Genetic characterization of nodular worm infections in Asian Apes

Yalcindag E., Stuart P., Hasegawa H., Streit A., Doležalová J., Morrogh-Bernard H., Cheyne S.M., Nurcahyo W., Foitová I.

Department of Botany and Zoology, Faculty of Science, Masaryk University, Kotlářská 2, Brno, 611 37, Czech Republic; The Roslin Institute, Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush, Midlothian, EH25 9RG, United Kingdom; Department of Biological and Pharmaceutical Sciences, Munster Technological University, Tralee, Co. Kerry, Ireland; Department of Biomedicine, Faculty of Medicine, Oita University, 1-1 Idaigaoka, Hasama, Yufu, Oita 879-5593, Japan; Department Evolutionary Biology, Max Planck Institute for Developmental Biology, Max-Planck-Ring 9, Tübingen, 72076, Germany; Department of Physiology, Faculty of Veterinary Medicine, University of Veterinary and Pharmaceutical Sciences, Brno, Palackého tř. 1, Brno, Czech Republic; Borneo Nature Foundation, Palangkaraya, Central Kalimantan, Indonesia; Department of Humanities and Social Sciences, Oxford Brookes University, Oxford, United Kingdom; Department of Parasitology, Faculty of Veterinary Medicine, Gadjah Mada University, Yogyakarta, Indonesia


Abstract

Parasitic nematodes of Oesophagostomum spp., commonly known, as ‘nodular worms’ are emerging as the most widely distributed and prevalent zoonotic nematodes. Oesophagostomum infections are well documented in African non-human primates; however, the taxonomy, distribution and transmission of Oesophagostomum in Asian non-human primates are not adequately studied. To better understand which Oesophagostomum species infect Asian non-human primates and determine their phylogeny we analysed 55 faecal samples from 50 orangutan and 5 gibbon individuals from Borneo and Sumatra. Both microscopy and molecular results revealed that semi-wild animals had higher Oesophagostomum infection prevalence than free ranging animals. Based on sequence genotyping analysis targeting the Internal transcribed spacer 2 of rDNA, we report for the first time the presence of O. aculeatum in Sumatran apes. Population genetic analysis shows that there is significant genetic differentiation between Bornean and Sumatran O. aculeatum populations. Our results clearly reveal that O. aculeatum in free-ranging animals have a higher genetic variation than those in semi-wild animals, demonstrating that O. aculeatum is circulating naturally in wildlife and zoonotic transmission is possible. Further studies should be conducted to better understand the epidemiology and dynamics of Oesophagostomum transmission between humans, non-human primates and other wild species and livestock in Southeast Asia. © 2021, The Author(s).


Journal

Scientific Reports

Publisher: Nature Research

Volume 11, Issue 1, Art No 7226, Page – , Page Count


Journal Link: https://www.scopus.com/inward/record.uri?eid=2-s2.0-85103744523&doi=10.1038%2fs41598-021-86518-2&partnerID=40&md5=7efe30803659d12b4f0bf4208bc6687f

doi: 10.1038/s41598-021-86518-2

Issn: 20452322

Type: All Open Access, Gold, Green


References

Locke, D.P., Comparative and demographic analysis of orang-utan genomes (2011) Nature, 469, pp. 529-533; Nater, A., Morphometric, behavioral, and genomic evidence for a new orangutan species (2017) Curr. Biol., 27, pp. 3487-3498. , https://doi.org/10.1016/j.cub.2017.09.047; Kim, S.K., Patterns of genetic variation within and between Gibbon species (2011) Mol. Biol. Evol., 28, pp. 2211-2218. , COI: 1:CAS:528:DC%2BC3MXps12lt7c%3D; Thinh, V.N., Mitochondrial evidence for multiple radiations in the evolutionary history of small apes (2010) BMC Evol. Biol., 10, p. 74; (2019) IUCN Red List of Threatened Species, , http://www.redlist.org; Kilbourn, A.M., Health evaluation of free-ranging and semi-captive orangutans (Pongo pygmaeus pygmaeus) in Sabah, Malaysia (2003) J. Wildl. Dis., 39, pp. 73-83; Klaus, A., Co-infection patterns of intestinal parasites in arboreal primates (proboscis monkeys, Nasalis larvatus) in Borneo (2017) Int J Parasitol Parasites Wildl, 6, pp. 320-329; Labes, E.M., Intestinal parasites of endangered orangutans (Pongo pygmaeus) in Central and East Kalimantan, Borneo, Indonesia (2010) Parasitology, 137, pp. 123-135; Goldberg, T.L., Fatal metacestode infection in Bornean orangutan caused by unknown Versteria species (2014) Emerg. Infect Dis., 20, pp. 109-113; Ihms, E.A., Daniels, J.B., Koivisto, C.S., Barrie, M.T., Russell, D.S., Fatal Streptococcus anginosus-associated pneumonia in a captive Sumatran orangutan (Pongo abelii) (2014) J. Med. Primatol., 43, pp. 48-51; Nidom, C.A., Serological evidence of Ebola virus infection in Indonesian orangutans (2012) PLoS ONE, 7; Stuart, P., Entamoeba histolytica infections in wild and semi-wild orangutans in Sumatra and Kalimantan (2020) Am. J. Primatol., 82; Utsumi, T., Full genome characterization and phylogenetic analysis of hepatitis B virus in gibbons and a caretaker in Central Kalimantan, Indonesia (2015) Arch Virol., 160, pp. 685-692. , COI: 1:CAS:528:DC%2BC2MXmtlWmsA%3D%3D; Collet, J.Y., Galdikas, B.M.F., Sugarjito, J., Jojosudharmo, S., A coprological study of parasitism in orangutans (Pongo-Pygmaeus) in Indonesia (1986) J. Med. Primatol., 15, pp. 121-129. , COI: 1:STN:280:DyaL287ntFOitg%3D%3D; Foitova, I., Civanova, K., Barus, V., Nurcahyo, W., Phylogenetic relationships between pinworms (Nematoda: Enterobiinae) parasitising the critically endangered orang-utan, according to the characterisation of molecular genomic and mitochondrial markers (2014) Parasitol. Res., 113, pp. 2455-2466; Foitova, I., Redescription and resurrection of Bertiella satyri (Cestoda, Anoplocephalidae) parasitizing the orangutan (Pongo abelii) in Indonesia (2011) Parasitol. Res., 109, pp. 689-697; Pacheco, M.A., The origin of malarial parasites in orangutans (2012) PLoS ONE, 7; Xie, Y., Complete mitochondrial genomes of chimpanzee- and gibbon-derived Ascaris isolated from a zoological garden in southwest China (2013) PLoS ONE, 8; Hasegawa, H., Humans and great apes cohabiting the forest ecosystem in central african republic harbour the same hookworms (2014) PLoS Negl Trop Dis, 8; Huffman, M.A., Gotoh, S., Turner, L.A., Hamai, M., Yoshida, K., Seasonal trends in intestinal nematode infection and medicinal plant use among chimpanzees in the Mahale Mountains, Tanzania (1997) Primates, 38. , &; Kalousova, B., Diversity and transmission of soil transmitted strongylid nematodes between humans and other primates in the wild (2014) J. Nematol., 46, p. 182; Nejsum, P., Bertelsen, M.F., Betson, M., Stothard, J.R., Murrell, K.D., Molecular evidence for sustained transmission of zoonotic Ascaris suum among zoo chimpanzees (Pan troglodytes) (2010) Vet. Parasitol., 171, pp. 273-276. , COI: 1:CAS:528:DC%2BC3cXos1Kiu78%3D; Ravasi, D.F., O’Riain, M.J., Davids, F., Illing, N., Phylogenetic Evidence That Two Distinct Trichuris Genotypes Infect both Humans and Non-Human Primates (2012) Plos One, 7. , &; Seguel, M., Gottdenker, N., The diversity and impact of hookworm infections in wildlife (2017) Int. J. Parasitol. Par., 6, pp. 177-194; Thanchomnang, T., First molecular identification and genetic diversity of Strongyloides stercoralis and Strongyloides fuelleborni in human communities having contact with long-tailed macaques in Thailand (2017) Parasitol. Res., 116, pp. 1917-1923; Huffman, M.A., Caton, J.M., Self-induced increase of gut motility and the control of parasitic infections in wild chimpanzees (2001) Int. J. Primatol., 22, pp. 329-346; Makouloutou, P., Prevalence and genetic diversity of Oesophagostomum stephanostomum in wild lowland gorillas at Moukalaba-Doudou National Park, Gabon (2014) Helminthologia, 51, pp. 83-93; Ghai, R.R., Chapman, C.A., Omeja, P.A., Davies, T.J., Goldberg, T.L., Nodule worm infection in humans and wild primates in Uganda: cryptic species in a newly identified region of human transmission (2014) PLoS Negl. Trop. Dis., 8; Patrelle, C., Ferte, H., Jouet, D., Identification of Chabertiidae (Nematoda, Strongylida) by PCR-RFLP based method: a new diagnostic tool for cross transmission investigation between domestic and wild ruminants in France (2014) Infect. Genet. Evol., 28, pp. 15-20. , COI: 1:CAS:528:DC%2BC2cXhsV2ktbzK; Petersen, H.H., Andreasen, A., Kringel, H., Roepstorff, A., Thamsborg, S.M., Parasite population dynamics in pigs infected with Trichuris suis and Oesophagostomum dentatum (2014) Vet Parasitol, 199, pp. 73-80; Schar, F., The prevalence and diversity of intestinal parasitic infections in humans and domestic animals in a rural Cambodian village (2014) Parasitol. Int., 63, pp. 597-603; Blotkamp, J., Observations on the morphology of adults and larval stages of Oesophagostomum sp. isolated from man in northern Togo and Ghana (1993) J Helminthol, 67, pp. 49-61; Polderman, A.M., Blotkamp, J., Oesophagostomum infections in humans (1995) Parasitol Today, 11, pp. 451-456. , COI: 1:STN:280:DC%2BD2cznsVOrtQ%3D%3D; Polderman, A.M., Krepel, H.P., Baeta, S., Blotkamp, J., Gigase, P., Oesophagostomiasis, a common infection of man in northern Togo and Ghana (1991) Am. J. Trop. Med. Hyg., 44, pp. 336-344. , COI: 1:STN:280:DyaK3M3ktFCnuw%3D%3D; Krief, S., Clinical and pathologic manifestation of oesophagostomosis in African great apes: does self-medication in wild apes influence disease progression? (2008) J Med Primatol, 37, pp. 188-195; Nurcahyo, W., Konstanzova, V., Foitova, I., Parasites of orangutans (Primates: Ponginae): An overview (2017) Am J Primatol, p. 79. , https://doi.org/10.1002/ajp.22650; Arizono, N., Yamada, M., Tegoshi, T., Onishi, K., Molecular Identification of Oesophagostomum and Trichuris Eggs Isolated from Wild Japanese Macaques (2012) Korean J. Parasitol., 50, pp. 253-257; Frias, L., Molecular characterization of nodule worm in a community of Bornean primates (2019) Ecol Evol, 9, pp. 3937-3945; Gillespie, T.R., Greiner, E.C., Chapman, C.A., Gastrointestinal parasites of the colobus monkeys of Uganda (2005) J Parasitol, 91, pp. 569-573; Posada, D., jModelTest: phylogenetic model averaging (2008) Mol Biol Evol, 25, pp. 1253-1256; Blouin, M.S., Molecular prospecting for cryptic species of nematodes: mitochondrial DNA versus internal transcribed spacer (2002) Int J Parasitol, 32, pp. 527-531; Pafco, B., Metabarcoding analysis of strongylid nematode diversity in two sympatric primate species (2018) Sci Rep, 8, p. 5933; De Gruijter, J.M., Ziem, J., Verweij, J.J., Polderman, A.M., Gasser, R.B., Genetic substructuring within Oesophagostomum bifurcum (Nematoda) from human and non-human primates from Ghana based on random amplified polymorphic DNA analysis (2004) Am. J. Trop. Med. Hyg, 71, pp. 227-233; Gasser, R.B., de Gruijter, J.M., Polderman, A.M., Insights into the epidemiology and genetic make-up of Oesophagostomum bifurcum from human and non-human primates using molecular tools (2006) Parasitology, 132, pp. 453-460. , COI: 1:CAS:528:DC%2BD28XivVCgsbw%3D; Krief, S., Nodular worm infection in wild chimpanzees in Western Uganda: a risk for human health? (2010) PLoS Negl. Trop. Dis., 4; Ota, N., Molecular identification of Oesophagostomum spp. from ‘village’ chimpanzees in Uganda and their phylogenetic relationship with those of other primates (2015) R Soc Open Sci, 2; Mul, I.F., Paembonan, W., Singleton, I., Wich, S.A., van Bolhuis, H.G., Intestinal parasites of free-ranging, semicaptive, and captive Pongo abelii in sumatra, indonesia (2007) Int J Primatol, 28, pp. 407-420; Mynarova, A., Prevalence of Cryptosporidium spp., Enterocytozoon bieneusi, Encephalitozoon spp. and Giardia intestinalis in Wild, Semi-Wild and Captive Orangutans (Pongo abelii and Pongo pygmaeus) on Sumatra and Borneo (2016) Plos One, 11. , https://doi.org/10.1371/journal.pone.0152771, Indonesia; Labes, E.M., Nurcahyo, W., Deplazes, P., Mathis, A., Genetic characterization of Strongyloides spp. From captive, semi-captive and wild Bornean orangutans (Pongo pygmaeus) in Central and East Kalimantan, Borneo, Indonesia (2011) Parasitology, 138, pp. 1417-1422. , https://doi.org/10.1017/S0031182011001284; Reid, M.J., Transmission of human and macaque Plasmodium spp. to ex-captive orangutans in Kalimantan, Indonesia (2006) Emerg Infect Dis, 12, pp. 1902-1908; Vitone, N.D., Altizer, S., Nunn, C.L., Body size, diet and sociality influence the species richness of parasitic worms in anthropoid primates (2004) Evol. Ecol. Res., 6, pp. 183-199; Campbell-Smith, G., Campbell-Smith, M., Singleton, I., Linkie, M., Apes in space: saving an imperilled orangutan population in Sumatra (2011) PLoS ONE, 6. , COI: 1:CAS:528:DC%2BC3MXislCgs78%3D; Huffman, M.A., Self-medicative behavior in the African great apes: an evolutionary perspective into the origins of human traditional medicine (2001) Bioscience, 51, pp. 651-661; Huffman, M.A., Leaf-swallowing by chimpanzees: a behavioral adaptation for the control of strongyle nematode infections (1996) Int J Primatol, 17, pp. 475-503; Barelli, C., Huffman, M.A., Leaf swallowing and parasite expulsion in Khao Yai white-handed gibbons (Hylobates lar), the first report in an Asian ape species (2017) Am J Primatol, 79, pp. 1-7; Dubey, J.P., Characterization of Toxoplasma gondii from raccoons (Procyon lotor), coyotes (Canis latrans), and striped skunks (Mephitis mephitis) in Wisconsin identified several atypical genotypes (2007) J Parasitol, 93, pp. 1524-1527. , COI: 1:STN:280:DC%2BD1c7ls12rtA%3D%3D; Mercier, A., Human impact on genetic diversity of Toxoplasma gondii: example of the anthropized environment from French Guiana (2010) Infect. Genet. Evol., 11, pp. 1378-1387; Phuphisut, O., Molecular identification of the strongyloid nematode Oesophagostomum aculeatum in the Asian wild elephant Elephas maximus (2015) J Helminthol, pp. 1-7; Malaivijitnond, S., Chaiyabutr, N., Urasopon, N., Hamada, Y., Proceedings of the 32Nd Congress on Science and Technology of Thailand, pp. 73-77; Kamel, A.G.M., Yang, C.O., Norazah, A., Oesophagostomum aculeatum, the nodular worm causing helminthoma in man in Malaysia (1995) Int. Med. J., 2, pp. 287-290; Karim, N., Yang, C.O., Oesophagostomiasis in man: report of the first Malaysian case with emphasis on its pathology (1992) Malays. J. Pathol., 14, pp. 19-24. , COI: 1:STN:280:DyaK3s7gvVOkuw%3D%3D, PID: 1469913; Ross, R.A., Gibson, D.I., Harris, E.A., Cutaneous oesophagostomiasis in man (1989) J Helminthol, 63, pp. 261-265. , COI: 1:STN:280:DyaK3c%2FhtVShug%3D%3D; Sheater, A.L., The detection of intestinal protozoa and mange parasites by a flotation technique (1923) J Comp Pathol, 36, pp. 266-275; Garcia, L.S., Practical Guidance for Clinical Microbiology Laboratories: Laboratory Diagnosis of Parasites from the Gastrointestinal Tract (2018) Clin Microbiol Rev, 31. , https://doi.org/10.1128/CMR.00025-17; (2018) R: A Language and Environment for Statistical Computing; Rozas, J., Sanchez-DelBarrio, J.C., Messeguer, X., Rozas, R., DnaSP, DNA polymorphism analyses by the coalescent and other methods (2003) Bioinformatics, 19, pp. 2496-2497. , COI: 1:CAS:528:DC%2BD3sXpvVSisLo%3D; Bandelt, H.J., Forster, P., Rohl, A., Median-joining networks for inferring intraspecific phylogenies (1999) Mol Biol Evol, 16, pp. 37-48. , COI: 1:CAS:528:DyaK1MXjvVGltA%3D%3D; Huelsenbeck, J.P., Ronquist, F., MRBAYES: Bayesian inference of phylogenetic trees (2001) Bioinformatics, 17, pp. 754-755; Guindon, S., New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0 (2010) Syst Biol, 59, pp. 307-321. , –,., https://doi.org/10.1093/sysbio/syq010; Letunic, I., Bork, P., Interactive Tree Of Life (iTOL) v4: recent updates and new developments (2019) Nucleic Acids Res, 47, pp. W256-W259; Excoffier, L., Laval, G., Schneider, S., Arlequin (Version 3.0): An integrated software package for population genetics data analysis (2005) Evol Bioinform Online, 1, pp. 47-50; Bohonak, A.J., IBD (Isolation by Distance): a program for analyses of isolation by distance (2002) J Hered, 93, pp. 153-154; Husson, S.J., Orangutans geographic variation in behavioral ecology and conservation (2009) Orangutan Distribution, Density, Abundance and Impacts of Disturbance., pp. 77-96. , S. A. Wich, S. U. Atmoko, T. M. Setia & C. P. van Schaik (Eds.); Cheyne, S.M., Thompson, C.J., Phillips, A.C., Hill, R.M., Limin, S.H., Density and population estimate of gibbons (Hylobates albibarbis) in the Sabangau catchment, Central Kalimantan (2008) Indonesia. Primates, 49, pp. 50-56; van Schaik, C.P., The socioecology of fission-fusion sociality in Orangutans (1999) Primates, 40, pp. 69-86

Indexed by Scopus

Leave a Comment