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Ancient, globally distributed lineage of Sarcocystis from sporocysts of the Eastern rat snake (Pantherophis alleghaniensis) and its relation to neurological sequalae in intermediate hosts

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Abstract

There is an emerging concern that snakes are definitive hosts of certain species of Sarcocystis that cause muscular sarcocystosis in human and non-human primates. Other species of Sarcocystis are known to cycle among snakes and rodents, but have been poorly characterized in the USA and elsewhere. Although neurological sequalae are known for certain species of Sarcocystis, no such neurological symptoms are known to typify parasites that naturally cycle in rodents. Here, sporocysts of a species of Sarcocystis were found in the intestinal contents of a rat snake (Pantherophis alleghaniensis) from Maryland, USA. The sporocysts were orally infective for interferon gamma gene knockout (KO) mice, but not to Swiss Webster outbred mice. The KO mice developed neurological signs, and were necropsied between 33 and 52 days post-inoculation. Only schizonts/merozoites were found, and they were confined to the brain. The predominant lesion was meningoencephalitis characterized by perivascular cuffs, granulomas, and necrosis of the neuropil. The schizonts and merozoites were located in neuropil, and apparently extravascular. Brain homogenates from infected KO mice were infective to KO mice and CV-1 cell line. DNA extracted from the infected mouse brain, and infected cell cultures revealed the highest identity with Sarcocystis species that employ snakes as definitive hosts. This is the first report of Sarcocystis infection in the endangered rat snake (P. alleghaniensis) and the first report of neurological sarcocystosis in mice induced by feeding sporocysts from a snake. These data underscore the likelihood that parasites in this genus that employ snakes as their definitive hosts constitute an ancient, globally distributed monophyletic group. These data also raise the possibility that neurological sequalae may be more common in intermediate hosts of Sarcocystis spp. than has previously been appreciated.

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References

  • Abubakar S, Teoh BT, Sam SS, Chang LY, Johari J, Hooi PS, Lakhbeer-Singh HK, Italiano CM, Syed Omar SF, Wong KT, Ramli N, Tan CT (2013) Outbreak of human infection with Sarcocystis nesbitti, Malaysia, 2012. Emerg Infect Dis 19:1989–1991

    Article  PubMed  PubMed Central  Google Scholar 

  • Arness MK, Brown JD, Dubey JP, Neafie RC, Granstrom DE (1999) An outbreak of acute eosinophilic myositis attributed to human Sarcocystis parasitism. Am J Trop Med Hyg 61:548–553

    CAS  PubMed  Google Scholar 

  • Conant R, Collins (1998) A field guide to reptile and amphibians: eastern north america. Houghton Mifflin Company, Boston

    Google Scholar 

  • Dolezel D, Koudela B, Jirku M, Hypsa V, Obornik M, Votypka J, Modry D, Slapeta JR, Lukes J (1999) Phylogenetic analysis of Sarcocystis spp. of mammals and reptiles supports the coevolution of Sarcocystis spp. with their final hosts. Int J Parasitol 29:795–798

    Article  CAS  PubMed  Google Scholar 

  • Dubey JP, Hamir AN (2000) Immunohistochemical confirmation of Sarcocystis neurona infections in raccoons, mink, cat, skunk and pony. J Parasitol 86:1150–1152

    Article  CAS  PubMed  Google Scholar 

  • Dubey JP, Mattson DE, Speer CA, Baker RJ, Mulrooney DM, Tornquist SJ, Hamir AN, Gerros TC (1999) Characterization of Sarcocystis neurona isolate (SN6) from a naturally infected horse from Oregon. J Eukaryot Microbiol 46:500–506

    Article  CAS  PubMed  Google Scholar 

  • Dubey JP, Calero-Bernal R, Rosenthal BM, Speer CA, Fayer R (2016) Sarcocystosis of Animals and Humans, 2nd edn. CRC Press, Boca Raton

  • Esposito DH, Freedman DO, Neumayr A, Parola P (2012) Ongoing outbreak of an acute muscular Sarocystis-like illness among travellers returning from Tioman Island, Malaysia, 2011–2012. Euro Surveill 17:

  • Gjerde B (2013) Phylogenetic relationships among Sarcocystis species in cervids, cattle and sheep inferred from the mitochondrial cytochrome c oxidase subunit I gene. Int J Parasitol 43:579–591

    Article  CAS  PubMed  Google Scholar 

  • Gjerde B, Josefsen TD (2015) Molecular characterisation of Sarcocystis lutrae n. sp. and Toxoplasma gondii from the musculature of two Eurasian otters (Lutra lutra) in Norway. Parasitol Res 114:873–886

    Article  PubMed  Google Scholar 

  • Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321

    Article  CAS  PubMed  Google Scholar 

  • Hu JJ, Ma TC, Li XR (2005) A new species of sarcocysts (Sporozoea, Eucoccidiida) from Rattus norvegicus. Acta Zootaxon Sin 30:287–290

    Google Scholar 

  • Hu JJ, Meng Y, Guo YM, Liao JY, Song JL (2012) Completion of the life cycle of Sarcocystis zuoi, a parasite from the Norway rat, Rattus norvegicus. J Parasitol 98:550–553

    Article  PubMed  Google Scholar 

  • Hu JJ, Liu Q, Yang YF, Esch GW, Guo YM, Zou FC (2014) Sarcocystis eothenomysi n. sp. (Apicomplexa: Sarcocystidae) from the large oriental vole Eothenomys miletus (Thomas) (Cricetidae: Microtinae) from Anning, China. Syst Parasitol 89:73–81

    Article  PubMed  Google Scholar 

  • Hu JJ, Liu TT, Liu Q, Esch GW, Chen JQ (2015) Sarcocystis clethrionomyelaphis Matuschka, 1986 (Apicomplexa: Sarcocystidae) infecting the large oriental vole Eothenomys miletus (Thomas) (Cricetidae: Microtinae) and its phylogenetic relationships with other species of Sarcocystis Lankester, 1882. Syst Parasitol 91:273–279

    Article  PubMed  Google Scholar 

  • Italiano CM, Wong KT, Abubakar S, Lau YL, Ramli N, Syed Omar SF, Kahar BM, Tan CT (2014) Sarcocystis nesbitti causes acute, relapsing febrile myositis with a high attack rate: description of a large outbreak of muscular sarcocystosis in Pangkor Island, Malaysia, 2012. PLoS Negl Trop Dis 8:e2876

    Article  PubMed  PubMed Central  Google Scholar 

  • Jinnai M, Kawabuchi-Kurata T, Tsuji M, Nakajima M, Fujisawa K, Nagata S, Koide H, Matoba Y, Asakawa M, Takahashi K, Ishihara C (2009) Molecular evidence for the presence of new Babesia species in feral raccoons (Procyon lotor) in Hokkaido, Japan. Vet Parasitol 162:241–247

    Article  CAS  PubMed  Google Scholar 

  • Lau YL, Chang PY, Subramaniam V, Ng YH, Mahmud R, Ahmad AF, Fong MY (2013) Genetic assemblage of Sarcocystis spp. in Malaysian snakes. Parasit Vectors 6:257

    Article  PubMed  PubMed Central  Google Scholar 

  • Lau YL, Chang PY, Tan CT, Fong MY, Mahmud R, Wong KT (2014) Sarcocystis nesbitti infection in human skeletal muscle: possible transmission from snakes. Am J Trop Med Hyg 90:361–364

    Article  PubMed  PubMed Central  Google Scholar 

  • More G, Pantchev N, Herrmann DC, Vrhovec MG, Ofner S, Conraths FJ, Schares G (2014) Molecular identification of Sarcocystis spp. helped to define the origin of green pythons (Morelia viridis) confiscated in Germany. Parasitology 141:646–651

    Article  CAS  PubMed  Google Scholar 

  • Slapeta JR, Modry D, Koudela B (1999) Sarcocystis atheridis sp. nov., a new sarcosporidian coccidium from Nitsche’s bush viper, Atheris nitschei Tornier, 1902, from Uganda. Parasitol Res 85:758–764

    Article  CAS  PubMed  Google Scholar 

  • Yang ZQ, Wei CG, Zen JS, Song JL, Zuo YX, He YS, Zhang HF, Attwood SW, Chen XW, Yang GC, Zhou X, Quan X, Li CY, Han D, Liu AW, Lin P (2005) A taxonomic re-appraisal of Sarcocystis nesbitti (Protozoa: Sarcocystidae) from the monkey Macaca fascicularis in Yunnan, PR China. Parasitol Int 54:75–81

    Article  PubMed  Google Scholar 

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Correspondence to Jitender P. Dubey.

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All investigations reported here were approved by the institutional animal care and use protocol committee of the US Department of Agriculture.

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Verma, S.K., Lindsay, D.S., Rosenthal, B.M. et al. Ancient, globally distributed lineage of Sarcocystis from sporocysts of the Eastern rat snake (Pantherophis alleghaniensis) and its relation to neurological sequalae in intermediate hosts. Parasitol Res 115, 2697–2704 (2016). https://doi.org/10.1007/s00436-016-5086-2

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  • DOI: https://doi.org/10.1007/s00436-016-5086-2

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