SciELO - Scientific Electronic Library Online

vol.75 issue2 author indexsubject indexarticles search
Home Pagealphabetic serial listing  

Services on Demand



Related links

  • On index processCited by Google
  • On index processSimilars in Google


Onderstepoort Journal of Veterinary Research

On-line version ISSN 2219-0635
Print version ISSN 0030-2465

Onderstepoort j. vet. res. vol.75 n.2 Pretoria  2008




Bovine intestinal cellular responses following primary and challenge infections with Calicophoron microbothrium metacercariae



M. MavenyengwaI; S. MukaratirwaIII; M. ObwoloI; J. MonradII

IFaculty of Veterinary Science, Department of Paraclinical Veterinary Studies, University of Zimbabwe, Harare
IIDanish Centre for Experimental Parasitology, Frederiksberg, Copenhagen, Denmark
IIISchool of Biological and Conservation Sciences, University of KwaZulu-Natal, Westville Campus, Durban 4001




This study was carried out to establish whether cattle can develop resistance to re-infection by Calicophoron microbothrium by assessing the response of intestinal mucosal globule leukocytes, eosinophils, mast cells and basophils, and the establishment of the parasite in the host. A total of 24 1-year-old Tuli steers were randomly divided into four groups of six animals each and infected with C. microbothrium metacercariae. On the first day of the study, animals in Groups I and II were immunized with 5 000 metacercariae and then challenged with 15 000 metacercariae on Day 150 post-immunization. Animals in Group III were immunized with 15 000 metacercariae at the same time that Groups I and II animals were challenged to act as a positive control group. Animals in Group IV were left uninfected and acted as a negative control group. Three animals from each group were slaughtered on Day 28 post-challenge and the remainder were slaughtered on Day 42 post-challenge. The established amphistomes were recovered and histopathological and cytological examinations were done on the jejunum, duodenum, abomasum and the rumen. The establishment rates of the challenge infection in the immunized and challenged groups were lower and ranged from 0 to 0.2 % as compared to 6 %> from naive animals infected as positive controls. Animals immunized and then challenged with C. microbothrium had significantly higher eosinophil, mast cell and globule leukocytes counts in the intestinal mucosa (P < 0.05) as compared to those of the control group. The study indicates that cattle can develop resistance to C. microbothrium re-infection and that eosinophils and mast cells may be important cells in the rejection of the parasite.

Keywords: Basophil, bovines, Calicophoron microbothrium, challenge, eosinophil, globule leukocyte, mast cell, metacercariae, resistance



“Full text available only in PDF format”




ANONYMOUS 1986. Manual of veterinary parasitological laboratory techniques. London: Her Majesty's Stationery Office.         [ Links ]

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.         [ Links ]

BORAY, J.C. 1969. Studies on intestinal paramphistomosis in sheep due to Paramphistomum ichikawai Fukui, 1922. Veterinary Medical Review, 4:290-308.         [ Links ]

BORAY, J.C. 1985. Flukes of domestic animals: Paramphistomata, in World animal science, disciplinary approach. Vol. B2. Parasites, pests and predators, edited by S.M. Gafaar, W.E. Howard & R.E Marsh. Amsterdam: Elsevier.         [ Links ]

BUTLER, R.W. & YEOMAN, G.H. 1962. Acute intestinal paramphistomiasis in Zebu cattle in Tanganyika. Veterinary Record, 74:227-231.         [ Links ]

BUTTERWORTH, A.E. 1984. Cell-mediated damage to helminths. Advances in Parasitology, 23:143-235.         [ Links ]

CHAUDHRI, S. 2000. Reduced responsivenesscof oxyclozanide and tetramisole hydrochloride combinations to gastrointestinal parasites of sheep. Indian Journal of Animal Science, 70: 396-398.         [ Links ]

CHERUIYOT, H.K. & WAMAE, L.W. 1988. Incidence of bovine paramphistomiasis in Kenya. Bulletin of Animal Health and Production in Africa, 36:55-57.         [ Links ]

CHHABRA, R.G., GILL, B.S. & DUTT, S.C. 1978. Paramphistomiasis of sheep and goats in the Punjab State and its treatment. Indian Journal of Parasitology, 2:43-45.         [ Links ]

CHRISTENSEN, C.M. 1991. Studies of the immune response in cattle infected with normal or inhibited larvae of Ostertagia ostertagi (Trichostrongylidae). Ph.D. thesis. The Royal Veterinary and Agricultural University.         [ Links ]

CHRISTOPHER, J. 1974. Zanil (oxyclozanide) in the treatment of amphistomiasis in sheep. Indian Journal of Animal Research, 8:79-80.         [ Links ]

DEORANI, S.V.P. & KATIYAR, R.D. 1967. Studies on the pathogenicity due to immature amphistomes among sheep and goats. Indian Veterinary Journal, 44:199-205.         [ Links ]

DOUCH, P.G.C. & MORUM, P.E. 1993. The effect of age on the response of Romney sheep to gastrointestinal nematodes during grazing. International Journal for Parasitology, 23: 651-655.         [ Links ]

DUTT, S.C. 1980. Paramphistomes and paramphistomiasis in domestic ruminants in India, edited by A. Singh. Ludhiana: Punjab Agricultural University Press.         [ Links ]

EDUARDO, S.L. 1983. The taxonomy of the family Paramphistomidae Fischoeder, 1901 with special reference to the morphology of the species occurring in ruminants. III. Revision of the genus Calicophoron Nasmark, 1937. Systematic Parasitology, 5:25-79.         [ Links ]

FALCONE, F.H., PRITCHARD, D.I. & GIBBS, B.F. 2001. Do basophils play a role in immunity against parasites? Trends in Parasitology, 17:126-126.         [ Links ]

GRENCIS, R.K. 1997. Enteric helminth infection: Immunopathology and resistance during intestinal nematode infection. Chemical Immunology, 66:41-61.         [ Links ]

GUPTA, N.K. 1993. Amphistomes, systematics and biology. New Dehli: Oxford and IBH Publishing Co.         [ Links ]

HORAK, I.G. & CLARK, R. 1963. Studies on Paramphistomiasis. V. The pathological physiology of the acute disease in sheep. Journal of the South African Veterinary Medical Association, 30:145-160.         [ Links ]

HORAK, I.G. 1965. Studies on paramphistomiasis. VII. The immunization of sheep, goats and cattle. Preliminary Report. Journal of the South African Veterinary Medical Association, 36:361-363.         [ Links ]

HORAK, I.G. 1966. Studies on paramphistomiasis. VIII. The pathogenesis and symptoms of the disease in sheep. Journal of the South African Veterinary Medical Association, 37: 428-430.         [ Links ]

HORAK, I.G. 1967. Host-parasite relationships of Paramphistomum microbothrium Fischoeder, 1901, in experimentally infested ruminants, with particular reference to sheep. Onder-stepoort Journal of Veterinary Research, 34:451-540.         [ Links ]

HORAK, I.G. 1971. Paramphistomiasis of domestic ruminants. Advances in Parasitology, 9:33-72.         [ Links ]

HUNTLEY, J.F., NEWLANDS, G. & MILLER, H.R.P. 1984. The isolation and characterization of globule leukocytes: their derivation from the mucosal mast cells in parasitised sheep. Parasite Immunology, 6:371-390.         [ Links ]

HUNTLEY, J.F. 1992. Mast cells and basophils: A review of their heterogeneity and function. Journal of Comparative Pathology, 107:349-372.         [ Links ]

HUNTLEY, J.F., PATTERSON, M., MACKELLAR, A., JACKSON, F., STEVENSON, L.M. & COOP, R.L. 1995. A comparison of mast cell and eosinophil responses of sheep and goats to gastrointestinal nematode infections. Research in Veterinary Science, 58:5-10.         [ Links ]

JAIN, N.C. 1993. Essentials of veterinary haematology. Philadelphia: Lea & Febiger.         [ Links ]

JONES, D.G. 1993. The eosinophil. Journal of Comparative Pathology, 108:317-335.         [ Links ]

LEE, T.G.D., SWIETER, M. & BEFUS, A.D. 1986. Mast cell response to helminth infection. Parasitology Today, 2:186-191.         [ Links ]

MAVENYENGWA, M. 2004. Pathophysiology of Calicophoron microbothrium in experimentally infected cattle and the effect of a challenge infection. Ph.D. thesis. University of Zimbabwe.         [ Links ]

MCLAREN, D.J., MCKEAN, J.R., OLSSON, I., VENGE, P. & KAY, A.B. 1981. Morphological studies on the killing of schistosomula of Schistosoma mansoni by human eosinophil and cationic proteins in vitro. Parasite Immunology, 3:359-373.         [ Links ]

MILLER, H.R.P. & JARRETT, W.F.H. 1971. Immune reactions in mucous membranes I. Intestinal mast cell response during helminth expulsion in the rat. Immunology, 20:277-287.         [ Links ]

MILLER, H.R.P. 1984. The protective mucosal response against gastrointestinal nematodes in ruminants and laboratory animals. Veterinary Immunology and Immunopathology, 6:167-259.         [ Links ]

MUKHERJEE, R.P. & DEORANI, S.V.P. 1962. Massive infection of a sheep with amphistomes and the histopathology of the parasitised rumen. Indian Veterinary Journal, 39:668-670.         [ Links ]

OVINGTON, K.S. & BEHM, C.A. 1997. The enigmatic eosinophil: Investigation of the biological role of eosinophils in parasitic helminth infection. Memórias do Instituto Oswaldo Cruz, 92: 93-104.         [ Links ]

PANDA, B.K. & MISRA, S.C. 1980. Observations on the aetiology, clinical pathology and chemotherapy of immature amphistomiasis in buffalo calves. Indian Journal of Animal Health, 19:131-135.         [ Links ]

PFEFFER, A., DOUCH, P.G.C., SHAW, R.J., GATEHOUSE, T.K., RABEL, B., GREEN, R.S., SHIRER, C.L., JONAS, W.E. & BISSET, S. 1996. Sequential cellular and humoral responses in the abomasal mucosa and blood of Romney sheep dosed with Trichostrongylus axei. International Journal for Parasitology, 26:765-773.         [ Links ]

PILLAI, U.N. & ALIKUTTY, K.M. 1995. Clinico-hematological observation in bovine amphistomiasis. Indian Journal of Veterinary Medicine, 15:38-39.         [ Links ]

RAHMAN, A., JAGANNATH, S. & SOUZ, P.D. 1985. Anthelmintic activity of niclosamide in sheep and goats. Livestock Advisor, 10:47-49.         [ Links ]

RAINBIRD, M.A., MACMILLAN, D. & MEEUSEN, E.N.T. 1998. Eosinophil mediated killing of Haemonchus contortus larvae: effect of eosinophil activation and role of antibody, compliment and interleukin-5. Parasite Immunology, 20:93-103.         [ Links ]

ROLFE, P.F. & BORAY, J.C. 1987. Chemotherapy of paramphistomosis in cattle. Australian Veterinary Journal, 64:328.         [ Links ]

ROLFE, F., BORAY, J.C., NICHOLS, P. & COLLINS, G.H. 1991. Epidemiology of paramphistomosis in cattle. International Journal for Parasitology, 21:813-819.         [ Links ]

ROLFE, P.F. & BORAY, J.C. 1993. Comparative efficacy of moxidectin, an ivermectin/clorsulon combination and closantel against immature paramphistomes in cattle. Australian Veterinary Journal, 70:265-266.         [ Links ]

ROLFE, F., BORAY, J.C., COLLINS, G.H. 1994. Pathology of infection with Paramhistomum ichikawai in sheep. International Journal for Parasitology, 24:995-1004.         [ Links ]

ROTHWELL, T.L.W. & DINEEN, J.K. 1972. Cellular reactions in guinea-pigs following primary and challenge infection with Trichostrongylus colubriformis with special reference to the roles played by eosinophils and basophils in rejection of the parasite. Immunology, 22:733-745.         [ Links ]

ROTHWELL, T.L.W. & LOVE, R.J. 1975. Studies of the response of basophil and eosinophil leukocytes and mast cells to the nematode Trichostrongylus colubriformis. II Changes in cell numbers following infection of thymectomised and adoptively or passively immunized guinea pigs. Journal of Pathology, 116:183-194.         [ Links ]

ROTHWELL, T.L.W., WINDON, R.G., HORSBURGH, B.A. & ANDERSON, B.H. 1993. Relationship between eosinophilia and responsiveness to infection with Trichostrongylus colubriformis in sheep. International Journal for Parasitology, 23:203-211.         [ Links ]

SINGH, C.D.N. & LAKRA, P. 1971. Pathologic changes in naturally occurring Cotylophoron cotylophorum infection in cattle. American Journal of Veterinary Research, 32:659-663.         [ Links ]

SINHA, B.K. 1975. Efficacy of resorantel (Terenol) against paramphistomiasis in goats and calves. Current Science, 44: 526.         [ Links ]

STANKIEWICZ, M., JONAS, W.E., DOUCH, P.C.G., RABEL, B., BISSET, S. & CABAJ, W. 1993. Globule leukocytes in the lumen of the small intestine and the resistance status of sheep infected with parasitic nematodes. Journal of Parasitology, 79:940-945.         [ Links ]

TECHAU, M.E. 2002. Characterisation of the humoral immune responses in pigs congenitally or postnatally exposed to Schistosoma japonicum. M.Sc. thesis. University of Copenhagen.         [ Links ]

TIZARD, I.R. 1982. An introduction to veterinary immunology, 2nd ed. Philadelphia: Saunders Co.         [ Links ]

URVASHI, H.S.B. & KUAR, A. 2000. Immunization of lambs and kids with gamma irradiated amphistome metacercariae. Indian Veterinary Journal, 77:13-15.         [ Links ]

WINTER, M.D., WRIGHT, C. & LEE, D.L. 1997. The mast cell and eosinophil response of young lambs to a primary infection with Nematodirus battus. Parasitology, 114:189-193.         [ Links ]



Accepted for publication 17 January 2008-Editor



* Author to whom correspondence is to be directed. E-mail:

Creative Commons License All the contents of this journal, except where otherwise noted, is licensed under a Creative Commons Attribution License