Zeitschrift für Parasitenkunde

, Volume 69, Issue 5, pp 551–570 | Cite as

A review of the biology and transmission ecology of African bovine species of the genusSchistosoma

  • N. Ø. Christensen
  • A. Mutani
  • F. Frandsen
Review Article


The present paper reviews the information available concerning the biology and transmission ecology of the African bovine speciesSchistosoma bovis, S. mattheei, S. margrebowiei andS. leiperi. Criteria for species identification (egg morphology, intermediate host spectra, definitive host-parasite relationships, etc.) are listed and the geographical distribution of the four species and factors determining the relative occurrence within their overall distributional ranges are described.S. bovis andS. mattheei occur north and south of 10° S, repectively, andS. margrebowiei occurs mainly, andS. leiperi only, in southern central Africa. Definitive host-related factors (susceptibility, water contact pattern, etc.) providing the background for being a primary definitive host and the primary definitive host spectra for the four schistosome species are deseribed. The primary definitive host spectrum forS. margrebowiei andS. leiperi comprise lechwe, puku and waterbuck, forS. mattheei lechwe, puku, waterbuck plus cattle, and forS. bovis cattle and possibly also some of the listed antelope species. In addition, wild bovines and cattle may provide a reservoir ofS. mattheei andS. margrebowiei in humans, but wild bovines and domestic stock play no major role in the transmission of other human species of schistosomes. The intermediate snail host spectra ofS. mattheei andS. leiperi only comprise members of theBulinus africanus species complex;S. bovis is transmitted by members of theB. truncatus, B. africanus andB. forskalii species groups, andS. margrebowiei is transmitted by members of theB. forskalli species group and possibly also by members of theB. tropicus andB. truncatus species groups. Factors determining the transmission ecology of the four schistosome species, and thereby the epidemiology of bovine schistosomiasis, are discussed. Influential factors comprise environmental conditions mediated via the effect of these on the size of the snail host population and on the rate of the intramolluscan development, behavioural patterns of the definitive host population and the course of the infection in the definitive host as related to aspects of susceptibility and level of endemicity. The epidemiological pattern (prevalence and intensity of infection, seasonality of transmission, etc.) is described and exemplified, and it is finally concluded that the increasing water conservation and changing methods of husbandry may result in bovine schistosomiasis becoming a major veterinary problem in Africa.


Schistosomiasis Host Population Definitive Host Contact Pattern Snail Host 
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.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Adam SEI, Magzoub M (1976) Susceptibility of desert sheep to infection withSchistosoma mansoni of Northern Sudan. Vet Pathol 13:211–215Google Scholar
  2. Adam SEI, Magzoub M (1977) Clinico-pathological changes associated with experimentalSchistosoma mansoni infection in the goat. Br vet J 133:201–210Google Scholar
  3. Appleton CC (1978) Review of literature on abiotic factors influencing the distribution and life cycles of bilharziasis intermediate host snails. Malacol Rev 11:1–25Google Scholar
  4. Appleton CC, Bruton MN (1979) The epidemiology of schistosomiasis in the vicinity of Lake Sibaya, with a note on other areas of Tongaland (Natal, South Africa). Ann Trop Med Parasitol 73:547–561Google Scholar
  5. Basson PA, McCully RM, Kruger SP, Niekerk JW Van, Young E, De Vos V (1970) Parasitic and other diseases of the African buffalo in the Kruger National Park. Onderstepoort J vet Res 37:11–28Google Scholar
  6. Berrie AD (1964) Observations on the lifecycle ofBulinus (Physopsis)ugandae Mandahl-Barth, its ecological relation toBiomphalaria sudanica tanganyicensis (Smith), and its role as an intermediate host ofSchistosoma. Ann Trop Med Parasitol 58:457–466Google Scholar
  7. Blair DM (1966) The occurrence of terminal spined eggs, other than those ofSchistosoma haematobium, in human beings in Rhodesia. Cent Afr J Med 12:103–109Google Scholar
  8. Brown DS (1980) Freshwater snails of Africa and their medical importance. Taylor & Francis Ltd., LondonGoogle Scholar
  9. Brown DS, Jelnes JE, Kinoti GK, Ouma J (1981) Distribution in Kenya of intermediate hosts forSchistosoma. Trop geogr Med 33:95–103Google Scholar
  10. Bushara HO, Majid AA, Saad AM, Hussein MF, Taylor MG, Dargie JD, Marshall TF de C, Nelson GS (1980) Observations on cattle shistosomiasis in the Sudan, a study in comparative medicine. II. The experimental demonstration of naturally acquired resistance toSchistosoma bovis. Am J Trop Med Hyg 29:442–451Google Scholar
  11. Christensen NØ, Nansen P, Frandsen F, Monrad J (1982)Schistosoma intercalatum (Fisher 1934) infection in sheep. J Helminthol 56:11–15Google Scholar
  12. Condy JB (1960) Bovine schistosomiasis in Southern Rhodesia. Cent Afr J Med 6:381–384Google Scholar
  13. Dargie JD (1980) The pathogenesis ofSchistosoma bovis infection in sudanese cattle. Trans R Soc Trop Med Hyg 74:560–562Google Scholar
  14. Dinnek JA, Dinnek NN (1965) The schistosomes of domestic ruminants in Eastern Africa. Bull Epizoot Dis Afr 13:341–359Google Scholar
  15. Dowdeswell RM (1938) Schistosomiasis in the Kavirondo district of Kenya colony. Trans R Soc Trop Med Hyg 31:673–688Google Scholar
  16. Eisa AM (1966) Parasitism — a challenge to animal health in the Sudan. Sudan J Vet Sci Anim Husbandry 7:85–98Google Scholar
  17. Frandsen F (1979) Studies of the relationships betweenSchistosoma and their intermediate hosts. IV. The genusBulinus andSchistosoma bovis from Morocco. J Helminthol 53:349–355Google Scholar
  18. Graber M (1969) Helminthes parasites de certains animaux domestiques et sauvages du Tchad. Bull Epizoot Dis Afr 17:403–428Google Scholar
  19. Graber M (1978)Schistosoma margrebowiei of cobs in Chad. J Helminthol 52:72–74Google Scholar
  20. Hill DH, Onabamino SD (1960) Vesical schistosomiasis in the domestic pig. Br vet J 116:145–150Google Scholar
  21. Hurter LR, Potgieter LND (1967) Schistosomiasis in small stock in the Potgietersrus veterinary area. J S Afr vet med Ass 38:444–446Google Scholar
  22. Hussein MF (1973) Animal schistosomiasis in Africa: a review ofSchistosoma bovis andSchistosoma mattheer. Vet Bull 43:341–347Google Scholar
  23. Hussein MF (1980) Prospects for the control ofSchistosoma bovis infection in sudanese cattle. Trans R Soc Trop Med Hyg 74:559–560Google Scholar
  24. Hussein MF, Saeed AA, Nelson GS (1970) Studies on heterologous immunity in schistosomiasis. 4. Heterologous schistosome immunity in cattle. Bull WHO 42:745–749Google Scholar
  25. Jordan P, Christie JD, Unrau GO (1970) Schistosomiasis transmission with particular reference to possible ecological and biological methods of control. Act Trop 37:95–135Google Scholar
  26. Kinoti G (1964a) A note on the susceptibility of some gastropod molluses toSchistosoma bovis andS. mattheei. Ann Trop Med Parasitol 58:270–275Google Scholar
  27. Kinoti G (1964b) Observations on the transmission ofSchistosoma haematobium andSchistosoma bovis in the Lake Region of Tanganyika. Bull WHO 31:815–823Google Scholar
  28. Kinoti G (1968) Observations on the infection of bulinid snails withSchistosoma mattheei. 1. The susceptibility ofBulinus africanus andBulinus truncatus. Ann Trop Med Parasitol 62:382–392Google Scholar
  29. Kinoti GK (1971) The epidemiology ofSchistosoma haematobium infection on the Kano Plain of Kenya. Trans R Soc Trop Med Hyg 65:637–645Google Scholar
  30. Lapierre J, Hien TV (1973) Un cas de triple infestation bilharzienne aSchistosoma mansoni, S. haematobium etRhodobilharzia margrebowiei? Ann Parasitol hum comp 48:301–306Google Scholar
  31. Lawrence JA (1973)Schistosoma mattheei in cattle: the host-parasite relationship. Res vet Sci 14:400–402Google Scholar
  32. Lawrence JA (1977a)Schistosoma mattheei in the ox: the chronic hepatic syndrome. J S Afr vet Ass 48:77–83Google Scholar
  33. Lawrence JA (1977b)Schistosoma mattheei infestation in the ox: the intestinal syndrome. J S Afr vet Ass 48:55–58Google Scholar
  34. Lawrence JA (1978) Bovine schistosomiasis in Southern Africa. Helm Abstr, Series A 47:261–270Google Scholar
  35. Lawrence JA (1980) The pathogenesis ofSchistosoma mattheei in the sheep. Res vet Sci 29:1–7Google Scholar
  36. Lawrence JA, Condy JB (1970) The developing problem of schistosomiasis in domestic stock in Rhodesia. Cent Afr J Med 16 suppl to no.7:19–22Google Scholar
  37. Lawrence JA, McKenzie RL (1972) Schistosomiasis in farm livestock. Rhod Agri J 69:79–83Google Scholar
  38. Lengy J (1962a) Studies onSchistosoma bovis (Sonsino 1876) in Israel. I. Larval stages from egg to cercaria. Bull Res Coun Israel 10E:1–36Google Scholar
  39. Lengy J (1962b) Studies onSchistosoma bovis (Sonsino, 1876) in Israel. II. The intra-mammalian phase of the life cycle. Bull Res Coun Israel 10E:73–95Google Scholar
  40. Le Roux PL (1955) A new mammalian schistosome (Schistosoma leiperi sp. nov.) from herbivora in Northern Rhodesia. Trans R Soc Trop Med Hyg 49:293–294Google Scholar
  41. Le Roux PL (1961) Some problems in bilharziasis in Africa and the adjoining countries. J Helminthol RT Leiper Supplement:117–126Google Scholar
  42. Lo CT, Lemma A (1975) Studies onSchistosoma bovis in Ethiopia. Ann Trop Med Parasitol 69:375–382Google Scholar
  43. Majid AA, Marshall TF de C, Hussein MF, Bushara HO, Taylor MG, Nelson GS, Dargie JD (1980) Observations on cattle schistosomiasis in the Sudan, a study in comparative medicine. I. Epizootiological observations onSchistosoma bovis in the White Nile Province. Am J Trop Med Hyg 29:435–441Google Scholar
  44. Malek EA (1969) Studies on bovine schistosomiasis in the Sudan. Ann Trop Med Parasitol 63: 501–513Google Scholar
  45. Marill FG (1961) Enseignements d'une première enquête sur l'épidémiologie de la billharziose àSchistosoma haematobium en Mauritanie. Med Trop 21:373–386Google Scholar
  46. McClelland WFJ (1955) Two species ofBulinus found naturally infected with a bovine schistosome in Western Kenya. Trans R Soc Trop Med Hyg 49:295Google Scholar
  47. McClelland WFJ (1956) Studies on snail vectors of schistosomiasis in Kenya. J Trop Med Hyg 59:229–242Google Scholar
  48. McConnell EE, Basson PA, De Vos V, Myers BJ, Kuntz RE (1974) A survey of diseases among 100 free-ranging baboons (Papio ursinus) from the Kruger National Park. Onderstepoort J vet Res 41:97–168Google Scholar
  49. McKenzie RL (1970) Investigations into schistosomiasis in sheep in Mashonaland. Cent Afr J Med 16 suppl to no. 7:27–28Google Scholar
  50. Mutani A, Christensen NØ, Frandsen F (1983) Studies on the relationship betweenSchistosoma and their intermediate hosts. V. The genusBulinus andSchistosoma bovis from Iringa, Tanzania. Z Parasitenkd 69:483–487Google Scholar
  51. Nelson GS, Teesdale C, Highton RB (1962) The role of animals as reservoirs of bilharziasis in Africa. In: Wolstenholme GEW, O'Connor M (eds.). Bilharziasis pp 127–156. Churchill, LondonGoogle Scholar
  52. Pitchford RJ (1958) Animal reservoirs of human bilharziasis in the Eastern Transvaal. Bull WNO 18:1080–1081Google Scholar
  53. Pitchford RJ (1959) Cattle schistosomiasis in man in the Eastern Transvaal. Trans R Soc Trop Med Hyg 53:285–290Google Scholar
  54. Pitchford RJ (1961) Observations on a possible hybrid between the two schistosomesS. haematobium andS. mattheei. Trans R Soc Trop Med Hyg 55:44–51Google Scholar
  55. Pitchford RJ (1965) Differences in the egg morphology and certain biological characteristics of some African and Middle Eastern schistosomes, genusSchistosoma, with terminal-spined eggs. Bull WHO 32:105–120Google Scholar
  56. Pitchford RJ (1974) Some preliminary observations on schistosomes occurring in antelope in Central Southern Africa. Rhod vet J 4:57–61Google Scholar
  57. Pitchford RJ (1975) Introduction ofSchistosoma leiperi Le Roux 1955, andSchistosoma margrebowiei Le Roux 1933 to the laboratory. Trans R Soc Trop Med Hyg 69:362Google Scholar
  58. Pitchford RJ (1976) Preliminary observations on the distribution, definitive hosts and possible relation with other schistosomes, ofSchistosoma margrebowiei Le Roux, 1933 andSchistosoma leiperi Le Roux, 1955. J Helminthol 50:111–123Google Scholar
  59. Pitchford RJ (1977) A check list of definitive hosts exhibiting evidence of the genusSchistosoma Weinland, 1858 acquired naturally in Africa and the Middle East. J Helminthol 51:229–252Google Scholar
  60. Pitchford RJ (1981) Temperature and schistosome distribution in South Africa. S Afr J Sci 77:252–261Google Scholar
  61. Pitchford RJ, Du Toit JF (1976) The shedding pattern of three little known African schistosomes under outdoor conditions. Ann Trop Med Parasitol 70:181–187Google Scholar
  62. Pitchford RJ, Lewis M (1978) Oxamniquine in the treatment of various schistosome infections in South Africa. S Afr Med J 53:677–680Google Scholar
  63. Pitchford RJ, Visser PS (1962) The role of naturally infected wild rodents in the epidemiology of schistosomiasis in the Eastern Transvaal. Trans R Soc Trop Med Hyg 56:126–135Google Scholar
  64. Pitchford RJ, Visser PS (1965) Some further observations on schistosome transmission in the Eastern Transvaal. Bull WHO 32:83–104Google Scholar
  65. Pitchford RJ, Visser PS (1966) The activity of various schistosome cercariae in outdoor aquaria. Ann Trop Med Parasitol 60:518–521Google Scholar
  66. Pitchford RJ, Visser PS (1969) The use of behaviour patterns of larval schistosomes in assessing the bilharizia poetential of non-endemic areas. S Afr Med J 43:983–995Google Scholar
  67. Pitchford RJ, Visser PS (1975) Excretion ofSchistosoma mattheei eggs from man, baboons and cattle living in their normal environment. J Helminthol 49:137–142Google Scholar
  68. Pitchford RJ, Wolstenholme B (1977) Further observations on the relationship and distribution ofSchistosoma margrebowiei andS. leiperi in central southern Africa. J Helminthol 51:327–336Google Scholar
  69. Pitchford RJ, Meyling AH, Meyling J, Du Toit JF (1969) Cercarial shedding patterns of various schistosome species under outdoor conditions in the Transvaal. Ann Trop Med Parasitol 63:359–371Google Scholar
  70. Pitchford RJ, Visser PS, Du Toit JF, Pienaar U de V, Young E (1973) Observations on the ecology ofSchistosoma mattheei Veglia & Le Roux 1929, in portion of the Kruger National Park and surrounding area using a new quantitative technique for egg output. J S Afr vet Ass 44:405–420Google Scholar
  71. Pitchford RJ, Visser PS, Pienaar U de V, Young E (1974) Further observations onSchistosoma mattheei Veglia & Le Roux, 1929, in Kruger National Park. J S Afr vet Ass 45:211–218Google Scholar
  72. Reinecke RK (1970) The epizootiology of an outbreak of bilharziasis in Zululand. Cent Afr J Med 16, suppl to no. 7:10–12Google Scholar
  73. Ross GC, Southgate VR, Knowles RJ (1978) Observations on some isoenzymes of strains ofSchistosoma bovis, S. mattheei, S. margrebowiei, andS. leiperi. Z Parasitenkd 57:49–56Google Scholar
  74. Saad AM, Hussein MF, Dargie JD, Taylor MG, Nelson GS (1980)Schistosoma bovis in calves: the development and clinical pathology of primary infections. Res vet Sci 28:105–111Google Scholar
  75. Saeed AA, Nelson GS (1974) ExperimentalSchistosoma mansoni infection in sheep. Trop Anim Hlth Prod 6:45–62Google Scholar
  76. Saeed AA, Hussein MF, Nelson GS (1969) Experimental infection of calves withSchistosoma mansoni. Trans R Soc Trop Med Hyg 63:456–458Google Scholar
  77. Santos Dias JAT (1954) Panorama noso-parasitologico veterinario em Mocambique. Anais do Instituto de Medicina Tropical, Lisbon 11:605–634Google Scholar
  78. Schillhorn TW van Veen, Folaranmi DOB, Usman S, Ishaya T (1980) Incidence of liver Fluke infections (Fasciola gigantica andDicrocoelium hospes) in ruminants in Northern Nigeria. Trop Anim Hlth Prod 12:97–104Google Scholar
  79. Schutte CHJ, Deventer JMG Van, Lamprecht T (1980)Schistosoma mansoni andS. mattheei infestation in Northern KwaZulu. S Afr Med J 58:66–70Google Scholar
  80. Schwetz J (1951)Physopsis nasuta as an invertebrate host ofSchistosoma haematobium andS. bovis in Uganda. Trans R Soc Trop Med Hyg 44:362–363Google Scholar
  81. Schwetz J (1956) Some new comparative investigations on threePhysopsis borne schistosomes;Schistosoma haematobium, S. bovis & S. intercalatum. Am J Trop Med Hyg 5:1071–1085Google Scholar
  82. Smithers SR (1956) On the ecology of schistosome vectors in the Gambia, with evidence of their role in transmission. Trans R Soc Trop Med Hyg 50:354–365Google Scholar
  83. Southgate VR, Knowles RJ (1975a) Observations onSchistosoma bovis Sonsino, 1876. J Nat Hist 9:273–314Google Scholar
  84. Southgate VR, Knowles RJ (1975b) The intermediate hosts ofSchistosoma bovis in Western Kenya. Trans R Soc Trop Med Hyg 69:356–357Google Scholar
  85. Southgate VR, Knowles RJ (1977) OnSchistosoma margrebowiei Le Roux, 1933: The morphology of the egg, miracidium, and cercaria, the compatibility with species ofBulinus, and development inMesocricetus auratus. Z Parasitenkd 54:233–250Google Scholar
  86. Southgate VR, Ross GC, Knowles RJ (1981) OnSchistosoma leiperi Le Roux, 1955: Scanning electron microscopy of adult worms, compatibility with species ofBulinus, development inMesocricetus auratus, and isoenzymes. Z Parasitenkd 66:63–81Google Scholar
  87. Southgate VR, Rollinson D, Ross GC, Knowles RJ (1980) Observations on an isolate ofSchistosoma bovis from Tanzania. Z Parasitenkd 63:241–249Google Scholar
  88. Strydom HF (1963) Bilharziasis in sheep and cattle in the Piet Retief district. J S Afr vet med Ass 34:69–72Google Scholar
  89. Taylor MG (1970) Hybridization experiments on five species of African schistosomes. J Helminthol 44:253–314Google Scholar
  90. Taylor MG (1971) Further observations on the sexual maturation of female schistosomes in single-sex infections. J Helminthol 45:89–92Google Scholar
  91. Taylor MG, Andrews BJ (1973) Comparison of the infectivity and pathogenecity of six species of African schistosomes and their hybrids. 1. Mice and hamsters. J Helminthol 47:439–453Google Scholar
  92. Taylor MG, Amin MBA, Nelson GS (1969) “Parthenogenesis” inSchistosoma mattheei. J Helminthol 43:197–206Google Scholar
  93. Taylor MG, Nelson GS, Smith M, Andrews BJ (1973) Comparison of the infectivity and pathogenecity of six species of African schistosomes and their hybrids. 2. Baboons. J Helminthol 47:455–485Google Scholar
  94. Teesdale C, Nelson GS (1958) Recent work on schistosomes and snails in Kenya. E Afr Med J 35:427–438Google Scholar
  95. Van Wyk JA (1977) Transimission ofSchistosoma mattheei from animals to man. In: Medicine in a tropical environment. Gear JHS (ed.). Cape Town: Balkema:705–717Google Scholar
  96. Van Wyk JA, Bartsch RC, Rensburg LJ Van, Heitman LP, Goosen PJ (1974) Studies on schistosomiasis. 6. A field outbreak of bilharzia in cattle. Onderstepoort J vet Res 41:39–50Google Scholar
  97. Walkiers J (1928) Cinq cas de schistosomiase avec des oeufs sans epines dans le haut Uélé. Ann Soc Belge Med Trop 8:21–22Google Scholar
  98. Webbe G (1971) The significance of infra-specific variations of hosts and parasites in the epidemiology of helminths of medical importance. J Helminthol 45:327–335Google Scholar
  99. Wright CA, Ross GC (1980) Hybrids betweenSchistosoma haematobium andS. mattheei and their identification by isoelectric focusing of enzymes. Trans R Soc Trop Med Hyg 74:326–332Google Scholar
  100. Wright CA, Southgate VR (1976) Hybridizatio of schistosomes and some of its implications. In: Taylor AER, Muller R (eds) Symposia of the British Society for Parasitology 14:55–86Google Scholar
  101. Wright CA, Southgate VR, Knowles RJ (1972) Waht isSchistosoma intercalatum Fisher, 1934? Trans R Soc Trop Med Hyg 66:28–64Google Scholar
  102. Wright CA, Rollinson D, Goll PH (1979a) Parasites inBulinus senegalensis (Mollusca: Planorbidae) and their detection. Parasitology 79:95–105Google Scholar
  103. Wright CA, Southgate VR, Howard GW (1979b) Observations on the life-cycle ofSchistosoma margrebowiei and its possible interactions withS. leiperi in Zambia. J Nat Hist 13:499–506Google Scholar

Copyright information

© Springer-Verlag 1983

Authors and Affiliations

  • N. Ø. Christensen
    • 1
  • A. Mutani
    • 1
  • F. Frandsen
    • 1
  1. 1.Danish Bilharziasis LaboratoryCharlottenlundDenmark

Personalised recommendations