Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-13T02:33:18.332Z Has data issue: false hasContentIssue false
  • English
  • Français

The effect of the hookworm Ancylostoma ceylanicum on the mucosal architecture of the small intestine in hamsters

Published online by Cambridge University Press:  12 April 2024

L.M.M. Alkazmi ,
M.S. Dehlawi  and
J.M. Behnke
L.M.M. Alkazmi
Affiliation:
School of Biology, University of Nottingham, University Park, Nottingham, NG7 2RD, UK Biology Department, Faculty of Applied Sciences, Umm Al-Qura University, Makkah, Saudi Arabia
M.S. Dehlawi
Affiliation:
School of Biology, University of Nottingham, University Park, Nottingham, NG7 2RD, UK Department of Biological Sciences, King Abdul Aziz University, Jeddah, Saudi Arabia
J.M. Behnke*
Affiliation:
School of Biology, University of Nottingham, University Park, Nottingham, NG7 2RD, UK
*
*Corresponding author: Fax: +44 (0) 115 951 3206, Email: jerzy.behnke@nottingham.ac.uk
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Hookworms are known to cause marked changes to the intestinal mucosa, especially in relation to erosion of the villi. However, since the development of enteropathy has not been examined thoroughly through quantitative experiments on infected animals, the results of experiments conducted in hamsters infected with Ancylostoma ceylanicum are reported. Changes to intestinal architecture were first apparent between 12 and 14 days after infection, and then increased in intensity for 3–4 weeks, persisting for as long as worms were present (>63 days). Following infection, the height of villi declined from a mean of 1002 μm in naïve controls to less than 200 μm and as low as 18 μm in one case. The depth of the crypts of Lieberkuhn increased from a baseline value of 166 μm in naïve controls to in excess of 600 μm within 6 weeks of infection. Mitotic figures had a baseline value of 5.5 per villus-crypt unit, and this rose to in excess of 25 in some experiments. Changes were dependent on the intensity of the parasite burden on day 20, but by 30 days after infection changes in all three values were maximal and density-dependent relationships were no longer clearly apparent. Villus height and crypt depth returned to near normal values within a week of the removal of worms, although group means for both remained different from naïve controls for at least 3 weeks after treatment. Cellular division, as reflected in numbers of mitotic figures, stayed elevated for over 5 weeks after removal of worms. The results suggest that enteropathy in hookworm infections stems from a combination of intestinal immune responses and from the grazing activities of the adult worms on the mucosal surface, but is not sufficient per se for expulsion of this parasite.

Type
Research Article
Information
Journal of Helminthology , Volume 80 , Issue 4 , December 2006 , pp. 397 - 407
Copyright
Copyright © Cambridge University Press 2006

References

Alkazmi, L.M.M. (2004) Mucosal immunity to the hookworm Ancylostoma ceylanicum, PhD thesis, University of Nottingham.Google Scholar
Aziz, M.A. & Siddiqui, A.R. (1968) Morphological and absorption studies of small intestine in hookworm disease (ancylostomiasis) in West Pakistan. Gastroenterology 55, 242–250.CrossRefGoogle ScholarPubMed
Behnke, J.M. (1990) Laboratory animal models. 105–128 in 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. 51–91 in Gilles, H.M. & Ball, P.A.J. (Eds) Human parasitic diseases, Volume 4, hookworm infections. Amsterdam, Elsevier.Google Scholar
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
Bonne, C. (1942) Invasion of the wall of the human intestine by ancylostomes. American Journal of Medicine 22, 507–509.Google Scholar
Bungiro, R.D., Greene, J., Kruglov, E. Jr & Capello, M. (2001) Mitigation of hookworm disease by immunization with soluble extracts of Ancylostoma ceylanicum. Journal of Infectious Diseases 183, 1380–1387.CrossRefGoogle ScholarPubMed
Burman, N.N., Sehgal, A.K., Chakravarti, R.N., Sodhi, J.S. & Chhuttani, P.N. (1970) Morphological and absorption studies of small intestine in hookworm infestation (ankylostomiasis). Indian Journal of Medical Research 58, 317–325.Google ScholarPubMed
Carroll, S.M., Grove, D.I. & Heenan, P.J. (1986) Kinetics of cells in the intestinal mucosa of mice following oral infection with Ancylostoma ceylancium. International Archives of Allergy and Applied Immunology 79, 26–32.CrossRefGoogle Scholar
Carroll, S.M., Robertson, T.A., Papadimitriou, J.M. & Grove, D.I. (1984) Transmission electron microscopical studies of the site of attachment of Ancylostoma ceylanicum to the small bowel mucosa of the dog. Journal of Helminthology 58, 313–320.CrossRefGoogle Scholar
Carroll, S.M., Robertson, T.A., Papadimitriou, J.M. & Grove, D.I. (1985) Scanning electron microscopy of Ancylostoma ceylanicum and its site of attachment to the small intestinal mucosa of dogs. Zeitschrift für Parasitenkunde 71, 79–85.CrossRefGoogle Scholar
Castro, G.A. (1990) Intestinal pathology. pp. 283–316 in Behnke, J.M. (Ed.) Parasites: immunity and pathology. London, Taylor & Francis.Google Scholar
Cheng-Li, W., Hsiao-Su, H., Hsing-Chen, W. & Yu-Fang, P. (1966) The blood sucking activities of hookworms with special reference to the volume of blood withdrawn by Ancylostoma caninum. Chinese Medical Journal 85, 11–20.Google Scholar
Cliffe, L.J., Humphreys, N.E., Lane, T.E., Potten, C.S., Booth, C. & Grencis, R.K. (2005) Accelerated intestinal epithelial cell turnover: a new mechanism of parasite expulsion. Science 308, 1463–1465.CrossRefGoogle ScholarPubMed
Coop, R.L., Angus, K.W. & Sykes, A.R. (1979) Chronic infection with Trichostrongylus vitrinus in sheep. Pathological changes in the small intestine. Research in Veterinary Science 26, 363–371.CrossRefGoogle ScholarPubMed
Cooper, E.S., Whyte-Alleng, C.A., Finzi-Smith, J.S. & MacDonald, T.T. (1992) Intestinal nematode infections in children: the pathophysiological price paid. Parasitology 104, S91–S103.CrossRefGoogle ScholarPubMed
Elliott, J.M. (1977) Some methods for the statistical analysis of samples of benthic invertebrates. Freshwater Biological Association, Cumbria, UK.Google Scholar
Ferguson, A. & Jarrett, E.E.E. (1975) Hypersensitivity reaction of the small intestine: thymus independent reactions of experimental –Partial villous atrophy–. Gut 16, 114–117.CrossRefGoogle Scholar
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
Garside, P., Behnke, J.M. & Rose, R.A. (1990) Acquired immunity to Ancylostoma ceylanicum in hamsters. Parasite Immunology 12, 247–258.CrossRefGoogle ScholarPubMed
Garside, P., Grencis, R.K. & Mowat, A.M. (1992) T lymphocyte dependent enteropathy in murine Trichinella spiralis infection. Parasite Immunology 14, 217–225.CrossRefGoogle ScholarPubMed
Garside, P., Kennedy, M.W., Wakelin, D. & Lawrence, C.E. (2000) Immunopathology of intestinal helminth infection. Parasite Immunology 22, 605–612.CrossRefGoogle ScholarPubMed
Graham, S., Courtois, P., Malaisse, W.J., Rozing, J., Scott, F.W. & Mowat, A.M. (2004) Enteropathy precedes type 1 diabetes in the BB rat. Gut 53, 1437–1444.CrossRefGoogle ScholarPubMed
Ido, A., Numata, M., Kodama, M. & Tsubouchi, H. (2005) Mucosal repair and growth factors: recombinant human hepatocyte growth factor as an innovative therapy for inflammatory bowel disease. Journal of Gastroenterology 40, 925–931.CrossRefGoogle ScholarPubMed
Kalkofen, U.P. (1970) Attachment and feeding behaviour of Ancylostoma caninum. Zeitschrift für Parasitenkunde 33, 339–354.CrossRefGoogle ScholarPubMed
Kalkofen, U.P. (1974) Intestinal trauma resulting from feeding activities of Ancylostoma caninum. American Journal of Tropical Medicine and Hygiene 23, 1046–1053.CrossRefGoogle ScholarPubMed
Kelly, P., Menzies, I., Crane, R., Zulu, I., Nickols, C., Feakins, R., Mwansa, J., Mudenda, V., Katubulushi, M., Greenwald, S. & Farthing, M. (2004) Responses of small intestinal architecture and function over time to environmental factors in a tropical population. American Journal of Tropical Medicine and Hygiene 70, 412–419.CrossRefGoogle Scholar
Lawrence, C.E., Paterson, J.C.M., Higgins, L.M., MacDonald, T.T., Kennedy, M.W. & Garside, P. (1998) IL-4 regulated enteropathy in an intestinal nematode infection. European Journal of Immunology 28, 2672–2684.3.0.CO;2-F>CrossRefGoogle Scholar
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, 4229–4234.CrossRefGoogle Scholar
Loukas, A., Constant, S.L. & Bethony, J.M. (2005) Immunobiology of hookworm infection. FEMS Immunology and Medical Microbiology 43, 115–124.CrossRefGoogle ScholarPubMed
MacDonald, T.T. & Monteleone, G. (2005) Immunity, inflammation, and allergy in the gut. Science 307, 1920–1925.CrossRefGoogle ScholarPubMed
MacDonald, T.T., Bajaj-Elliott, M. & Pender, S.L.F. (1999) T cells orchestrate intestinal mucosal shape and integrity. Immunology Today 20, 505–510.CrossRefGoogle ScholarPubMed
MacDonald, T.T., Monteleone, G. & Pender, L.F. (2000) Recent developments in the immunology of inflammatory bowel disease. Scandinavian Journal of Immunology 51, 2–9.CrossRefGoogle ScholarPubMed
McDermott, J.R., Humphreys, N.E., Forman, S.P., Donaldson, D.D. & Grencis, R.K. (2005) Intraepithelial NK cell-derived IL-13 induces intestinal pathology associated with nematode infection. Journal of Immunology 175, 3207–3213.CrossRefGoogle ScholarPubMed
Menon, S. & Bhopale, M.K. (1985) Ancylostoma ceylanicum (Looss, 1911) in golden hamsters ( Mesocricetus auratus ): pathogenicity and humoral immune response to a primary infection. Journal of Helminthology 59, 143–146.CrossRefGoogle ScholarPubMed
Migasena, S., Gilles, H.M. & Maegraith, B.G. (1972) Studies in Ancylostoma caninum infection in dogs II. Anatomical changes in the gastrointestinal tract. Annals of Tropical Medicine and Parasitology 66, 203–207.CrossRefGoogle ScholarPubMed
Miller, T.A. (1979) Hookworm infection in man. Advances in Parasitology 17, 315–384.CrossRefGoogle ScholarPubMed
Pritchard, D.I., Quinnell, R.J., Moustafa, M., McKean, P.G., Slater, A.F.G., Raiko, A., Dale, D.D.S. & Keymer, A.E. (1991) Hookworm ( Necator americanus ) infection and storage iron depletion. Transactions of the Royal Society of Tropical Medicine and Hygiene 85, 235–238.CrossRefGoogle ScholarPubMed
Prociv, P. (1997) Pathogenesis of human hookworm infection: insight from a (new) zoonosis. Chemical Immunology 66, 62–98.Google ScholarPubMed
Radtke, F. & Clevers, H. (2005) Self-renewal and cancer of the gut: two sides of a coin. Science 307, 1904–1909.CrossRefGoogle ScholarPubMed
Rajasekariah, G.R., Dhage, K.R., Deb, B.N. & Bose, S. (1985) Necator americanus and Ancylostoma ceylanicum: development of protocols for dual infection in hamsters. Acta Tropica 42, 45–54.Google ScholarPubMed
Ray, D.K., Bhopale, K.K. & Shrivastava, V.B. (1972) Migration and growth of Ancylostoma ceylanicum in golden hamsters. Journal of Helminthology 46, 357–362.CrossRefGoogle ScholarPubMed
Roche, M. & Layrisse, M. (1966) The nature and causes of hookworm anemia. American Journal of Tropical Medicine and Hygiene 15, 1031–1100.CrossRefGoogle ScholarPubMed
Sheehy, T.W., Meroney, W.H., Cox, R.S. Jr & Soler, J.E. (1962) Hookworm disease and malabsorption. Gastroenterology 42, 148–156.CrossRefGoogle ScholarPubMed
Symons, L.E.A. (1965) Kinetics of the epithelial cells and morphology of the villi and crypts in the jejunum of the rat infected by the nematode Nippostrongylus brasiliensis. Gastroenterology 49, 158–168.CrossRefGoogle ScholarPubMed
Symons, L.E.A. (1976) Scanning electron microscopy of the jejunum of the rat infected by the nematode Nippostrongylus brasiliensis. International Journal for Parasitology 6, 107–111.CrossRefGoogle ScholarPubMed
Verma, S., Sehgal, A.H., Chakravarti, R.N. & Chuttani, P.N. (1968) Intestinal villi in the dog and effect of Ancylostoma caninum infection. Journal of Pathology and Bacteriology 95, 568–571.CrossRefGoogle Scholar
Wells, H.S. (1931) Observations on the blood sucking activities of the hookworm Ancylostoma caninum. Journal of Parasitology 17, 167–182.CrossRefGoogle Scholar