Hostname: page-component-78c5997874-lj6df Total loading time: 0 Render date: 2024-11-17T13:12:44.723Z Has data issue: false hasContentIssue false
  • English
  • Français

The mucosal response of hamsters exposed to weekly repeated infections with the hookworm Ancylostoma ceylanicum

Published online by Cambridge University Press:  15 August 2012

L.M.M. Alkazmi  and
J.M. Behnke
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 3251, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

An experiment was carried out to assess mucosal changes in hamsters exposed to weekly repeated low-intensity infections with the hookworm Ancylostoma ceylanicum. The experiment included control groups of naïve, uninfected hamsters and groups that received a single-pulse primary infection. Changes in the intestinal architecture and in the density of inflammatory cells in the mucosa, including mast cells, goblet cells, Paneth cells and eosinophils were examined in relation to changes in hookworm burdens. As in the single-pulse primary infection, hamsters exposed to repeated infections responded with marked changes in the intestinal architecture and in mucosal populations of inflammatory cells. However, there were distinct differences in the kinetics of the responses to these two types of infection (primary single-pulse and repeated). The reduction in villous height and the increase in crypt depth in animals exposed to repeated infections were both initially slower but eventually equalled and exceeded the responses in hamsters given a chronic primary infection, despite the presence of fewer adult worms in the former. Similarly, changes in the mitotic figures of epithelial cells in the mucosa and the mast cell response were both initially slower and less intense in repeatedly infected hamsters, but eventually exceeded the response to primary infection. Furthermore, the eosinophil response was found to be initially greater in repeated infections and overall more persistent. In contrast, both goblet and Paneth cell responses were less marked in repeatedly infected animals compared to those carrying a primary infection. These results are discussed in the context of host protective resistance to infection with A. ceylanicum.

Type
Research Papers
Information
Journal of Helminthology , Volume 87 , Issue 3 , September 2013 , pp. 309 - 317
Copyright
Copyright © Cambridge University Press 2012 

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.A (2004) Mucosal immunity to the hookworm Ancylostoma ceylanicum Unpublished PhD thesis, University of Nottingham, UK.Google Scholar
Alkazmi, L. & Behnke, J.M. (2010) The mucosal response to secondary infection with Ancylostoma ceylanicum in hamsters immunized by abbreviated primary infection. Parasite Immunology 32, 47–56.CrossRefGoogle ScholarPubMed
Alkazmi, L. & Behnke, J.M. (2011) The mucosal response of hamsters to a low-intensity superimposed secondary infection with the hookworm Ancylostoma ceylanicum. Journal of Helminthology 85, 56–65.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, 397–407.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, 33–44.CrossRefGoogle ScholarPubMed
Bancroft, A.J., Else, K.J., Humphreys, N.E. & Grencis, R.K. (2001) The effect of challenge and trickle Trichuris muris infections on the polarisation of the immune response. International Journal for Parasitology 31, 1627–1637.CrossRefGoogle ScholarPubMed
Barger, I.A., Le Jambre, L.F., Georgi, J.R. & Davies, H.I. (1985) Regulation of Haemonchus contortus populations in sheep exposed to continuous infection. International Journal for Parasitology 15, 529–533.CrossRefGoogle ScholarPubMed
Barnard, C., Gilbert, F. & McGregor, P. (2007) Asking questions in biology. 3rd edn.London, Prentice Hall.Google Scholar
Beaver, P.C. (1953) Persistence of hookworm larvae in soil. American Journal of Tropical Medicine and Hygiene 2, 102–108.CrossRefGoogle ScholarPubMed
Behm, C.A. & Ovington, K.S. (2000) The role of eosinophils in parasitic helminth infections: insights from genetically modified mice. Parasitology Today 16, 202–209.CrossRefGoogle ScholarPubMed
Behnke, J.M. (1987) Do hookworms elicit protective immunity in man? Parasitology Today 3, 200–206.CrossRefGoogle ScholarPubMed
Behnke, J.M. (1990) Laboratory animal models. pp. 105–128in Schad, G.A. & Warren, K.S. (Eds) Hookworm disease. Current status and new directions. London, Taylor & Francis.Google Scholar
Behnke, J.M. & Wakelin, D. (1973) The survival of Trichuris muris in wild populations of its natural hosts. Parasitology 67, 157–164.CrossRefGoogle ScholarPubMed
Behnke, J.M., Guest, J. & Rose, R. (1997) Expression of acquired immunity to the hookworm Ancylostoma ceylanicum in hamsters. Parasite Immunology 19, 309–318.CrossRefGoogle Scholar
Behnke, J.M., Lowe, A., Clifford, S. & Wakelin, D. (2003) Cellular and serological responses in resistant and susceptible mice exposed to repeated infection with Heligmosomoides polygyrus bakeri. Parasite Immunology 25, 333–340.CrossRefGoogle ScholarPubMed
Bethony, J.M., Cole, R.N., Guo, X., Kamhawi, S., Lightowlers, M.W., Loukas, A., Petri, W., Reed, S., Valenzuela, J.G. & Hotez, P.J. (2011) Vaccines to combat the neglected tropical diseases. Immunological Reviews 239, 237–270.CrossRefGoogle ScholarPubMed
Brailsford, T.J. & Behnke, J.M. (1992a) The dynamics of trickle infections with Heligmosomoides polygyrus in syngeneic strains of mice. International Journal for Parasitology 22, 351–359.CrossRefGoogle ScholarPubMed
Brailsford, T.J. & Behnke, J.M. (1992b) The dynamics of trickle infection with Ancylostoma ceylanicum in inbred hamsters. Parasitology 105, 247–253.CrossRefGoogle ScholarPubMed
Cadman, E.T. & Lawrence, R.A. (2009) Granulocytes: effector cells or immunomodulators in the immune response to helminth infection? Parasite Immunology 31, 1–19.Google Scholar
Chiejina, S.N., Behnke, J.M., Musongong, G.A., Nnadia, P.A. & Ngongeha, L.A. (2010) Resistance and resilience of West African Dwarf goats of the Nigerian savanna zone exposed to experimental escalating primary and challenge infections with Haemonchus contortus. Veterinary Parasitology 171, 81–90.CrossRefGoogle ScholarPubMed
Courtney, C.H., Parker, C.F., McClure, K.E. & Herd, R.P. (1983) Population dynamics of Haemonchus contortus and Trichostrongylus spp. in sheep. International Journal for Parasitology 13, 557–560.CrossRefGoogle ScholarPubMed
Desakorn, V., Suntharasamai, P., Pukrittayakamee, S., Migasena, S. & Bunnag, D. (1987) Adherence of human eosinophils to infective filariform larvae of Necator americanus in vitro. Southeast Asian Journal of Tropical Medicine and Public Health 18, 66–72.Google ScholarPubMed
Donald, A.D. & Waller, P.J. (1982) Problems in the control of helminthiasis in sheep. pp. 157–186in Symons, L.E.A., Domald, A.D. & Dineen, J.K. (Eds) Biology and control of endoparasites. Sydney, Australia, Academic Press.Google Scholar
Elphick, D.A. & Mahida, Y.R. (2005) Paneth cells: their role in innate immunity and inflammatory disease. Gut 54, 1802–1809.CrossRefGoogle ScholarPubMed
Else, K.J. & Finkelman, F.D. (1998) Intestinal nematode parasites, cytokines and effector mechanisms. International Journal for Parasitology 28, 1145–1158.CrossRefGoogle ScholarPubMed
Fujiwara, R.T., Cancado, G.G.L., Freitas, P.A., Santiago, H.C., Massara, C.L., Santos Carvalho, O., Correa-Oliveira, R., Geiger, S.M. & Bethony, J. (2009) Necator americanus infection: a possible cause of altered dendritic cell differentiation and eosinophil profile in chronically infected individuals. PLoS Neglected Tropical Diseases 3, e399.CrossRefGoogle ScholarPubMed
Garside, P. & Behnke, J.M. (1989) Ancylostoma ceylanicum in the hamster. Observations on the host–parasite relationship during primary infection. Parasitology 98, 283–289.CrossRefGoogle ScholarPubMed
Hominick, W.M., Dean, C.G. & Schad, G.A. (1987) Population biology of hookworms in West Bengal: analysis of numbers of infective larvae recovered from damp pads applied to the soil surface at defaecation sites. Transactions of the Royal Society of Tropical Medicine and Hygiene 81, 978–986.CrossRefGoogle Scholar
Hotez, P.J., Hawdon, J.M., Capello, M., Jones, B.F. & Pritchard, D.I. (1995) Molecular pathobiology of hookworm infection. Infectious Agents and Disease 4, 71–75.Google ScholarPubMed
Hsieh, G.C., Loukas, A., Wahl, A.M., Bhatia, M., Wang, Y., Williamson, A.L., Kehn, K.W., Maruyama, H., Hotez, P.J., Leitenberg, D., Bethony, J. & Constant, S. (2004) A secreted protein from the human hookworm Necator americanus binds selectively to NK cells and induces IFN-γ production. Journal of Immunology 173, 2699–2704.CrossRefGoogle ScholarPubMed
Jackson, F., Angus, K.W. & Coop, R.L. (1983) Development of morphological changes in the small intestine of lambs continuously infected with Trichostrongylus vitrinus. Research in Veterinary Science 34, 301–304.CrossRefGoogle ScholarPubMed
Jenkins, D.C. & Phillipson, R.F. (1971) The kinetics of repeated low-level infections of Nippostrongylus brasiliensis in the laboratory rat. Parasitology 62, 457–465.CrossRefGoogle ScholarPubMed
Kazura, J.W. & Aikawa, M. (1980) Host defense mechanisms against Trichinella spiralis infection in the mouse: eosinophil-mediated destruction of newborn larvae in vitro. Journal of Immunology 124, 355–361.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
Klion, A.D. & Nutman, T.B. (2004) The role of eosinophils in host defense against helminth parasites. Journal of Allergy and Clinical Immunology 113, 30–37.CrossRefGoogle ScholarPubMed
Loukas, A., Constant, S.L. & Bethony, J.M. (2005) Immunobiology of hookworm infection. FEMS Immunology and Medical Microbiology 43, 115–124.CrossRefGoogle ScholarPubMed
Meeusen, E.N.T. & Balic, A. (2000) Do eosinophils have a role in the killing of helminth parasites? Parasitology Today 16, 95–101.CrossRefGoogle ScholarPubMed
Michel, J.F. (1970) The regulation of population of Ostertagia ostertagi in calves. Parasitology 61, 435–447.CrossRefGoogle ScholarPubMed
Nair, M.G., Guild, K.J. & Artis, D. (2006) Novel effector molecules in the type 2 inflammation: lessons drawn from helminth infection and allergy. Journal of Immunology 177, 1393–1399.CrossRefGoogle ScholarPubMed
Teixeira-Carvalho, A., Fujiwara, R.T., Stemmy, E.J., Olive, D., Damsker, J.M., Loukas, A., Corrêa-Oliveira, R., Constant, S.L. & Bethony, J.M. (2008) Binding of excreted and/or secreted products of adult hookworms to human NK cells in Necator americanus-infected individuals from Brazil. Infection and Immunity 76, 5810–5816.CrossRefGoogle ScholarPubMed
Udonsi, J.K., Nwosu, A.B.C. & Anya, A.O. (1980) Necator americanus: population structure, distribution, and fluctuations in population densities of infective larvae in contaminated farmlands. Zeitschrift für Parasitenkunde 63, 251–259.CrossRefGoogle ScholarPubMed
Wakelin, D. (1973) The stimulation of immunity to Trichuris muris in mice exposed to low-level infections. Parasitology 66, 181–189.CrossRefGoogle ScholarPubMed