Parasitology Research

, Volume 107, Issue 1, pp 1–8 | Cite as

Murine schistosomiasis as a model for human schistosomiasis mansoni: similarities and discrepancies

  • Rashad A. Abdul-Ghani
  • Azza A. Hassan


Human schistosomiasis has been studied extensively since its discovery by Theodore Bilharz in 1851. Because of its medical importance as a chronic debilitating disease in the tropics and subtropics, continuing research efforts are still going on. The use of animal models still represents a major cornerstone in this field, with murine hosts, especially mice, as the most preferable experimental units. Murine schistosomiasis has been employed as a model for studying various aspects of human schistosomiasis, including biology, pathogenesis, immunology, chemotherapy screening, and vaccine development. However, there may be differences between murine and human schistosomiasis. The present article tries to explore some of these aspects that may help researchers in the field of schistosomiasis.


DHEA Schistosomiasis Praziquantel Worm Burden Schistosome Infection 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Abath FG, Morais CN, Montenegro CE, Wynn TA, Montenegro SM (2006) Immunopathogenic mechanisms in schistosomiasis: what can be learnt from human studies? Trends Parasitol 22:85–91CrossRefPubMedGoogle Scholar
  2. Aitken R, Wilson RA (1989) The growth and development of Schistosoma mansoni in mice exposed to sublethal doses of radiation. J Parasitol 75:958–963CrossRefPubMedGoogle Scholar
  3. Amiri P, Locksley RM, Parslow TG, Sadick M, Rector E, Ritter D, McKerrow JH (1992) Tumour necrosis factor alpha restores granulomas and induces parasite egg-laying in schistosome-infected SCID mice. Nature 356:604–607CrossRefPubMedGoogle Scholar
  4. Andrade ZA, Baptista AP, Santana TS (2006) Remodeling of hepatic vascular changes after specific chemotherapy of schistosomal periportal fibrosis. Mem Inst Oswaldo Cruz 101(Suppl 1):267–272PubMedGoogle Scholar
  5. Balloul JM, Grzych JM, Pierce RJ, Capron A (1987a) A purified 28, 000 dalton protein from Schistosoma mansoni adult worms protects rats and mice against experimental schistosomiasis. J Immunol 138:3448–3453PubMedGoogle Scholar
  6. Balloul JM, Sondermeyer P, Dreyer D, Capron M, Grzych JM, Pierce RJ, Carvallo D, Lecocq JP, Capron A (1987b) Molecular cloning of a protective antigen of schistosomes. Nature 326:149–153CrossRefPubMedGoogle Scholar
  7. Botros SS, El-Din SH, El-Lakkany NM, Sabra AN, Ebeid FA (2006) Drug-metabolizing enzymes and praziquantel bioavailability in mice harboring Schistosoma mansoni isolates of different drug susceptibilities. J Parasitol 92:1344–1349CrossRefPubMedGoogle Scholar
  8. Capron M, Capron A (1986) Rats, mice and men—models for immune effector mechanisms against schistosomiasis. Parasitol Today 2:69–75CrossRefPubMedGoogle Scholar
  9. Capron M, Capron A (1994) Immunoglobulin E and effector cells in schistosomiasis. Science 264:1876–1877CrossRefPubMedGoogle Scholar
  10. Cheever AW (1968) Conditions affecting the accuracy of potassium hydroxide digestion techniques for counting Schistosoma mansoni eggs in tissues. Bull World Health Organ 39:328–331PubMedGoogle Scholar
  11. Cheever AW (1969) Quantitative comparison of the intensity of Schistosoma mansoni infections in man and experimental animals. Trans R Soc Trop Med Hyg 63:781–795CrossRefPubMedGoogle Scholar
  12. Cheever AW, Yap GS (1997) Immunologic basis of disease and disease regulation in schistosomiasis. Chem Immunol 66:159–176CrossRefPubMedGoogle Scholar
  13. Cheever AW, Eltoum IA, Andrade ZA, Cox TM (1993) Biology and pathology of Schistosoma mansoni and Schistosoma japonicum infections in several strains of nude mice. Am J Trop Med Hyg 48:496–503PubMedGoogle Scholar
  14. Cheever AW, Mosimann JE, Deb S, Cheever EA, Duvall AH (1994a) Natural history of Schistosoma mansoni infection in mice: egg production, egg passage in the feces, and contribution of host and parasite death to changes in worm numbers. Am J Trop Med Hyg 50:269–280PubMedGoogle Scholar
  15. Cheever AW, Macedonia JG, Mosimann JE, Cheever EA (1994b) Kinetics of egg production and egg excretion by Schistosoma mansoni and S. japonicum in mice infected with a single pair of worms. Am J Trop Med Hyg 50:281–295PubMedGoogle Scholar
  16. Cheever AW, Lenzi JA, Lenzi HL, Andrade ZA (2002) Experimental models of Schistosoma mansoni infection. Mem Inst Oswaldo Cruz 97:917–940CrossRefPubMedGoogle Scholar
  17. Chensue SW, Boros DL (1979) Modulation of granulomatous Hypersensitivity. I. Characterization of T lymphocytes involved in the adoptive suppression of granuloma formation in Schistosoma mansoni-infected mice. J Immunol 123:1409–1414PubMedGoogle Scholar
  18. Chiaramonte MG, Donaldson DD, Cheever AW, Wynn TA (1999) An IL-13 inhibitor blocks the development of hepatic fibrosis during a T-helper type 2-dominated inflammatory response. J Clin Invest 104:777–785CrossRefPubMedGoogle Scholar
  19. Cioli D, Knopf PM, Senft AW (1977) A study of Schistosoma mansoni transferred into permissive and nonpermissive hosts. Int J Parasitol 7:293–298CrossRefPubMedGoogle Scholar
  20. Cles GC (1999) Schistosomiasis. In: Zak O, Sande MA (eds) Handbook of animal models of infection. Academic Press, San Diego, pp 873–876CrossRefGoogle Scholar
  21. Corrêa-Oliveira R, Malaquias LC, Falcão PL, Viana IR, Bahia Oliveira LM, Silveira AM et al. (1998) Cytokines as determinants of resistance and pathology in human Schistosoma mansoni infection. Braz J Med Biol Res 31:171–177CrossRefPubMedGoogle Scholar
  22. Czaja MJ, Weiner FR, Takahashi S, Giambrone M-A, van der Meide PH, Schellekens H et al. (1989) Gamma-interferon treatment inhibits collagen deposition in murine schistosomiasis. Hepatology 10:795–800CrossRefPubMedGoogle Scholar
  23. Davies SJ, Grogan JL, Blank RB, Lim KC, Locksley RM, McKerrow JH (2001) Modulation of blood fluke development in the liver by hepatic CD4+ lymphocytes. Science 294:1358–1361CrossRefPubMedGoogle Scholar
  24. Doenhoff M, Musallam R, Bain J, McGregor A (1978) Studies on the host–parasite relationship in Schistosoma mansoni-infected mice: the immunological dependence of parasite egg excretion. Immunology 35:771–778PubMedGoogle Scholar
  25. Dunn MA, Rojkind M, Warren KS, Hait PK, Rifas L, Seifter S (1977) Liver collagen synthesis in murine schistosomiasis. J Clin Invest 59:666–674CrossRefPubMedGoogle Scholar
  26. Dunne DW, Mountford AP (2001) Resistance to infection in humans and animal models. In: Mahmoud AAF (ed) Schistosomiasis. Imperial College Press pp 133–212Google Scholar
  27. Eloi-Santos S, Olsen NJ, Correa-Oliveira R, Colley DG (1992) Schistosoma mansoni: mortality, pathophysiology, and susceptibility differences in male and female mice. Exp Parasitol 75:168–175CrossRefPubMedGoogle Scholar
  28. Fallon PG (2000) Immunopathology of schistosomiasis: a cautionary tale of mice and men. Immunol Today 21:29–35CrossRefPubMedGoogle Scholar
  29. Fallon PG, Richardson EJ, McKenzie GJ, McKenzie AN (2000) Schistosome infection of transgenic mice defines distinct and contrasting pathogenic roles for IL-4 and IL-13: IL-13 is a profibrotic agent. J Immunol 164:2585–2591PubMedGoogle Scholar
  30. Farah IO, Kariuki TM, King CL, Hau J (2001) An overview of animal models in experimental schistosomiasis and refinements in the use of non-human primates. Lab Anim 35:205–212CrossRefPubMedGoogle Scholar
  31. Farah IO, Ngotho M, Kariuki T,Jeneby M, Irura L, Maina N et al (2005) Animal models for tropical parasitic diseases. In: Hau J, Van Hoosier Jr GL (eds) Handbook of laboratory animal science, Vol. III. Animal models, 2nd edn. CRC Press, pp 169–224Google Scholar
  32. Farias LP, Cardoso FC, Miyasato PA, Montoya BO, Tararam CA, Roffato HK et al. (2010) Schistosoma mansoni Stomatin like protein-2 is located in the tegument and induces partial protection against challenge infection. PLoS Negl Trop Dis 4:e597CrossRefPubMedGoogle Scholar
  33. Fulford AJ, Webster M, Ouma JH, Kimani G, Dunne DW (1998) Puberty and age-related changes in susceptibility to schistosome infection. Parasitol Today 14:23–26CrossRefPubMedGoogle Scholar
  34. Goble FC, Konopka EA (1973) Sex as a factor in infectious disease. Trans N Y Acad Sci 35:325–346Google Scholar
  35. Grzych JM, Pearce E, Cheever A, Caulada ZA, Caspar P, Heiny S et al. (1991) Egg deposition is the major stimulus for the production of Th2 cytokines in murine schistosomiasis mansoni. J Immunol 146:1322–1327PubMedGoogle Scholar
  36. Hagan P (1993) IgE and protective immunity to helminth infections. Parasite immunol 15:1–4CrossRefPubMedGoogle Scholar
  37. Harrison RA, Doenhoff MJ (1983) Retarded development of Schistosoma mansoni in immunodepressed mice. Parasitology 86:429–438CrossRefPubMedGoogle Scholar
  38. Henderson GS, Nix NA, Montesano MA, Gold D, Freeman GL Jr, McCurley TL et al (1993) Two distinct pathologic syndromes in male CBA/J inbred mice with chronic Schistosoma mansoni infections. Am J Pathol 142:703–714PubMedGoogle Scholar
  39. Herbert DR, Hölscher C, Mohrs M, Arendse B, Schwegmann A, Radwanska M et al (2004) Alternative macrophage activation is essential for survival during schistosomiasis and downmodulates T helper 1 responses and immunopathology. Immunity 20:623–635CrossRefPubMedGoogle Scholar
  40. Hernandez DC, Lim KC, McKerrow JH, Davies SJ (2004) Schistosoma mansoni: sex-specific modulation of parasite growth by host immune signals. Exp Parasitol 106:59–61CrossRefPubMedGoogle Scholar
  41. Hesse M, Piccirillo CA, Belkaid Y, Prufer J, Mentink-Kane M, Leusink M et al (2004) The pathogenesis of schistosomiasis is controlled by cooperating IL-10-producing innate effector and regulatory T cells. J Immunol 172:3157–3166PubMedGoogle Scholar
  42. Karanja DM, Colley DG, Nahlen BL, Ouma JH, Secor WE (1997) Studies on schistosomiasis in western Kenya: I. Evidence for immune-facilitated excretion of schistosome eggs from patients with Schistosoma mansoni and human immunodeficiency virus coinfections. Am J Trop Med Hyg 56:515–521PubMedGoogle Scholar
  43. Lacroix C, Akarid K, Chau F, Sinet M, Verola O, Carbon C et al (1998) The Th1 to Th2 shift induced by Schistosoma mansoni does not exacerbate murine aids (MAIDS). Parasite Immunol 20:497–501CrossRefPubMedGoogle Scholar
  44. Lanar DE, Pearce EJ, James SL, Sher A (1986) Identification of paramyosin as schistosome antigen recognized by intradermally vaccinated mice. Science 234:593–596CrossRefPubMedGoogle Scholar
  45. Maizels RM, Balic A, Gomez-Escobar N, Nair M, Taylor MD, Allen JE (2004) Helminth parasites- -masters of regulation. Immunol Rev 201:89–116CrossRefPubMedGoogle Scholar
  46. Mathew RC, Boros DL (1986) Anti-L3T4 antibody treatment suppresses hepatic granuloma formation and abrogates antigen-induced IL-2 production in Schistosoma mansoni infection. Infect Immun 54:820–826PubMedGoogle Scholar
  47. Mehlhorn H (2008) Encyclopedia of parasitology, 3rd edn. Springer-Veralg, Berlin Heidelberg New YorkGoogle Scholar
  48. Montesano MA, Lima MS, Correa-Oliveira R, Gazzinelli G, Colley DG (1989) Immune responses during human schistosomiasis mansoni. XVI. Idiotypic differences in antibody preparations from patients with different clinical forms of infection. J Immunol 142:2501–2506PubMedGoogle Scholar
  49. Montesano MA, Freeman GL Jr, Secor WE, Colley DG (1997) Immunoregulatory idiotypes stimulate T helper 1 cytokine responses in experimental Schistosoma mansoni infections. J Immunol 158:3800–3804PubMedGoogle Scholar
  50. Nakazawa M, Fantappie MR, Freeman GL Jr, Eloi-Santos S, Olsen NJ, Kovacs WJ et al (1997) Schistosoma mansoni: susceptibility differences between male and female mice can be mediated by testosterone during early infection. Exp Parasitol 85:240–234CrossRefGoogle Scholar
  51. Nyindo M, Farah IO (1999) The baboon as a non-human primate model of human schistosome infection. Parasitol Today 15:478–482CrossRefPubMedGoogle Scholar
  52. Olds GR, Griffin A, Kresina TF (1985) Dynamics of collagen accumulation and polymorphism in murine Schistosoma japonicum. Gastroenterology 89:617–624PubMedGoogle Scholar
  53. Pearce EJ, James SL, Hieny S, Lanar DE, Sher A (1988) Induction of protective immunity against Schistosoma mansoni by vaccination with schistosome paramyosin (Sm97), a nonsurface parasite antigen. Proc Natl Acad Sci 85:5678–5682CrossRefPubMedGoogle Scholar
  54. Pearce EJ, Caspar P, Grzych JM, Lewis FA, Sher A (1991) Downregulation of Th1 cytokine production accompanies induction of Th2 responses by a parasitic helminth, Schistosoma mansoni. J Exp Med 173:159–166CrossRefPubMedGoogle Scholar
  55. Pellegrino J, Oliveira CA, Faria J, Cunha AS (1962) New approach to the screening of drugs in experimental schistosomiasis mansoni in mice. Am J Trop Med Hyg 11:201–215PubMedGoogle Scholar
  56. Ramirez B, Bickle Q, Yousif F, Fakorede F, Mouries M-A, Nwaka S (2007) Schistosomes: challenges in compound screening. Expert Opin Drug Discov 2(suppl 1):S53–S61CrossRefGoogle Scholar
  57. Rumbley CA, Sugaya H, Zekavat SA, Perrin PJ, Phillips SM (2001) Elimination of lymphocytes, but not eosinophils, by Fas-mediated apoptosis in murine schistosomiasis. Am J Trop Med Hyg 65:442–449PubMedGoogle Scholar
  58. Santos Rde O, Barbosa Júnior AA, Andrade ZA (1992) Dynamics of fibrosis production and resorption in intestinal schistosomiasis of mice. Mem Inst Oswaldo Cruz 87:25–31PubMedGoogle Scholar
  59. Sher A, Coffman RL, Hieny S, Scott P, Cheever AW (1990) Interleukin 5 is required for the blood and tissue eosinophilia but not granuloma formation induced by infection with Schistosoma mansoni. Proc Natl Acad Sci USA 87:61–65CrossRefPubMedGoogle Scholar
  60. Siddiqui AA, Ahmad G, Damian RT, Kennedy RC (2008) Experimental vaccines in animal models for schistosomiasis. Parasitol Res 102:825–833CrossRefPubMedGoogle Scholar
  61. Smithers SR, Doenhoff MJ (1982) Schistosomiasis. In: Cohen S, Warren KS (eds) Immunology of parasitic infections, 2nd edn. Blackwell, London, pp 527–607Google Scholar
  62. Smithers SR, Terry RJ (1965) The infection of laboratory hosts with cercariae of Schistosoma mansoni and the recovery of adult worms. Parasitology 55:695–700PubMedGoogle Scholar
  63. Stadecker MJ, Asahi H, Finger E, Hernandez HJ, Rutitzky LI, Sun J (2004) The immunobiology of Th1 polarization in high-pathology schistosomiasis. Immunol Rev 201:168–179CrossRefPubMedGoogle Scholar
  64. Stavitsky AB (2004) Regulation of granulomatous inflammation in experimental models of schistosomiasis. Infect Immun 72:1–12CrossRefPubMedGoogle Scholar
  65. Takahashi S, Simpser E (1981) Granuloma collagenase and EDTA-sensitive neutral protease production in hepatic murine schistosomiasis. Hepatology 1:211–220CrossRefPubMedGoogle Scholar
  66. Takahashi S, Dunn MA, Seifter S (1980) Liver collagenase in murine schistosomiasis. Gastroenterology 78:1425–1431PubMedGoogle Scholar
  67. Tallima H, Salah M, Guirguis FR, El Ridi R (2009) Transforming growth factor-β and Th17 responses in resistance to primary murine schistosomiasis mansoni. Cytokine 48:239–245CrossRefPubMedGoogle Scholar
  68. Tiboldi T (1979) Intestinal parameters in acute murine schistosomiasis mansoni. Trans R Soc Trop Med Hyg 73:81–84CrossRefPubMedGoogle Scholar
  69. Warren KS, Peters PA (1967) Comparison of penetration and maturation of Schistosoma mansoni in the hamster, mouse, guinea pig, rabbit, and rat. Am J Trop Med Hyg 16:718–722Google Scholar
  70. Watanabe K, Carter JM, Neely-Burnam M, Colley DG (2009) Relative imbalance between T regulatory cells and activated T cells in mice with differential morbidity in chronic Schistosoma mansoni infections. Parasite Immunol 31:440–446CrossRefPubMedGoogle Scholar
  71. Weinstock JV, Boros DL (1983a) Organ dependent differences in composition and function observed in hepatic and intestinal granulomas isolated from mice with schistosomiasis mansoni. J Immunol 130:418–422PubMedGoogle Scholar
  72. Weinstock JV, Boros DL (1983b) Modulation of granulomatous Hypersensitivity. VI. T lymphocyte subsets influence mast cell density in liver granulomas of Schistosoma mansoni-infected mice. J Immunol 131:959–961PubMedGoogle Scholar
  73. Wilson RA (1990) Leaky livers, portal shunting and immunity to schistosomes. Parasitol Today 6:354–358CrossRefPubMedGoogle Scholar
  74. Wilson MS, Mentink-Kane MM, Pesce JT, Ramalingam TR, Thompson R, Wynn TA (2007) Immunopathology of schistosomiasis. Immunol Cell Biol 85:148–154CrossRefPubMedGoogle Scholar
  75. Wynn TA, Thompson RW, Cheever AW, Mentink-Kane MM (2004) Immunopathogenesis of schistosomiasis. Immunol Rev 201:156–167CrossRefPubMedGoogle Scholar
  76. Zwingenberger K, Hohmann A, de Brito MC, Ritter M (1991) Impaired balance of interleukin-4 and interferon-gamma production in infections with Schistosoma mansoni and intestinal nematodes. Scand J Immunol 34:243–251CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  1. 1.Department of Medical Parasitology, Faculty of Medicine and Health SciencesSana’a UniversitySana’aYemen
  2. 2.Tropical Health Department, High Institute of Public HealthAlexandria UniversityAlexandriaEgypt

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