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Soil-transmitted helminth infections in free-ranging non-human primates from Cameroon and Gabon

. 2021 Jul 05 ; 14 (1) : 354. [epub] 20210705

Language English Country England, Great Britain Media electronic

Document type Journal Article

Grant support
R01 AI050529 NIAID NIH HHS - United States

Links

PubMed 34225777
PubMed Central PMC8259424
DOI 10.1186/s13071-021-04855-7
PII: 10.1186/s13071-021-04855-7
Knihovny.cz E-resources

BACKGROUND: Zoonotic diseases are a serious threat to both public health and animal conservation. Most non-human primates (NHP) are facing the threat of forest loss and fragmentation and are increasingly living in closer spatial proximity to humans. Humans are infected with soil-transmitted helminths (STH) at a high prevalence, and bidirectional infection with NHP has been observed. The aim of this study was to determine the prevalence, genetic diversity, distribution and presence of co-infections of STH in free-ranging gorillas, chimpanzees and other NHP species, and to determine the potential role of these NHP as reservoir hosts contributing to the environmental sustenance of zoonotic nematode infections in forested areas of Cameroon and Gabon. METHODS: A total of 315 faecal samples from six species of NHPs were analysed. We performed PCR amplification, sequencing and maximum likelihood analysis of DNA fragments of the internal transcribed spacer 2 (ITS2) nuclear ribosomal DNA to detect the presence and determine the genetic diversity of Oesophagostomum spp., Necator spp. and Trichuris spp., and of targeted DNA fragments of the internal transcribed spacer 1 (ITS1) to detect the presence of Ascaris spp. RESULTS: Necator spp. infections were most common in gorillas (35 of 65 individuals), but also present in chimpanzees (100 of 222 individuals) and in one of four samples from greater spot-nosed monkeys. These clustered with previously described type II and III Necator spp. Gorillas were also the most infected NHP with Oesophagostomum (51/65 individuals), followed by chimpanzees (157/222 individuals), mandrills (8/12 samples) and mangabeys (7/12 samples), with O. stephanostomum being the most prevalent species. Oesophagostomum bifurcum was detected in chimpanzees and a red-capped mangabey, and a non-classified Oesophagostomum species was detected in a mandrill and a red-capped mangabey. In addition, Ternidens deminutus was detected in samples from one chimpanzee and three greater spot-nosed monkeys. A significant relative overabundance of co-infections with Necator and Oesophagostomum was observed in chimpanzees and gorillas. Trichuris sp. was detected at low prevalence in a gorilla, a chimpanzee and a greater spot-nosed monkey. No Ascaris was observed in any of the samples analysed. CONCLUSIONS: Our results on STH prevalence and genetic diversity in NHP from Cameroon and Gabon corroborate those obtained from other wild NHP populations in other African countries. Future research should focus on better identifying, at a molecular level, the species of Necator and Oesophagostomum infecting NHP and determining how human populations may be affected by increased proximity resulting from encroachment into sylvatic STH reservoir habitats.

See more in PubMed

Wolfe ND, Dunavan CP, Diamond J. Origins of major human infectious diseases. Nature. 2007;447(7142):279–283. doi: 10.1038/nature05775. PubMed DOI PMC

Calvignac-Spencer S, Leendertz SA, Gillespie TR, Leendertz FH. Wild great apes as sentinels and sources of infectious disease. Clin Microbiol Infect. 2012;18(6):521–527. doi: 10.1111/j.1469-0691.2012.03816.x. PubMed DOI

Junker J, Blake S, Boesch C, Campbell G, Du TL, Duvall C, et al. Recent decline in suitable environmental conditions for African great apes. Divers Distrib. 2012;18(11):1077–91. doi: 10.1111/ddi.12005. DOI

Hockings KJ, McLennan MR, Carvalho S, Ancrenaz M, Bobe R, Byrne RW, et al. Apes in the Anthropocene: flexibility and survival. Trends Ecol Evol. 2015;30(4):215–222. doi: 10.1016/j.tree.2015.02.002. PubMed DOI

Legesse M, Erko B. Zoonotic intestinal parasites in Papio anubis (baboon) and Cercopithecus aethiops (vervet) from four localities in Ethiopia. Acta Trop. 2004;90(3):231–236. doi: 10.1016/j.actatropica.2003.12.003. PubMed DOI

Krief S, Vermeulen B, Lafosse S, Kasenene JM, Nieguitsila A, Berthelemy M, et al. Nodular worm infection in wild chimpanzees in Western Uganda: a risk for human health? PLoS Negl Trop Dis. 2010;4(3):e630. doi: 10.1371/journal.pntd.0000630. PubMed DOI PMC

Cibot M, Guillot J, Lafosse S, Bon C, Seguya A, Krief S. 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 Negl Trop Dis. 2015;9(10):e0004133. doi: 10.1371/journal.pntd.0004133. PubMed DOI PMC

Schuster FL, Visvesvara GS. Amebae and ciliated protozoa as causal agents of waterborne zoonotic disease. Vet Parasitol. 2004;126(1–2):91–120. doi: 10.1016/j.vetpar.2004.09.019. PubMed DOI

Mossoun A, Pauly M, Akoua-Koffi C, Couacy-Hymann E, Leendertz SA, Anoh AE, et al. Contact to non-human primates and risk factors for zoonotic disease emergence in the Tai Region. Cote d'Ivoire Ecohealth. 2015;12(4):580–591. doi: 10.1007/s10393-015-1056-x. PubMed DOI

Narat V, Guillot J, Pennec F, Lafosse S, Gruner AC, Simmen B, et al. Intestinal helminths of wild bonobos in forest-Savanna Mosaic: risk assessment of cross-species transmission with local people in the Democratic Republic of the Congo. EcoHealth. 2015;12(4):621–633. doi: 10.1007/s10393-015-1058-8. PubMed DOI

Bethony J, Brooker S, Albonico M, Geiger SM, Loukas A, Diemert D, et al. Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet. 2006;367(9521):1521–1532. doi: 10.1016/S0140-6736(06)68653-4. PubMed DOI

World Health Organisation. Soil-transmitted helminth infections—fact sheets. 2020. https://www.who.int/news-room/fact-sheets/detail/soil-transmitted-helminth-infections. Accessed 21 May 2021.

Huffman MA, Gotoh S, Turner LA, Hamai M, Yoshida K. Seasonal trends in intestinal nematode infection and medicinal plant use among chimpanzees in the Mahale Mountains National Park. Tanzania Primates. 1997;38:111–125. doi: 10.1007/BF02382002. DOI

Terio KA, Kinsel MJ, Raphael J, Mlengeya T, Lipende I, Kirchhoff CA, et al. Pathologic lesions in chimpanzees (Pan trogylodytes schweinfurthii) from Gombe National Park, Tanzania, 2004–2010. J Zoo Wildl Med. 2011;42(4):597–607. doi: 10.1638/2010-0237.1. PubMed DOI PMC

Ghai RR, Chapman CA, Omeja PA, Davies TJ, Goldberg TL. Nodule worm infection in humans and wild primates in Uganda: cryptic species in a newly identified region of human transmission. PLoS Negl Trop Dis. 2014;8(1):e2641. doi: 10.1371/journal.pntd.0002641. PubMed DOI PMC

Ghai RR, Simons ND, Chapman CA, Omeja PA, Davies TJ, Ting N, et al. Hidden population structure and cross-species transmission of whipworms (Trichuris sp.) in humans and non-human primates in Uganda. PLoS Negl Trop Dis. 2014;8(10):e3256. doi: 10.1371/journal.pntd.0003256. PubMed DOI PMC

Hasegawa H, Modry D, Kitagawa M, Shutt KA, Todd A, Kalousova B, et al. Humans and great apes cohabiting the forest ecosystem in central african republic harbour the same hookworms. PLoS Negl Trop Dis. 2014;8(3):e2715. doi: 10.1371/journal.pntd.0002715. PubMed DOI PMC

McLennan MR, Hasegawa H, Bardi M, Huffman MA. Gastrointestinal parasite infections and self-medication in wild chimpanzees surviving in degraded forest fragments within an agricultural landscape mosaic in Uganda. PLoS ONE. 2017;12(7):e0180431. doi: 10.1371/journal.pone.0180431. PubMed DOI PMC

Ashford RW, Reid GD, Wrangham RW. Intestinal parasites of the chimpanzee Pan troglodytes in Kibale Forest, Uganda. Ann Trop Med Parasitol. 2000;94(2):173–179. doi: 10.1080/00034983.2000.11813526. PubMed DOI

Kalema-Zikusoka G, Rothman JM, Fox MT. Intestinal parasites and bacteria of mountain gorillas (Gorilla beringei beringei) in Bwindi Impenetrable National Park, Uganda. Primates. 2005;46(1):59–63. doi: 10.1007/s10329-004-0103-y. PubMed DOI

Doležalová J, Oborník M, Hajdušková E, Jirků M, Petrželková KJ, Bolechová P, et al. How many species of whipworms do we share? Whipworms from man and other primates form two phylogenetic lineages. Folia Parasitol. 2015;62:1–2. doi: 10.14411/fp.2015.063. PubMed DOI

Acha PN, Szyfres B. Zoonoses and communicable diseases common to man and animals. Volume III: Parasitoses. Washington: Pan American Health Organization; 2003. p. 285–324.

Landsoud-Soukate J, Tutin CE, Fernandez M. Intestinal parasites of sympatric gorillas and chimpanzees in the Lope Reserve. Gabon Ann Trop Med Parasitol. 1995;89(1):73–79. doi: 10.1080/00034983.1995.11812931. PubMed DOI

Ocaido M, Dranzoa C, Cheli P. Gastrointestinal parasites of baboons (Papio anubis) interacting with humans in West Bugwe Forest Reserve. Uganda Afr J Ecol. 2003;41:356–359. doi: 10.1111/j.1365-2028.2003.00483.x. DOI

Ashford RW, Crewe W. The parasites of Homo sapiens. London: Taylor & Francis; 2003.

Kalousova B, Hasegawa H, Petrzelkova KJ, Sakamaki T, Kooriyma T, Modry D. Adult hookworms (Necator spp.) collected from researchers working with wild western lowland gorillas. Parasites Vectors. 2016;9:75. doi: 10.1186/s13071-016-1357-0. PubMed DOI PMC

Pafco B, Kreisinger J, Cizkova D, Psenkova-Profousova I, Shutt-Phillips K, Todd A, et al. Genetic diversity of primate strongylid nematodes: do sympatric nonhuman primates and humans share their strongylid worms? Mol Ecol. 2019;28(21):4786–4797. doi: 10.1111/mec.15257. PubMed DOI

Krief S, Huffman M, Sevenet T, Guillot J, Bories C, Hladik CM, et al. Non-invasive monitoring of the health of Pan troglodytes schweinfurthii in Kibale National Park. Uganda Int J Primatol. 2005;26:467–490. doi: 10.1007/s10764-005-2934-9. DOI

Gillespie TR, Greiner EC, Chapman CA. Gastrointestinal parasites of the guenons of western Uganda. J Parasitol. 2004;90(6):1356–1360. doi: 10.1645/GE-311R. PubMed DOI

Gillespie TR, Greiner EC, Chapman CA. Gastrointestinal parasites of the colobus monkeys of Uganda. J Parasitol. 2005;91(3):569–573. doi: 10.1645/GE-434R. PubMed DOI

Nunn CL, Altizer S. Infectious diseases in primates: behavior, ecology and evolution. Oxford: Oxford University Press; 2006.

Zuk M, McKean KA. Sex differences in parasite infections: patterns and processes. Int J Parasitol. 1996;26(10):1009–1023. doi: 10.1016/S0020-7519(96)80001-4. PubMed DOI

Jourdan PM, Lamberton PHL, Fenwick A, Addiss DG. Soil-transmitted helminth infections. Lancet. 2018;391(10117):252–265. doi: 10.1016/S0140-6736(17)31930-X. PubMed DOI

Jia TW, Melville S, Utzinger J, King CH, Zhou XN. Soil-transmitted helminth reinfection after drug treatment: a systematic review and meta-analysis. PLoS Negl Trop Dis. 2012;6(5):e1621. doi: 10.1371/journal.pntd.0001621. PubMed DOI PMC

Neel C, Etienne L, Li Y, Takehisa J, Rudicell RS, Bass IN, et al. Molecular epidemiology of simian immunodeficiency virus infection in wild-living gorillas. J Virol. 2010;84(3):1464–1476. doi: 10.1128/JVI.02129-09. PubMed DOI PMC

Boue V, Locatelli S, Boucher F, Ayouba A, Butel C, Esteban A, et al. High rate of Simian Immunodeficiency Virus (SIV) infections in wild Chimpanzees in Northeastern Gabon. Viruses. 2015;7(9):4997–5015. doi: 10.3390/v7092855. PubMed DOI PMC

Gaillard CM, Pion SD, Hamou H, Sirima C, Bizet C, Lemarcis T, et al. Detection of DNA of filariae closely related to Mansonella perstans in faecal samples from wild non-human primates from Cameroon and Gabon. Parasites Vectors. 2020;13(1):313. doi: 10.1186/s13071-020-04184-1. PubMed DOI PMC

van der Kuyl AC, Kuiken CL, Dekker JT, Goudsmit J. Phylogeny of African monkeys based upon mitochondrial 12S rRNA sequences. J Mol Evol. 1995;40(2):173–180. doi: 10.1007/BF00167111. PubMed DOI

Etienne L, Locatelli S, Ayouba A, Esteban A, Butel C, Liegeois F, et al. Noninvasive follow-up of simian immunodeficiency virus infection in wild-living nonhabituated western lowland gorillas in Cameroon. J Virol. 2012;86(18):9760–9772. doi: 10.1128/JVI.01186-12. PubMed DOI PMC

Sullivan KM, Mannucci A, Kimpton CP, Gill P. A rapid and quantitative DNA sex test: fluorescence-based PCR analysis of X-Y homologous gene amelogenin. Biotechniques. 1993;15(4):636–8. PubMed

Gasser RB, Chilton NB, Hoste H, Beveridge I. Rapid sequencing of rDNA from single worms and eggs of parasitic helminths. Nucleic Acids Res. 1993;21(10):2525–2526. doi: 10.1093/nar/21.10.2525. PubMed DOI PMC

Romstad A, Gasser RB, Monti JR, Polderman AM, Nansen P, Pit DS, et al. Differentiation of Oesophagostomum bifurcum from Necator americanus by PCR using genetic markers in spacer ribosomal DNA. Mol Cell Probes. 1997;11(3):169–176. doi: 10.1006/mcpr.1996.0094. PubMed DOI

Das K, Chowdhury P, Ganguly S. Internal Transcribed Spacer 1 (ITS1) based sequence typing reveals phylogenetically distinct Ascaris population. Comput Struct Biotechnol J. 2015;13:478–483. doi: 10.1016/j.csbj.2015.08.006. PubMed DOI PMC

Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. PubMed DOI

Rozas J, Ferrer-Mata A, Sanchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, et al. DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol. 2017;34(12):3299–3302. doi: 10.1093/molbev/msx248. PubMed DOI

Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2015;32(1):268–274. doi: 10.1093/molbev/msu300. PubMed DOI PMC

Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods. 2017;14(6):587–589. doi: 10.1038/nmeth.4285. PubMed DOI PMC

Hoang DT, Chernomor O, von Haeseler A, Minh BQ, Vinh LS. UFBoot2: improving the ultrafast bootstrap approximation. Mol Biol Evol. 2018;35(2):518–522. doi: 10.1093/molbev/msx281. PubMed DOI PMC

Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 2010;59(3):307–21. doi: 10.1093/sysbio/syq010. PubMed DOI

Hasegawa H, Kalousova B, McLennan MR, Modry D, Profousova-Psenkova I, Shutt-Phillips KA, et al. Strongyloides infections of humans and great apes in Dzanga-Sangha Protected Areas, Central African Republic and in degraded forest fragments in Bulindi, Uganda. Parasitol Int. 2016;65:367–70. doi: 10.1016/j.parint.2016.05.004. PubMed DOI

Makouloutou P, Mbehang Nguema PP, Fujita S, Takenoshita Y, Hasegawa H, Yanagida T, et al. Prevalence and genetic diversity of Oesophagostomum stephanostomum in wild lowland gorillas at Moukalaba-Doudou National Park, Gabon. Helminthologia. 2014;51(2):83–93. doi: 10.2478/s11687-014-0214-y. DOI

Sleeman JM, Meader LL, Mudakikwa AB, Foster JW, Patton S. Gastrointestinal parasites of mountain gorillas (Gorilla gorilla beringei) in the Parc National des Volcans. Rwanda J Zoo Wildl Med. 2000;31(3):322–328. doi: 10.1638/1042-7260(2000)031[0322:GPOMGG]2.0.CO;2. PubMed DOI

Lilly AA, Mehlman PT, Doran D. Intestinal parasites in gorillas, chimpanzees, and humans at Mondika ResearchSite, Dzanga-Ndoki National Park, Central African Republic. Int J Parasitol. 2002;23:555–573.

Huffman MA, Pebsworth P, Bakuneeta C, Gotoh S, Bardi M. Chimpanzee–parasite ecology at Budongo Forest (Uganda) and the Mahale Mountains (Tanzania): influence of climatic differences on self-medicative behavior. In: Huffman MA, Chapman CA, editors. Primate parasite ecology: the dynamics and study of host–parasite relationships. Cambridge: Cambridge University Press; 2009. pp. 331–50.

Ota N, Hasegawa H, McLennan MR, Kooriyama T, Sato H, Pebsworth PA, et al. Molecular identification of Oesophagostomum spp from 'village' chimpanzees in Uganda and their phylogenetic relationship with those of other primates. R Soc Open Sci. 2015;2(11):150471. doi: 10.1098/rsos.150471. PubMed DOI PMC

Gillespie TR, Lonsdorf EV, Canfield EP, Meyer DJ, Nadler Y, Raphael J, et al. Demographic and ecological effects on patterns of parasitism in eastern chimpanzees (Pan troglodytes schweinfurthii) in Gombe National Park, Tanzania. Am J Phys Anthropol. 2010;143(4):534–544. doi: 10.1002/ajpa.21348. PubMed DOI PMC

Bakuza JS, Nkwengulila G. Variation over time in parasite prevalence among free-ranging chimpanzees at Gombe National Park, Tanzania. Int J Primatol. 2009;30:43. doi: 10.1007/s10764-008-9329-7. DOI

Kalousová B, Piel AK, Pomajbíková K, Modrý D, Stewart FA, Petrželková KJ. Gastrointestinal parasites of savanna chimpanzees (Pan troglodytes schweinfurthii) in Uganda, Tanzania. Int J Primatol. 2014;35:463–475. doi: 10.1007/s10764-014-9753-9. DOI

Petrzelkova KJ, Hasegawa H, Appleton CC, Huffman MA, Archer CE, Moscovice LR, et al. Gastrointestinal parasites of the chimpanzee population introduced onto Rubondo Island National Park, Tanzania. Am J Primatol. 2010;72(4):307–316. doi: 10.1002/ajp.20783. PubMed DOI

Drakulovski P, Bertout S, Locatelli S, Butel C, Pion S, Mpoudi-Ngole E, et al. Assessment of gastrointestinal parasites in wild chimpanzees (Pan troglodytes troglodytes) in southeast Cameroon. Parasitol Res. 2014;113(7):2541–2550. doi: 10.1007/s00436-014-3904-y. PubMed DOI PMC

Howells ME, Pruetz J, Gillespie TR. Patterns of gastro-intestinal parasites and commensals as an index of population and ecosystem health: the case of sympatric western chimpanzees (Pan troglodytes verus) and guinea baboons (Papio hamadryas papio) at Fongoli. Senegal Am J Primatol. 2011;73(2):173–179. doi: 10.1002/ajp.20884. PubMed DOI

Sa RM, Petrasova J, Pomajbikova K, Profousova I, Petrzelkova KJ, Sousa C, et al. Gastrointestinal symbionts of chimpanzees in Cantanhez National Park, Guinea-Bissau with respect to habitat fragmentation. Am J Primatol. 2013;75(10):1032–1041. doi: 10.1002/ajp.22170. PubMed DOI

Maisels F, Hicks TC, Hart J, Shah N. Cercocebus agilis (amended version of 2019 assessment). The IUCN Red List of Threatened Species 2020: e.T136615A167735266. 10.2305/IUCN.UK.2020-1.RLTS.T136615A167735266.en. Accessed 01 July 2021. DOI

Ankel-Simons F. Primate anatomy: an introduction. 3. San Diego: Elsevier Academic Press; 2007.

Kooriyama T, Hasegawa H, Shimozuru M, Tsubota T, Nishida T, Iwaki T. Parasitology of five primates in Mahale Mountains National Park, Tanzania. Primates. 2012;53(4):365–375. doi: 10.1007/s10329-012-0311-9. PubMed DOI

Arneberg P. Host population density and body mass as determinants of species richness in parasite communities: Comparative analyses of directly transmitted nematodes of mammals. Ecography. 2002;25(1):88–94. doi: 10.1034/j.1600-0587.2002.250110.x. DOI

Klein SL. Hormonal and immunological mechanisms mediating sex differences in parasite infection. Parasite Immunol. 2004;26(6–7):247–264. doi: 10.1111/j.0141-9838.2004.00710.x. PubMed DOI

van Bogaert O. A park for people and wildlife: World Wildlife Fund report. 2000. https://wwf.panda.org/?2085/A-park-for-people-and-wildlife. Accessed 01.12.2020.

von Linstow O. The American hookworm in chimpanzee. Am J Med. 1903;6:611.

Dollfus RP, Chabaud AJ. Cinq espèces de Nématodes chez un Atèle [Ateles ater (G. Cuvier 1823)] mort à la Ménagerie du Muséum. Arch Mus Histoire Nat. 1955;3:27–40.

Buckley JJC. On two new species of Enterobius from the monkey Lagothrix humboldtii. J Helminthol. 1931;9:133–140. doi: 10.1017/S0022149X00030364. DOI

Orihel TC. Necator americanus infection in primates. J Parasitol. 1971;57:117–121. doi: 10.2307/3277764. PubMed DOI

Ackert JE, Payne FK. Investigations on the control of hookworm disease XII. Studies on the occurrence, distribution and morphology of Necator suillus, including descriptions of the other species of Necator. Am J Hyg. 1922;3:1–25.

Noda R, Yamada H. On two species of nematodes, Necator gorillae sp. nov. (Ancylostomidae) and Chitwoodspirura wehri Chabaud and Rousselot, 1956 (Spiruridae), from a gorilla. Bull Univ Osaka Pref Ser B. 1964;15:175–180.

Gasser RB, Woods WG, Blotkamp C, Verweij J, Storey PA, Polderman AM. Screening for nucleotide variations in ribosomal DNA arrays of Oesophagostomum bifurcum by polymerase chain reaction-coupled single-strand conformation polymorphism. Electrophoresis. 1999;20(7):1486–1491. doi: 10.1002/(SICI)1522-2683(19990601)20:7<1486::AID-ELPS1486>3.0.CO;2-9. PubMed DOI

Polderman AM, Blotkamp J. Oesophagostomum infections in humans. Parasitol Today. 1995;11(12):451–456. doi: 10.1016/0169-4758(95)80058-1. PubMed DOI

Eberhard ML, Kovacs-Nace E, Blotkamp J, Verwij JJ, Asigri VA, Polderman AM. Experimental Oesophagostomum bifurcum in monkeys. J Helminthol. 2001;75(1):51–56. doi: 10.1079/joh200031. PubMed DOI

Bradbury RS. Ternidens deminutus revisited: a review of human infections with the false hookworm. Trop Med Infect Dis. 2019;4(3):106. 10.3390/tropicalmed4030106. PubMed PMC

Goldsmid JM. Ternidens infection. Parasitic zoonoses. Boca Raton: CRC Press; 1982. pp. 269–88.

Gasser RB, de Gruijter JM, Polderman AM. Insights into the epidemiology and genetic make-up of Oesophagostomum bifurcum from human and non-human primates using molecular tools. Parasitology. 2006;132(Pt 4):453–460. doi: 10.1017/S0031182005009406. PubMed DOI

Lello J, Boag B, Fenton A, Stevenson IR, Hudson PJ. Competition and mutualism among the gut helminths of a mammalian host. Nature. 2004;428(6985):840–844. doi: 10.1038/nature02490. PubMed DOI

Telfer S, Lambin X, Birtles R, Beldomenico P, Burthe S, Paterson S, et al. Species interactions in a parasite community drive infection risk in a wildlife population. Science. 2010;330(6001):243–246. doi: 10.1126/science.1190333. PubMed DOI PMC

Hotez PJ, Beaumier CM, Gillespie PM, Strych U, Hayward T, Bottazzi ME. Advancing a vaccine to prevent hookworm disease and anemia. Vaccine. 2016;34(26):3001–3005. doi: 10.1016/j.vaccine.2016.03.078. PubMed DOI

Periago MV, Bethony JM. Hookworm virulence factors: making the most of the host. Microbes Infect. 2012;14(15):1451–1464. doi: 10.1016/j.micinf.2012.09.002. PubMed DOI

Seguel M, Munoz F, Navarrete MJ, Paredes E, Howerth E, Gottdenker N. Hookworm Infection in South American Fur Seal (Arctocephalus australis) Pups. Vet Pathol. 2017;54(2):288–297. doi: 10.1177/0300985816677151. PubMed DOI

Traversa D. Pet roundworms and hookworms: a continuing need for global worming. Parasites Vectors. 2012;5:91. doi: 10.1186/1756-3305-5-91. PubMed DOI PMC

Orihel TC. Necator americanus infection in primates. J Parasitol. 1971;57(1):117–121. doi: 10.2307/3277764. PubMed DOI

Rijksen HD. Diseases and mortality factors. A field study on Sumatran orangutans (Pongo pygmaueus abelii Lesson 1827): ecology, behaviour and conservation. Wageningen: H. Veenman & Zonen BV; 1978. pp. 134–48.

Storey PA, Faile G, Hewitt E, Yelifari L, Polderman AM, Magnussen P. Clinical epidemiology and classification of human oesophagostomiasis. Trans R Soc Trop Med Hyg. 2000;94(2):177–182. doi: 10.1016/s0035-9203(00)90267-0. PubMed DOI

Rousselot R, Pellissier A. Esophagostomose nodulaire à Oesophagostomum stephanostomum. Pathologie du gorille et du chimpanzé. Bull Soc Pathol Exot. 1952;9:569–74.

Crestian J, Crespeau F. Observation d’un cas d’Oesophagostomose du chimpanzé. Rec Méd Vét. 1975;151:13–18.

Krief S, Jamart A, Mahe S, Leendertz FH, Matz-Rensing K, Crespeau F, et al. Clinical and pathologic manifestation of oesophagostomosis in African great apes: does self-medication in wild apes influence disease progression? J Med Primatol. 2008;37(4):188–195. doi: 10.1111/j.1600-0684.2008.00285.x. PubMed DOI

Fowler A, Koutsioni Y, Sommer V. Leaf-swallowing in Nigerian chimpanzees: evidence for assumed self-medication. Primates. 2007;48:73–76. doi: 10.1007/s10329-006-0001-6. PubMed DOI

Muehlenbein MP. Parasitological analyses of the male chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Kibale National Park, Uganda. Am J Primatol. 2005;65(2):167–179. doi: 10.1002/ajp.20106. PubMed DOI

Ebbert MA, McGrew WC, Marchant LF. Differences between chimpanzee and baboon gastrointestinal parasite communities. Parasitology. 2015;142(7):958–967. doi: 10.1017/S0031182015000104. PubMed DOI

Yao C, Walkush J, Shim D, Cruz K, Ketzis J. Molecular species identification of Trichuris trichiura in African green monkey on St. Kitts, West Indies. Vet Parasitol Reg Stud Rep. 2018;11:22–6. doi: 10.1016/j.vprsr.2017.11.004. PubMed DOI

Ravasi DF, O'Riain MJ, Davids F, Illing N. Phylogenetic evidence that two distinct Trichuris genotypes infect both humans and non-human primates. PLoS ONE. 2012;7(8):e44187. doi: 10.1371/journal.pone.0044187. PubMed DOI PMC

Cavallero S, Nejsum P, Cutillas C, Callejon R, Dolezalova J, Modry D, et al. Insights into the molecular systematics of Trichuris infecting captive primates based on mitochondrial DNA analysis. Vet Parasitol. 2019;272:23–30. doi: 10.1016/j.vetpar.2019.06.019. PubMed DOI

Cutillas C, de Rojas M, Zurita A, Oliveros R, Callejon R. Trichuris colobae n. sp. (Nematoda: Trichuridae), a new species of Trichuris from Colobus guereza kikuyensis. Parasitol Res. 2014;113(7):2725–32. doi: 10.1007/s00436-014-3933-6. PubMed DOI

Callejon R, Halajian A, Cutillas C. Description of a new species, Trichuris ursinus n. sp. (Nematoda: Trichuridae) from Papio ursinus Keer, 1792 from South Africa. Infect Genet Evol. 2017;51:182–93. doi: 10.1016/j.meegid.2017.04.002. PubMed DOI

Xie Y, Niu L, Zhao B, Wang Q, Nong X, Chen L, et al. Complete mitochondrial genomes of chimpanzee- and gibbon-derived Ascaris isolated from a zoological garden in southwest China. PLoS ONE. 2013;8(12):e82795. doi: 10.1371/journal.pone.0082795. PubMed DOI PMC

Nejsum P, Bertelsen MF, Betson M, Stothard JR, Murrell KD. Molecular evidence for sustained transmission of zoonotic Ascaris suum among zoo chimpanzees (Pan troglodytes) Vet Parasitol. 2010;171(3–4):273–276. doi: 10.1016/j.vetpar.2010.03.030. PubMed DOI

Pafco B, Benavides JA, Psenkova-Profousova I, Modry D, Cervena B, Shutt KA, et al. Do habituation, host traits and seasonality have an impact on protist and helminth infections of wild western lowland gorillas? Parasitol Res. 2017;116(12):3401–3410. doi: 10.1007/s00436-017-5667-8. PubMed DOI

Basuni M, Muhi J, Othman N, Verweij JJ, Ahmad M, Miswan N, et al. A pentaplex real-time polymerase chain reaction assay for detection of four species of soil-transmitted helminths. Am J Trop Med Hyg. 2011;84(2):338–343. doi: 10.4269/ajtmh.2011.10-0499. PubMed DOI PMC

Knopp S, Salim N, Schindler T, Karagiannis Voules DA, Rothen J, Lweno O, et al. Diagnostic accuracy of Kato-Katz, FLOTAC, Baermann, and PCR methods for the detection of light-intensity hookworm and Strongyloides stercoralis infections in Tanzania. Am J Trop Med Hyg. 2014;90(3):535–545. doi: 10.4269/ajtmh.13-0268. PubMed DOI PMC

Pilotte N, Papaiakovou M, Grant JR, Bierwert LA, Llewellyn S, McCarthy JS, et al. Improved PCR-based detection of soil transmitted helminth infections using a next-generation sequencing approach to assay design. PLoS Negl Trop Dis. 2016;10(3):e0004578. doi: 10.1371/journal.pntd.0004578. PubMed DOI PMC

Vlckova K, Kreisinger J, Pafco B, Cizkova D, Tagg N, Hehl AB, et al. Diversity of Entamoeba spp. in African great apes and humans: an insight from Illumina MiSeq high-throughput sequencing. Int J Parasitol. 2018;48(7):519–30. doi: 10.1016/j.ijpara.2017.11.008. PubMed DOI

Pafco B, Cizkova D, Kreisinger J, Hasegawa H, Vallo P, Shutt K, et al. Metabarcoding analysis of strongylid nematode diversity in two sympatric primate species. Sci Rep. 2018;8(1):5933. doi: 10.1038/s41598-018-24126-3. PubMed DOI PMC

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