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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, Indonesia

. 2016 ; 11 (3) : e0152771. [epub] 20160331

Language English Country United States Media electronic-ecollection

Document type Journal Article, Research Support, Non-U.S. Gov't

BACKGROUND: Orangutans are critically endangered primarily due to loss and fragmentation of their natural habitat. This could bring them into closer contact with humans and increase the risk of zoonotic pathogen transmission. AIMS: To describe the prevalence and diversity of Cryptosporidium spp., microsporidia and Giardia intestinalis in orangutans at seven sites on Sumatra and Kalimantan, and to evaluate the impact of orangutans' habituation and location on the occurrence of these zoonotic protists. RESULT: The overall prevalence of parasites in 298 examined animals was 11.1%. The most prevalent microsporidia was Encephalitozoon cuniculi genotype II, found in 21 animals (7.0%). Enterocytozoon bieneusi genotype D (n = 5) and novel genotype Pongo 2 were detected only in six individuals (2.0%). To the best of our knowledge, this is the first report of these parasites in orangutans. Eight animals were positive for Cryptosporidium spp. (2.7%), including C. parvum (n = 2) and C. muris (n = 6). Giardia intestinalis assemblage B, subtype MB6, was identified in a single individual. While no significant differences between the different human contact level groups (p = 0.479-0.670) or between the different islands (p = 0.992) were reported in case of E. bieneusi or E. cuniculi, Cryptosporidium spp. was significantly less frequently detected in wild individuals (p < 2×10-16) and was significantly more prevalent in orangutans on Kalimantan than on Sumatra (p < 2×10-16). CONCLUSION: Our results revealed that wild orangutans are significantly less frequently infected by Cryptosporidium spp. than captive and semi-wild animals. In addition, this parasite was more frequently detected at localities on Kalimantan. In contrast, we did not detect any significant difference in the prevalence of microsporidia between the studied groups of animals. The sources and transmission modes of infections were not determined, as this would require repeated sampling of individuals, examination of water sources, and sampling of humans and animals sharing the habitat with orangutans.

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Nater A, Arora N, Greminger MP, van Schaik CP, Singleton I, Wich SA, et al. Marked population structure and recent migration in the critically endangered Sumatran orangutan ( PubMed DOI

Wich SA. Distribution and conservation status of the orang-utan (

Wich SA, Fredriksson GM, Usher G, Peters HH, Priatna D, Basalamah F, et al. Hunting of Sumatran orang-utans and its importance in determining distribution and density. Biol Conserv. 2012;146(1):163–9. 10.1016/j.biocon.2011.12.006 WOS:000301814300018. DOI

Husson SJ, Wich SA, Marshall AJ, Dennis RD, Ancrenaz M, Brassey R, et al. Orangutan distribution, density, abundance and impacts of disturbance. 2009. p. 77–96.

Feng YY, Xiao LH. Zoonotic Potential and Molecular Epidemiology of PubMed DOI PMC

Xiao LH, Fayer R. Molecular characterisation of species and genotypes of PubMed DOI

Graczyk TK, Bosco-Nizeyi J, da Silva AJ, Moura INS, Pieniazek NJ, Cranfield MR, et al. A single genotype of PubMed DOI

Sak B, Kváč M, Petrželková K, Květoňová D, Pomajbíková K, Mulama M, et al. Diversity of microsporidia (Fungi: Microsporidia) among captive great apes in European zoos and African sanctuaries: evidence for zoonotic transmission? Folia Parasitol (Praha). 2011;58(2):81–6. . PubMed

Sak B, Petrželková KJ, Květoňová D, Mynářová A, Pomajbíková K, Modrý D, et al. Diversity of microsporidia, PubMed DOI PMC

Sak B, Petrželková KJ, Květoňová D, Mynařová A, Shutt KA, Pomajbíková K, et al. Long-term monitoring of microsporidia, PubMed DOI PMC

Butel C, Mundeke SA, Drakulovski P, Krasteva D, Ngole EM, Mallie M, et al. Assessment of Infections with Microsporidia and Cryptosporidium spp. in Fecal Samples from Wild Primate Populations from Cameroon and Democratic Republic of Congo. Int J Primatol. 2015;36(2):227–43. 10.1007/s10764-015-9820-x WOS:000353811400002. DOI

Nizeyi JB, Mwebe R, Nanteza A, Cranfield MR, Kalema GR, Graczyk TK. PubMed

Nizeyi JB, Cranfield MR, Graczyk TK. Cattle near the Bwindi Impenetrable National Park, Uganda, as a reservoir of PubMed

van Zijll Langhout M, Reed P, Fox M. Validation of multiple diagnostic techniques to detect PubMed

Mul IF, Paembonan W, Singleton I, Wich SA, van Bolhuis HG. Intestinal parasites of free-ranging, semicaptive, and captive DOI

Labes EM, Hegglin D, Grimm F, Nurcahyo W, Harrison ME, Bastian ML, et al. Intestinal parasites of endangered orangutans ( PubMed DOI

Hardus ME, Lameira AR, Menken SBJ, Wich SA. Effects of logging on orangutan behavior. Biol Conserv. 2012;146(1):177–87. 10.1016/j.biocon.2011.12.014 WOS:000301814300020. DOI

Warren KS, Heeney JL, Swan RA, Heriyanto, Verschoor EJ. A new group of hepadnaviruses naturally infecting orangutans ( PubMed PMC

Warren KS, Niphuis H, Heriyanto, Verschoor EJ, Swan RA, Heeney JL. Seroprevalence of specific viral infections in confiscated orangutans ( PubMed

Foitova I, Huffman MA, Wisnu N, Olsansky M. Parasites and their impacts on orangutan health In Orangutans: Geographic variation in Behavioral Ecology and Conservation. 2009:157–70.

Boubli J, Grelle CE, van Schaik C. Small mammal species diversity and composition in two ecologically distinct rain forest sites in Northen Sumatra, Indonesia. Ecotropica. 2004;10:149–54.

Rijksen HD. A field study on sumatran orangutans (

van Schaik CP, Wich SA, Utami SS, Odom K. A simple alternative to line transects of nests for estimating orangutan densities. Primates. 2005;46(4):249–54. 10.1007/s10329-005-0134-z PubMed DOI

van Schaik CP, Poniran S, Utami S, Griffiths M, Djojosudharmo S, Setia TM, et al. Estimates of orangutan distribution and status in Sumatra Neglected Ape. 1995:109–16. WOS:A1995BE97E00015.

van Schaik CP. The socioecology of fission-fusion sociality in Orangutans. Primates. 1999;40(1):69–86. 10.1007/BF02557703 . PubMed DOI

Mirmanto E. Vegetation analyses of Sebangau peat swamp forest, Central Kalimantan. Bioversitas. 2010;11:82–8.

Manduell KL, Harrison ME, Thorpe SK. Forest structure and support availability influence orangutan locomotion in Sumatra and Borneo. Am J Primatol. 2012;74(12):1128–42. PubMed

Descovich KA, Galdikas BM, Tribe A, Lisle A, Phillips CJ. Fostering Appropriate Behavior in Rehabilitant Orangutans ( DOI

Galdikas BFM. Orangutan diet, range, and activity at Tanjung Puting, Central Borneo. Int J Primatol. 1988;9:1–35.

Galdikas BM, Ashbury A. Reproductive parameters of female orangutans ( PubMed DOI

Buckholt MA, Lee JH, Tzipori S. Prevalence of PubMed PMC

Jiang J, Alderisio KA, Xiao L. Distribution of PubMed DOI PMC

Sulaiman IM, Fayer R, Bern C, Gilman RH, Trout JM, Schantz PM, et al. Triosephosphate isomerase gene characterization and potential zoonotic transmission of PubMed DOI PMC

Didier ES, Vossbrinck CR, Baker MD, Rogers LB, Bertucci DC, Shadduck JA. Identification and characterization of three PubMed

Katzwinkel-Wladarsch S, Lieb M, Helse W, Loscher T, Rinder H. Direct amplification and species determination of microsporidian DNA from stool specimens. Trop Med Int Health. 1996;1(3):373–8. . PubMed

Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987;4(4):406–25. PubMed

Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol. 2013;30(12):2725–9. 10.1093/molbev/mst197 PubMed DOI PMC

Le Blancq SM, Khramtsov NV, Zamani F, Upton SJ, Wu TW. Ribosomal RNA gene organization in PubMed

Keita MB, Hamad I, Bittar F. Looking in apes as a source of human pathogens. Microb Pathog. 2014;77:149–54. 10.1016/j.micpath.2014.09.003 WOS:000346459800024. PubMed DOI

Raoult D. The apes as reservoir of human pathogens. Clin Microbiol Infec. 2012;18(6):513- 10.1111/j.1469-0691.2012.03810.x WOS:000303981500010. PubMed DOI

Jones-Engel L, May CC, Engel GA, Steinkraus KA, Schillaci MA, Fuentes A, et al. Diverse contexts of zoonotic transmission of simian foamy viruses in Asia. Emerg Infect Dis. 2008;14(8):1200–8. 10.3201/eid1408.071430 WOS:000258216900003. PubMed DOI PMC

Messenger AM, Barnes AN, Gray GC. Reverse Zoonotic Disease Transmission (Zooanthroponosis): A Systematic Review of Seldom-Documented Human Biological Threats to Animals. PloS one. 2014;9(2). 10.1371/journal.pone.0089055 WOS:000332396200032. PubMed DOI PMC

Ye J X L, Ma J, Guo M, Liu L, Feng Y. Anthroponotic enteric parasites in monkeys in public park, China. Emerg Infect Dis. 2012;18:1640–3. 10.3201/eid1810.120653 PubMed DOI PMC

Wilson HB, Meijaard E, Venter O, Ancrenaz M, Possingham HP. Conservation Strategies for Orangutans: Reintroduction versus Habitat Preservation and the Benefits of Sustainably Logged Forest. PloS one. 2014;9(7):1–10. 10.1371/journal.pone.0102174 WOS:000339992400047. PubMed DOI PMC

Norhayati M, Al-Mekhlafi HM, Azlin M, Aini UN, Shaik A, Sa'iah A, et al. Intestinal microsporidial infections among Orang Asli (aborigine) children from Malaysia. Ann Trop Med Parasit. 2007;101(6):547–50. 10.1179/136485907x193789 WOS:000249554100013. PubMed DOI

Lono A, Kumar GS, Chye TT. Prevalence of microsporidia in an indigenous Orang Asli community in Pahang, Malaysia. T Roy Soc Trop Med H. 2010;104(3):214–8. 10.1016/j.trstmh.2009.07.006 WOS:000276000000007. PubMed DOI

Lono A, Kumar S, Chye TT. Detection of microsporidia in local HIV-positive population in Malaysia. T Roy Soc Trop Med H. 2011;105(7):409–13. 10.1016/j.trstmh.2011.03.006 WOS:000292789400009. PubMed DOI

Asma L, Johari S, Sim BLH, Lim YAL. How common is intestinal parasitism in HIV-infected patients in Malaysia? Trop Biomed. 2011;28(2):400–10. WOS:000295948100023. PubMed

Anuar TS, Al-Mekhlafi HM, Salleh FM, Moktar N. New Insights of Microsporidial Infection among Asymptomatic Aboriginal Population in Malaysia. PloS one. 2013;8(8). 10.1371/journal.pone.0071870 WOS:000323815200020. PubMed DOI PMC

Kurniawan A, Dwintasari W, Connelly L, Nichols RAB, Yunihastuti E, Karyadi T, et al. Cryptosporidium species from human immunodeficiency-infected patients with chronic diarrhea in Jakarta, Indonesia. Ann Epidemiol. 2013;23(11):720–3. 10.1016/j.annepidem.2013.07.019 WOS:000326137000009. PubMed DOI

Leelayoova S, Subrungruang I, Suputtamongkol Y, Worapong J, Petmitr PC, Mungthin M. Identification of genotypes of PubMed DOI PMC

Thellier M, Breton J. PubMed

Lim YA, Ngui R, Shukri J, Rohela M, Mat Naim HR. Intestinal parasites in various animals at a zoo in Malaysia. Vet Parasitol. 2008;157(1–2):154–9. Epub 2008/08/30. 10.1016/j.vetpar.2008.07.015 . PubMed DOI

Farizawati S, Lim YA, Ahmad RA, Fatimah CT, Siti-Nor Y. Contribution of cattle farms towards river contamination with PubMed

Ahmad SR, Reynolds DM. Synchronous fluorescence spectroscopy of wastewater and some potential constituents. Water research. 1995;29(6):1599–602.

Ananta SM, Suharno, Hidayat SA, Matsubayashi M. Survey on gastrointestinal parasites and detection of PubMed DOI

Lim YA, Aahmad RA. Occurrence of PubMed

Lim YA, Jex AR, Smith HV, Gasser RB. Cryptosporidiosis in Southeast Asia: what’s out there? Adv Parasitol. 2010;71:1–31.

Lai KP. Intestinal protozoan infections in Malaysia. Southeast Asian J Trop Med Public Health. 1992;23(4):578–86. . PubMed

Menon BS, Abdullah S, Mahamud F, Morgan UM, Malik AS, Choo KE, et al. Low prevalence of PubMed

Katsumata T, Hosea D, Wasito EB, Kohno S, Hara K, Soeparto P, et al. Cryptosporidiosis in Indonesia: a hospital-based study and a community-based survey. Am J Trop Med Hyg. 1998;59(4):628–32. Epub 1998/10/28. . PubMed

Kváč M, McEvoy J, Stenger B, Clark M. Cryptosporidiosis in other vertebrates In: Cacciò SM, Widmer G, editors.

Legesse M, Erko B. Zoonotic intestinal parasites in PubMed

da Silva AJ, Cacciò S, Williams C, Won KY, Nace EK, Whittier C, et al. Molecular and morphologic characterization of a PubMed

Gomez MS, Gracenea M, Gosalbez P, Feliu C, Ensenat C, Hidalgo R. Detection of Oocysts of Cryptosporidium in Several Species of Monkeys and in One Prosimian Species at the Barcelona-Zoo. Parasitol Res. 1992;78(7):619–20. 10.1007/Bf00936462 WOS:A1992JQ58900015. PubMed DOI

Gómez MS, Torres J, Gracenea M, Fernandez-Morán J, Gonzalez-Moreno O. Further report on PubMed

Karim MR, Zhang S, Jian F, Li J, Zhou C, Zhang L, et al. Multilocus typing of PubMed DOI

Muriuki SM, Murugu RK, Munene E, Karere GM, Chai DC. Some gastro-intestinal parasites of zoonotic (public health) importance commonly observed in old world non-human primates in Kenya. Acta Trop. 1998;71(1):73–82. . PubMed

Muriuki SM, Farah IO, Kagwiria RM, Chai DC, Njamunge G, Suleman M, et al. The presence of PubMed

Hope K, Goldsmith ML, Graczyk T. Parasitic health of olive baboons in Bwindi Impenetrable National Park, Uganda. Vet Parasitol. 2004;122(2):165–70. 10.1016/j.vetpar.2004.03.017 . PubMed DOI

Miller RA, Bronsdon MA, Kuller L, Morton WR. Clinical and parasitologic aspects of cryptosporidiosis in nonhuman primates. Lab Anim Sci. 1990;40(1):42–6. . PubMed

Heuschele WP, Oosterhuis J, Janssen D, Robinson PT, Ensley PK, Meier JE, et al. Cryptosporidial infections in captive wild animals. J Wildl Dis. 1986;22(4):493–6. Epub 1986/10/01. . PubMed

Russell RG, Rosenkranz SL, Lee LA, Howard H, Digiacomo RF, Bronsdon MA, et al. Epidemiology and Etiology of Diarrhea in Colony-Born Macaca-Nemestrina. Lab Anim Sci. 1987;37(3):309–16. WOS:A1987J026100005. PubMed

Du SZ, Zhao GH, Shao JF, Fang YQ, Tian GR, Zhang LX, et al. PubMed DOI PMC

Graczyk TK, DaSilva AJ, Cranfield MR, Nizeyi JB, Kalema GR, Pieniazek NJ. PubMed

Soba B, Petrovec M, Mioc V, Logar J. Molecular characterisation of PubMed DOI

Pedraza-Diaz S, Ortega-Mora LM, Carrion BA, Navarro V, Gomez-Bautista M. Molecular characterisation of PubMed DOI

Meireles MV, Soares RM, Bonello F, Gennari SM. Natural infection with zoonotic subtype of PubMed DOI

Meamar AR, Guyot K, Certad G, Dei-Cas E, Mohraz M, Mohebali M, et al. Molecular characterization of PubMed DOI PMC

McEvoy JM, Giddings CW. Cryptosporidium in commercially produced turkeys on-farm and postslaughter. Lett Appl Microbiol. 2009;48(3):302–6. Epub 2009/02/04. 10.1111/j.1472-765X.2008.02516.x . PubMed DOI

Hasajova A, Valencakova A, Malcekova B, Danisova O, Halan M, Goldova M, et al. Significantly higher occurrence of PubMed DOI

Iseki M, Maekawa T, Moriya K, Uni S, Takada S. Infectivity of PubMed DOI

Ryan U, Caccio SM. Zoonotic potential of PubMed DOI

Johnston AR, Gillespie TR, Rwego IB, McLachlan TLT, Kent AD, Goldberg TL. Molecular Epidemiology of Cross-Species PubMed DOI PMC

Majewska AC, Kasprzak W. Axenic Isolation of Giardia Strains from Primates and Rodents. Vet Parasitol. 1990;35(1–2):169–74. 10.1016/0304-4017(90)90127-W WOS:A1990CX61400017. PubMed DOI

Koehler AV, Jex AR, Haydon SR, Stevens MA, Gasser RB. PubMed DOI

Lalle M, Jimenez-Cardosa E, Caccio SM, Pozio E. Genotyping of PubMed DOI

Graczyk TK, Bosco-Nizeyi J, Ssebide B, Thompson RC, Read C, Cranfield MR. Anthropozoonotic PubMed DOI

Mahdy AKM, Lim YAL, Surin J, Wan KL, Al-Mekhlafi MSH. Risk factors for endemic giardiasis: highlighting the possible association of contaminated water and food. T Roy Soc Trop Med H. 2008;102(5):465–70. 10.1016/j.trstmh.2008.02.004 WOS:000256558800012. PubMed DOI

Al-Mekhlafi MSH, Azlin M, Aini UN, Shaik A, Sa'iah A, Fatmah MS, et al. Giardiasis as a predictor of childhood malnutrition in Orang Asli children in Malaysia. T Roy Soc Trop Med H. 2005;99(9):686–91. 10.1016/j.trstmh.2005.02.006 WOS:000230881700007. PubMed DOI

Choy SH, Al-Mekhlafi HM, Mahdy MA, Nasr NN, Sulaiman M, Lim YA, et al. Prevalence and associated risk factors of PubMed DOI PMC

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