Digestive Diseases and Sciences

, Volume 56, Issue 1, pp 70–78

Schistosoma mansoni Infection but Not Egg Antigen Promotes Recovery from Colitis in Outbred NMRI Mice

  • Peggy Bodammer
  • Grit Waitz
  • Micha Loebermann
  • Martha Charlotte Holtfreter
  • Claudia Maletzki
  • Marzena Renata Krueger
  • Horst Nizze
  • Joerg Emmrich
  • Emil Christian Reisinger
Original Article



The ability of intestinal helminths to manipulate the immune system of their host towards a Th2 response has been proposed to modulate auto-immune and allergic diseases.


This initial study investigated the anti-inflammatory potential of S. mansoni and soluble egg antigen (SEA) in a murine model of colitis.


Colitis was induced in female NMRI mice by 5% dextran sulfate sodium (DSS) for 7 days, either 9 weeks post-infection with S. mansoni or during treatment with SEA. In addition to clinical signs of colitis, colon histology, immunohistochemistry, and flow cytometry of leukocytes were performed. Colon cytokines were measured using a quantitative real-time technique.


Infection with cercariae of S. mansoni attenuated DSS-induced colitis. Clinical symptoms such as weight loss and shortening of colon length were significantly prevented. Histological scores and cell infiltration were affected and expression of pro-inflammatory cytokines in the colons of infected DSS colitis mice was reduced. In contrast, application of SEA failed to improve colitis, even though some findings like earlier manifestation of inflammation and local induction of Th2 cytokines were similar to the effects of cercarial infection.


The results presented here suggest that SEA treatment could not protect mice from acute colitis. However, both infection with S. mansoni and injection of SEA affect mucosal immune responses.


Schistosoma mansoni Soluble egg antigen DSS colitis Outbred mice 


  1. 1.
    Sood A, Midha V. Epidemiology of inflammatory bowel disease in Asia. Indian J Gastroenterol. 2007;26:285–289.PubMedGoogle Scholar
  2. 2.
    Strachan DP. Hay fever, hygiene, and household size. BMJ. 1989;299:1259–1260.CrossRefPubMedGoogle Scholar
  3. 3.
    Kitagaki K, Businga TR, Racila D, et al. Intestinal helminths protect in a murine model of asthma. J Immunol. 2006;177:1628–1635.PubMedGoogle Scholar
  4. 4.
    Weinstock JV, Summers R, Elliott DE. Helminths and harmony. Gut. 2004;53:7–9.CrossRefPubMedGoogle Scholar
  5. 5.
    Araújo MI, Hoppe BS, Medeiros M, et al. Schistosoma mansoni infection modulates the immune response against allergic and auto-immune disease. Mem Inst Oswaldo Cruz. 2004;99:27–32.PubMedGoogle Scholar
  6. 6.
    Setiawan T, Metwali A, Blum AM, et al. Heligmosomoides polygyrus promotes regulatory T-cell cytokine production in the murine distal intestine. Infect Immun. 2007;75:4655–4663.CrossRefPubMedGoogle Scholar
  7. 7.
    Hunter MM, Wang A, Hirota CL, et al. Neutralizing anti-IL-10 antibody blocks the protective effect of tapeworm infection in am murine model of chemically induced colitis. J Immunol. 2005;174:7368–7375.PubMedGoogle Scholar
  8. 8.
    Khan WI, Blennerhasset PA, Varghese AK, et al. Intestinal nematode infection ameliorates experimental colitis in mice. Infect Immun. 2002;70:5931–5937.CrossRefPubMedGoogle Scholar
  9. 9.
    Moreels TG, Nieuwendijk RJ, De Man JG, et al. Concurrent infection with Schistosoma mansoni attenuates inflammation induced changes in colonic morphology, cytokine levels, and smooth muscle contractility of trinitrobenzene sulphonic acid induced colitis in rats. Gut. 2004;53:99–107.CrossRefPubMedGoogle Scholar
  10. 10.
    Elliott DE, Li J, Blum A, et al. Exposure to schistosome eggs protects mice from TNBS-induced colitis. Am J Physiol Gastrointest Liver Physiol. 2003;284:385–391.Google Scholar
  11. 11.
    Mo HM, Liu WQ, Lei JH, et al. Schistosoma japonicum eggs modulate the activity of CD4 + CD25 + Tregs and prevent development of colitis in mice. Exp Parasitol. 2007;116:385–389.CrossRefPubMedGoogle Scholar
  12. 12.
    Summers RW, Elliott DE, Qadir K, et al. Trichuris suis seems to be safe and possible effective in the treatment of inflammatory bowel disease. Am J Gastroenterol. 2003;98:2034–2041.CrossRefPubMedGoogle Scholar
  13. 13.
    Summers RW, Elliott DE, Urban JF, et al. Trichuris suis therapy for active ulcerative colitis: a randomized controlled trial. Gastroenterology. 2005;128:825–832.CrossRefPubMedGoogle Scholar
  14. 14.
    Summers RW, Elliott DE, Urban JF, et al. Trichuris suis therapy in Crohn′s disease. Gut. 2005;54:87–90.CrossRefPubMedGoogle Scholar
  15. 15.
    Kradin RL, Badizadegan K, Auluck P, et al. Iatrogenic Trichuris suis infection in a patient with Crohn disease. Arch Pathol Lab Med. 2006;130:718–720.PubMedGoogle Scholar
  16. 16.
    Smith P, Mangan NE, Walsh CM, et al. Infection with a helminth parasite prevents experimental colitis via a macrophage-mediated mechanism. J Immunol. 2007;178:4557–4566.PubMedGoogle Scholar
  17. 17.
    Okayasu I, Hatakeyama S, Yamada M, et al. A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice. Gastroenterology. 1990;98:694–702.PubMedGoogle Scholar
  18. 18.
    Kawada M, Arihiro A, Mizoguchi E. Insights from advances in research of chemically induced experimental models of human inflammatory bowel disease. World J Gastroenteol. 2007;13:5581–5593.Google Scholar
  19. 19.
    Melgar S, Karlsson L, Rehnström E, et al. Validation of murine dextran sulfate sodium-induced colitis using four therapeutic agents for human inflammatory bowel disease. Int Immunopharmacol. 2008;8:836–844.CrossRefPubMedGoogle Scholar
  20. 20.
    Wirtz S, Neufert C, Weigmann B, et al. Chemically induced mouse models of intestinal inflammation. Nat Protoc. 2007;2:541–546.CrossRefPubMedGoogle Scholar
  21. 21.
    Cruickshank SM, English NR, Felsburg PJ, et al. Characterization of colonic dendritic cells in normal and colitic mice. World J Gastroenterol. 2005;11:6338–6347.PubMedGoogle Scholar
  22. 22.
    Maul J, Loddenkemper C, Mundt P, et al. Peripheral and intestinal regulatory CD4 + CD25 (high) T-cells in inflammatory bowel diseases. Gastroenterology. 2005;128:1868–1878.CrossRefPubMedGoogle Scholar
  23. 23.
    Pearce EJ, Kane CM, Sun J, et al. Th2 response polarization during infection with the helminth parasite Schistosoma mansoni. Immunol Rev. 2004;201:117–126.CrossRefPubMedGoogle Scholar
  24. 24.
    Ashton PD, Harrop R, Shah B, et al. The schistosome egg development and secretions. Parasitology. 2001;122:329–338.CrossRefPubMedGoogle Scholar
  25. 25.
    Ruyssers NE, De Winter BY, De Man JG, et al. Therapeutic potential of helminth soluble proteins in TNBS-induced colitis in mice. Inflamm Bowel Dis. 2009;15:491–500.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Peggy Bodammer
    • 1
    • 2
  • Grit Waitz
    • 2
  • Micha Loebermann
    • 1
  • Martha Charlotte Holtfreter
    • 1
  • Claudia Maletzki
    • 2
  • Marzena Renata Krueger
    • 3
  • Horst Nizze
    • 3
  • Joerg Emmrich
    • 2
  • Emil Christian Reisinger
    • 1
  1. 1.Division of Tropical Medicine and Infectious Diseases, Department of Internal MedicineUniversity of RostockRostockGermany
  2. 2.Division of Gastroenterology, Department of Internal MedicineUniversity of RostockRostockGermany
  3. 3.Institute of PathologyUniversity of RostockRostockGermany

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