Prevalence and morphotype diversity of Trichuris species and other soil-transmitted helminths in captive non-human primates in northern Nigeria
Article Sidebar
Main Article Content
Abstract
A study to determine the prevalence and morphotype diversity of soil-transmitted helminths in captive non-human primates (NHPs) in northern Nigeria was conducted. Simple flotation and sedimentation methods were used to examine fecal samples. A Morphometric analysis was done on Trichuris spp. eggs to determine the diversity of whipworm circulating in NHPs in the study area. High prevalence (60%) of infection was recorded in captive NHPs; Patas Monkey (n=17), Tantalus Monkey (n=9), Mona Monkey (n=7), Vervet Monkey (n=2), Mangabey Monkey (n=1), Baboon (n=14), and Chimpanzee (n=8) from parks and zoological gardens located in four Nigerian states (Borno, Gombe, Kano, and Plateau) and the Federal Capital Territory (FCT), Abuja. Captive NHPs examined were infected with helminths either as single, double or triple infections. Four zoonotic soil transmitted helminth (STH) genera, Trichuris, Strongyloides, Ancylostoma, and Enterobius were detected in the examined animals. Eggs of Trichuris spp. were the most prevalent with four morphotypes suggesting several morphotypes of whipworm were circulating among the NHPs in this region. Further studies are required to elucidate the epidemiologic and public health implications of these findings.
Article Details
Authors own the copyright to the articles published in JoTT. This is indicated explicitly in each publication. The authors grant permission to the publisher Wildlife Information Liaison Development (WILD) Society to publish the article in the Journal of Threatened Taxa. The authors recognize WILD as the original publisher, and to sell hard copies of the Journal and article to any buyer. JoTT is registered under the Creative Commons Attribution 4.0 International License (CC BY), which allows authors to retain copyright ownership. Under this license the authors allow anyone to download, cite, use the data, modify, reprint, copy and distribute provided the authors and source of publication are credited through appropriate citations (e.g., Son et al. (2016). Bats (Mammalia: Chiroptera) of the southeastern Truong Son Mountains, Quang Ngai Province, Vietnam. Journal of Threatened Taxa 8(7): 8953–8969. https://doi.org/10.11609/jott.2785.8.7.8953-8969). Users of the data do not require specific permission from the authors or the publisher.
References
Adedokun, O.A., R.A.M. Adedokun, B.O. Emikpe, O.G. Ohore, D.O. Oluwayele & O.I. Ajayi (2002). Concurrent fatal helminthosis and balantidiosis in a red monkey (Erythrocebus pattas) in Ibadan, Nigeria. Nigeria Veterinary Journal 23: 56–59.
Adetunji, V.E. (2014). Prevalence of gastro-intestinal parasites in primates and their keepers from two zoological gardens in Ibadan, Nigeria. Sokoto Journal of Veterinary Science 12(2): 25–30.
Aviruppola, A.J.M.K., R.P.V.J. Rajapakse & R.S. Rajakaruna (2016). Coprological survey of gastrointestinal parasites of mammals in Dehiwala National Zoological Gardens, Sri Lanka. Ceylon Journal of Science 45(1): 83–96. https://doi.org/10.4038/cjs.v45i1.7367 DOI: https://doi.org/10.4038/cjs.v45i1.7367
Bethony, J., S. Brooker, M. Albonico, S.M. Geiger, A. Loukas, D. Diemert & P.J. Hotez (2006). Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet 367: 1521–32 DOI: https://doi.org/10.1016/S0140-6736(06)68653-4
Bezjian, M., T.R. Gillespie, C.A. Chapman & E.C. Greiner (2008). Coprologic evidence of gastrointestinal helminths of forest baboons, Papio anubis, in Kibale National Park, Uganda. Journal of Wildlife Diseases 44: 878–887.
Cavallero, S., C. De Liberato, K.G. Friedrich, D. Di Cave, V. Masella, S. D’amelio & F. Berrilli (2015). Genetic heterogeneity and phylogeny of Trichuris spp. from captive non-human primates based on ribosomal DNA sequence data. Infection, Genetics and Evolution. 34: 450–456.
Cordon, G.P., A.H. Prados, D. Romero, M.S. Moreno, A. Pontes, A. Osuna & M.J. Rosales (2008). Intestinal parasitism in the animals of the zoological garden ‘‘Pena Escrita’’ (Almunecar, Spain). Veterinary Parasitology 156: 302–309.
Dawet, A., D.P. Yakubu & H.M. Butu (2013). Survey of gastrointestinal parasites of non-human primates in Jos Zoological Garden. Journal of Primatology 2: 108. https://doi.org/10.4172/2167–6801.1000108 DOI: https://doi.org/10.4172/2167-6801.1000108
Dupain J., C. Nell, K. J. Petrzelkova, P. Garcia, D. Modry & F.P. Gordo (2009). Gastrointestinal parasites of bonobos in the Lomako Forest, Democratic Republic of Congo, pp. 297–310. In: Huffman M.A. & C. Chapman (eds.). Primate parasite ecology, the dynamics and study of host parasite relationships. Cambridge University Press, UK.
Egbetade, A., O. Akinkuotu, O. Jayeola, A.N. Niniola, N. Emmanuel, E.S. Olugbogi & S. Onadeko (2014). Gastrointestinal helminths of resident wildlife at the Federal University of Agriculture Zoological Park, Abeokuta. Sokoto Journal of Veterinary Science 12(3): 26–31.
Emikpe, B.O., J.O. Ayoade, O.G. Ohore, O.O. Olaniyan, & M.O. Akusu (2002). Fatal trichuriosis in a captive baboon (Papio anubis) in Ibadan. Tropical Veterinarian 20: 36–39.
Ghai, R.R., N.D. Simons, C.A. Chapman, P.A. Omeja, T.J. Davies, N. Ting & T.L. Goldberg (2014). Hidden population structure and cross-species transmission of whipworms (Trichuris sp.) in humans and non-human primates in Uganda. PLoS Neglected Tropical Disease 8: e3256. https://doi.org/10.1371/journal.pntd.0003256 DOI: https://doi.org/10.1371/journal.pntd.0003256
Gillespie, T.R., C.L. Nunn & F.H. Leendertz (2008). Integrative approaches to the study of primate infectious disease: implications for biodiversity conservation and global health. American Journal of Physical Anthropology Suppl 47: 53–69. https://doi.org/10.1002/ajpa.20949 DOI: https://doi.org/10.1002/ajpa.20949
Gracenea, M., M.S. Gomez, J. Torres, E. Carne & J. Fernandez-Moran (2002). Transmission dynamics of Cryptosporidium in primates and herbivores at the Barcelona zoo: a long-term study. Veterinary Parasitology 104: 19–26.
Greiner, E.C & A. McIntosh (2009). Collection methods and diagnostic procedures for primate parasitology, pp. 3–27. In: Huffman, M.A. & C.A. Chapman (eds.). Primates Parasite Ecology. The Dynamics and Study of Host-parasite Relationships. Cambridge University Press, 531pp.
Hasegawa, H., C.A. Chapman & M.A. Huffman (2009). Useful diagnostic references and images found in wild primates, pp. 507–513. In: Huffman M.A. & C. Chapman (editors). Primates Parasite Ecology. The Dynamics and Study of Host-parasite Relationships. Cambridge University Press, 531pp.
Hasegawa, H., D. Modrý, M. Kitagawa, K.A. Shutt, A. Todd, B. Kalousova, I. Profousova & K.J. Petrzelkova (2014). Humans and great apes cohabiting the forest ecosystem in Central African Republic harbour the same hookworms. PLoS Neglected Tropical Disease 8: e2715. https://doi.org/10.1371/journal.pntd.0002715 DOI: https://doi.org/10.1371/journal.pntd.0002715
Hasegawa, H., T. Kano & M. Mulavwa (1983). A parasitological survey on the feces of pygmy chimpanzees, Pan paniscus, at Wamba, Zaire. Primates 24: 419–423.
Hussain, S., M.S. Ram, A. Kumar, S. Shivaji & G. Umapathy (2013). Human presence increases parasitic load in endangered Lion-tailed Macaques (Macaca silenus) in its fragmented rainforest habitats in southern India. PLoS One 8: e63685. https://doi.org/10.1371/journal.pone.0063685 DOI: https://doi.org/10.1371/journal.pone.0063685
Kimberley, A.P., E.H. Meghan, W.G. Brian & Y. Mirtha (2004). Survey of the gastrointestinal parasites of the primate community at Tambopata National Reserve, Peru. Journal of Zoology 264: 149–151.
Klaus, A., E. Zimmermann, M.K. Roper, U. Radespiel, S. Nathan, B. Goossens & C. Strube (2017). Co-infection patterns of intestinal parasites in arboreal primates (proboscis monkeys, Nasalis larvatus) in Borneo. International Journal of Parasitology, Parasite and Wildlife 6: 320–329.
Kouassi, R.Y., S.W. Mcgraw, P.K. Yao, A. Abou-Bacar, J. Brunet, B. Pesson, B. Bonfoh, E.K. N’goran & E. Candolfi (2015). Diversity and prevalence of gastrointestinal parasites in seven non-human primates of the Taï National Park, Côte d’Ivoire. Parasite 22: 1.
Li, J., H. Dong, R. Wang, F. Yu, Y. Wu, Y. Chang, C. Wang, M. Qi & L. Zhang (2017). An investigation of parasitic infections and review of molecular characterization of the intestinal protozoa in nonhuman primates in China from 2009 to 2015. International Journal of Parasitology, Parasite and Wildlife 6: 8–15.
Lim, Y.A.L., R. Ngui, J. Shukri, M. Rohela & N.H.R. Mat (2008). Intestinal parasites in various animals at a zoo in Malaysia. Veterinary Parasitology 157: 154–159.
Lynn, M.S. (2010). Primate viability in a fragmented landscape: Genetic diversity and parasite burden of long-tailed macaques and proboscis monkeys in the lower Kinabatangan Flood plain, Sabah, Malaysia. PhD Thesis. Cardiff University, Cardiff, 228pp.
Mbaya, A.W. & E.U.J. Udendey (2011). Gastrointestinal parasites of captive and free-roaming primates at the Afi mountain Primate Conservation area in Calabar, Nigeria and their zoonotic implications. Pakistan Journal of Biological Science 14(13): 709–714.
Mbaya, A.W. & C.O. Nwosu (2006). Outbreak of clinical amoebiasis among captive chimpanzees (Pan troglodytes) at the Sanda Kyarimi Park, Maiduguri, Nigeria. Nigerian Veterinary Journal 1: 68–73.
Mbaya, A.W., C.O. Nwosu, M.M. Aliyu & T.A. Ahmed (2006a). Comparative study of gastrointestinal parasites of captive and free-living wild animals in the semi-arid zone of north-eastern Nigeria. Nigerian Journal of Experimental and Applied Biology 7: 185–193.
Mbaya, A.W., M.M. Aliyu & C.O. Nwosu (2006b). Outbreak of balantidiosis among captive chimpanzees (Pan troglodytes) at the Sanda Kyarimi Park, Maiduguri, Nigeria. Sahel Journal of Veterinary Science 5: 55–58.
Melfi, V. & F. Poyser (2007). Trichuris burdens in zoo-housed Colobus guereza. International Journal of Primatology 28: 1449–1456.
Nwosu, C.O. (1995). Helminth parasites of captive wild animals in Borno State Nigeria. Tropical Veterinarian 13: 1–13.
Opara, M.N., C.T. Osuji & J.A. Opara (2010). Gastrointestinal parasitism in captive animals at the zoological garden, Nekede Owerri, southeast Nigeria. Report and Opinion 2: 21–28.
Petrželkova, K.J., H. Hasegawa, C.C. Appleton, M.A. Huffman, C.E. Archer, L.R. Moscovice, M.I. Mapua, J. Singh & T. Kaur (2010). Gastrointestinal parasites of the chimpanzee population introduced onto Rubondo Island National Park, Tanzania. American Journal of Primatology 72: 307–316.
Raja, M.M.R.U., A.R. Dey, M. Begum, U.K. Kundu & A.F. Ashad (2014). Coprological prevalence of gastrointestinal parasites in carnivores and small mammals at Dhaka Zoo, Bangladesh. Journal of Threatened Taxa 6(3): 5574–5579. https://doi.org/10.11609/JoTT.o3569.5574-9 DOI: https://doi.org/10.11609/JoTT.o3569.5574-9
Ranglack, G.S & C.P. Yeager (1986). Survey of intestinal parasites found in Proboscis Monkeys (Nasalis larvatus) and Long-tailed Macaques (Macaca fascicularis). Primate Reports 14: 249.
Rao, A.T & L.N. Acharjyo (1984). Diagnosis and classification of common diseases of captive animals at Nandankanan Zoo in Orissa (India). Indian Journal of Animal Health 33: 147–152.
Samuel, W.M., M. J. Pybus & A. Kocan (eds.). (2001). Parasitic Diseases of Wild Mammals 2nd ed. Iowa State University Press, Ames, 568pp.
Singh, P., L.D. Singla, M.P. Gupta, S. Sharma & D.R. Sharma (2009). Epidemiology and chemotherapy of parasitic infections in wild omnivores in the Mechendra Choudhury Zoological park, Chhat Bir, Punjab. Journal of Threatened Taxa 1(1): 62–64. https://doi.org/10.11609/JoTT.o1767a.62-4 DOI: https://doi.org/10.11609/JoTT.o1767a.62-4
Strait K., J. Else & M.L. Eberhard (2012). Parasitic diseases of nonhuman primates, pp. 197–298. In: Abee C.R., K. Mansfield, S.D. Tardif & T. Morris (eds.) Nonhuman Primates in Biomedical Research: Diseases. Academic Press, London, 536pp.
Vanitha, V., K. Thiyagesan & N. Baskaran (2011). Prevalence of intestinal parasites among captive Asian Elephants Elephas maximus: effect of season, host demography, and management systems in Tamil Nadu, India. Journal of Threatened Taxa 3(2): 1527–1534. https://doi.org/10.11609/JoTT.o2488.1527-34 DOI: https://doi.org/10.11609/JoTT.o2488.1527-34
Wren, B.T., T.R. Gillespie, J.W. Camp & M.J. Remis (2015). Helminths of Vervet Monkeys, Chlorocebus aethiops, from Loskop Dam Nature Reserve, South Africa. Comparative Parasitology 82: 101–108.