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Studies on Globidial Schizonts in the Abomasum of Norwegian Sheep

The Fine Structure of One of the Four Merozoite forms Investigated

Studier av schizonter av Globidium i løpen hos norske sauer. Ultrastrukturen til en av de fire undersøkte merozoit-typene

Abstract

Norwegian sheep were investigated for globidial schizont infection in the abomasum. The frequency of infection was found to be 78.2 %. Light microscope studies of the various mature schizonts revealed the existence of four morphologically different merozoites, small A, small B, intermediate and long forms. Each globidial schizont was found to contain only one form of these merozoites. However, these four schizont types occurred in the same abomasum.

The intermediate form of globidial schizont merozoites was investigated by the aid of an electron microscope, with the aim of comparing its internal morphology with that previously published for Eimeria species. A striking resemblance was observed between the fine structures of the intermediate merozoite and that of Eimeria species, particularly the first generation merozoites described in giant schizonts of Eimeria bovis.

The present status of globidial schizonts infecting the abomasum of sheep was discussed. It was concluded that these four forms of merozoites could represent different generations of one Eimeria species or different E. species producing giant schizonts in the abomasum.

Due to the practical difficulties in studying the life histories of the different Eimeria species infecting sheep, it was proposed that the in vitro propagation of the individual species in cultured cells may shed some light on the corresponding asexual, as well as the sexual, stages. This would offer a new approach to the study of the ultra-structure of the developing parasite.

Sammendrag

Forekomsten av schizonter av Globidium i løpen er undersøkt hos norske sauer. Infeksjonsfrekvensen var 78,2 %.

Ved undersøkelse med vanlig mikroskop ble det funnet 4 forskjellige typer av merozoitter, liten A, liten B, intermediære og lange former. I hver enkelt schizont var det bare 1 av disse formene. Alle 4 typene kunne imidlertid forekomme i den samme løpen.

Den intermediære form av merozoitter ble undersøkt ved elektronmikroskopi. Det ble funnet en påfallende likhet av de finere cellestrukturer med det som er funnet for merozoitter av Eimeria arter, spesielt for schizonter av Eimeria bovis.

Den systematiske posisjon av Globidium schizonter er diskutert. Det konkluderes med at de fire typene av merozoitter kan være forskjeilige stadier av en av sauens Eimeria spp., eller representerer flere Eimeria spp. som har kjempeschizonter i løpen.

På grunn av praktiske vanskeligheter ved studiet av livscyklus til Eimeria spp., pekes det på mulighetene av å studere utviklingen av både ukjønnede og kjønnede stadier i cellekulturer. Dette ville kunne gi ytterligere opplysninger om ultrastrukturen av utviklingsstadiene av parasittene.

References

  • Aikawa, M., C. G. Huff & H. Sprinz: Comparative feeding mechanisms of avian and primate malarial parasites. Milit. Med. 1966a, 131, Suppl., 969–983.

  • Aikawa, M., P. K. Hepler, C. G. Huff & H. Sprinz: The feeding mechanism of avian malarial parasites. J. Cell Biol. 1966b, 28, 355–373.

  • Alicata, J. E.: Note, read in the 123rd meeting of the Helminthological Society of Washington. J. Parasit. 1930, 16, 162–163.

    Google Scholar 

  • Andreassen, J. & O. Behnke: Fine structure of merozoites of a rat coccidian Eimeria miyairii with a comparison of the fine structure of other sporozoa. J. Parasit. 1968, 54, 150–163.

    Article  CAS  PubMed  Google Scholar 

  • Becker, E. R.: Catalogue of Eimeriidae in genera occurring in vertebrates and not requiring intermediate hosts. Iowa Sta. Coll. J. Sci. 1956, 31, 85–139.

    Google Scholar 

  • Bedrnik, P.: Further development of the second generation of Eimeria tenella merozoites in tissue culture. Folia Parasitol. 1967, 14, 361–364.

    Google Scholar 

  • Canham, A. S.: A note on the occurrence of Globidium gilruthi in Natal. J. S. Afr. vet. med. Ass. 1931, 2, 45–46.

    Google Scholar 

  • Chatton, E.: Le Kyste de Gilruth dans la muqueuse stomacale des ovidés. (The cyst of Gilruth in the ovine stomach mucosa). Arch. Zool. Exp. Gen. 1910, 5me Ser. Vol. V, Notes et Revue 114–124.

  • Cheissin, E. M. & E. S. Snigirevskaya: Some new data on the fine structure of the merozoites of Eimeria intestinalis (Sporozoa, Eimeriidea). Protistologica 1965, 1, 121–126.

    Google Scholar 

  • Colley, F. C.: Fine structure of sporozoites of Eimeria nieschulzi. J. Protozool. 1967, 14, 217–220.

    Article  CAS  PubMed  Google Scholar 

  • Colley, F. C.: Fine structure of schizonts and merozoites of E. nieschulzi. J. Protozool. 1968, 15, 374–382.

    Article  CAS  PubMed  Google Scholar 

  • Davis, L. R., G. W. Bowman & W. N. Smith: Observations on the endogenous cycle of Eimeria ahsata Honess, 1942, in domestic sheep. J. Protozool. 1963, 10, Suppl. 18.

  • Doran, D. J. & J. M. Vetterling: Cultivation of the turkey coccidium, Eimeria meleagrimitis Tyzzer, 1929, in mammalian kidney cell cultures. Proc. helminth. Soc. Wash. 1967a, 34, 59–65.

  • Doran, D. J. & J. M. Vetterling: Comparative cultivation of poultry coccidia in mammalian kidney cell cultures. J. Protozool. 1967b, 14, 657–662.

  • Doran, D. J. & J. M. Vetterling: Survival and development of Eimeria meleagrimitis Tyzzer, 1929, in bovine kidney and in turkey intestine cell culture. J. Protozool. 1968, 15, 796–902.

    Article  CAS  PubMed  Google Scholar 

  • Fayer, R. & D. M. Hammond: Development of first generation schizonts of Eimeria bovis in cultured bovine cells. J. Protozool. 1967, 14, 764–772.

    Article  CAS  PubMed  Google Scholar 

  • Garnham, P. C. C., R. G. Bird & J. R. Baker: Electron microscope study of motile stages of malarial parasites. 1. The fine structure of the sporozoites of Haemamoeba (= Plasmodium) gallinacea. Trans, roy. Soc. trop. Med. Hyg. 1960, 54, 274–278.

    Article  CAS  Google Scholar 

  • Garnham, P. C. C., J. R. Baker & R. G. Bird: The fine structure of Lankesterella garnhami. J. Protozool. 1962, 9, 107–114.

    Article  Google Scholar 

  • Garnham, P. C. C., R. G. Bird & J. R. Baker: Electron microscope studies of motile stages of malaria parasites. IV. The fine structure of the sporozoites of four species of Plasmodium. Trans. roy. Soc. trop. Med. Hyg. 1963, 57, 27–31.

    Article  CAS  PubMed  Google Scholar 

  • Garnham, P. C. C., S. S. Desser & H. M. S. El-Nahal: Electron microscope studies on motile stages of malaria parasites. VI. The ookinete of Plasmodium berghei yoelii and its transformation into the early oocyst. Trans. roy. Soc. trop. Med. Hyg. 1969, 63, 187–194.

    Article  CAS  PubMed  Google Scholar 

  • Gilruth, J. A.: Notes on a protozoal parasite found in the mucous membrane of the abomasum of sheep. Bull. Soc. Path. exot. 1910, 3, 297–298.

    Google Scholar 

  • Guralp, N. & H. K. Urman: Koyunlarimizda tesbit ettigimiz Globidium gilruthi Chatton 1910 Olaylari. (Globidium gilruthi in sheep in Turkey). Vet. Fak. Derg. 1957, 4, 131–134. (Vide Vet. Bull. 28, 707).

  • Haiba, M. H.: Studies on the morphology and biology of Giardia. Thesis. Cairo Univ. Press 1953.

  • Hammon, D. M. & R. Fayer: Cultivation of Eimeria bovis in three established cell lines and in bovine tracheal cell line cultures. J. Parasit. 1968, 54, 559–567.

    Article  Google Scholar 

  • Hammond, D. M., E. Scholtyseck & M. L. Miner: The fine structures of microgametocytes of Eimeria perforans, E. stiedae, E. bovis, E. auburnensis. J. Parasit. 1967, 53, 235–247.

    Article  CAS  PubMed  Google Scholar 

  • Helle, O. & M. Hilali: Differentiation of Eimeria species infecting sheep during the grazing season on permanent and new pastures under Norwegian conditions. Acta vet. scand. 1973, 14, 57–68.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jacobs, L.: Toxoplasmosis. In Advances in Parasitology. Acad. Press, New York 1968, Vol. 5.

  • Kotlan, A., L. Pellérdy & L. Versényi: Zur Kenntnis der endogenen Entwicklung der Schafkokzidien mit besonderer Rücksicht auf die Schizogonie. (Knowledge on the endogenous development of coccidia in sheep with special reference to the schizogony). Acta vet. Acad. Sci. hung. 1951 a, 1, 137–144.

  • Kotlan, A., L. Pellérdy & L. Versényi: Experimentelle Studien über die Kokzidiose der Schafe. I. Die endogene Entwicklung von Eimeria parva. (Experimental studies on coccidiosis in sheep. I. The endogenous development of Eimeria parva). Acta vet. Acad. Sci. hung. 1951b, 1, 317–331.

  • Levine, N. D.: Protozoan parasites of domestic animals and of man. Burgess, Minneapolis 1961, III, 412 pp.

  • Levine, N. D.: Uniform terminology for sporozoan protozoa. In Progress in Protozoology. Academy of Sciences of the USSR, Publishing House NAUKA, Leningrad 1969a, 340.

  • Levine, N. D.: Taxonomy of sporozoa. In Progress in Protozoology. Academy of Sciences of the USSR, Publishing House NAUKA, Leningrad 1969b, 365–366.

  • Lotze, J. C.: Life history of the coccidian parasite, Eimeria arloingi in domestic sheep. Amer. J. vet. Res. 1953, 14, 86–95.

    CAS  PubMed  Google Scholar 

  • Ludvik, J.: Toxoplasma im elektronenmikroskopischen Bilde. (Electron microscopic picture of Toxoplasma). Med. Bild 1958, 1, 59–61.

    Google Scholar 

  • Ludvik, J.: Electron microscopy study of some parasitic protozoa. Proc. 1st Int. Congr. Protozool. Prague (1961), 1963, 387–392.

    Google Scholar 

  • Luft, J. H.: Improvements in epoxy resin embedding methods. J. biophys. biochem. Cytol. 1961, 6, 409–414.

    Article  Google Scholar 

  • Marsh, H. & E. A. Tunnicliff: Enteritis in sheep caused by infection with the protozoan parasite Globidium gilruthi. Amer. J. vet. Res. 1941, 2, 174–177.

    Google Scholar 

  • Maske, H.: Gregarinen im Labmagen des Schafes. (Gregarines in the abomasum of sheep). Z. Fleisch- u. Milch.-Hyg. 1893, 4, 28–29.

    Google Scholar 

  • Matsuoka, T., M. Callender & R. Schumard: Embryonic bovine tracheal cell line for in vitro cultivation of Eimeria tenella. Amer. J. vet. Res. 1969, 30, 1119–1122.

    CAS  PubMed  Google Scholar 

  • Matta, S. C. & B. P. Pande: On globidial schizonts in abomasum of sheep. — A histological study. Indian J. vet. Sci. 1966, 36, 211– 220.

  • Millonig, G.: Advantages of a phosphate buffer for osmium tetraoxide solution in fixation. J. appl. Physiol. 1961, 32, 1637.

    Google Scholar 

  • Patton, W.: Eimeria tenella: Cultivation of the asexual stages in cultured animal cells. Science 1965, 150, 767–769.

    Article  CAS  PubMed  Google Scholar 

  • Pease, D. C.: Histological techniques for electron microscopy. Acad. Press, New York 1964.

  • Pellérdy, L. P.: Intestinal coccidiosis of the coypu II. The endogenous development of Eimeria seideli and the present status of the group “Globidium”. Acta vet. Acad. Sci. hung. 1960, 10, 389– 399.

  • Rac, R. & R. L. Willson: Globidiosis in sheep. Aust. vet. J. 1959, 35, 455–456.

    Article  Google Scholar 

  • Rakoveč, R., L. Senk & J. Brglez: Globidienbefall (Globidium gilruthi) bei Fettsteibschafen (Ovis aries stcatopyga var. somalica) im Zoologischen Garten Ljubljana. (Globidial infestation (Globidium gilruthi) of steatopygous sheep (Ovis aries steatopyga var. somalica) in the Zoological Garden of Ljubljana). Verhandlungsbericht XII Int. Symp. Erkrankungen der Zootiere. Budapest 1970, Akademie-Verlag, Berlin 1970, 293–296.

    Google Scholar 

  • Reichenow, E.: Über das Kokzid der Equiden Globidium leuckarti. (On the equine coccidia Globidium leuckarti). Z. Infekt.-Kr. Haustiere 1940, 56, 126–134.

    Google Scholar 

  • Reichenow, E.: Doflein’s Lehrbuch der Protozoenkunde. II (Zweite Hälfte) Sporozoa und Ciliophora. (Doflein’s textbook of protozoology. II (2nd half) Sporozoa and Ciliophora). Gustav Fischer, Jena 1953, 6th Ed., pp. IV+437+VIII.

  • Reichenow, E. & A. Carini: Über Eimeria travassosi und die Gattung Globidium. (Eimeria travassosi and the genus Globidium). Arch. Protistenk. 1937, 88, 347–386.

    Google Scholar 

  • Reynolds, E. S.: The use of lead citrate at high pH as an electron opaque stain in electron microscopy. J. Cell Biol. 1963, 17, 208–212.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ryley, J.: Ultrastructural studies on the sporozoite of Eimeria tenella. Parasitology 1969, 59, 67–72.

    Article  CAS  PubMed  Google Scholar 

  • Ryley, J. F., D. J. Manners & J. R. Stark: Amylopectin, the storage polysaccharide of Eimeria tenella. J. Protozool. 1968, 15, Suppl., p. 31.

  • Sarwar, M. M.: Occurrence of Globidium gilruthi, a protozoon parasite of sheep and goats, from the Indo-Pakistan subcontinent. Parasitology 1951, 41, 282.

    Article  Google Scholar 

  • Scholtyseck, E.: Elektronenmikroskopisch-Cytochemischer Nachweis von Glykogen bei Eimeria perforans. (Electron microscopic and cytochemical evidence of glycogen in Eimeria perforans). Z. Zellforsch. 1964, 64, 688–707.

    Article  CAS  PubMed  Google Scholar 

  • Scholtyseck, E. & G. Piekarski: Elektronenmikroskopische Untersuchungen an Merozoiten von Eimerien (E. perforans und E. stidae) und Toxoplasma gondii. Zur systematischen Stellung von T. gondii. (Electron microscope studies of merozoites of Eimeria species (E. perforans and E. stidae) and Toxoplasma gondii. A contribution to the systematic position of T. gondii). Z. Parasitenk. 1965, 26, 91–115.

    Article  CAS  PubMed  Google Scholar 

  • Scholtyseck, E. & R, Strout: Feinstrukturuntersuchungen über die Nahrungsaufnahme bei Coccidien in Gewebekulturen (Eimeria tenella). (Electron microscope studies of the nutrition of coccidia in cell culture). Z. Parasitenk. 1968, 30, 291–300.

    Article  CAS  PubMed  Google Scholar 

  • Scholtyseck, E. & H. Mehlhorn: Ultrastructural study of characteristic organelles (Paired organelles, Micronemes, Micropores) of sporozoa and related organisms. Z. Parasitenk. 1970, 34, 97–127.

    CAS  PubMed  Google Scholar 

  • Scholtyseck, E., H. Mehlhorn & K. Friedhoff: The fine structure of the conoid of sporozoa and related organisms. Z. Parasitenk. 1970, 34, 68–94.

    Article  Google Scholar 

  • Senaud, J.: Contribution a l’étude des sarcosporidies et des toxoplasmes (Toxoplasmea). (Contribution to the study of sarcosporidia and toxoplasma (Toxoplasmea)). Protistologica 1967, 3, 170— 232.

  • Sénaud, J. & Z. Černa: Étude en microscopie électronique des mérozoites et de la mérogonie chez Eimeria pragensis (Černa et Sénaud, 1968), coccidie parasite de l’intestin de la souris (Mus musculus). (Electron microscope studies on the merozoites and the merogony of Eimeria pragensis (Cerna et Sénaud, 1968). A parasitic coccidia of the intestine of mice (Mus musculus)). Ann. Sta. biol. Besse-en-Chandesse 1968, no. 3, 221–241.

  • Sénaud, J. & Z. Černa: Étude ultrastructurale des mérozoites et de la schizogonie des coccidies (Eimeriina): Eimeria magna (Pérard, 1925) de l’intestin des lapins et de E. tenella (Raillet et Lucet, 1891) des coecums des Poulets. (Ultrastructural study of merozoites and schizogony of the coccidia (Eimeriina): Eimeria magna (Pérard, 1925) from the intestine of rabbits and E. tenella (Raillet and Lucet, 1891) from the caecum of chickens). J. Protozool. 1969, 16, 155–165.

    Article  PubMed  Google Scholar 

  • Sheffield, H. H. & D. M. Hammond: Fine structure of first generation merozoites of Eimeria bovis. J. Parasit. 1966, 52, 595–606.

    Article  CAS  PubMed  Google Scholar 

  • Sheffield, H. H. & D. M. Hammond: Electron microscope observations on the development of first-generation merozoites of E. bovis. J. Parasit. 1967, 53, 831–840.

    Article  CAS  PubMed  Google Scholar 

  • Soliman, K. N.: Globidium gilruthi (Chatton, 1910) infection in the digestive tract of sheep and goat in Egypt. Parasitology 1958, 48, 291–292.

    Article  CAS  PubMed  Google Scholar 

  • Soliman, K. N.: Globidium infection in Sudan with special reference to Globidium gilruthi (Chatton, 1910) in sheep and goats. J. Parasit. 1960, 46, 29–32.

    Article  CAS  PubMed  Google Scholar 

  • Soulsby, E. J. L.: Helminths, arthropods and protozoa of domesticated animals, Bailliere, Tindall and Cassell, London 1968, p. 824.

  • Stehbens, W. E.: The ultrastructure of Lankesterella hylae. J. Protozool. 1966, 13, 63–73.

    Article  CAS  PubMed  Google Scholar 

  • Strout, R. G. & C. Quellette: Gametogony of Eimeria tenella (Coccidia) in cell cultures. Science 1969, 163, 695–696.

    Article  CAS  PubMed  Google Scholar 

  • Strout, R. G. & E. Scholtyseck: The ultrastructure of first generation development of Eimeria tenella (Raillet and Lucet, 1891) Fantham, 1909 in cell cultures. Z. Parasitenk. 1970, 35, 87–96.

    Article  CAS  PubMed  Google Scholar 

  • Strout, R. G., J. Solis, S. Smith & W. Dunlop: In vitro cultivation of Eimeria acervulina (Coccidia). Exp. Parasit. 1965, 17, 241–246.

    Article  CAS  PubMed  Google Scholar 

  • Strout, R. G., C. Quellette & D. Gangi: Effect of inoculum size on development of Eimeria tenella in cell cultures, J. Parasit. 1969 a, 17, 241–246.

  • Strout, R. G., C. Quellette & D. Gangi: Temperature and asexual development in cell culture. Exp. Parasit. 1969 b, 25, 324–328.

  • Triffitt, M. J.: Observations on Gastrocystis gilruthi, a parasite of sheep in Britain. J. Protozool. 1925, 1, 7–18.

    Google Scholar 

  • Triffitt, M. J.: Further observations on the development of G. gilruthi. J. Protozool. 1928, 4, 83–90.

    Google Scholar 

  • Trump, B. F., E. A. Smuckler & E. P. Benditt: A method for staining epoxy sections for light microscopy. J. Ultrastruct. Res, 1961, 7, 343–348.

    Article  Google Scholar 

  • Vivier, E. & E. Hennere: Ultrastructure des stades vegetatifs de la coccidie Coelotropha durchoni. (Ultrastructure of the vegetative stage of the coccidia Coelotropha durchoni). Protistologica 1965, 1, 89–113.

    Google Scholar 

  • Wenyon, C. M.: Protozoology. Bailiiere. Tindall and Cox, London 1926, Vol. I.

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This work was supported by a grant from the Norwegian Agency for International Development (NORAD).

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Hilali, M. Studies on Globidial Schizonts in the Abomasum of Norwegian Sheep. Acta Vet Scand 14, 22–43 (1973). https://doi.org/10.1186/BF03547408

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