Hostname: page-component-cc8bf7c57-llmch Total loading time: 0 Render date: 2024-12-12T04:45:12.675Z Has data issue: false hasContentIssue false

The mucosal response of hamsters to a low-intensity superimposed secondary infection with the hookworm Ancylostoma ceylanicum

Published online by Cambridge University Press:  29 April 2010

L.M.M. Alkazmi
Affiliation:
School of Biology, University of Nottingham, University Park, NottinghamNG7 2RD, UK
J.M. Behnke*
Affiliation:
School of Biology, University of Nottingham, University Park, NottinghamNG7 2RD, UK
*
*Fax: +44(0) 115 951 3251 E-mail: [email protected]

Abstract

An experiment was conducted to assess the mucosal response to low-dose superimposed challenge with Ancylostoma ceylanicum. Hamsters were assigned to five treatment groups (1–5 respectively): naïve controls; primary immunizing infection controls; challenge controls; immunized, anthelmintic–treated, challenged group; immunized, superimposed challenge group. Group 4 hamsters were resistant to challenge, whereas most of the challenge inoculum larvae established in Group 5. Villus height and crypt depth measurements were initially markedly divergent between these two groups but over time post-challenge (pc) values for both parameters drew nearer and by day 31 pc they were indistinguishable. The greatest change was experienced by Group 4 which showed increasing inflammation and gut pathology during the challenge infection. Mitotic activity in crypts and mast cell counts in the mucosa were highest in Group 5 on day 10 pc, but there was little to distinguish between Groups 4 and 5 by day 31 pc. Goblet cell, eosinophil and Paneth cell counts were very similar throughout in both groups but, in the case of Paneth cells, they were consistent with a possible role in protective immunity to challenge. Some adult worms survived throughout the period of intense inflammation, emphasizing their tremendous resilience and resistance to mucosal host protective responses.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alkazmi, L.M.M. & Behnke, J.M. (2010) The mucosal response to secondary infection with the hookworm Ancylostoma ceylanicum in hamsters immunized by abbreviated primary infection. Parasite Immunology 32, 4756.CrossRefGoogle ScholarPubMed
Alkazmi, L.M.M., Dehlawi, M.S. & Behnke, J.M. (2006) The effect of the hookworm Ancylostoma ceylanicum on the mucosal architecture of the small intestine. Journal of Helminthology 80, 397407.CrossRefGoogle ScholarPubMed
Alkazmi, L.M.M., Dehlawi, M.S. & Behnke, J.M. (2008) The mucosal cellular response to infection with Ancylostoma ceylanicum. Journal of Helminthology 82, 3344.CrossRefGoogle ScholarPubMed
Ball, P.A.J. & Bartlett, A. (1969) Serological reactions to infection with Necator americanus. Transactions of the Royal Society of Tropical Medicine and Hygiene 63, 362369.CrossRefGoogle ScholarPubMed
Barnard, C., Gilbert, F. & McGregor, P. (2007) Asking questions in biology. 3rd edn.London, Prentice Hall.Google Scholar
Behnke, J.M. (1987) Do hookworms elicit protective immunity in man? Parasitology Today 3, 200206.CrossRefGoogle ScholarPubMed
Behnke, J.M. (1990) Laboratory animal models. pp. 105128in Schad, G.A. & Warren, K.S. (Eds) Hookworm disease. Current status and new directions. London, Taylor and Francis.Google Scholar
Behnke, J.M. (1991) Pathology. pp. 5191in Gilles, H.M. & Ball, P.A.J. (Eds) Human parasitic diseases, Vol. 4, Hookworm infections. Amsterdam, The Netherlands, Elsevier.Google Scholar
Behnke, J.M., Hannah, J. & Pritchard, D.I. (1983) Nematospiroides dubius in the mouse: evidence that adult worms depress the expression of homologous immunity. Parasite Immunology 5, 397408.CrossRefGoogle ScholarPubMed
Behnke, J.M., Rose, R. & Little, J. (1994) Resistance of the hookworms Ancylostoma ceylanicum and Necator americanus to intestinal inflammatory responses induced by heterologous infection. International Journal for Parasitology 24, 91101.CrossRefGoogle ScholarPubMed
Behnke, J.M., Guest, J. & Rose, R. (1997) Expression of acquired immunity to the hookworm Ancylostoma ceylanicum in hamsters. Parasite Immunology 19, 309318.CrossRefGoogle Scholar
Brailsford, T.J. & Behnke, J.M. (1992) The dynamics of trickle infection with Ancylostoma ceylanicum in inbred hamsters. Parasitology 105, 247253.CrossRefGoogle ScholarPubMed
Bungiro, R.D., Greene, J. Jr, Kruglov, E. & Capello, M. (2001) Mitigation of hookworm disease by immunization with soluble extracts of Ancylostoma ceylanicum. Journal of Infectious Diseases 183, 13801387.CrossRefGoogle ScholarPubMed
Bungiro, R.D. Jr, Sun, T., Harrison, L.M., Shoemaker, C.B. & Capello, M. (2008) Mucosal antibody responses in experimental hookworm infection. Parasite Immunology 30, 293303.CrossRefGoogle ScholarPubMed
Carroll, S.M. & Grove, D.I. (1986) Resistance of dogs to challenge with Ancylostoma ceylanicum during the tenure of a primary hookworm infection. Transactions of the Royal Society of Tropical Medicine and Hygiene 80, 406411.CrossRefGoogle ScholarPubMed
Dondji, B., Bungiro, R.D., Harrison, L.M., Vermeire, J.J., Bifulco, C., McMahon-Pratt, D. & Cappello, M. (2008) Role for nitric oxide in hookworm-associated immune suppression. Infection and Immunity 76, 25602567.CrossRefGoogle ScholarPubMed
Elphick, D.A. & Mahida, Y.R. (2005) Paneth cells: their role in innate immunity and inflammatory disease. Gut 54, 18021809.CrossRefGoogle ScholarPubMed
Else, K.J. & Finkelman, F.D. (1998) Intestinal nematode parasites, cytokines and effector mechanisms. International Journal for Parasitology 28, 11451158.CrossRefGoogle ScholarPubMed
Fujiwara, R.T., Geiger, S.M., Bethony, J. & Mendez, S. (2006) Comparative immunology of human and animal models of hookworm. Parasite Immunology 28, 285293.CrossRefGoogle ScholarPubMed
Garside, P. & Behnke, J.M. (1989) Ancylostoma ceylanicum in the hamster. Observations on the host–parasite relationship during primary infection. Parasitology 98, 283289.CrossRefGoogle ScholarPubMed
Garside, P., Behnke, J.M. & Rose, R.A. (1989) The immune response of male DSN hamsters to a primary infection with Ancylstoma ceylanicum. Journal of Helminthology 63, 251260.CrossRefGoogle ScholarPubMed
Garside, P., Behnke, J.M. & Rose, R.A. (1990) Acquired immunity to Ancylostoma ceylanicum in hamsters. Parasite Immunology 12, 247258.CrossRefGoogle ScholarPubMed
Garside, P., Grencis, R.K. & Mowatt, M.A.C.I. (1992) T lymphocyte dependent enteropathy in murine Trichinella spiralis infection. Parasite Immunology 14, 217225.CrossRefGoogle ScholarPubMed
Gause, W.C., Urban, J.F. Jr & Stadecker, M.J. (2003) The immune response to parasitic helminths: insights from murine models. Trends in Immunology 24, 269277.CrossRefGoogle ScholarPubMed
Geiger, S.M., Massara, C.L., Bethony, J., Soboslay, P.T. & Correa-Oliveira, R. (2004) Cellular responses and cytokine production in post-treatment hookworm patients from an endemic area in Brazil. Clinical and Experimental Immunology 136, 334340.CrossRefGoogle ScholarPubMed
Ghosh, K., Wu, W., Antione, A.D., Bottazzi, M.E., Valenzuela, J.G., Hotez, P.J. & Mendez, S. (2006) The impact of concurrent and treated Ancylostoma ceylanicum hookworm infections on the immunogenicity of a recombinant hookworm vaccine in hamsters. Journal of Infectious Diseases 193, 155162.CrossRefGoogle ScholarPubMed
Kalkofen, U.P. (1970) Attachment and feeding behaviour of Ancylostoma caninum. Zeitschrift fur Parasitenkunde 33, 339354.CrossRefGoogle ScholarPubMed
Kamal, M., Wakelin, D., Ouellette, A.J., Smith, S., Podolsky, D.K. & Mahida, Y.R. (2001) Mucosal T cells regulate Paneth and intermediate cell numbers in the small intestine of T. spiralis-infected mice. Clinical and Experimental Immunology 126, 117125.CrossRefGoogle ScholarPubMed
Kamal, M., Dehlawi, M.S., Rosa Brunet, L. & Wakelin, D. (2002) Paneth and intermediate cell hyperplasia induced in mice by helminth infections. Parasitology 125, 275281.CrossRefGoogle ScholarPubMed
Kermanizadeh, P., Crompton, D.W.T. & Hagan, P. (1997) A simple method for counting cells in tissue sections. Parasitology Today 13, 405.CrossRefGoogle ScholarPubMed
Lawrence, C.E., Paterson, J.C.M., Wei, X.-Q., Liew, F.Y., Garside, P. & Kennedy, M.W. (2000) Nitric oxide mediates intestinal pathology but not immune expulsion during Trichinella spiralis infection in mice. Journal of Immunology 164, 42294234.CrossRefGoogle Scholar
Loukas, A., Constant, S.L. & Bethony, J.M. (2005) Immunobiology of hookworm infection. FEMS Immunology and Medical Microbiology 43, 115124.CrossRefGoogle ScholarPubMed
Meddis, R. (1984) Statistics using ranks. A unified approach. New York, Basil Blackwell.Google Scholar
Mendez, S., Valenzuela, J.G., Wu, W. & Hotez, P.J. (2005a) Host cytokine production, lymphoproliferation, and antibody responses during the course of Ancylostoma ceylanicum infection in the golden Syrian hamster. Infection and Immunity 73, 34023407.CrossRefGoogle ScholarPubMed
Mendez, S., Zhan, B., Goud, G., Ghosh, K., Dobardzic, A., Wu, W., Liu, S., Deumic, V., Dobardzic, R., Liu, Y., Bethony, J. & Hotez, P.J. (2005b) Effect of combining the larval antigens Ancylostoma secreted protein 2 (ASP-2) and metalloprotease 1 (MTP-1) in protecting hamsters against hookworm infection and disease caused by Ancylostoma ceylanicum. Vaccine 23, 31233130.CrossRefGoogle ScholarPubMed
Ogilvie, B.M., Bartlett, A., Godfrey, R.C., Turton, J.A., Worms, M.J. & Yeates, R.A. (1978) Antibody responses in self-infections with Necator americanus. Transactions of the Royal Society of Tropical Medicine and Hygiene 72, 6671.CrossRefGoogle ScholarPubMed
Quinnell, R.J., Pritchard, D.I., Raiko, A., Brown, A.P. & Shaw, M. (2004) Immune responses in human Necatoriasis: association between interleukin-5 responses and resistance to reinfection. The Journal of Infectious Diseases 190, 430438.CrossRefGoogle ScholarPubMed
Ray, D.K. & Bhopale, K.K. (1972) Complete development of Ancylostoma ceylanicum (Looss, 1911) in golden hamsters, Mesocricetus auratus. Experientia 28, 359.CrossRefGoogle ScholarPubMed
Ray, D.K., Bhopale, K.K. & Shrivastava, V.B. (1972) Migration and growth of Ancylostoma ceylanicum in golden hamsters. Journal of Helminthology 46, 357362.CrossRefGoogle ScholarPubMed
Schopf, L.R., Hoffman, K.F., Cheever, A.W., Urban, J.E. Jr & Wynn, T.A. (2002) IL-10 is critical for host resistance and survival during gastrointestinal helminth infection. Journal of Immunology 168, 23832392.CrossRefGoogle ScholarPubMed
Wahid, F.N., Behnke, J.M. & Conway, D.J. (1989) Factors affecting the efficacy of ivermectin against Heligmosomoides polygyrus (Nematospiroides dubius) in mice. Veterinary Parasitology 32, 325340.CrossRefGoogle ScholarPubMed
Wright, V. & Bickle, Q. (2005) Immune responses following experimental human hookworm infection. Clinical and Experimental Immunology 142, 398403.CrossRefGoogle ScholarPubMed