Diversity of microsporidia, Cryptosporidium and Giardia in mountain gorillas (Gorilla beringei beringei) in Volcanoes National Park, Rwanda

. 2014 ; 9 (11) : e109751. [epub] 20141111

Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid25386754

BACKGROUND: Infectious diseases represent the greatest threats to endangered species, and transmission from humans to wildlife under increased anthropogenic pressure has been always stated as a major risk of habituation. AIMS: To evaluate the impact of close contact with humans on the occurrence of potentially zoonotic protists in great apes, one hundred mountain gorillas (Gorilla beringei beringei) from seven groups habituated either for tourism or for research in Volcanoes National Park, Rwanda were screened for the presence of microsporidia, Cryptosporidium spp. and Giardia spp. using molecular diagnostics. RESULTS: The most frequently detected parasites were Enterocytozoon bieneusi found in 18 samples (including genotype EbpA, D, C, gorilla 2 and five novel genotypes gorilla 4-8) and Encephalitozoon cuniculi with genotype II being more prevalent (10 cases) compared to genotype I (1 case). Cryptosporidium muris (2 cases) and C. meleagridis (2 cases) were documented in great apes for the first time. Cryptosporidium sp. infections were identified only in research groups and occurrence of E. cuniculi in research groups was significantly higher in comparison to tourist groups. No difference in prevalence of E. bieneusi was observed between research and tourist groups. CONCLUSION: Although our data showed the presence and diversity of important opportunistic protists in Volcanoes gorillas, the source and the routes of the circulation remain unknown. Repeated individual sampling, broad sampling of other hosts sharing the habitat with gorillas and quantification of studied protists would be necessary to acquire more complex data.

Department of Pathology and Parasitology Faculty of Veterinary Medicine University of Veterinary and Pharmaceutical Sciences Brno Czech Republic

Faculty of Science University of South Bohemia in České Budějovice České Budějovice Czech Republic

Gorilla Doctors Karen C Drayer Wildlife Health Center Davis CA United States of America

Institute of Parasitology Biology Centre of the Academy of Sciences of the Czech Republic v v i České Budějovice Czech Republic

Institute of Parasitology Biology Centre of the Academy of Sciences of the Czech Republic v v i České Budějovice Czech Republic; Department of Pathology and Parasitology Faculty of Veterinary Medicine University of Veterinary and Pharmaceutical Sciences Brno Czech Republic; CEITEC Central European Institute of Technology University of Veterinary and Pharmaceutical Sciences Brno Czech Republic

Institute of Parasitology Biology Centre of the Academy of Sciences of the Czech Republic v v i České Budějovice Czech Republic; Faculty of Agriculture University of South Bohemia in České Budějovice České Budějovice Czech Republic

Institute of Parasitology Biology Centre of the Academy of Sciences of the Czech Republic v v i České Budějovice Czech Republic; Institute of Vertebrate Biology Academy of Sciences of the Czech Republic v v i Brno Czech Republic; Liberec Zoo Liberec Czech Republic; Department of Pathology and Parasitology Faculty of Veterinary Medicine University of Veterinary and Pharmaceutical Sciences Brno Czech Republic

Rwanda Development Board Kigali Rwanda

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Nizeyi JB, Mwebe R, Nanteza A, Cranfield MR, Kalema GR, et al. (1999) Cryptosporidium sp. and Giardia sp. infections in mountain gorillas (Gorilla gorilla beringei) of the Bwindi Impenetrable National Park, Uganda. J Parasitol 85: 1084–1088. PubMed

Graczyk TK, Bosco-Nizeyi J, da Silva AJ, Moura INS, Pieniazek NJ, et al. (2002a) A single genotype of Encephalitozoon intestinalis infects free-ranging gorillas and people sharing their habitats in Uganda. Parasitol Res 88: 926–931. PubMed

Graczyk TK, Bosco-Nizeyi J, Ssebide B, Thompson RCA, Read C, et al. (2002b) Anthropozoonotic Giardia duodenalis genotype (assemblage) A infections in habitats of free-ranging human-habituated gorillas, Uganda. J Parasitol 88: 905–909. PubMed

Salzer JS, Rwego IB, Goldberg TL, Kuhlenschmidt MS, Gillespie TR (2007) Giardia sp. and Cryptosporidium sp infections in primates in fragmented and undisturbed forest in western Uganda. J Parasitol 93: 439–440. PubMed

Sak B, Kváč M, Petrželková K, Květoňová D, Pomajbíková K, et al. (2011c) Diversity of microsporidia (Fungi: Microsporidia) among captive great apes in European zoos and African sanctuaries: evidence for zoonotic transmission? Folia Parasitol 58: 81–86. PubMed

Weber R, Kuster H, Keller R, Bächi T, Spycher MA, et al. (1992) Pulmonary and intestinal microsporidiosis in a patient with the acquired immunodeficiency syndrome. Am Rev Respir Dis 146: 1603–1605. PubMed

Stark D, Barratt JL, van Hal S, Marriott D, Harkness J, et al. (2009) Clinical significance of enteric protozoa in the immunosuppressed human population. Clin Microbiol Rev 22: 634–650. PubMed PMC

Didier ES, Weiss LM (2006) Microsporidiosis: Current status. Curr Opin Infect Dis 19: 485–492. PubMed PMC

Gillespie TR, Morgan D, Deutsch JC, Kuhlenschmidt MS, Salzer JS, et al. (2009) A legacy of low-impact logging does not elevate prevalence of potentially pathogenic protozoa in free-ranging gorillas and chimpanzees in the Republic of Congo: logging and parasitism in African apes. Ecohealth 6: 557–564. PubMed PMC

Nizeyi JB, Cranfield MR, Graczyk TK (2002) Cattle near the Bwindi Impenetrable National Park, Uganda, as a reservoir of Cryptosporidium parvum and Giardia duodenalis for local community and free-ranging gorillas. Parasitol Res 88: 380–385. PubMed

Salyer SJ, Gillespie TR, Rwego IB, Chapman CA, Goldberg TL (2012) Epidemiology and molecular relationships of Cryptosporidium spp. in people, primates, and livestock from Western Uganda. PLoS Negl Trop Dis 6: e1597. PubMed PMC

Sak B, Petrželková KJ, Květoňová D, Mynářová A, Shutt KA, et al. (2013) Long-term monitoring of microsporidia, Cryptosporidium and Giardia infections in western lowland gorillas (Gorilla gorilla gorilla) at different stages of habituation in Dzanga Sangha Protected Areas, Central African Republic. PlosOne 8: e71840. PubMed PMC

Thompson RCA (2004) Epidemiology and zoonotic potential of Giardia infections. In: Sterling CR, Adam RD (eds.) World Class Parasites, Vol 8: The Pathogenic Enteric Protozoa: Giardia, Entamoeba, Cryptosporidium and Cyclospora, 1–14. Boston, Kluwer Academic Publishers, 169.

Mathis A, Weber R, Deplazes P (2005) Zoonotic potential of the Microsporidia. Clin Microbiol Rev 18: 423–445. PubMed PMC

Franzen C (2008) Microsporidia: a review of 150 years of research. Open Parasitol J 2: 1–34.

Waldron LS, Cheung-Kwok-Sang C, Power ML (2010) Wildlife-associated Cryptosporidium fayeri in human, Australia. Emerg Infect Dis 16: 2006–2007. PubMed PMC

Johnston AR, Gillespie TR, Rwego IB, McLachlan TL, Kent AD, et al. (2010) Molecular epidemiology of cross-species Giardia duodenalis transmission in western Uganda. PloS Negl Trop Dis 4: e683. PubMed PMC

Liu W, Li Y, Learn GH, Rudicell RS, Robertson JD, et al. (2010) Origin of the human malaria parasite Plasmodium falciparum in gorillas. Nature 467: 420–425. PubMed PMC

Petrášová J, Uzlíková M, Kostka M, Petrželková KJ, Huffman MA, et al. (2011) Diversity and host specificity of Blastocystis in syntopic primates on Rubondo Island, Tanzania. Int J Parasitol 41: 1113–1120. PubMed

Caldecott J, Miles L (2005) World atlas of great apes and their conservation. Berkeley: Univ California Press. 456 p.

Robbins M, Gray M, Kümpel N, Lanjouw A, Maisels F, et al.. (2008) Gorilla beringei ssp. beringei In: IUCN 2013. IUCN Red List of Threatened Species. Version 2013.1. www.iucnredlist.org.

Maekawa M, Lanjouw A, Rutagarama E, Sharp D (2013) Mountain gorilla tourism generating wealth and peace in post-conflict Rwanda. Natural Resources Forum 37: 127–137.

Williamson EA, Feistner ATC (2003) Habituating primates: processes, techniques, variables and ethics. In: Setchell JM, Curtis DJ (eds.) Field and laboratory methods in primatology: a practical guide. Cambridge University Press, Cambridge, UK, 25–39.

Butynski TM, Kalina J (1998) Gorilla tourism: a critical look. In: Milner-Gulland EJ, Mace R (eds.) Conservation of biological resources. Oxford: Blackwell Science, 294–385.

Goldsmith ML (2000) Effects of ecotourism on the behavioral ecology of Bwindi gorillas, Uganda: Preliminairy results. Am J Phys Anthropol Suppl 30: 161

Goldsmith ML (2005) Impacts of habituation for ecotourism on the gorillas of Nkuringo. Gorilla J 30: 14–15.

Woodford MH, Butynski TM, Karesh WB (2002) Habituating the great apes: the disease risks. Oryx 36: 153–160.

Williamson EA, Fawcett KA (2008) Long-term research and conservation of the Virunga mountain gorillas. In: Wrangham R, Ross E (eds.) Science and Conservation in African Forests: The Benefits of Long-term Research. Cambridge University Press, Cambridge, UK, 213–229.

Klailova M, Hodgkinson C, Lee PC (2010) Behavioral responses of one western lowland gorilla (Gorilla gorilla gorilla) group at Bai Hokou, Central African Republic, to tourists, researchers and trackers. Am J Primatol 72: 897–906. PubMed

Gillespie TR, Nunn CL, Leendertz FH (2008) Integrative approaches to the study of primate infectious disease: implications for biodiversity conservation and global health. Am J Phys Anthropol. 47: 53–69. PubMed

Zommers Z, McDonald DW, Johnson PJ, Gillespie TR (2013) Impact of human activities on chimpanzee ground use and parasitism (Pan troglodytes) Konserv Letters. 6: 264–273.

Sleeman JM, Meader LL, Mudakikwa AB, Foster JW, Patton S (2000) Gastrointestinal parasites of mountain gorillas (Gorilla gorilla beringei) in the Parc National des Volcans, Rwanda. J Zoo Wildl Med 31: 322–328. PubMed

Graczyk TK, da Silva AJ, Cranfield MR, Nizeyi JB, Kalema GRNN, et al. (2001) Cryptosporidium parvum Genotype 2 infections in free-ranging mountain gorillas (Gorilla gorilla beringei) of the Bwindi Impenetrable National Park, Uganda. Parasitol Res 87: 368–370. PubMed

Hogan JN, Miller WA, Cranfield MR, Ramer J, Hassell J, et al. (2014) Giardia in mountain gorillas (Gorilla beringei beringei), forest buffalo (Syncerus caffer), and domestic cattle in Volcanoes National Park, Rwanda. J Wildl Dis 50: 21–30. PubMed

Vedder AL (1984) Movement patterns of a group of free-ranging mountain gorillas (Gorilla gorilla beringei) and their relation to food availability. Am J Primatol 7: 73–88. PubMed

Watts DP (1984) Composition and variability of mountain gorilla diets in the Central Virungas. Am J Primatol 7: 323–356. PubMed

Gray M, Kalpers J (2005) Ranger based monitoring in the Virunga-Bwindi region of East-Central Africa: A simple data collection tool for park management. Biodivers Conserv 14: 2723–2741.

Harcourt AH, Parks SA, Woodroffe R (2001) Human density as an influence on species/area relationships: double jeopardy for small African reserves? Biodivers Conserv 10: 1011–1026.

Robbins M, Williamson L (2008) Gorilla beringei In: IUCN 2013. IUCN Red List of Threatened Species. Version 2013.2. www.iucnredlist.org.

Plumptre AJ, Williamson EA (2001) Conservation-oriented research in the Virunga region. In: Robbins MM, Sicotte P, Stewart KJ (eds.) Mountain gorillas: three decades of research at Karisoke. Cambridge: Cambridge University Press. 361–390.

Mudakikwa AB, Cranfield MR, Sleeman JM, Eilenberger U (2001) Clinical medicine, preventive health care and research on mountain gorillas in the Virunga Volcanoes region. In: Robbins MM, Sicotte P, Stewart KJ (eds.) Mountain gorillas: three decades of research at Karisoke. Cambridge: Cambridge University Press. 341–360.

Rwanda Development Board (2011) Highlights on National Parks Visitation in Rwanda - January–March 2011. Unpublished Report. Available: http://www.rdb.rw/fileadmin/user_upload/Documents/tourism%20conservation/RDB_Parks_Statistics_2011.pdf.

Buckholt MA, Lee JH, Tzipori S (2002) Prevalence of Enterocytozoon bieneusi in swine: an 18-month survey at a slaughterhouse in Massachusetts. Appl Environ Microbiol 68: 2595–2599. PubMed PMC

Jiang J, Alderisio KA, Xiao L (2005) Distribution of Cryptosporidium genotypes in storm ebeny water samples from three watersheds in New York. Appl Environ Microbiol 71: 4446–4454. PubMed PMC

Sulaiman IM, Fayer R, Bern C, Gilman RH, Trout JM, et al. (2003) Triosephosphate isomerase gene characterization and potential zoonotic transmission of Giardia duodenalis . Emerg Infect Dis 9: 1444–1452. PubMed PMC

Didier ES, Vossbrinck CR, Baker MD, Rogers LB, Bertucci DC, et al. (1995) Identification and characterization of three Encephalitozoon cuniculi strains. Parasitology 111: 411–421. PubMed

Katzwinkel-Wladarsch S, Lieb M, Heise W, Löscher T, Rinder H (1996) Direct amplification and species determination of microsporidian DNA from stool specimens. Trop Med Int Health 1: 373–378. PubMed

Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731–2739. PubMed PMC

R Development Core Team (2011) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/.

Breitenmoser AC, Mathis A, Burgi E, Weber R, Deplazes P (1999) High prevalence of Enterocytozoon bieneusi in swine with four genotypes that differ from those identified in humans. Parasitology 11: 447–453. PubMed

Rinder H, Dengjel B, Gothe R, Loscher T (2000) Microsporidosis of man: where is the reservoir? Mitt Osterr Ges Trop Med Parasitol 22: 1–6.

Li W, Kiulia NM, Mwenda JM, Nyachieo A, Taylor MB, et al. (2011) Cyclospora papionis, Cryptosporidium hominis, and human-pathogenic Enterocytozoon bieneusi in captive baboons in Kenya. J Clin Microbiol 49: 4326–4329. PubMed PMC

Sak B, Brady D, Pelikánová M, Květoňová D, Rost M, et al. (2011a) Unapparent microsporidial infection among immunocompetent humans in the Czech Republic. J Clin Microbiol 49: 1064–1070. PubMed PMC

Santín M, Fayer R (2011) Microsporidiosis: Enterocytozoon bieneusi in domesticated and wild animals. Res Vet Sci 90: 363–371. PubMed

Thellier M, Breton J (2008) Enterocytozoon bieneusi in human and animals, focus on laboratory identification and molecular epidemiology. Parasite 15: 349–358. PubMed

Canning EU, Hollister WS (1987) Microsporidia of mammals – widespread pathogens or opportunistic curiosities? Parasitol Today 3: 267–273. PubMed

Reetz J (1993) Naturally-acquired microsporidia (Encephalitozoon cuniculi) infections in hens. Tierarztl Prax 21: 429–435. PubMed

Kašičková D, Sak B, Kváč M, Ditrich O (2009) Sources of potentially infectious human microsporidia: molecular characterisation of microsporidia isolates from exotic birds in the Czech Republic prevalence study and importance of birds in epidemiology of the human microsporidial infections. Vet Parasitol 165: 125–130. PubMed

Wagnerová P, Sak B, Květoňová D, Buňatová Z, Civišová H, et al. (2012) Enterocytozoon bieneusi and Encephalitozoon cuniculi in horses kept under different management systems in the Czech Republic. Vet Parasitol 190: 573–577. PubMed

Hofmannová L, Sak B, Jekl V, Mináriková A, Skorič M, et al. (2014) Lethal Encephalitozoon cuniculi genotype III infection in Steppe lemmings (Lagurus lagurus). Vet Parasitol 205: 357–360. PubMed

Tanriverdi S, Arslan MO, Akiyoshi DE, Tzipori S, Widmer G (2003) Identification of genotypically mixed Cryptosporidium parvum populations in humans and calves. Mol Biochem Parasitol 130: 13–22. PubMed

Sak B, Kašičková D, Kváč M, Květoňová D, Ditrich O (2010) Microsporidia in exotic birds: intermittent spore excretion of Encephalitozoon spp. in naturally infected budgerigars (Melopsittacus undulatus). Vet Parasitol 168: 196–200. PubMed

Sak B, Kváč M, Kučerová Z, Květoňová D, Saková K (2011b) Latent microsporidial infection in immunocompetent individuals - a longitudinal study. PLoS Negl Trop Dis 5: e1162. PubMed PMC

Kotková M, Sak B, Květoňová D, Kváč M (2013) Latent microsporidiosis caused by Encephalitozoon cuniculi in immunocompetent hosts: using murine model demonstrated the ineffectiveness of immune system and the treatment with albendazole. PloS One 8: e60941. PubMed PMC

Ryan U, Xiao L, Read C, Zhou L, Lal AA, et al. (2003) Identification of novel Cryptosporidium genotypes from the Czech Republic. Appl Environ Microbiol 69: 4302–4307. PubMed PMC

Ng J, Pavlásek I, Ryan U (2006) Identification of novel Cryptosporidium genotypes from avian hosts. Appl Environ Microbiol 72: 7548–7553. PubMed PMC

Qi M, Wang R, Ning C, Li X, Zhang L, et al. (2011) Cryptosporidium spp. in pet birds: genetic diversity and potential public health significance. Exp Parasitol 128: 336–340. PubMed

Kodádková A, Kváč M, Ditrich O, Sak B, Xiao L (2010) Cryptosporidium muris in a reticulated giraffe (Giraffa camelopardalis reticulata). J Parasitol 96: 211–212. PubMed

Dubey JP, Markovits JE, Killary KA (2002) Cryptosporidium muris-like infection in stomach of cynomolgus monkeys (Macaca fascicularis). Vet Pathol 39: 363–371. PubMed

Robinson G, Elwin K, Chalmers RM (2008) Unusual Cryptosporidium genotypes in human cases of diarrhea. Emerg Infect Dis 14: 1800–1802. PubMed PMC

Kváč M, Květoňová D, Sak B, Ditrich O (2009) Cryptosporidium pig genotype II in immunocompetent man. Emerg Infect Dis 15: 982–983. PubMed PMC

Nichols G (2008) Epidemiology. In: Fayer R, Xiao L (eds.) Cryptosporidium and cryptosporidiosis. CRC Press, Boca Raton, 79–118.

Katsumata T, Hosea D, Ranuh IG, Uga S, Yanagi T, et al. (2000) Short report: possible Cryptosporidium muris infection in humans. Am J Trop Med Hyg 62: 70–72. PubMed

Gatei W, Ashford RW, Beeching NJ, Kamwati SK, Greensill J, et al. (2002) Cryptosporidium muris infection in an HIV-infected adult, Kenya. Emerg Infect Dis 8: 204–206. PubMed PMC

Gatei W, Greensill J, Ashford RW, Cuevas LE, Parry CM, et al. (2003) Molecular analysis of the 18 S rRNA gene of Cryptosporidium parasites from patients with or without human immunodeficiency virus infections living in Kenya, Malawi, Brazil, the United Kingdom, and Vietnam. J Clin Microbiol 41: 1458–1462. PubMed PMC

Gatei W, Wamae CN, Mbae C, Waruru A, Mulinge E, et al. (2006) Cryptosporidiosis: prevalence, genotype analysis, and symptoms associated with infections in children in Kenya. Am J Trop Med Hyg 75: 78–82. PubMed

Muthusamy D, Rao SS, Ramani S, Monica B, Banerjee I, et al. (2006) Multilocus genotyping of Cryptosporidium sp. isolates from human immunodeficiency virus infected individuals in South India. J Clin Microbiol 44: 632–634. PubMed PMC

Owiunji I, Nkuutu D, Kujirakwinja D, Liengola I, Plumptre AJ, et al.. (2005) Biodiversity survey of the Virunga Volcanoes. Unpublished Report by WCS. www.albertinerift.org.

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