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Besnoitia besnoiti infection in cattle and mice: ultrastructural pathology in acute and chronic besnoitiosis

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Abstract

Current knowledge on bovine besnoitiosis, caused by the emerging apicomplexan pathogen Besnoitia besnoiti, is still fragmentary. So far, studies dealing with ultrastructural pathology focused mainly on the easily accessible chronic stage, whereas ultrastructural investigations of tachyzoites were confined to in vitro studies. In the study presented here, the ultrastructural pathology of naturally B. besnoiti-infected cattle in the acute and chronic disease stages and experimentally B. besnoiti-infected mice was monitored. Further, the ultrastructure of tachyzoites and bradyzoites was investigated. Skin samples of two adult Limousin cows and one adult Limousin bull naturally infected with B. besnoiti and liver and skin samples of gamma-interferon knockout mice infected with B. besnoiti were examined in semithin sections stained with toluidine blue and safranin and in ultrathin sections contrasted with uranyl acetate and lead citrate. Samples of vessel walls of the bull and nasal mucosa of one cow were examined by scanning electron microscopy. Few tachyzoites-like endozoites were detected for the first time in bovine skin, and large numbers of tachyzoites were detected in murine skin and liver. Within tissue cysts in bovine skin, numerous bradyzoites were observed displaying signs of degeneration. Tachyzoites had apicomplexan endozoite ultrastructure. B. besnoiti tachyzoites and bradyzoites differed in shape and the number of amylopectin granules. Transmission and scanning electron microscopy confirmed the presence of two different cyst wall layers, and the present results on cyst wall ultrastructure were in accordance with those previously obtained by histological sections.

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References

  • Arbustini E, Brega A, Narula J (2008) Ultrastructural definition of apoptosis in heart failure. Heart Fail Rev 13:121–135

    Article  PubMed  Google Scholar 

  • Basson PA, McCully RM, Bigalke RD (1970) Observations on the pathogenesis of bovine and antelope strains of Besnoitia besnoiti (Marotel, 1912) infection in cattle and rabbits. Onderstepoort J Vet Res 37:105–126

    PubMed  CAS  Google Scholar 

  • Besnoit C, Robin V (1912) Sarcosporidiose cutanée chez une vache. Rev Vét 37:649–663

    Google Scholar 

  • Bigalke RD (1968) New concepts on the epidemiological features of bovine besnoitiosis as determined by laboratory and field investigations. Onderstepoort J Vet Res 35:3–137

    PubMed  CAS  Google Scholar 

  • Bigalke RD (1970) The present concept of the life cycle of Besnoitia besnoiti of cattle. J Parasitol 56:29–30

    Google Scholar 

  • Bigalke RD (1981) Besnoitiosis and globidiosis. In: Ristic M, McIntyre I (eds) Diseases of cattle in tropics, vol 6. Martinus Nijhoff Publishers, The Hague, pp 429–442

    Google Scholar 

  • Bigalke RD, Prozesky L (2004) Besnoitiosis. In: Coetzer JAW, Tustin RC (eds) Infectious diseases of livestock, vol 1, 2nd edn. Oxford University Press, Oxford, pp 351–359

    Google Scholar 

  • Cortes H, Leitao A, Vidal R, Vila-Vicosa MJ, Ferreira ML, Caeiro V, Hjerpe CA (2005) Besnoitiosis in bulls in Portugal. Vet Rec 157:262–264

    Article  PubMed  CAS  Google Scholar 

  • Cortes HC et al (2006) Isolation of Besnoitia besnoiti from infected cattle in Portugal. Vet Parasitol 141:226–233

    Article  PubMed  CAS  Google Scholar 

  • Cortes HC, Mueller N, Esposito M, Leitao A, Naguleswaran A, Hemphill A (2007) In vitro efficacy of nitro- and bromo-thiazolyl-salicylamide compounds (thiazolides) against Besnoitia besnoiti infection in Vero cells. Parasitology 134:975–985

    Article  PubMed  CAS  Google Scholar 

  • Cortes H, Leitao A, Gottstein B, Hemphill A (2014) A review on bovine besnoitiosis: a disease with economic impact in herd health management, caused by Besnoitia besnoiti (Franco and Borges, 1916). Parasitology 1–12

  • Dubey JP, Lindsay DS (2003) Development and ultrastructure of Besnoitia oryctofelisi tachyzoites, tissue cysts, bradyzoites, schizonts and merozoites. Int J Parasitol 33:807–819

    Article  PubMed  CAS  Google Scholar 

  • Dubey JP, Yabsley MJ (2010) Besnoitia neotomofelis n. sp. (Protozoa: Apicomplexa) from the southern plains woodrat (Neotoma micropus). Parasitology 137:1731–1747

    Article  PubMed  CAS  Google Scholar 

  • Dubey JP, Lindsay DS, Speer CA (1998) Structures of Toxoplasma gondii tachyzoites, bradyzoites, and sporozoites and biology and development of tissue cysts. Clin Microbiol Rev 11:267–299

    PubMed Central  PubMed  CAS  Google Scholar 

  • Dubey JP, Lindsay DS, Rosenthal BM, Sreekumar C, Hill DE, Shen SK, Kwok OC, Rickard LG, Black SS, Rashmir-Raven A (2002) Establishment of Besnoitia darlingi from opossums (Didelphis virginiana) in experimental intermediate and definitive hosts, propagation in cell culture, and description of ultrastructural and genetic characteristics. Int J Parasitol 32:1053–1064

    Article  PubMed  CAS  Google Scholar 

  • Dubey JP, Shkap V, Pipano E, Fish L, Fritz DL (2003) Ultrastructure of Besnoitia besnoiti tissue cysts and bradyzoites. J Eukaryot Microbiol 50:240–244

    Article  PubMed  CAS  Google Scholar 

  • Dubey JP, Sreekumar C, Rosenthal BM, Vianna MC, Nylund M, Nikander S, Oksanen A (2004) Redescription of Besnoitia tarandi (Protozoa: Apicomplexa) from the reindeer (Rangifer tarandus). Int J Parasitol 34:1273–1287

    Article  PubMed  CAS  Google Scholar 

  • Dubey JP, Sreekumar C, Donovan T, Rozmanec M, Rosenthal BM, Vianna MC, Davis WP, Belden JS (2005) Redescription of Besnoitia bennetti (Protozoa: Apicomplexa) from the donkey (Equus asinus). Int J Parasitol 35:659–672

    Article  PubMed  CAS  Google Scholar 

  • Dubey JP, Wilpe E, Blignaut DJC, Schares G, Williams JH (2013) Development of early tissue cysts and associated pathology of Besnoitia besnoiti in a naturally infected bull (Bos taurus) from South Africa. J Parasitol 99:459–466

    Article  PubMed  CAS  Google Scholar 

  • EFSA (2010) European Food Safety Authority—bovine besnoitiosis: an emerging disease in Europe. EFSA J 8:1499

    Google Scholar 

  • Fernandez-Garcia A, Risco-Castillo V, Pedraza-Diaz S, Aguado-Martinez A, Alvarez-Garcia G, Gomez-Bautista M, Collantes-Fernandez E, Ortega-Mora LM (2009) First isolation of Besnoitia besnoiti from a chronically infected cow in Spain. J Parasitol 95:474–476

    Article  PubMed  CAS  Google Scholar 

  • Frey CF et al (2013) Chronic bovine besnoitiosis: intra-organ parasite distribution, parasite loads and parasite-associated lesions in subclinical cases. Vet Parasitol 197:95–103

    Article  PubMed  CAS  Google Scholar 

  • Froelich S, Entzeroth R, Wallach M (2012) Comparison of protective immune responses to apicomplexan parasites. J Parasitol Res 2012:852591

    Google Scholar 

  • Gentile A, Militerno G, Bassi P, Schares G, Majzoub M, Gollnick NS (2010) Su di un episodio di besnoitiosi bovina in Italia. Buiatria J Ital Ass Buiatrics 5:3–15

    Google Scholar 

  • Gentile A, Militerno G, Schares G, Nanni A, Testoni S, Bassi P, Gollnick NS (2012) Evidence for bovine besnoitiosis being endemic in Italy—first in vitro isolation of Besnoitia besnoiti from cattle born in Italy. Vet Parasitol 184:108–115

    Article  PubMed  CAS  Google Scholar 

  • Ghadially FN (1988) Ultrastructural pathology of the cell and matrix, vol II, 3rd edn. Butterworths, London

    Google Scholar 

  • Goebel E, Widauer R, Reimann M, Munz E (1985) Ultrastructure of the asexual multiplication of Besnoitia besnoiti (Marotel, 1912) in Vero- and CRFK-cell cultures. Zentralbl Veterinarmed B 32:202–212

    Article  Google Scholar 

  • Gollnick NS, Scharr JC, Schares G, Langenmayer MC (2014) Natural Besnoitia besnoiti infections in cattle: chronology of disease progression. BMC Vet Res accepted

  • Heydorn AO, Senaud J, Mehlhorn H, Heinonen R (1984) Besnoitia sp. from goats in Kenya. Z Parasitenkd 70:709–713

    Article  PubMed  CAS  Google Scholar 

  • Hornok S, Fedak A, Baska F, Hofmann-Lehmann R, Basso W (2014) Bovine besnoitiosis emerging in Central-Eastern Europe, Hungary. Parasit Vectors 7:20

    Article  PubMed Central  PubMed  Google Scholar 

  • Jacquiet P, Lienard E, Franc M (2010) Bovine besnoitiosis: epidemiological and clinical aspects. Vet Parasitol 174:30–36

    Article  PubMed  CAS  Google Scholar 

  • Kumi-Diaka J, Wilson S, Sanusi A, Njoku CE, Osori DI (1981) Bovine besnoitiosis and its effect on the male reproductive system. Theriogenology 16:523–530

    Article  PubMed  CAS  Google Scholar 

  • Langenmayer MC, Gollnick NS, Majzoub-Altweck M, Scharr JC, Schares G, Hermanns W (2014) Naturally acquired bovine besnoitiosis: histological and immunohistochemical findings in acute, subacute and chronic disease. Vet Pathol. doi:10.1177/0300985814541705

    PubMed  Google Scholar 

  • Lesser M, Braun U, Deplazes P, Gottstein B, Hilbe M, Basso W (2012) First cases of besnoitiosis in cattle in Switzerland. Schweiz Arch Tierheilkd 154:469–474

    Article  PubMed  CAS  Google Scholar 

  • Majzoub M, Breuer W, Gollnick NS, Rostaher A, Schares G, Hermanns W (2010) Ein Ausbruch von Besnoitiose bei Rindern in Deutschland: pathomorphologische, ultrastrukturelle und molekularbiologische Untersuchungen. Wien Tieraerztl Mschr 97:9–15

    Google Scholar 

  • McCully RM, Basson PA, Van Niekerk JW, Bigalke RD (1966) Observations on Besnoitia cysts in the cardiovascular system of some wild antilopes and domestic cattle. Onderstepoort J Vet Res 33:245–276

    Google Scholar 

  • Mehlhorn H, Klimpel S, Schein E, Heydorn AO, Al-Quraishy S, Selmair J (2009) Another African disease in Central Europa: besnoitiosis of cattle. I. Light and electron microscopical study. Parasitol Res 104:861–868

    Article  PubMed  Google Scholar 

  • Njenga JM, Bwangamoi O, Kangethe EK, Mugera GM, Mutiga ER (1995) Comparative ultrastructural studies on Besnoitia besnoiti and Besnoitia caprae. Vet Res Commun 19:295–308

    Article  PubMed  CAS  Google Scholar 

  • Nobel TA, Klopfer U, Perl S, Nyska A, Neumann M, Brenner G (1981) Histopathology of genital besnoitiosis of cows in Israel. Vet Parasitol 8:271–276

    Article  Google Scholar 

  • Pols JW (1960) Studies on bovine besnoitiosis with special reference to the aetiology. Onderstepoort J Vet Res 28:265–356

    Google Scholar 

  • Rostaher A, Mueller RS, Majzoub M, Schares G, Gollnick NS (2010) Bovine besnoitiosis in Germany. Vet Dermatol 21:329–339

    PubMed  Google Scholar 

  • Schares G, Basso W, Majzoub M, Cortes HC, Rostaher A, Selmair J, Hermanns W, Conraths FJ, Gollnick NS (2009) First in vitro isolation of Besnoitia besnoiti from chronically infected cattle in Germany. Vet Parasitol 163:315–322

    Article  PubMed  CAS  Google Scholar 

  • Schares G et al (2013) Novel tools for the diagnosis and differentiation of acute and chronic bovine besnoitiosis. Int J Parasitol 43:143–154

    Article  PubMed  CAS  Google Scholar 

  • Schoenthal AH (2012) Endoplasmic reticulum stress: its role in disease and novel prospects for therapy. Scientifica

  • Scholtyseck E, Mehlhorn H (1970) Ultrastructural study of characteristic organelles (paired organelles, micronemes, micropores) of sporozoa and related organisms. Z Parasitenkd 34:97–127

    PubMed  CAS  Google Scholar 

  • Scholtyseck E, Mehlhorn H, Muller BE (1973) Identification of merozoites of 4 cyst-forming Coccidia (Sarcocystis, Toxoplasma, Besnoitia, Frenkelia) by means of electron microscopy. Z Parasitenkd 42:185–206

    Article  PubMed  CAS  Google Scholar 

  • Scholtyseck E, Mehlhorn H, Müller BEG (1974) Feinstruktur der Cyste und Cystenwand von Sarcocystis tenella, Besnoitia jellisoni, Frenkelia sp. und Toxoplasma gondii. J Protozool 21:284–294

    Article  Google Scholar 

  • Schulz KCA (1960) A report on naturally acquired besnoitiosis with special reference to its pathology. J S Afr Vet Med Assoc 31:21–35

    Google Scholar 

  • Shkap V, Yakobson BA, Pipano E (1988) Transmission and scanning electron microscopy of Besnoitia besnoiti. Int J Parasitol 18:761–766

    Article  PubMed  CAS  Google Scholar 

  • Shkap V, Matuschka FR, Yakobson B, Perl S, Frank M, Pipano E (1995) Differentiating between Besnoitia besnoiti from cattle and Sarcocystis hoarensis from rodents. Parasitol Res 81:490–493

    Article  PubMed  CAS  Google Scholar 

  • Speer CA, Dubey JP, McAllister MM, Blixt JA (1999) Comparative ultrastructure of tachyzoites, bradyzoites, and tissue cysts of Neospora caninum and Toxoplasma gondii. Int J Parasitol 29:1509–1519

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We acknowledge the excellent technical assistance of Claudia Mair, Heidrun Schoel and Angela Siebert. Furthermore, we would like to thank Maite Schneider for the schematic drawings. NSG was supported by the BGF research stipend provided by the German State of Bavaria.

Conflict of interest

The authors declared no potential conflicts of interest. Prionics AG, Schlieren, Switzerland, funded parts of the study but had no influence on the design of the experiment, data collection and analysis and was not involved in writing the manuscript.

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Langenmayer, M.C., Gollnick, N.S., Scharr, J.C. et al. Besnoitia besnoiti infection in cattle and mice: ultrastructural pathology in acute and chronic besnoitiosis. Parasitol Res 114, 955–963 (2015). https://doi.org/10.1007/s00436-014-4261-6

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