma A, Volta U, Auricchio R et al (2019) European Society for the Study of Coeliac Disease (ESsCD) guideline for coeliac disease and other gluten-related disorders. United European Gastroenterol J 7(5):583–613

    PubMed  PubMed Central  Google Scholar 

  2. Reilly NR, Green PH (2012) Epidemiology and clinical presentations of celiac disease. Semin Immunopathol 34(4):473–478

    PubMed  Google Scholar 

  3. Jacob S, Zarei M, Kenton A, Allroggen H (2005) Gluten sensitivity and neuromyelitis optica: two case reports. J Neurol Neurosurg Psychiatry 76(7):1028–1030

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Kowalski K, Mulak A, Jasinska M, Paradowski L (2017) Diagnostic challenges in celiac disease. Adv Clin Exp Med 26(4):729–737

    PubMed  Google Scholar 

  5. Green PH, Lebwohl B, Greywoode R (2015) Celiac disease. J Allergy Clin Immunol 135(5):1099–1106 quiz 107

    CAS  PubMed  Google Scholar 

  6. Woodward J (2016) Improving outcomes of refractory celiac disease - current and emerging treatment strategies. Clin Exp Gastroenterol 9:225–236

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Dominguez Castro P, Harkin G, Hussey M et al (2017) Changes in presentation of celiac disease in Ireland from the 1960s to 2015. Clin Gastroenterol Hepatol. 15(6):864–871 e3

    PubMed  Google Scholar 

  8. Volta U, Caio G, Stanghellini V, De Giorgio R (2014) The changing clinical profile of celiac disease: a 15-year experience (1998-2012) in an Italian referral center. BMC Gastroenterol 14:194

    PubMed  PubMed Central  Google Scholar 

  9. Jones S, D'Souza C, Haboubi NY (2006) Patterns of clinical presentation of adult coeliac disease in a rural setting. Nutr J 5:24

    PubMed  PubMed Central  Google Scholar 

  10. Pinto-Sanchez MI, Bercik P, Verdu EF, Bai JC (2015) Extraintestinal manifestations of celiac disease. Dig Dis 33(2):147–154

    PubMed  Google Scholar 

  11. Korpimaki S, Kaukinen K, Collin P et al (2011) Gluten-sensitive hypertransaminasemia in celiac disease: an infrequent and often subclinical finding. Am J Gastroenterol 106(9):1689–1696

    PubMed  Google Scholar 

  12. Leffler DA, Green PH, Fasano A (2015) Extraintestinal manifestations of coeliac disease. Nat Rev Gastroenterol Hepatol 12(10):561–571

    CAS  PubMed  Google Scholar 

  13. Hujoel IA, Reilly NR, Rubio-Tapia A (2019) Celiac disease: clinical features and diagnosis. Gastroenterol Clin N Am 48(1):19–37

    Google Scholar 

  14. Lerner A, Blank M (2014) Hypercoagulability in celiac disease--an update. Autoimmun Rev 13(11):1138–1141

    CAS  PubMed  Google Scholar 

  15. Rubio-Jurado B, Iniguez-Franco P, Reyes PA et al (2012) The clinical significance of coagulation and the inflammatory response in autoimmunity. Clin Rev Allergy Immunol 42(2):172–180

    CAS  PubMed  Google Scholar 

  16. de Groot PG, de Laat B (2017) Mechanisms of thrombosis in systemic lupus erythematosus and antiphospholipid syndrome. Best Pract Res Clin Rheumatol 31(3):334–341

    PubMed  Google Scholar 

  17. Zezos P, Kouklakis G, Saibil F (2014) Inflammatory bowel disease and thromboembolism. World J Gastroenterol 20(38):13863–13878

    PubMed  PubMed Central  Google Scholar 

  18. Mameli A, Barcellona D, Marongiu F (2009) Rheumatoid arthritis and thrombosis. Clin Exp Rheumatol 27(5):846–855

    CAS  PubMed  Google Scholar 

  19. Ludvigsson JF, West J, Card T, Appelros P (2012) Risk of stroke in 28,000 patients with celiac disease: a nationwide cohort study in Sweden. J Stroke Cerebrovasc Dis 21(8):860–867

    PubMed  Google Scholar 

  20. Johannesdottir SA, Erichsen R, Horvath-Puho E et al (2012) Coeliac disease and risk of venous thromboembolism: a nationwide population-based case-control study. Br J Haematol 157(4):499–501

    PubMed  Google Scholar 

  21. Ludvigsson JF, Welander A, Lassila R et al (2007) Risk of thromboembolism in 14,000 individuals with coeliac disease. Br J Haematol 139(1):121–127

    PubMed  Google Scholar 

  22. Ungprasert P, Wijarnpreecha K, Tanratana P (2016) Risk of venous thromboembolism in patients with celiac disease: a systematic review and meta-analysis. J Gastroenterol Hepatol 31(7):1240–1245

    PubMed  Google Scholar 

  23. Zoller B, Li X, Sundquist J, Sundquist K (2012) Risk of pulmonary embolism in patients with autoimmune disorders: a nationwide follow-up study from Sweden. Lancet. 379(9812):244–249

    PubMed  Google Scholar 

  24. Ludvigsson JF, James S, Askling J et al (2011) Nationwide cohort study of risk of ischemic heart disease in patients with celiac disease. Circulation. 123(5):483–490

    PubMed  Google Scholar 

  25. Beyan E, Pamukcuoglu M, Beyan C (2009) Deep vein thrombosis associated with celiac disease. Bratisl Lek Listy 110(4):263–264

    CAS  PubMed  Google Scholar 

  26. Dumic I, Martin S, Salfiti N et al (2017) Deep venous thrombosis and bilateral pulmonary embolism revealing silent celiac disease: case report and review of the literature. Case Rep Gastrointest Med 2017:5236918

    PubMed  PubMed Central  Google Scholar 

  27. Kochhar R, Masoodi I, Dutta U et al (2009) Celiac disease and Budd Chiari syndrome: report of a case with review of literature. Eur J Gastroenterol Hepatol 21(9):1092–1094

    PubMed  Google Scholar 

  28. Meena DS, Sonwal VS, Bohra GK et al (2019) Celiac disease with Budd-Chiari syndrome: A rare association. SAGE Open Med Case Rep 7:2050313X19842697

    PubMed  PubMed Central  Google Scholar 

  29. Khanna S, Chaudhary D, Kumar P, Mazumdar S (2008) Occult celiac disease presenting as splenic vein thrombosis. Indian J Gastroenterol 27(1):38–39

    PubMed  Google Scholar 

  30. Zenjari T, Boruchowicz A, Desreumaux P et al (1995) Association of coeliac disease and portal venous thrombosis. Gastroenterol Clin Biol 19(11):953–954

    CAS  PubMed  Google Scholar 

  31. Azzam NA, Al Ashgar H, Dababo M et al (2006) Mesentric vein thrombosis as a presentation of subclinical celiac disease. Ann Saudi Med 26(6):471–473

    PubMed  PubMed Central  Google Scholar 

  32. McNeill A, Duthie F, Galloway DJ (2006) Small bowel infarction in a patient with coeliac disease. J Clin Pathol 59(2):216–218

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Jadallah KA, Sarsak EW, Khazaleh YM, Barakat RM (2016) Budd-Chiari syndrome associated with coeliac disease: case report and literature review. Gastroenterol Rep 6(4):308–312

  34. Goodwin FC, Beattie RM, Millar J, Kirkham FJ (2004) Celiac disease and childhood stroke. Pediatr Neurol 31(2):139–142

    PubMed  Google Scholar 

  35. Poulin W, Gaertner S, Cordeanu EM et al (2015) Stroke revealing celiac disease associated with multiple arterial thrombotic locations. Presse Med 44(5):537–538

    PubMed  Google Scholar 

  36. Dogan M, Peker E, Akbayram S et al (2011) Cerebral venous sinus thrombosis in 2 children with celiac disease. Clin Appl Thromb Hemost 17(5):466–469

    PubMed  Google Scholar 

  37. Boucelma M, Saadi M, Boukrara H et al (2013) Association of celiac disease and cerebral venous thrombosis: report of two cases. J Mal Vasc 38(1):47–51

    CAS  PubMed  Google Scholar 

  38. Zoubeidi H, Ben Salem T, Ben Ghorbel I, Houman MH (2016) Central retinal vein occlusion revealing coeliac disease. Eur J Case Rep Intern Med 3(7):000492

    PubMed  PubMed Central  Google Scholar 

  39. Santoro L, De Matteis G, Fuorlo M et al (2017) Atherosclerosis and cardiovascular involvement in celiac disease: the role of autoimmunity and inflammation. Eur Rev Med Pharmacol Sci 21(23):5437–5444

    CAS  PubMed  Google Scholar 

  40. Curione M, Barbato M, De Biase L et al (1999) Prevalence of coeliac disease in idiopathic dilated cardiomyopathy. Lancet. 354(9174):222–223

    CAS  PubMed  Google Scholar 

  41. De Bem RS, Da Ro Sa Utiyama SR, Nisihara RM et al (2006) Celiac disease prevalence in Brazilian dilated cardiomyopathy patients. Dig Dis Sci 51(5):1016–1019

    PubMed  Google Scholar 

  42. Barrio JP, Cura G, Ramallo G et al (2011) Heart transplantation in rapidly progressive end-stage heart failure associated with celiac disease. BMJ Case Rep 2011:bcr1220103624

    PubMed  PubMed Central  Google Scholar 

  43. Zahmatkeshan M, Fallahpoor M, Amoozgar H (2014) Prevalence of celiac disease in children with idiopathic dilated cardiomyopathy. Iran J Pediatr 24(5):587–592

    PubMed  PubMed Central  Google Scholar 

  44. McGrath S, Thomas A, Gorard DA (2016) Cardiomyopathy responsive to gluten withdrawal in a patient with coeliac disease. BMJ Case Rep 2016:bcr2015213301

  45. Curione M, Barbato M, Viola F et al (2002) Idiopathic dilated cardiomyopathy associated with coeliac disease: the effect of a gluten-free diet on cardiac performance. Dig Liver Dis 34(12):866–869

    CAS  PubMed  Google Scholar 

  46. Emilsson L, Andersson B, Elfstrom P et al (2012) Risk of idiopathic dilated cardiomyopathy in 29 000 patients with celiac disease. J Am Heart Assoc 1(3):e001594

    PubMed  PubMed Central  Google Scholar 

  47. Vizzardi E, Lanzarotto F, Carabellese N et al (2008) Lack of association of coeliac disease with idiopathic and ischaemic dilated cardiomyopathies. Scand J Clin Lab Invest 68(8):692–695

    CAS  PubMed  Google Scholar 

  48. Gajulapalli RD, Pattanshetty DJ (2017) Risk of coronary artery disease in celiac disease population. Saudi J Gastroenterol 23(4):253–258

    PubMed  PubMed Central  Google Scholar 

  49. Emilsson L, Lebwohl B, Sundstrom J, Ludvigsson JF (2015) Cardiovascular disease in patients with coeliac disease: a systematic review and meta-analysis. Dig Liver Dis. 47(10):847–852

    PubMed  Google Scholar 

  50. Emilsson L, Carlsson R, James S et al (2015) Follow-up of ischaemic heart disease in patients with coeliac disease. Eur J Prev Cardiol 22(1):83–90

    PubMed  Google Scholar 

  51. Potter MDE, Brienesse SC, Walker MM et al (2018) Effect of the gluten-free diet on cardiovascular risk factors in patients with coeliac disease: a systematic review. J Gastroenterol Hepatol 33(4):781–791

    PubMed  Google Scholar 

  52. Norsa L, Shamir R, Zevit N et al (2013) Cardiovascular disease risk factor profiles in children with celiac disease on gluten-free diets. World J Gastroenterol 19(34):5658–5664

    PubMed  PubMed Central  Google Scholar 

  53. Zanini B, Mazzoncini E, Lanzarotto F et al (2013) Impact of gluten-free diet on cardiovascular risk factors. A retrospective analysis in a large cohort of coeliac patients. Dig Liver Dis. 45(10):810–815

    CAS  PubMed  Google Scholar 

  54. Zifman E, Waisbourd-Zinman O, Marderfeld L et al (2019) The effect of gluten-free diet on cardiovascular risk factors in newly diagnosed pediatric celiac disease patients. J Pediatr Gastroenterol Nutr 68(5):684–688

    PubMed  Google Scholar 

  55. Ashrafi F, Darakhshandeh A, Heidarpour M et al (2014) Pericardial effusion in celiac disease. Int J Prev Med 5(3):356–359

    PubMed  PubMed Central  Google Scholar 

  56. Emilsson L, Smith JG, West J et al (2011) Increased risk of atrial fibrillation in patients with coeliac disease: a nationwide cohort study. Eur Heart J 32(19):2430–2437

    PubMed  Google Scholar 

  57. Hidalgo DF, Boonpheng B, Nasr L et al (2020) Celiac Disease and Risk of Atrial Fibrillation: A meta-analysis and systematic review. Cureus 12(2):e6997

  58. Efe TH, Ertem AG, Coskun Y et al (2016) Atrial electromechanical properties in coeliac disease. Heart Lung Circ 25(2):160–165

    PubMed  Google Scholar 

  59. Riccabona M, Rossipal E (2000) Pericardial effusion in celiac disease--an incidental finding? Wien Klin Wochenschr 112(1):27–31

    CAS  PubMed  Google Scholar 

  60. Frustaci A, Cuoco L, Chimenti C et al (2002) Celiac disease associated with autoimmune myocarditis. Circulation. 105(22):2611–2618

    PubMed  Google Scholar 

  61. Dickey W (2002) Low serum vitamin B12 is common in coeliac disease and is not due to autoimmune gastritis. Eur J Gastroenterol Hepatol 14(4):425–427

    CAS  PubMed  Google Scholar 

  62. Wierdsma NJ, van Bokhorst-de van der Schueren MA, Berkenpas M et al (2013) Vitamin and mineral deficiencies are highly prevalent in newly diagnosed celiac disease patients. Nutrients. 5(10):3975–3992

    PubMed  PubMed Central  Google Scholar 

  63. Theethira TG, Dennis M, Leffler DA (2014) Nutritional consequences of celiac disease and the gluten-free diet. Expert Rev Gastroenterol Hepatol 8(2):123–129

    CAS  PubMed  Google Scholar 

  64. Kim J, Kim H, Roh H, Kwon Y (2018) Causes of hyperhomocysteinemia and its pathological significance. Arch Pharm Res 41(4):372–383

    CAS  PubMed  Google Scholar 

  65. Fanapour PC, Yug B, Kochar MS (1999) Hyperhomocysteinemia: an additional cardiovascular risk factor. WMJ 98(8):51–54

    CAS  PubMed  Google Scholar 

  66. Sharma P, Senthilkumar RD, Brahmachari V et al (2006) Mining literature for a comprehensive pathway analysis: a case study for retrieval of homocysteine related genes for genetic and epigenetic studies. Lipids Health Dis 5:1

    PubMed  PubMed Central  Google Scholar 

  67. Lai WK, Kan MY (2015) Homocysteine-induced endothelial dysfunction. Ann Nutr Metab 67(1):1–12

    CAS  PubMed  Google Scholar 

  68. Holick MF (2007) Vitamin D deficiency. N Engl J Med 357(3):266–281

    CAS  Google Scholar 

  69. Skaaby T, Thuesen BH, Linneberg A (2017) Vitamin D, Cardiovascular disease and risk factors. Adv Exp Med Biol 996:221–230

    CAS  PubMed  Google Scholar 

  70. Agnetti A, Bitton L, Tchana B et al (2013) Primary carnitine deficiency dilated cardiomyopathy: 28 years follow-up. Int J Cardiol 162(2):e34–e35

    PubMed  Google Scholar 

  71. Lerner A, Gruener N, Iancu TC (1993) Serum carnitine concentrations in coeliac disease. Gut. 34(7):933–935

    CAS  PubMed  PubMed Central  Google Scholar 

  72. Yuce A, Demir H, Temizel IN, Kocak N (2004) Serum carnitine and selenium levels in children with celiac disease. Indian J Gastroenterol 23(3):87–88

    PubMed  Google Scholar 

  73. Curione M, Danese C, Viola F et al (2005) Carnitine deficiency in patients with coeliac disease and idiopathic dilated cardiomyopathy. Nutr Metab Cardiovasc Dis 15(4):279–283

    CAS  PubMed  Google Scholar 

  74. Hadi HA, Carr CS, Al Suwaidi J (2005) Endothelial dysfunction: cardiovascular risk factors, therapy, and outcome. Vasc Health Risk Manag 1(3):183–198

    CAS  PubMed  PubMed Central  Google Scholar 

  75. Comba A, Caltepe G, Yank K et al (2016) Assessment of endothelial dysfunction with adhesion molecules in patients with celiac disease. J Pediatr Gastroenterol Nutr 63(2):247–252

    CAS  PubMed  Google Scholar 

  76. Sari C, Bayram NA, Dogan FE et al (2012) The evaluation of endothelial functions in patients with celiac disease. Echocardiography. 29(4):471–477

    PubMed  Google Scholar 

  77. Mormile R (2016) Celiac disease and atherosclerosis: an immunologic puzzle to be solved? Immunol Lett 180:75–76

    CAS  PubMed  Google Scholar 

  78. Kablak-Ziembicka A, Tracz W, Przewlocki T et al (2004) Association of increased carotid intima-media thickness with the extent of coronary artery disease. Heart. 90(11):1286–1290

    CAS  PubMed  PubMed Central  Google Scholar 

  79. Redheuil A, Yu WC, Wu CO et al (2010) Reduced ascending aortic strain and distensibility: earliest manifestations of vascular aging in humans. Hypertension. 55(2):319–326

    CAS  PubMed  PubMed Central  Google Scholar 

  80. De Marchi S, Chiarioni G, Prior M, Arosio E (2013) Young adults with coeliac disease may be at increased risk of early atherosclerosis. Aliment Pharmacol Ther 38(2):162–169

    PubMed  Google Scholar 

  81. Sari C, Ertem AG, Sari S et al (2015) Impaired aortic function in patients with coeliac disease. Kardiol Pol 73(11):1108–1113

    PubMed  Google Scholar 

  82. Kim SM, Mayassi T, Jabri B (2015) Innate immunity: actuating the gears of celiac disease pathogenesis. Best Pract Res Clin Gastroenterol 29(3):425–435

    CAS  PubMed  PubMed Central  Google Scholar 

  83. Fatkhullina AR, Peshkova IO, Koltsova EK (2016) The role of cytokines in the development of atherosclerosis. Biochemistry 81(11):1358–1370

    CAS  PubMed  Google Scholar 

  84. Neuhausen SL, Steele L, Ryan S et al (2008) Co-occurrence of celiac disease and other autoimmune diseases in celiacs and their first-degree relatives. J Autoimmun 31(2):160–165

    CAS  PubMed  PubMed Central  Google Scholar 

  85. Bayturan O (2010) The metabolic syndrome, its component risk factors, and progression of coronary atherosclerosis. Arch Intern Med 170(5):478–484

    CAS  PubMed  Google Scholar 

  86. Tortora R, Capone P, De Stefano G et al (2015) Metabolic syndrome in patients with coeliac disease on a gluten-free diet. Aliment Pharmacol Ther 41(4):352–359

    CAS  PubMed  Google Scholar 

  87. Remes-Troche JM, Cobos-Quevedo ODJ, Rivera-Gutiérrez X et al (2020) Metabolic effects in patients with celiac disease, patients with nonceliac gluten sensitivity, and asymptomatic controls, after six months of a gluten-free diet. Revista de Gastroenterología de México 85(2):109–117

  88. Aksu K, Donmez A, Keser G (2012) Inflammation-induced thrombosis: mechanisms, disease associations and management. Curr Pharm Des 18(11):1478–1493

    CAS  PubMed  Google Scholar 

  89. Feighery C, O'Keefe J (2003) TNF-alpha production by intraepithelial T cells in celiac disease. Gastroenterology. 125(5):1560–1561 author reply 1-2

    PubMed  Google Scholar 

  90. Garrote JA, Gomez-Gonzalez E, Bernardo D et al (2008) Celiac disease pathogenesis: the proinflammatory cytokine network. J Pediatr Gastroenterol Nutr 47(Suppl 1):S27–S32

    CAS  PubMed  Google Scholar 

  91. van Hinsbergh VW, Kooistra T, van den Berg EA et al (1988) Tumor necrosis factor increases the production of plasminogen activator inhibitor in human endothelial cells in vitro and in rats in vivo. Blood. 72(5):1467–1473

    PubMed  Google Scholar 

  92. Tjarnlund-Wolf A, Brogren H, Lo EH, Wang X (2012) Plasminogen activator inhibitor-1 and thrombotic cerebrovascular diseases. Stroke. 43(10):2833–2839

    PubMed  PubMed Central  Google Scholar 

  93. Levi M, van der Poll T (2010) Inflammation and coagulation. Crit Care Med 38(2 Suppl):S26–S34

    CAS  PubMed  Google Scholar 

  94. Turcu A, Bonnotte B, Fein F et al (1998) Association of celiac disease and antiphospholipid syndrome. Presse Med 27(35):1789

    CAS  PubMed  Google Scholar 

  95. Gupta D, Mirza N (2008) Systemic lupus erythematosus, celiac disease and antiphospholipid antibody syndrome: a rare association. Rheumatol Int 28(11):1179–1180

    CAS  PubMed  Google Scholar 

  96. Jorge O, Jorge A, Camus G (2008) Celiac disease associated with antiphospholipid syndrome. Rev Esp Enferm Dig 100(2):102–103

    CAS  PubMed  Google Scholar 

  97. Karoui S, Sellami MK, Laatar AB et al (2007) Prevalence of anticardiolipin and anti-beta2-glycoprotein I antibodies in celiac disease. Dig Dis Sci 52(4):1096–1100

    CAS  PubMed  Google Scholar 

  98. Laine O, Pitkanen K, Lindfors K et al (2018) Elevated serum antiphospholipid antibodies in adults with celiac disease. Dig Liver Dis 50(5):457–461

    CAS  PubMed  Google Scholar 

  99. Shamir R, Shoenfeld Y, Blank M et al (2003) The prevalence of coeliac disease antibodies in patients with the antiphospholipid syndrome. Lupus. 12(5):394–399

    CAS  PubMed  Google Scholar 

  100. Lerner A, Agmon-Levin N, Shapira Y et al (2013) The thrombophilic network of autoantibodies in celiac disease. BMC Med 11:89

    PubMed  PubMed Central  Google Scholar 

  101. Berthoux E, Fabien N, Chayvialle JA et al (2011) Adult celiac disease with thrombosis: a case series of seven patients. Role of thrombophilic factors. Rev Med Interne 32(10):600–604

    CAS  PubMed  Google Scholar 

  102. Ghannouchi Jaafoura N, Atig A, Bouker A et al (2014) Intracardiac thrombosis during celiac disease. J Mal Vasc 39(3):203–206

    CAS  PubMed  Google Scholar 

  103. Halfdanarson TR, Litzow MR, Murray JA (2007) Hematologic manifestations of celiac disease. Blood. 109(2):412–421

    CAS  PubMed  PubMed Central  Google Scholar 

  104. Nelson EW, Ertan A, Brooks FP, Cerda JJ (1976) Thrombocytosis in patients with celiac sprue. Gastroenterology. 70(6):1042–1044

    CAS  PubMed  Google Scholar 

  105. Carroccio A, Giannitrapani L, Di Prima L et al (2002) Extreme thrombocytosis as a sign of coeliac disease in the elderly: case report. Eur J Gastroenterol Hepatol 14(8):897–900

    PubMed  Google Scholar 

  106. Baydoun A, Maakaron JE, Halawi H et al (2012) Hematological manifestations of celiac disease. Scand J Gastroenterol 47(12):1401–1411

    PubMed  Google Scholar 

  107. Corazza GR, Zoli G, Di Sabatino A et al (1999) A reassessment of splenic hypofunction in celiac disease. Am J Gastroenterol 94(2):391–397

    CAS  PubMed  Google Scholar 

  108. Robinson PJ, Bullen AW, Hall R et al (1980) Splenic size and function in adult coeliac disease. Br J Radiol 53(630):532–537

    CAS  PubMed  Google Scholar 

  109. Corazza GR, Lazzari R, Frisoni M et al (1982) Splenic function in childhood coeliac disease. Gut. 23(5):415–416

    CAS  PubMed  PubMed Central  Google Scholar 

  110. Di Sabatino A, Rosado MM, Cazzola P et al (2006) Splenic hypofunction and the spectrum of autoimmune and malignant complications in celiac disease. Clin Gastroenterol Hepatol 4(2):179–186

    PubMed  Google Scholar 

  111. Dean L (2012) Methylenetetrahydrofolate Reductase Deficiency. In: Pratt V, McLeod H, Rubinstein W, Dean L, Kattman B, Malheiro A (eds) Medical Genetics Summaries, Bethesda (MD). https://www.ncbi.nlm.nih.gov/books/NBK66131/

  112. Fabbri E, Rustignoli L, Muscari A et al (2012) Recurrent ischemic strokes in a young celiac woman with MTHFR gene mutation. World J Gastroenterol 18(26):3472–3476

    CAS  PubMed  PubMed Central  Google Scholar 

  113. Picchi A, Pasqualini P, D'Aiello I et al (2008) Acute ST-elevation myocardial infarction in a 15-year-old boy with celiac disease and multifactorial thrombotic risk. Thromb Haemost 99(6):1116–1118

    CAS  PubMed  Google Scholar 

  114. Hozyasz KK, Mostowska A, Szaflarska-Poplawska A et al (2012) Polymorphic variants of genes involved in homocysteine metabolism in celiac disease. Mol Biol Rep 39(3):3123–3130

    CAS  PubMed  Google Scholar 

  115. Saibeni S, Lecchi A, Meucci G et al (2005) Prevalence of hyperhomocysteinemia in adult gluten-sensitive enteropathy at diagnosis: role of B12, folate, and genetics. Clin Gastroenterol Hepatol 3(6):574–580

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Contributions

DKC and HM conceived, designed, and critically revised the study for important intellectual content;

FSF drafted the article, performed the research, and analyzed and interpreted the literature data for important intellectual content;

ETB and IVM performed the research, and analyzed and interpreted the literature data for important intellectual content, as well as contributed substantially in the manuscript preparation; all authors approved the final version of the article to be published.

Corresponding author

Correspondence to Dimitrios K. Christodoulou.

Ethics declarations

This article does not contain any studies with human participants or animals performed by any of the authors.

Conflict of interest

The authors declare that they have no conflicts of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fousekis, F.S., Beka, E.T., Mitselos, I.V. et al. Thromboembolic complications and cardiovascular events associated with celiac disease. Ir J Med Sci 190, 133–141 (2021). https://doi.org/10.1007/s11845-020-02315-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11845-020-02315-2

Keywords

Navigation