Identification of potentially zoonotic parasites in captive orangutans and semi-captive mandrills: Phylogeny and morphological comparison
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
36776131
DOI
10.1002/ajp.23475
Knihovny.cz E-zdroje
- Klíčová slova
- Balantioides coli, Buxtonella-like, Mandrillus sphinx, Pongo abelii, Pongo pygmaeus, Strongyloides stercoralis, molecular phylogeny, semi-captive animals, zoo animals,
- MeSH
- fylogeneze MeSH
- lidé MeSH
- Mandrillus * MeSH
- paraziti * genetika MeSH
- Pongo pygmaeus MeSH
- Pongo genetika MeSH
- primáti genetika MeSH
- psi MeSH
- ribozomální DNA genetika MeSH
- zvířata MeSH
- Check Tag
- lidé MeSH
- psi MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- ribozomální DNA MeSH
Cysts and trophozoites of vestibuliferid ciliates and larvae of Strongyloides were found in fecal samples from captive orangutans Pongo pygmaeus and P. abelii from Czech and Slovak zoological gardens. As comparative material, ciliates from semi-captive mandrills Mandrillus sphinx from Gabon were included in the study. Phylogenetic analysis of the detected vestibuliferid ciliates using ITS1-5.8s-rRNA-ITS2 and partial 18S ribosomal deoxyribonucleic acid (rDNA) revealed that the ciliates from orangutans are conspecific with Balantioides coli lineage A, while the ciliates from mandrills clustered with Buxtonella-like ciliates from other primates. Morphological examination of the cysts and trophozoites using light microscopy did not reveal differences robust enough to identify the genera of the ciliates. Phylogenetic analysis of detected L1 larvae of Strongyloides using partial cox1 revealed Strongyloides stercoralis clustering within the cox1 lineage A infecting dogs, humans, and other primates. The sequences of 18S rDNA support these results. As both B. coli and S. stercoralis are zoonotic parasites and the conditions in captive and semi-captive settings may facilitate transmission to humans, prophylactic measures should reflect the findings.
Department of Botany and Zoology Faculty of Science Masaryk University Brno Czech Republic
Department of Psychology Faculty of Natural Sciences University of Stirling Stirling Scotland
Institute of Parasitology Biology Centre Czech Academy of Sciences České Budějovice Czech Republic
Institute of Vertebrate Biology Czech Academy of Sciences Brno Czech Republic
Liberec Zoo Liberec Czech Republic
Prague Zoo Prague Czech Republic
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Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology, 215(3), 403-410. https://doi.org/10.1016/S0022-2836(05)80360-2
Barbosa, A. S., Ponce-Gordo, F., Dib, L. V., Antunes Uchôa, C. M., Bastos, O. M. P., Pissinatti, A., & Amendoeira, M. R. R. (2017). First molecular characterization of Balantioides coli (Malmstein, 1857) isolates maintained in vitro culture and from feces of captive animals, Rio de Janeiro, Brazil. Veterinary Parasitology: Regional Studies and Reports, 10(8), 102-113. https://doi.org/10.1016/j.vprsr.2017.08.014
Barratt, J. L. N., Lane, M., Talundzic, E., Richins, T., Robertson, G., Formenti, F., Pritt, B., Verocai, G., de Souza, J. N., Soares, N. M., Traub, R., Buonfrate, D., & Bradbury, R. S. (2019). Correction: A global genotyping survey of Strongyloides stercoralis and Strongyloides fuelleborni using deep amplicon sequencing. PLoS Neglected Tropical Diseases, 13(9), 1-26. https://doi.org/10.1371/journal.pntd.0009538
Bradbury, R. S., Pafčo, B., Nosková, E., & Hasegawa, H. (2021). Strongyloides genotyping: A review of methods and application in public health and population genetics. International Journal for Parasitology, 51(13-14), 1153-1166. https://doi.org/10.1016/j.ijpara.2021.10.001
Chistyakova, L. V., Kostygov, A. Y., Kornilova, O. A., & Yurchenko, V. (2014). Reisolation and redescription of Balantidium duodeni Stein, 1867 (Litostomatea, Trichostomatia). Parasitology Research, 113(11), 4207-4215. https://doi.org/10.1007/s00436-014-4096-1
Cockburn, T. A. (1948). Balantidium infection associated with diarrhoea in primates. Transactions of the Royal Society of Tropical Medicine and Hygiene, 42(3), 291-293. https://doi.org/10.1016/0035-9203(48)90011-X
Dunay, E., Apakupakul, K., Leard, S., Palmer, J. L., & Deem, S. L. (2018). Pathogen transmission from humans to great apes is a growing threat to primate conservation. EcoHealth, 15(1), 148-162. https://doi.org/10.1007/s10393-017-1306-1
Edwards, M. S., & Ullrey, D. E. (1999). Effect of dietary fiber concentration on apparent digestibility and digesta passage in non-human primates. II. Hindgut- and foregut-fermenting folivores. Zoo Biology, 18(6), 537-549. https://doi.org/10.1002/(SICI)1098-2361(1999)18:6<537::AID-ZOO8>3.0.CO;2-F
Foitová, I., Huffman, M. A., Wisnu, N., & Olšanský, M. (2009). Parasites and their impacts on orangutan health. In S. A. Wich (Ed.), Orangutans: Geographic Variation in Behavioral Ecology and Conservation157-169). Oxford University Press. https://doi.org/10.1093/acprof:oso/9780199213276.003.0010
Frias, L., Stark, D. J., Lynn, M. S., Nathan, S. K., Goossens, B., Okamoto, M., & MacIntosh, A. (2018). Lurking in the dark: Cryptic Strongyloides in a Bornean slow loris. International Journal for Parasitology: Parasites and Wildlife, 7(2), 141-146. https://doi.org/10.1016/j.ijppaw.2018.03.003
Geurden, T., Chartier, C., Fanke, J., di Regalbono, A. F., Traversa, D., von Samson-Himmelstjerna, G., Demeler, J., Vanimisetti, H. B., Bartram, D. J., & Denwood, M. J. (2015). Anthelmintic resistance to ivermectin and moxidectin in gastrointestinal nematodes of cattle in Europe. International Journal for Parasitology: Drugs and Drug Resistance, 5(3), 163-171. https://doi.org/10.1016/j.ijpddr.2015.08.001
Guindon, S., Dufayard, J. F., 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. Systematic Biology, 59(3), 307-321. https://doi.org/10.1093/sysbio/syq010
Hasegawa, H., & Pafčo, B. (2018). Strongyloides. In D. Modrý, B. Pafčo, J. K. Petrželková & H. Hasegawa (Eds.), Parasites of Apes. An atlas of coproscopic diagnostics (pp. 152-155). Edition Chimaira.
Hassell, J. M., Blake, D. P., Cranfield, M. R., Ramer, J., Hogan, J. N., Noheli, J. B., Waters, M., & Hermosilla, C. (2013). Occurrence and molecular analysis of Balantidium coli in mountain gorilla (Gorilla beringei beringei) in the Volcanoes National Park, Rwanda. Journal of Wildlife Diseases, 49(4), 1063-1065. https://doi.org/10.7589/2013-02-041
Huelsenbeck, J. P., & Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics, 17(8), 754-755. https://doi.org/10.1093/bioinformatics/17.8.754
Islam, S., Rahman, M. K., Uddin, M. H., Rahman, M. M., Chowdhury, M. N. U., Hassan, M. M., Magalhaes, R. S., & Islam, A. (2022). Prevalence and diversity of gastrointestinal parasites in free-ranging rhesus macaques (Macaca mulatta) in different land gradients of Bangladesh. American Journal of Primatology, 84, e23345. https://doi.org/10.1002/ajp.23345
Jaleta, T. G., Zhou, S., Bemm, F. M., Schär, F., Khieu, V., Muth, S., Odermatt, P., Lok, J. B., & Streit, A. (2017). Different but overlapping populations of Strongyloides stercoralis in dogs and humans-dogs as a possible source for zoonotic strongyloidiasis. PLoS Neglected Tropical Diseases, 11(8), e0005752. https://doi.org/10.1371/journal.pntd.0005752
Janwan, P., Rodpai, R., Intapan, P. M., Sanpool, O., Tourtip, S., Maleewong, W., & Thanchomnang, T. (2020). Possible transmission of Strongyloides fuelleborni between working Southern pig-tailed macaques (Macaca nemestrina) and their owners in Southern Thailand: Molecular identification and diversity. Infection, Genetics and Evolution, 85(6), 104516. https://doi.org/10.1016/j.meegid.2020.104516
Jirků-Pomajbíková, K., Čepička, I., Kalousová, B., Jirků, M., Stewart, F., Levecke, B., Modrý, D., Piel, A. K., & Petrželková, K. J. (2016). Molecular identification of Entamoeba species in savanna woodland chimpanzees (Pan troglodytes schweinfurthii). Parasitology, 143(6), 741-748. https://doi.org/10.1017/S0031182016000263
Jirků-Pomajbíková, K., & Hůzová, Z. (2018). Coproscopic examination techniques. In D. Modrý, B. Pafčo, J. K. Petrželková & H. Hasegawa (Eds.), Parasites of Apes. An atlas of coproscopic diagnostics (pp. 22-28). Edition Chimaira.
Jirků-Pomajbíková, K., & Modrý, D. (2018). Balantioides coli and related cyst-forming ciliates. In D. Modrý, B. Pafčo, J. K. Petrželková & H. Hasegawa (Eds.), Parasites of Apes. An atlas of coproscopic diagnostics (pp. 112-115). Edition Chimaira.
Jirků-Pomajbíková, K., & Vlčková, K. (2018). Intestinal amoebas. In D. Modrý, B. Pafčo, J. K. Petrželková & H. Hasegawa (Eds.), Parasites of Apes. An atlas of coproscopic diagnostics (pp. 104-106). Edition Chimaira.
Keane, T. M., Creevey, C. J., Pentony, M. M., Naughton, T. J., & Mclnerney, J. O. (2006). Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified. BMC Evolutionary Biology, 6, 29. https://doi.org/10.1186/1471-2148-6-29
Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P., & Drummond, A. (2012). Geneious basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28(12), 1647-1649. https://doi.org/10.1093/bioinformatics/bts199
Keita, M. B., Hamad, I., & Bittar, F. (2014). Looking in apes as a source of human pathogens. Microbial Pathogenesis, 77, 149-154. https://doi.org/10.1016/j.micpath.2014.09.003
Kilbourn, A. M., Karesh, W. B., Wolfe, N. D., Bosi, E. J., Cook, R. A., & Andau, M. (2003). Health evaluation of free-ranging and semi-captive orangutans (Pongo pygmaeus pygmaeus) in Sabah, Malaysia. Journal of Wildlife Diseases, 39(1), 73-83. https://doi.org/10.7589/0090-3558-39.1.73
Kleinschmidt, L. M., Kinney, M. E., & Hanley, C. S. (2018). Treatment of disseminated Strongyloides spp. infection in an infant Sumatran orangutan (Pongo abelii). Journal of Medical Primatology, 47(3), 201-204. https://doi.org/10.1111/jmp.12338
Kooriyama, T., Okamoto, M., Yoshida, T., Nishida, T., Tsubota, T., Saito, A., Tomonaga, M., Matsuzawa, T., Akari, H., Nishimura, H., & Miyabe-Nishiwaki, T. (2013). Epidemiological study of zoonoses derived from humans in captive chimpanzees. Primates, 54(1), 89-98. https://doi.org/10.1007/s10329-012-0320-8
Kuhar, C. W., Fuller, G. A., & Dennis, P. M. (2013). A survey of diabetes prevalence in zoo-housed primates. Zoo Biology, 32(1), 63-69. https://doi.org/10.1002/zoo.21038
Kuze, N., Kanamori, T., Malim, T. P., Bernard, H., Zamma, K., Kooriyama, T., Morimoto, A., & Hasegawa, H. (2010). Parasites found from the feces of Bornean orangutans in Danum Valley, Sabah, Malaysia, with a redescription of Pongobius hugoti and the description of a new species of Pongobius (Nematoda: Oxyuridae). Journal of Parasitology, 96(5), 954-960. https://doi.org/10.1645/GE-2379.1
Kváč, M., & McEvoy, J. (2018). Chilomastix mesnili. In D. Modrý, B. Pafčo, J. K. Petrželková & H. Hasegawa (Eds.), Parasites of Apes. An atlas of coproscopic diagnostics (pp. 100-101). Edition Chimaira.
Labes, E. M., Wijayanti, N., Deplazes, P., & Mathis, A. (2011). Genetic characterization of Strongyloides spp. from captive, semi-captive and wild Bornean orangutans (Pongo pygmaeus) in Central and East Kalimantan, Borneo, east kalimantan, Borneo, Indonesia. Parasitology, 138(11), 1417-1422. https://doi.org/10.1017/S0031182011001284
Lankester, F., Mätz-rensing, K., Kiyang, J., Jensen, S. A., Weiss, S., & Leendertz, F. H. (2008). Fatal ulcerative colitis in a western lowland gorilla (Gorilla gorilla gorilla). Journal of Medical Primatology, 37(6), 297-302. https://doi.org/10.1111/j.1600-0684.2008.00287.x
Malmstein, P. H. (1857). Infusorien als Intestinal-Thiere beim Menschen. Virchows Archiv für pathologische Anatomie und Physiologie und für klinische Medizin, 12, 302-309.
McClure, H. M., Strozier, L. M., Keeling, M. E., & Healy, G. R. (1973). Strongyloidosis in two infant orangutans. Journal of the American Veterinary Medical Association, 163, 629-632.
Modrý, D., & Escalante, A. (2018). Parasites of orangutans. In D. Modrý, B. Pafčo, J. K. Petrželková & H. Hasegawa (EDS.), Parasites of Apes. An atlas of coproscopic diagnostics (pp. 71-79). Edition Chimaira.
Mul, I. F., Paembonan, W., Singleton, I., Wich, S. A., & Van Bolhuis, H. G. (2007). Intestinal parasites of free-ranging, semicaptive, and captive Pongo abelii in Sumatra, Indonesia. International Journal of Primatology, 28(2), 407-420. https://doi.org/10.1007/s10764-007-9119-7
Norman Grim, J., Jirků-Pomajbíková, K., & Ponce-Gordo, F. (2015). Light microscopic morphometrics, ultrastructure, and molecular phylogeny of the putative pycnotrichid Ciliate, Buxtonella sulcata. European Journal of Protistology, 51(5), 425-436. https://doi.org/10.1016/j.ejop.2015.06.003
Nurcahyo, W., Konstanzová, V., & Foitová, I. (2017). Parasites of orangutans (primates: ponginae): An overview. American Journal of Primatology, 79(6), e22650. https://doi.org/10.1002/ajp.22650
Nutman, T. B. (2017). Human infection with Strongyloides stercoralis and other related Strongyloides species. Parasitology, 144(3), 263-273. https://doi.org/10.1017/S0031182016000834
de Oliveira, A. S., Gómez-Hernández, C., & Rezende-Oliveira, K. (2022). Balantidium coli infections, immune status and comorbidities: Literature review. Journal of Tropical Pathology, 50(4), 265-284. https://doi.org/10.5216/rpt.v50i4.70600
Pafčo, B. (2018). Larvoscopic techniques. In D. Modrý, B. Pafčo, J. K. Petrželková, & H. Hasegawa (Eds.), Parasites of Apes. An atlas of coproscopic diagnostics (pp. 39-45). Edition Chimaira.
Pafčo, B., Tehlárová, Z., Jirků Pomajbíková, K., Todd, A., Hasegawa, H., Petrželková, K. J., & Modrý, D. (2018). Gastrointestinal protists and helminths of habituated agile mangabeys (Cercocebus agilis) at Bai Hokou, Central African Republic. American Journal of Primatology, 80(2), e22736. https://doi.org/10.1002/ajp.22736
Penner, L. R. (1981). Concerning threadworm (Strongyloides stercoralis) in great apes: Lowland gorillas (Gorilla gorilla) and chimpanzees (Pan troglodytes). The Journal of Zoo Animal Medicine, 12, 128-131.
Plowman, A. (2013). Diet review and change for monkeys at Paignton Zoo Environmental Park. Journal of Zoo and Aquarium Research, 1(2), 73-77. http://www.jzar.org/jzar/article/view/35
Poirotte, C., Basset, D., Willaume, E., Makaba, F., Kappeler, P. M., & Charpentier, M. J. E. (2016). Environmental and individual determinants of parasite richness across seasons in a free-ranging population of Mandrills (Mandrillus sphinx): Determinants of parasite richness in Mandrills. American Journal of Physical Anthropology, 159(3), 442-456. https://doi.org/10.1002/ajpa.22888
Pomajbíková, K., Oborník, M., Horák, A., Petrželková, K. J., Grim, J. N., Levecke, B., Todd, A., Mulama, M., Kiyang, J., & Modrý, D. (2013). Novel insights into the genetic diversity of Balantidium and Balantidium-like cyst-forming ciliates. PLoS Neglected Tropical Diseases, 7(3), e2140. https://doi.org/10.1371/journal.pntd.0002140
Pomajbíková, K., Petrželková, K. J., Profousová, I., Petrášová, J., & Modrý, D. (2010). Discrepancies in the occurrence of Balantidium coli between wild and captive African great apes. Journal of Parasitology, 96(6), 1139-1144. https://doi.org/10.1645/GE-2433.1
Ponce-Gordo, F., Fonseca-Salamanca, F., & Martínez-Díaz, R. A. (2011). Genetic heterogeneity in internal transcribed spacer genes of Balantidium coli (Litostomatea, Ciliophora). Protist, 162(5), 774-794. https://doi.org/10.1016/j.protis.2011.06.008
Sak, B., Petrzelkova, K. J., Kvetonova, D., Mynarova, A., Shutt, K. A., Pomajbikova, K., Kalousova, B., Modry, D., Benavides, J., Todd, A., & Kvac, M. (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. PLoS One, 8(8), e71840. https://doi.org/10.1371/journal.pone.0071840
Sanchez, C. R., & Pich, A. (2018). Manegament of parasitoses of apes under human care settings. In D. Modrý, B. Pafčo, J. K. Petrželková & H. Hasegawa (Eds.), Parasites of Apes. An atlas of coproscopic diagnostics (pp. 87-91). Edition Chimaira.
Schovancová, K., Pomajbíková, K., Procházka, P., Modrý, D., Bolechová, P., & Petrželková, K. J. (2013). Preliminary insights into the impact of dietary starch on the ciliate, Neobalantidium coli, in captive chimpanzees. PLoS One, 8(11), e81374. https://doi.org/10.1371/journal.pone.0081374
Schuster, F. L., & Ramirez-Avila, L. (2008). Current world status of Balantidium coli. Clinical Microbiology Reviews, 21(4), 626-638. https://doi.org/10.1128/CMR.00021-08
Setchell, J. M., Bedjabaga, I. B., Goossens, B., Reed, P., Wickings, E. J., & Knapp, L. A. (2007). Parasite prevalence, abundance, and diversity in a semi-free-ranging colony of Mandrillus sphinx. International Journal of Primatology, 28(6), 1345-1362. https://doi.org/10.1007/s10764-007-9225-6
Solórzano-García, B., & Pérez-Ponce de León, G. (2017). Helminth parasites of howler and spider monkeys in Mexico: Insights into molecular diagnostic methods and their importance for zoonotic diseases and host conservation. International Journal for Parasitology: Parasites and Wildlife, 6(2), 76-84. https://doi.org/10.1016/j.ijppaw.2017.04.001
Speare, R. (1989). Identification of species of Strongyloides. In D. I. Grove (Eds.), Strongyloidiasis a major roundworm infection of man (pp. 11-84). Taylor and Francis.
Strait, K., Else, J. G., & Eberhard, M. L. (2012). Parasitic diseases of nonhuman primates. In C. R. Abee, K. Mansfield, Tardif Nonhuman Primates in Biomedical Research (pp. 221-231). Elsevier Inc. https://doi.org/10.1016/B978-0-12-381366-4.00004-3
Supriadi, S., Fitria, A., & Nurcahyo, W. (2012). Balantidium sp. Infection in faeces samples of orangutan (Pongo pygmaeus) from care center and Tanjung Puting National Park Area, Central Borneo. Biology, Medicine & Natural Product Chemistry, 1(1), 47-52.
Teare, J. A., & Loomis, M. R. (1982). Epizootic of balantidiasis in lowland gorillas. Journal of the American Veterinary Medical Association, 181(11), 1345-1347.
Uemura, E., Houser, W. D., & Cupp, C. J. (1979). Strongyloidiasis in an infant orangutan (Pongo pygmaeus). Journal of Medical Primatology, 8(5), 282-288. https://doi.org/10.1159/000460212
Wright, A. D. G., Dehority, B. A., & Lynn, D. H. (1997). Phylogeny of the rumen ciliates Entodinium, Epidinium, and Polyplastron (Litostomatea: Entodiniomorphida) inferred from small subunit ribosomal RNA sequences. The Journal of Eukaryotic Microbiology, 44(1), 61-67. https://doi.org/10.1111/j.1550-7408.1997.tb05693.x
Yan, W., He, K., Qian, W., Wang, T., Zong, Y., Zhang, M., Wei, Z., & Han, L. (2018). First molecular identification of Buxtonella ciliates from captive-bred mangabeys (Cercocebus torquatus) from China. Parasitology Research, 117(12), 3753-3759. https://doi.org/10.1007/s00436-018-6075-4
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