Key to the success of orangutan conservation management practices is the prevention of the introduction of infectious diseases to the remaining populations. Previous reports of Entamoeba spp. positive orangutans are of concern as Entamoeba spp. infection has been linked to morbidity and mortality in primates. It remains to be determined if the Entamoeba species infecting orangutans is the pathogenic Entamoeba histolytica. Orangutan fecal samples have been collected from orangutans from sites in Sumatra (Bukit Lawang, Ketambe, and Suaq, 241 samples from 64 individuals), and two sites in Kalimantan (Sebangau and Tuanan, 129 samples from 39 individuals). All samples were from wild orangutans except for a proportion from Sumatra which were from semi-wild (108 samples, 10 individuals). E. histolytica-specific nested PCR assays were carried out on the fecal samples. A total of 36 samples from 17 individuals tested positive for E. histolytica. When compared with published sequences using NCBI BLAST the E. histolytica positive samples showed a 98-99% concordance. The majority (76%, n = 36) of the positive isolates came from semi-wild orangutans in Bukit Lawang. This study supports the growing body of evidence that contact with humans is an important risk factor for infection of wild primates with E. histolytica.

Borneo Nature Foundation Palankaraya Central Kalimantan Indonesia

College of Life and Environmental Sciences University of Exeter Penryn Campus Cornwall UK

Department of Botany and Zoology Masaryk University Brno Czech Republic

Department of Parasitology Gadjah Mada University Yogyakarta Indonesia

Department of Zoology School of Natural Sciences Trinity College Dublin Dublin Ireland

Royal School of Veterinary Studies University of Edinburgh Easter Bush Midlothian UK

Waterborne Disease Prevention Branch Centers for Disease Control and Prevention Atlanta Georgia

Zobrazit více v PubMed

Ali, I. K. M., Zaki, M., & Clark, C. G. (2005). Use of PCR amplification of tRNA gene-linked short tandem repeats for genotyping Entamoeba histolytica. Journal of Clinical Microbiology, 43(12), 5842-5847. https://doi.org/10.1128/JCM.43.12.5842-5847.2005

Ayeh-Kumi, P. F., Ali, I. M., Lockhart, L. A., Gilchrist, C. A., Petri, W. A., & Haque, R. (2001). Entamoeba histolytica: Genetic diversity of clinical isolates from Bangladesh as demonstrated by polymorphisms in the serine-rich gene. Experimental Parasitology, 99(2), 80-88. https://doi.org/10.1006/expr.2001.4652

Bangs, M. J., Purnomo, E. M. A., & Anderson, R. L. (1996). Intestinal parasites of humans in a highland community of Irian Jaya, Indonesia. Annals of Tropical Medicine & Parasitology, 90(1), 49-53. https://doi.org/10.1080/00034983.1996.11813025

Chang, A. M., Chen, C. C., & Huffman, M. A. (2019). Entamoeba spp. in wild formosan rock macaques (Macaca cyclopis) in an area with frequent human-macaque contact. Journal of Wildlife Diseases, 55, 608. https://doi.org/10.7589/2018-04-113

Clark, C. G., Kaffashian, F., Tawari, B., Windsor, J. J., Twigg-Flesner, A., Davies-Morel, M. C. G., … Tannich, E. (2006). New insights into the phylogeny of Entamoeba species provided by analysis of four new small-subunit rRNA genes. International Journal of Systematic and Evolutionary Microbiology, 56(Pt 9), 2235-2239. https://doi.org/10.1099/ijs.0.64208-0

Deere, J. R., Parsons, M. B., Lonsdorf, E. V., Lipende, I., Kamenya, S., Collins, D. A., … Gillespie, T. R. (2018). Entamoeba histolytica infection in humans, chimpanzees and baboons in the Greater Gombe Ecosystem, Tanzania. Parasitology, 146, 1116-1122. https://doi.org/10.1017/S0031182018001397

Diamond, L. S., & Clark, C. G. (1993). A redescription of Entamoeba histolytica Schaudinn, 1903 (Emended Walker, 1911) separating it from Entamoeba dispar Brumpt, 1925. Journal of Eukaryotic Microbiology, 40(3), 340-344. https://doi.org/10.1111/j.1550-7408.1993.tb04926.x

Ericsson, C. D. (1998). Travelers' diarrhea. Epidemiology, prevention, and self-treatment. Infectious Disease Clinics of North America, 12(2), 285-303. https://doi.org/10.1016/S0891-5520(05)70006-4

Feng, M., Cai, J., Min, X., Fu, Y., Xu, Q., Tachibana, H., & Cheng, X. (2013). Prevalence and genetic diversity of Entamoeba species infecting macaques in southwest China. Parasitology Research, 112(4), 1529-1536. https://doi.org/10.1007/s00436-013-3299-1

Feng, M., Yang, B., Yang, L., Fu, Y., Zhuang, Y., Liang, L., … Tachibana, H. (2011). High prevalence of Entamoeba infections in captive long-tailed macaques in China. Parasitology Research, 109(4), 1093-1097. https://doi.org/10.1007/s00436-011-2351-2

Foitová, I. (2002). Parasites in orangutans (Pongo pygmaeus Linnaeus 1760) with connection to the ecology and ethology factors. Veterinary and Farmaceutical University Brno, Czech Republic (unpublished doctoral dissertation).

Fotedar, R., Stark, D., Beebe, N., Marriott, D., Ellis, J., & Harkness, J. (2007). Laboratory diagnostic techniques for Entamoeba species. Clinical Microbiology Reviews, 20(3), 511-532. https://doi.org/10.1128/CMR.00004-07

Haq, A., Sharma, A., Ahmad, S., Khan, H. M., & Khan, N. (1985). Experimental infection of rhesus monkeys with Entamoeba histolytica mimics human infection. Laboratory Animal Science, 35(5), 481-484. https://www.ncbi.nlm.nih.gov/pubmed/2865401

Hardus, M. E., Lameira, A. R., Menken, S. B. J., & Wich, S. A. (2012). Effects of logging on orangutan behavior. Biological Conservation, 146(1), 177-187. https://doi.org/10.1016/j.biocon.2011.12.014

Husson, S. J., Wich, S. A., Marshall, A. J., Dennis, R. D., Ancrenaz, M., Brassey, R., … Singleton, I. (2009). Orangutans geographic variation in behavioral ecology and conservation. In S. A. Wich, S. U. Atmoko, T. M. Setia & C. P. van Schaik (Eds.), Orangutan distribution, density, abundance and impacts of disturbance (pp. 77-96). Oxford University Press.

IUCN. (2019). IUCN Red List of Threatened Species. Version 2019.2. Retrieved from www.iucnredlist.org

Jelinek, T., Peyerl, G., Löscher, T., & Nothdurft, H. D. (1996). Evaluation of an antigen-capture enzyme immunoassay for detection of Entamoeba histolytica in stool samples. European Journal of Clinical Microbiology and Infectious Diseases, 15(9), 752-755. https://doi.org/10.1007/BF01691966

Jirků-Pomajbíková, K., Čepička, I., Kalousová, B., Jirků, M., Stewart, F., Levecke, B., … Petrželková, K. J. (2016). Molecular identification of Entamoeba species in savanna woodland chimpanzees (Pan troglodytes schweinfurthii). Parasitology, 143(06), 741-748. https://doi.org/10.1017/S0031182016000263

Khairnar, K., & Parija, S. C. (2007). A novel nested multiplex polymerase chain reaction (PCR) assay for differential detection of Entamoeba histolytica, E. moshkovskii and E. dispar DNA in stool samples. BMC Microbiology, 7, 47. https://doi.org/10.1186/1471-2180-7-47

Kilbourn, A. M., Karesh, W. B., Wolfe, N. D., Bosi, E. J., Cook, R. A., & Andau, M. (2003). Health evaluation of free-ranging and semi-captive orangutans (Pongo pygmaeus pygmaeus) in Sabah, Malaysia. Journal of Wildlife Diseases, 39(1), 73-83. https://doi.org/10.7589/0090-3558-39.1.73, http://www.ncbi.nlm.nih.gov/pubmed/12685070

Leach, M., & Scoones, I. (2013). The social and political lives of zoonotic disease models: Narratives, science and policy. Social Science and Medicine, 88, 10-17. https://doi.org/10.1016/j.socscimed.2013.03.017

Levecke, B., Dorny, P., Vercammen, F., Visser, L. G., Van Esbroeck, M., Vercruysse, J., & Verweij, J. J. (2015). Transmission of Entamoeba nuttalli and Trichuris trichiura from nonhuman primates to humans. Emerging Infectious Diseases, 21, 1871-1872. https://doi.org/10.3201/eid2110.141456

Levecke, B., Dreesen, L., Dorny, P., Verweij, J. J., Vercammen, F., Casaert, S., … Geldhof, P. (2010). Molecular identification of Entamoeba spp. in captive nonhuman primates. Journal of Clinical Microbiology, 48(8), 2988-2990. https://doi.org/10.1128/JCM.00013-10

Macpherson, C. N. L. (2005). Human behaviour and the epidemiology of parasitic zoonoses. International Journal for Parasitology, 35, 1319-1331. https://doi.org/10.1016/j.ijpara.2005.06.004

Manduell, K. L., Harrison, M. E., & Thorpe, S. K. S. (2012). Forest structure and support availability influence orangutan locomotion in Sumatra and Borneo. American Journal of Primatology, 74(12), 1128-1142. https://doi.org/10.1002/ajp.22072

Marie, C., & Petri, W. A. (2014). Regulation of virulence of Entamoeba histolytica. Annual Review of Microbiology, 68(1), 493-520. https://doi.org/10.1146/annurev-micro-091313-103550

Messenger, A. M., Barnes, A. N., & Gray, G. C. (2014). Reverse zoonotic disease transmission (Zooanthroponosis): A systematic review of seldom-documented human biological threats to animals. PLoS One, 9(2):e89055. https://doi.org/10.1371/journal.pone.0089055

Muehlenbein, M. P., Martinez, L. A., Lemke, A. A., Ambu, L., Nathan, S., Alsisto, S., … Sakong, R. (2008). Perceived vaccination status in ecotourists and risks of anthropozoonoses. EcoHealth, 5(3), 371-378. https://doi.org/10.1007/s10393-008-0192-y

Muehlenbein, M. P., Martinez, L. A., Lemke, A. A., Ambu, L., Nathan, S., Alsisto, S., & Sakong, R. (2010). Unhealthy travelers present challenges to sustainable primate ecotourism. Travel Medicine and Infectious Disease, 8(3), 169-175. https://doi.org/10.1016/j.tmaid.2010.03.004

Mul, I. F., Paembonan, W., Singleton, I., Wich, S. A., Van Bolhuis, H. G., & Bolhuis, H. G. (2007). Intestinal parasites of free-ranging, semicaptive, and captive Pongo abelii in Sumatra, Indonesia. International Journal of Primatology, 28(2), 407-420. https://doi.org/10.1007/s10764-007-9119-7

Mynářová, A., Foitová, I., Kváč, M., Květoňová, D., Rost, M., Morrogh-Bernard, H., … Sak, B. (2016). 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. PLoS One, 11(3):e0152771. https://doi.org/10.1371/journal.pone.0152771

Nurcahyo, W., Konstanzová, V., & Foitová, I. (2017). Parasites of orangutans (primates: Ponginae): An overview. American Journal of Primatology, 79, e22650. https://doi.org/10.1002/ajp.22650

Peters, T. (1977). Serum albumin: Recent progress in the understanding of its structure and biosynthesis. Clinical Chemistry, 23(1), 5-12. https://www.ncbi.nlm.nih.gov/pubmed/318940

R Core Team. (2018). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. https://doi.org/10.1108/eb003648

Ragazzo, L. J., Zohdy, S., Velonabison, M., Herrera, J., Wright, P. C., & Gillespie, T. R. (2018). Entamoeba histolytica infection in wild lemurs associated with proximity to humans. Veterinary Parasitology, 249(December 2017), 98-101. https://doi.org/10.1016/j.vetpar.2017.12.002

Rijksen, H. D. (1978). A field study on Sumatran orangutans (Pongo pygmaeus abelii, Lesson 1827): ecology, behaviour, and conservation. University Wageningen, The Netherlands (unpublished doctoral dissertation).

Rivera, W. L., & Kanbara, H. (1999). Detection of Entamoeba dispar DNA in macaque feces by polymerase chain reaction. Parasitology Research, 85(6), 493-495. https://doi.org/10.1007/s.004360050583. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/10344544

Robertson, L. J., Clark, C. G., Debenham, J. J., Dubey, J. P., Kváč, M., Li, J., … Tsaousis, A. D. (2019). Are molecular tools clarifying or confusing our understanding of the public health threat from zoonotic enteric protozoa in wildlife? International Journal for Parasitology: Parasites and Wildlife, 9, 323-341. https://doi.org/10.1016/j.ijppaw.2019.01.010

Russon, A. E. (2009). Orangutans geographic variation in behavioral ecology and conservation. In S. A. Wich, S. U. Atmoko, T. M. Setia & C. P. van Schaik (Eds.), Orangutan rehabilitation and reintroduction: Successes, failures, and role in conservation (pp. 327-350). Oxford University Press.

Tachibana, H., Cheng, X. J., Kobayashi, S., Fujita, Y., & Udono, T. (2000). Entamoeba dispar, but not E. histolytica, detected in a colony of chimpanzees in Japan. Parasitology Research, 86(7), 537-541. https://doi.org/10.1007/s004360000205, http://www.ncbi.nlm.nih.gov/pubmed/10935902

Tachibana, H., Cheng, X. J., Kobayashi, S., Matsubayashi, N., Gotoh, S., & Matsubayashi, K. (2001). High prevalence of infection with Entamoeba dispar, but not E. histolytica, in captive macaques. Parasitology Research, 87(1), 14-17. https://doi.org/10.1007/s004360000289, http://www.ncbi.nlm.nih.gov/pubmed/11199843

Tachibana, H., Yanagi, T., Pandey, K., Cheng, X. J., Kobayashi, S., Sherchand, J. B., & Kanbara, H. (2007). An Entamoeba sp. strain isolated from rhesus monkey is virulent but genetically different from Entamoeba histolytica. Molecular and Biochemical Parasitology, 153(2), 107-114. https://doi.org/10.1016/j.molbiopara.2007.02.006

Tawari, B., Ali, I. K. M., Scott, C., Quail, M. A., Berriman, M., Hall, N., & Clark, C. G. (2008). Patterns of evolution in the unique tRNA gene arrays of the genus Entamoeba. Molecular Biology and Evolution, 25(1), 187-198. https://doi.org/10.1093/molbev/msm238

Tengku, S., & Norhayati, M. (2011). Public health and clinical importance of amoebiasis in Malaysia: A review. Tropical biomedicine, 58(11), 3516-3522. https://www.ncbi.nlm.nih.gov/pubmed/22041740

van Schaik, C. P. (1999). The socioecology of fission-fusion sociality in Orangutans. Primates, 40(1), 69-86. https://doi.org/10.1007/BF02557703

van Schaik, C. P., Poniran, S., Utami, S., Griffiths, M., Djojosudharmo, S., Setia, T. M., … Tilson, R. (1995). Estimates of orangutan distribution and status in Sumatra. In R. D. Nadler, B. F. M. Galdikas, L. K. Sheeran & N. Rosen (Eds.), The Neglected Ape (pp. 109-116). Boston, MA: Springer US. https://doi.org/10.1007/978-1-4899-1091-2_12

Verweij, J. J., Vermeer, J., Brienen, E. A. T., Blotkamp, C., Laeijendecker, D., van Lieshout, L., & Polderman, A. M. (2003). Entamoeba histolytica infections in captive primates. Parasitology Research, 90(2), 100-103. https://doi.org/10.1007/s00436-002-0808-z

Vlčková, K., Kreisinger, J., Pafčo, B., Čížková, D., Tagg, N., Hehl, A. B., & Modrý, D. (2018). Diversity of Entamoeba spp. in African great apes and humans: An insight from Illumina MiSeq high-throughput sequencing. International Journal for Parasitology, 48, 519-530. https://doi.org/10.1016/j.ijpara.2017.11.008

Walderich, B., Weber, A., & Knobloch, J. (1997). Differentiation of Entamoeba histolytica and Entamoeba dispar from German Travelers and Residents of Endemic Areas. The American Journal of Tropical Medicine and Hygiene, 57(1), 70-74. https://doi.org/10.4269/ajtmh.1997.57.70

Wilson, I. W., Weedall, G. D., & Hall, N. (2012). Host-Parasite interactions in Entamoeba histolytica and Entamoeba dispar: What have we learned from their genomes? Parasite Immunology, 34(2-3), 90-99. https://doi.org/10.1111/j.1365-3024.2011.01325.x

Wolfe, N. D., Escalante, A. A., Karesh, W. B., Kilbourn, A., Spielman, A., & Lal, A. A. (1998). Wild primate populations in emerging infectious disease research: The missing link? Emerging Infectious Diseases, 4(2), 149-158. https://doi.org/10.3201/eid0402.980202

Wolfe, N. D., Kilbourn, A. M., Karesh, W. B., Rahman, H. A., Bosi, E. J., Cropp, B. C., … Gubler, D. J. (2001). Sylvatic transmission of arboviruses among Bornean orangutans. American Journal of Tropical Medicine and Hygiene, 64, 310-316. https://doi.org/10.4269/ajtmh.2001.64.310

Yeager, C. P. (1997). Orangutan rehabilitation in Tanjung Puting National Park, Indonesia. Conservation Biology, 11, 802-805. https://doi.org/10.1046/j.1523-1739.1997.95500.x

Effect of selected Indonesian plants on Giardia intestinalis in an experimental in vitro model

Genetic characterization of nodular worm infections in Asian Apes