Skip to main content
Log in

Diagnostic Value of Anti-Saccharomyces cerevisiae and Antineutrophil Cytoplasmic Antibodies for Inflammatory Bowel Disease: High Prevalence in Patients with Celiac Disease

  • Published:
Journal of Clinical Immunology Aims and scope Submit manuscript

Abstract

Both celiac disease and inflammatory bowel disease (IBD) are characterized by chronic diarrhea and the presence of distinct (auto)antibodies. In the present study we wanted to determine the prevalence of serological markers for inflammatory bowel disease, i.e., perinuclear antineutrophil cytoplasmic antibodies (pANCA) and/or anti-Saccharomyces cerevisiae antibodies (ASCA), in 37 patients with biopsy-confirmed celiac disease (Marsh IIIb/c). The majority of the patients was positive for IgA (auto)antibodies typically associated with celiac disease, i.e., antiendomysium antibodies (EMA) (86.5%), antigliadin antibodies (AGA) (73%), and antirecombinant human tissue transglutaminase antibodies (rh-tTGA) (86.5%). Four patients with selective IgA deficiency could be identified by analyzing EMA, AGA, and rh-tTGA for the IgG isotype. The prevalence of pANCA and ASCA, markers that are used for IBD, was unexpectedly high in our cohort of patients with celiac disease: 8 patients were positive for pANCA (IgG) and 16 patients were positive for ASCA (IgG and/or IgA). These results indicate that the presence of pANCA or ASCA in the serum of patients with chronic diarrhea does not exclude celiac disease. A prospective study is required to determine whether pANCA and/or ASCA identify patients at risk for developing secondary autoimmune disease.

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. Marsh MN: Gluten, major histocompatibility complex, and the small intestine. A molecular and immunobiologic approach to the spectrum of gluten sensitivity (“celiac sprue”). Gastroenterology 102:330–354, 1992

    Google Scholar 

  2. Parnell ND, Ciclitira PJ: Review article: Coeliac disease and its management. Aliment Pharmacol Ther 13:1–13, 1999

    Google Scholar 

  3. Loughran TP, Kadin ME, Deeg HJ: T-cell intestinal lymphoma associated with celiac sprue. Ann Intern Med 104:44–47, 1986

    Google Scholar 

  4. Holmes GK, Prior P, Lane MR, Pope D, Allan RN: Malignancy in coeliac disease—Effect of a gluten free diet. Gut 30:333–338, 1989

    Google Scholar 

  5. Walker-Smith JA, Guandalini S, Schmitz J, Shmerling DH, Visakorpi JK: Revised criteria for diagnosis of coeliac disease. Report of Working Group of European Society of Paediatric Gastroenterology and Nutrition. Arch Dis Child 65:909–911, 1990

    Google Scholar 

  6. Dieterich W, Ehnis T, Bauer M, Donner P, Volta U, Riecken EO, Schuppan D: Identification of tissue transglutaminase as the autoantigen of celiac disease [see comments]. Nat Med 3:797–801, 1997

    Google Scholar 

  7. Sblattero D, Berti I, Trevisiol C, Marzari R, Tommasini A, Bradbury A, Fasano A, Ventura A, Not T: Human recombinant tissue transglutaminase ELISA: An innovative diagnostic assay for celiac disease. Am J Gastroenterol 95:1253–1257, 2000

    Google Scholar 

  8. Collin P, Maki M, Keyrilainen O, Hallstrom O, Reunala T, Pasternack A: Selective IgA deficiency and coeliac disease. Scand J Gastroenterol 27:367–371, 1992

    Google Scholar 

  9. Cataldo F, Marino V, Bottaro G, Greco P, Ventura A: Celiac disease and selective immunoglobulin A deficiency. J Pediatr 131:306–308, 1997

    Google Scholar 

  10. Ferreira M, Davies SL, Butler M, Scott D, Clark M, Kumar P: Endomysial antibody: Is it the best screening test for coeliac disease? Gut 33:1633–1637, 1992

    Google Scholar 

  11. Lerner A, Kumar V, Iancu TC: Immunological diagnosis of childhood coeliac disease: Comparison between antigliadin, antireticulin and antiendomysial antibodies. Clin Exp Immunol 95:78–82, 1994

    Google Scholar 

  12. Broekroelofs J, Mulder AH, Nelis GF, Westerveld BD, Cohen Tervaert JW, Kallenberg CG: Anti-neutrophil cytoplasmic antibodies (ANCA) in sera from patients with inflammatory bowel disease (IBD). Relation to disease pattern and disease activity. Dig Dis Sci 39:545–549, 1994

    Google Scholar 

  13. Quinton JF, Sendid B, Reumaux D, Duthilleul P, Cortot A, Grandbastien B, Charrier G, Targan SR, Colombel JF, Poulain D: Anti-Saccharomyces cerevisiae mannan antibodies combined with antineutrophil cytoplasmic autoantibodies in inflammatory bowel disease: Prevalence and diagnostic role. Gut 42:788–791, 1998

    Google Scholar 

  14. O'Morain C, Tobin A, Leen E, Suzuki Y, O'Riordan T: Criteria of case definition in Crohn' disease and ulcerative colitis. Scand J Gastroenterol Suppl 170:7–11, 1989

    Google Scholar 

  15. Roozendaal C, Zhao MH, Horst G, Lockwood CM, Kleibeuker JH, Limburg PC, Nelis GF, Kallenberg CG: Catalase and alphaenolase: Two novel granulocyte autoantigens in inflammatory bowel disease (IBD). Clin Exp Immunol 112:10–16, 1998

    Google Scholar 

  16. Kallenberg CG, Mulder AH, Cohen Tervaert JW: Antineutrophil cytoplasmic antibodies: A still-growing class of autoantibodies in inflammatory disorders. Am J Med 93:675–682, 1992

    Google Scholar 

  17. Hansson T, Dahlbom I, Hall J, Holtz A, Elfman L, Dannaeus A, Klareskog L: Antibody reactivity against human and guinea pig tissue transglutaminase in children with celiac disease. J Pediatr Gastroenterol Nutr 30:379–384, 2000

    Google Scholar 

  18. Stern M: Comparative evaluation of serologic tests for celiac disease: A European initiative toward standardization. Working Group on Serologic Screening for Celiac Disease. J Pediatr Gastroenterol Nutr 31:513–519, 2000

    Google Scholar 

  19. Cataldo F, Marino V, Ventura A, Bottaro G, Corazza GR: Prevalence and clinical features of selective immunoglobulin A deficiency in coeliac disease: An Italian multicentre study. Italian Society of Paediatric Gastroenterology and Hepatology (SIGEP) and “Club del Tenue” Working Groups on Coeliac Disease. Gut 42:362–365, 1998

    Google Scholar 

  20. Hoffenberg EJ, Fidanza S, Sauaia A: Serologic testing for inflammatory bowel disease. J Pediatr 134:447–452, 1999

    Google Scholar 

  21. Ruemmele FM, Targan SR, Levy G, Dubinsky M, Braun J, Seidman EG: Diagnostic accuracy of serological assays in pediatric inflammatory bowel disease. Gastroenterology 115:822–829, 1998

    Google Scholar 

  22. Papo M, Quer JC, Pastor RM, Garcia-Pardo G, Prats E, Mirapeix E, Rodriguez R, Richart C: Antineutrophil cytoplasmic antibodies in relatives of patients with inflammatory bowel disease. Am J Gastroenterol 91:1512–1515, 1996

    Google Scholar 

  23. Vecchi M, Bianchi MB, Sinico RA, Radice A, Meucci G, Torgano G, Omodei P, Forzenigo L, Landoni M, Arrigoni M, Pozzi C, De Francis R: Antibodies to neutrophil cytoplasm in Italian patients with ulcerative colitis: Sensitivity, specificity and recognition of putative antigens. Digestion 55:34–39, 1994

    Google Scholar 

  24. Freeman HJ: Perinuclear antineutrophil cytoplasmic antibodies in collagenous or lymphocytic colitis with or without celiac disease. Can J Gastroenterol 11:417–420, 1997

    Google Scholar 

  25. Bansi DS, Fleming KA, Chapman RW: Importance of antineutrophil cytoplasmic antibodies in primary sclerosing cholangitis and ulcerative colitis: Prevalence, titre, and IgG subclass. Gut 38:384–389, 1996

    Google Scholar 

  26. Sugi K, Saitoh O, Matsuse R, Tabata K, Uchida K, Kojima K, Nakagawa K, Tanaka S, Teranishi T, Hirata I, Katsu K: Antineutrophil cytoplasmic antibodies in Japanese patients with inflammatory bowel disease: Prevalence and recognition of putative antigens. Am J Gastroenterol 94:1304–1312, 1999

    Google Scholar 

  27. Stoffel MP, Csernok E, Herzberg C, Johnson T, Carroll SF, Gross WL: Anti-neutrophil cytoplasmic antibodies (ANCA) directed against bactericidal/permeability increasing protein (BPI): A new seromarker for inflammatory bowel disease and associated disorders. Clin Exp Immunol 104:54–59, 1996

    Google Scholar 

  28. Schmitt WH, Csernok E, Flesch BK, Hauschild S, Gross WL: Autoantibodies directed against lysozyme: A new target antigen for anti-neutrophil cytoplasmic antibodies (ANCA). Adv Exp Med Biol 336:267–272, 1993

    Google Scholar 

  29. Kossa K, Coulthart A, Ives CT, Pusey CD, Hodgson HJ: Antigen specificity of circulating anti-neutrophil cytoplasmic antibodies in inflammatory bowel disease. Eur J Gastroenterol Hepatol 7:783–789, 1995

    Google Scholar 

  30. Giaffer MH, Clark A, Holdsworth CD: Antibodies to Saccharomyces cerevisiae in patients with Crohn' disease and their possible pathogenic importance. Gut 33:1071–1075, 1992

    Google Scholar 

  31. Darroch CJ, Barnes RM, Dawson J: Circulating antibodies to Saccharomyces cerevisiae (bakers'/brewers' yeast) in gastrointestinal disease. J Clin Pathol 52:47–53, 1999

    Google Scholar 

  32. Peeters M, Gcypens B, Claus D, Nevens H, Ghoos Y, Verbeke G, Baert F, Vermeire S, Vlietinck R, Rutgeerts P: Clustering of increased small intestinal permeability in families with Crohn' disease. Gastroenterology 113:802–807, 1997

    Google Scholar 

  33. Sendid B, Quinton JF, Charrier G, Goulet O, Cortot A, Grandbastien B, Poulain D, Colombel JF: Anti-Saccharomyces cerevisiae mannan antibodies in familial Crohn' disease. Am J Gastroenterol 93:1306–1310, 1998

    Google Scholar 

  34. Rioux JD, Silverberg MS, Daly MJ, Steinhart AH, McLeod RS, Griffiths AM, Green T, Brettin TS, Stone V, Bull SB, Bitton A, Williams CN, Greenberg GR, Cohen Z, Lander ES, Hudson TJ, Siminovitch KA: Genomewide search in Canadian families with inflammatory bowel disease reveals two novel susceptibility loci. Am J Hum Genet 66:1863–1870, 2000

    Google Scholar 

  35. Hugot JP, Chamaillard M, Zouali H, Lesage S, Cezard JP, Belaiche J, Almer S, Tysk C, O'Morain CA, Gassull M, Binder V, Finkel Y, Cortot A, Modigliani R, Laurent-Puig P, Gower-Rousseau C, Macr J, Colombel JF, Sahbatou M, Thomas G: Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn' disease. Nature 411:599–603, 2001

    Google Scholar 

  36. Liu J, Juo SH, Holopainen P, Terwilliger J, Tong X, Grunn A, Brito M, Green P, Mustalahti K, Maki M, Gilliam TC, Partanen J: Genomewide linkage analysis of celiac disease in Finnish families. Am J Hum Genet 70:51–59, 2002

    Google Scholar 

  37. Peeters M, Joossens S, Vermeire S, Vlietinck R, Bosuyt X, Rutgeers P: Diagnostic value of anti-Saccharomyces cerevisiae and antineutrophil cytoplasmic autoantibodies in inflammatory bowel disease. Am J Gastroenterol 96:730–734, 2001

    Google Scholar 

  38. Lepore L, Martelossi S, Pennesi M, Falcini F, Ermini ML, Ferrari R, Perticarari S, Presani G, Lucchesi A, Lapini M, Ventura A: Prevalence of celiac disease in patients with juvenile chronic arthritis. J Pediatr 129:311–313, 1996

    Google Scholar 

  39. Pocecco M, Ventura A: Coeliac disease and insulin-dependent diabetes mellitus: A causal association? Acta Paediatr 84:1432–1433, 1995

    Google Scholar 

  40. Collin P, Salmi J, Hallstrom O, Reunala T, Pasternack A: Autoimmune thyroid disorders and coeliac disease. Eur J Endocrinol 130:137–140, 1994

    Google Scholar 

  41. Kitis G, Holmes GK, Cooper BT, Thompson H, Allan RN: Association of cocliac disease and inflammatory bowel disease. Gut 21:636–641, 1980

    Google Scholar 

  42. Ventura A, Magazzu 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 117:297–303, 1999

    Google Scholar 

  43. Maki M: Coeliac disease and autoimmunity due to unmasking of cryptic epitopes? Lancet 348:1046–1047, 1996

    Google Scholar 

  44. Badenhoop K, Dieterich W, Segni M, Hofmann S, Hufner M, Usadel KH, Hahn EG, Schuppan D: HLA DQ2 and/or DQ8 is associated with celiac disease-specific autoantibodies to tissue transglutaminase in families with thyroid autoimmunity. Am J Gastroenterol 96:1648–1649, 2001

    Google Scholar 

  45. Schuppan D, Hahn EG: Celiac disease and its link to type 1 diabetes mellitus. J Pediatr Endocrinol Metab 14(S):597–605, 2001

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Damoiseaux, J.G., Bouten, B., Linders, A.M. et al. Diagnostic Value of Anti-Saccharomyces cerevisiae and Antineutrophil Cytoplasmic Antibodies for Inflammatory Bowel Disease: High Prevalence in Patients with Celiac Disease. J Clin Immunol 22, 281–288 (2002). https://doi.org/10.1023/A:1019926121972

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1019926121972

Navigation