Zoonotic potential of gastrointestinal parasite in long-tailed Macaque Macaca fascicularis at Baluran National Park, Situbondo, East Java, Indonesia
Abstract
Baluran National Park (BNP) is one of the highest number of tourist visit among Indonesian national park. In the past decades, excessive feeding has induced change in macaque behaviour which increased the number of recorded human-macaque interaction. The close contact between macaque and humans can increase the risk of disease transmissions. This study aimed to identify gastro intestinal (GI) parasite in the long-tailed macaque. To provide identification, we adopted morphologic methods. We collected 100 faeces from unidentified individuals of Long-tailed macaque in BNP. Fecal samples were tested using direct smear and modified sugar floatation techniques. Microscopic examination showed 89% (89/100) samples were found to be positive of GI parasite. The prevalence of protozoa infection was higher (89%) than helminth (83%). The most prevalent GI parasite is Trichostrongylus sp (66%) following with Entamoeba sp. (53%), Strongyloides sp. (32%), Blastocystis sp. (32%), Trichuris sp.(17%), Giardia sp. (10%) and Enterobius sp. (3%). All of GI parasite that successfully identified have zoonotic concern. In conclusion, GI parasites found in faeces of long-tailed macaque at Baluran National Park potentially a zoonotic transmission.
Keywords : GI Parasite; Long tailed Macaque; Baluran National Park; Zoonosis
Full Text:
PDFReferences
Adhikari, P., P. Dhakal. 2018. Prevalence of gastro-intestinal parasites of Rhesus macaque (Macaca mulatta Zimmermann, 1780) and hanuman langur (Semnopithecus Entellus Dufresne, 1797) in Devghat, Chitwan, Nepal. Journal of Institute of Science and Technology, 22(2):12-18.
Alfellani, M.A., A.S. Jacob, N.O. Perea, R.C. Krecek, D.Taner-Mulla, J.J. Verweij, B. Levecke, E. Tannich, C.G. Clark, C. Stensvold. 2013. Diversity and distribution of Blastocystis sp. subtipes in non-human primates. Parasitology, 140 (08):966-971.
Arjun, C.P., T. Anoopkumar, R. Reghu. 2015. A Study of gastrointestinal parasites in Bonnet macaques (Macaca radiata) of Pookode, Wayanad, Kerala. Zoos' Print Journal, 30(10): 7-8
Barutzki, D., R. Schaper. 2011. Results of parasitological examinations of faecal samples from cats and dogs in Germany between 2003 and 2010. Parasitology Research, 109:45–60.
Beaumier, C.M., P.M. Gillespie, P.J. Hotez, M.E. Bottazzi. 2013. New vaccines for neglected parasitic diseases and dengue. Translational Research, 162(3): 144-155.
Betson, M., M. Jensen Søe, P. Nejsum. 2015. Human Trichuriasis: Whipworm Genetics, Phylogeny, Transmission and Future Research Directions. Current Tropical Medicine Reports, 2(4): 209–217.
Chang, T.K., C.W. Liao, Y.C. Huang, C.C. Chang, C.M. Chou, H.C. Tsay, A. Huang, S.F. Guu, T.C. Kao, C.K. Fan. 2009. Prevalence of Enterobius vermicularis infection among preschool children in kindergartens of Taipei City, Taiwan in 2008. Korean Journal of Parasitology, 47(2): 185-187.
Chekley, W., A.C. White Jr, D. Jaganath, M.J. Arrowood, R.M. Chalmers, X.M. Chen. 2015. A review of the global burden, novel diagnostics, therapeutics, and vaccine targets for cryptosporidium. Lancet Infecttious Disease, 15: 85-94.
Chrisnawaty, D. 2008. Infeksi Cacing saluran pencernaan pada monyet ekor panjang (Macaca fascicularis) di Pulau Tinjil. Skripsi, Fakultas Kedokteran Hewan, Institut Pertanian Bogor, Bogor.
Choong, S.S., M.M Armiladiana, H.H. Ruhil, T.L. Peng. 2019. Prevalence of parasites in working pig-tailed Macaques (Macaca nemestrina) in Kelantan, Malaysia. Journal of Medical Primatology, 48: 207–210.
Cibot, M., J. Guillot, S. Lafosse, C. Bon, A. Seguya, S. Krief. 2015. Nodular worm infections in wild non-human primates and humans living in the Sebitoli area (Kibale National Park, Uganda): do high spatial proximity favor zoonotic transmission?. PLoS neglected tropical diseases, 9(10): e0004133.
Daszak, P., A.A. Cunnigham. 2003. Anthropogenic change, biodiversity loss, and a new agenda for emerging diseases. Journal of Parasitology, 89:37–41.
Dong, H., L. Junqiang, Q. Meng, W. Rongjun, Y. Fuchang, J. Fuchun, N. Changsen, Z. Longxian. 2017. Prevalence, molecular epidemiology, and zoonotic potential of Entamoeba spp in nohuman primates in China. Journal of Molecular Epidemiology and Evolutionary, 54: 216-220.
Du S.Z., G.H. Zhao, J.F. Shao, Y.Q. Fang, G.R. Tia, L.X. Zhang L. 2015. Cryptosporidium spp., Giardia intestinalis, and Enterocytozoon bieneusi in captive non-Human primates in Qinling mountains. Korean Journal of Parasitology, 53: 395–402.
Dwipayanti, K.A., I.B.M. Oka, A.L.R. Tenden. 2014. Infeksi cacing saluran pencernaan monyet ekor panjang (Macaca fascicularis) yang diperdagangkan di Pasar Satria Denpasar. Buletin Veteriner Udayana, 6(1): 59-66.
Eckert, K.A., N.E. Hanh, A. Genz, D.M. Kitchen, M.D. Stuart, G.A. Averbeck, B.E. Stromberg, H. Markowitz. 2006. Coprological survey of aloutta pigra at two site Belize. International Journal of Primatology, 27(1): 227-238.
Fan, C., T. Chuang, Y. Huang, A. Yin, C. Chou, Y. Hsu, R. Kios, S. Hsu, Y. Wang, M. Szu, J. Lin, K. Briand, C. Tu. 2019. Enterobius vermicularis infection: prevalence and risk factors among preschool children in kindergarten in the capital area, Republic of the Marshall Islands. BMC Infectious Disease, 19: 536. https://doi.org/10.1186/s12879-019-4159-0
Feng, Ye., L. Xiao. 2011. Zoonotic potential and molecular epidemiology of Giardia species and Giardiasis. Clinical Microbiology Reviews, 24: 110-140.
Friishansen, M., H.A. Wahyudi, S. Supriyanto, R.A. Damanik. 2015. The interactions between long-tailed macaques (Macaca fascicularis) and tourists in Baluran National Park, Indonesia. Journal of Indonesian Natural History, 3: 36-41.
Gruijter, J.M., R.B. Gasser, A.M. Polderman, V. Asigri, L. Dijkshoorn. 2005. High resolution DNA fingerprinting by AFLP to study the genetic variation among Oesophagostomum bifurcum (Nematoda) from human and non-human primates from Ghana. Parasitology, 130: 229-23.
Hartman, C., J. Gottling, T. Nadler, U. Streicher. 2015.Effect of orally applied ivermectin on GI nematode in duoc langur (Pygatrix spp). Vietnam Journal of Primatology, 2:39-44.
Islam, S., Md.K. Rahman, M.N.U. Chowdhury., M.M. Hasan, M.S. Flora, A. Islam. 2017. Diversity of GI parasite in rhesus macaque (Macaca mulatta) in human-wild life ecosystem in Bangladesh. 9th one Health Bangladesh Conference.
Jones, E.L., G.A. Engel, M.A. Schillaci, J. Froehlich, U. Paputunganand, R.C. Kyes. 2004. Prevalence of enteric parasites in pet macaques in Sulawesi, Indonesia. American Journal of Primatology, 62: 71‐82.
Joesoef , J.A., D. Sajuthi, A. Wijaya, M.U.E. Sanam. 2018. Keragaman Endoparasit pada Macaca fascicularis dan Potensi Zoonotiknya dengan Cuaca Berbeda di Kota Kupang. Jurnal Veteriner, 19(4): 451-459.
Junqiang, L., H. Dong, R. Wang, F. Yu, Y. Wu, Y. Chang, C.R. 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 for Parasitology: Parasites and Wildlife, 6(1): 8-15.
Klaus, A., E. Zimmermann, K.M. Roper, U. Radespiel, S. Nathan, B. Goossens, C. Strube. 2017. Co-Infection patterns of intestinalparasite in arboreal primate (probocis monkeys) in Borneo. International Journal of Parasitology, 6: 320-329.
Kumar, S., P. Sundararaj, H.N. Kumara, A. Pal, K. Santhosh, S. Vinoth. 2018. Prevalence of GI parasites in bonnet macaque and possible consequences of their unmanaged relocations. PLoS ONE, 13(11): e0207495.
Kotloff, K.L., J.P. Nataro, W.C. Blackwelder, D. Nasrin, T.H. Farag, S. Panchalingam. 2013. Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): a prospective, case-control study. Lancet, 382:209-222.
Lane‐Degraaf, K.E., I.G.A.P. Arta, I.N. Wandia, A. Rompis, H. Hollocher, A. Fuentes. 2014. Human behavior and opportunities for parasite transmission in communities surrounding long‐tailed macaque populations in Bali, Indonesia. American Journal of Primatology, 76: 159–167.
Lane‐Degraaf, K.E., C. Holley, H. Hollocher, A. Fuentes. 2011. The anthropogenic environment lessens the intensity and prevalence of GI parasites in Balinese longtailed macaque populations. Primates, 52:117–128.
Matsubayashi, M., K. Takami, I. Kimata, T. Nakanishi, H. Tani, K. Sasai, E. Baba. 2005. Survey of Cryptosporidium spp. and Giardia spp. infections in various animals at a zoo in Japan. Journal Zoo and Wildlife Medicine, 36:331–335.
Muehlenbain, M.P., M. Ancrenaz. 2009. Minimizing pathogent transmission at primate ecoturism destinations: the need for input from travel medicine. Journal of Travel Medicine, 16:229-232.
Nunn C.L., S.M. Altizer. 2006. Infectious diseases in primates: behavior, ecology and evolution. Oxford University Press, Oxford.
Nutman, T.B.2017. Human infection with Strongyloides stercoralis and other related Strongyloides species. Parasitology, 144: 263–273.
Obanda, V., N. Maingi, G. Muchemi, C.J. Ng’ang’a, S. Angelone, E.A. Archie. 2019. Infection dynamics of gastrointestinal helminths in sympatric non-human primates, livestock and wild ruminants in Kenya. PLoS ONE, 14(6): e0217929.
Olsen. A., L. Lieshout, H. Marti, T. Polderman, K. Polman, P. Steinmann, R. Stothard, S. Thybo, J.J. Verweij, P. Magnussen. 2009. Strongyloidiasis the most neglected of the neglected tropical diseases?. Transactions of The Royal Society of Tropical Medicine and Hygiene, 103: 967-972.
Pedersen, A.B., S. Altizer, M. Poss, A.A. Cunningham, C.L. Nunn. 2005. Patterns of host specificity and transmission among parasites of wild primates. International Journal of Primatollogy, 35: 647-657.
Pafco, B., Z. Tehlárová, K.J. Pomajbíková, A. Todd, H. Hasegawa, K.J. Petrželková, D. Modrý. 2017. GI protists and helminths of habituated agile mangabeys (Cercocebus agilis) at Bai Hokou, Central African Republic. American Journal of Primatology, 80(2): e22736
Parr, N.A., L.M. Fedigan, S.J Kutz. 2013. A coprological survey of parasites in white faced capuchins (Cebus capucinus) from Sector Santa Rosa, ACG, Costa Rica. Folia Primatology, 84: 102–114.
Rahmah, F., S.S. Dahelmi. 2013. Gastrointestinal helminths of the primates in Taman Satwa Kandi Sawahlunto, West Sumatra. Jurnal Biologi Universitas Andalas, 2(1): 14-19.
Shirley, D.A., S.N. Moonah, K.L. Kotloff. 2012. Burden of disease from cryptosporidiosis. Current Opinion of Infectious Disease, 25: 555-563.
Soulsby, E.J.L. 1982. Helminth, Anthrophods and Protozoa of Domesticated Animals. (7th Ed). Williams and Wilkins, Bailliere Tindall London.
Sow, S.O., K. Muhsen. D. Nasrin. W.C. Blackwelder, Y. Wu, T.H. Farag. 2016. The burden of Cryptosporidium diarrheal disease among children < 24 months of age in moderate/high mortality regions of Sub-Saharan Africa and South Asia, utilizing data from the Global Enteric Multicenter Study (GEMS). PLoS Neglected Tropical Disease, 10: e0004729.
Sricharern, W., T. Inpankaew, S. Keawmongkol, J. Supanam, R. Stich, S. Jittapalapong. 2016. Molecular detection and prevalence of Giardia duodenalis and Cryptosporidium spp. among long-tailed macaques (Macaca fascicularis) in Thailand. Infection, Genetics and Evolution, 40: 310-314.
Stanley Jr.S.L. 2003. Amoebiasis. Lancet, 361: 1025-1034.
Stensvold, C.R., C.G. Clark. 2016. Current status of Blastocystis: A personal view. Parasitology International, 65(6): 763-771.
Thanchomnang, T., P.M. Intapan, O. Sanpool, R. Rodpai, L. Sadaow, I. Phosuk, C. Somboonpatarakun, S. Laymanivong, S. Tourtip, W. Maleewong. 2019. First molecular identification of Strongyloides fuelleborni in long-tailed macaques in Thailand and Lao People's Democratic Republic reveals considerable genetic diversity. Journal of Helminthology, 93(5): 608-615.
Williamson, E., E. Macfie. 2010. Best practice guidelines for Great Ape tourism. IUCN/SSC Primate Specialist Group No. 38. Gland, Switzerland.
Xiao L., J. Ye, J. Ma, M. Guo, L. Liu, Y. Feng. 2012. Anthroponotic enteric parasites in monkeys in public park, China. Emerging Infectious Disease, 18: 1640-1643.
Yoshikawa., H, Z. Wu, K. Pandey, B.D. Pandey, J.B. Sherchand, T. Yanagi, H. Kanbara. 2009. Molecular characterization of Blastocystis isolates from children and rhesus monkeys in Kathmandu, Nepal. Veterinary Parasitology, 160(3-4): 295-300.
Zanzani, S.A., A.L. Gazzonis, S. Epis, M.T. Manfredi. 2016. Study of the gastrointestinal parasitic fauna of captive non-human primates (Macaca fascicularis). Parasitology Research, 115: 307–312.
Zhang, Q., S.H.L. Kongshang, J.L.L. Jiqi, H. He. 2019. Occurrence of Selected Zoonotic Fecal Pathogens and First Molecular Identification of Hafnia paralvei in Wild Taihangshan Macaques (Macaca mulatta tcheliensis) in China. BioMed Research International, Article ID 2494913.
Zinner, D., G. Fickenscher, C. Roos. 2013. Family cercopithecidae (Old World Monkey). In: Mittermeier, R.A., Rylands, A.B.,
DOI: https://doi.org/10.13170/ajas.5.1.15397
Article Metrics
Abstract view : 11 timesPDF - 10 times
Refbacks
- There are currently no refbacks.
DETAIL VISITORS STATISTIC COUNTER CLICK HERE
This work is licensed under a Creative Commons Attribution - 4.0 International Public License (CC - BY 4.0).