Diversity of Entamoeba spp. in Long-tailed Macaque (Macaca fascicularis) in Baluran and Alas Purwo National Parks, Indonesia




Abstract. Chrismanto D, Lastutui NDR, Suwanti LT, Hastutiek P, Kurniawati DA, Witaningrum AM, Paramita CA, Pratiwi A. 2022. Diversity of Entamoeba spp. in Long-tailed Macaque (Macaca fascicularis) in Baluran and Alas Purwo National Parks, Indonesia. Biodiversitas 23: 4524-4531. Entamoeba spp. is one of the most common protozoa in humans and non-human primates. Several species of Entamoeba are considered pathogenic, andone of them is Entamoeba histolytica has become a major public health concern. Contact between humans and Long-tailed Macaques (Macaca fascicularis) in Baluran National Park and Alas Purwo National Park has become more frequent in the last 10 years due to the habit of tourists providing food. This condition increases the potential of zoonoses between humans and Long-tailed Macaques. The aims of this study are to determine the diversity of species of Entamoeba spp. and the potential zoonosis from the Long-Tailed Macaque in Baluran and Alas Purwo National Park. In this study, 200 Fecal samples were collected from Long-tailed Macaques from Baluran National Park (100 samples) and Alas Purwo National Park (100 samples), examined both morphological and molecular examination with Entamoeba genus-specific primer. Positive samples were continued to be examined for the presence of 7 Entamoeba species by PCR amplification of the SSU rRNA gene. The results were found that 53% (53/100) of the samples were identified as Entamoeba spp. from Baluran National Park, and four Entamoeba species were identified, Entamoeba coli 84.9% (45/53), Entamoeba chattoni 58.9% (31/53), Entamoeba hartmanni 7.5% (4/53), and Entamoeba moshkovskii 13.2% (7/53), and among these, 58.49% (31/53) were mixed infections. The results from Alas Purwo National Park showed 82% (82/100) and three species of Entamoeba were detected by molecular tests, E. chattoni (90%), E. coli (85%) and E. moshkovskii (8.5%). The conclusion of the current study revealed the prevalence and diversity of Entamoeba species in Long-tailed Macaques in Baluran National Park and Alas Purwo National Park, Indonesia. This study is the first report on the diversity of Entamoeba species with molecular detection. The risk of zoonosis transmission in the region needs to be closely monitored.


Adhikari P and Dhakal P. 2018. Prevalence of Gastrointestinal Parasite of Rhesus Macaque (Macaca mulatta, 1780) and Hanuman langur (Semnopithecus Entellus Dufresne, 1797) In Devghat, Chitwan, Nepal. Journal of Institute of Science and Technology 22(2):12-18. DOI:https://doi.org/10.3126/jist.v22i2.19590
Atabati H, Kassiri H, Shamloo E, Akbari M, Atamaleki A. 2020. The association between the lack of safe drinking water and sanitation facilities with intestinal Entamoeba spp infection risk: A systematic review and meta-analysis. PLOS ONE 15(11): e0237102. DOI: https://doi.org/10.1371/journal.pone.0237102
Al-Areeqi MA, Sady H, Al-Mekhlafi HM, Anuar TS, Al-Adhroey AH, Atroosh WM, Dawaki S, Elyana FN, Nasr NA, Ithoi I, Lau YL, Surin J. 2017. First molecular epidemiology of Entamoeba histolytica, E. dispar and E. moshkovskii infections in Yemen: different species-specific associated risk factors. Tropical Medicine & International Health 22(4):493–504. DOI. 2017:https://doi.org/10.1111/tmi.12848
Ben Ayed L and Sabbahi S. 2017. Entamoeba histolytica. In: J.B. Rose and B. Jiménez-Cisneros (eds), Water and Sanitation for the 21st Century: Health and Microbiological Aspects of Excreta and Wastewater Management (Global Water Pathogen Project). (R. Fayer and W. Jakubowski (eds), Part 3: Specific Excreted Pathogens: Environmental and Epidemiology Aspects - Section 3: Protists), Michigan State University, E. Lansing, MI, UNESCO 3-35 p. DOI: https://doi.org/10.14321/waterpathogens.34
Calegar, D A., Nunes, B. C., Monteiro, K. J., Santos, J. P., Toma, H. K., Gomes, T. F., Lima, M. M., Bóia, M. N., & Carvalho-Costa, F A. 2016. Frequency and molecular characterisation of Entamoeba histolytica, Entamoeba dispar, Entamoeba moshkovskii, and Entamoeba hartmanni in the context of water scarcity in northeastern Brazil. Memorias do Instituto Oswaldo Cruz 111(2):114–119.DOI: https://doi.org/10.1590/0074-02760150383
Carrero JC, Reyes-Lopez M, Serrano-Luna J, Shibayama M, Unzueta J, Leon-Sicairos N, de la Garza M.2020. Intestinal amoebiasis: 160 years of its frst detection and still remains as a health problem in developing countries. Int J Med Microbiol IJMM 310(1):151358. DOI: 10.1016/j.ijmm.2019.151358
Chang AM, Chen CC, Huffman MA. 2019. Entamoeba Spp. In Wild Formosan Rock Macaques (Macaca Cyclopis) In An Area With Frequent Humanmacaque Contact. Journal of Wildlife Diseases 55(3): 608–618. DOI: https://doi.org/10.7589/2018-04-113
Debenham JJ, Tysnes K, Khunger S, Robertson LJ. 2017. Occurrence of Giardia, Cryptosporidium, and Entamoeba in wild rhesus macaques (Macaca mulatta) living in urban and semi-rural North-West India. International Journal for Parasitology: Parasites and Wildlife 6:29–34. DOI: https://doi.org/10.1016/j.ijppaw.2016.12.002
Deere JR, Parsons MB, Lonsdorf EV, Lipende I, Kamenya S, Collins DA, Travis DA, Gillespie TR. 2019. Entamoeba histolytica infection in humans, chimpanzees and baboons in the greater Gombe ecosystem, Tanzania. Parasitology 146:1116–1122. DOI: https://doi.org/10.1017/S0031182018001397.
Dong H, Li J, Qi M, Wang R, Yu F, Jian F, Ning C, Zhang L.2017. Prevalence, molecular epidemiology, and zoonotic potential of Entamoeba spp. in nonhuman primates in China. Infection, Genetics and Evolution 54:216–220. DOI: https://doi.org/10.1016/j.meegid.2017.07.002
Feng M, Yang B, Yang L, Fu Y, Zhuang Y, Liang L, Xu Q, Cheng X, Tachibana H. 2011. High prevalence of Entamoeba infections in captive long-tailed macaques in China. Parasitology Research 109:1093–1097. DOI: https://doi.org/10.1007/s00436-011-2351-2
Feng M, Cai J, Min X, Fu Y, Qing Xu, Tachibana H, Cheng X. 2013. Prevalence and genetic diversity of Entamoeba species infecting macaques in southwest China. Parasitology Research 112:1529–1536. DOI: https://doi.org/10.1007/s00436-013-3299-1
Fu B, Wang J. & Fu X. 2022. A rare case of extraintestinal amebiasis. BMC Infect Dis 22, 364. https://doi.org/10.1186/s12879-022-07348-9
Guan Y, Feng M, Cai J, Min X, Zhou X, Xu Q, Tan, Cheng X, Tachibana H. 2016. Comparative analysis of genotypic diversity in Entamoeba nuttalli isolates from Tibetan macaques and rhesus macaques in China. Infect. Genet. Evol. 38, 126–131. DOI: 10.1016/j.meegid.2015.12.014
Hamzah Z, Petmitr S, Mungthin M, Leelayoova S, Chavalitshewinkoon-Petmitr P. 2006. Differential detection of Entamoeba histolytica, Entamoeba dispar, and Entamoeba moshkovskii by a single-round PCR assay. Journal of Clinical Microbiology 44: 3196–3200. DOI: https://doi.org/10.1128/JCM.00778-06
Hansen MF, Hariyawan AW, Supriyanto S, Damanik AR. 2015. The interactions between long-tailed macaques (Macaca fascicularis) and tourists in Baluran National Park, Indonesia. Journal of Indonesian Natural History. 3: 36-41.DOI: http://jinh.fmipa.unand.ac.id/index.php/jinh/article/view/70
Hemmati A, Hooshmand E and Hosseini MJ. 2015. Identification of Entamoeba histolytica by molecular method in surface water of Rasht City, Iran. Iranian Journal of Public Health 44, 238–243. PMC:4401882; PMID: 25905058
Heredia RD, Fonseca JA, Lopez MC. 2015. Entamoeba moshkovskii perspectives of a new agent to be considered in
the diagnosis of amebiasis. Acta Tropica123(3):139–145.DOI: https://doi.org/10.1016/j.actatropica.2012.05.012
Jirku-Pomajbikova K, Cepicka I, Kalousova B, Jirku M, Stewart F, Levecke B, Modry D, Piel AK, Petrzelkova KJ.2016. Molecular identification of Entamoeba species in savanna woodland chimpanzees (Pan troglodytes schweinfurthii). Parasitology 143:741–748. DOI: https://doi.org/10.1017/S0031182016000263
Joesoef JA, Sajuthi D , Wijaya A, Sanam MUE. 2018. Endoparasitic Diversity in Macaca Fascicularis and Its Zoonotic Potential on Different Weather in Kupang City. Jurnal Veteriner 19(4): 451-459. DOI: https://doi.org/10.19087/jveteriner.2018.19.4.451
Lastuti NDR, Suwanti LT, Hastutiek P, Kurniawati DA, Puspitasari H. 2021. Molecular Detection of Entamoeba Spp in Long-tailed Macaque (Macaca fascicularis) at Baluran National Park, Indonesia. The Mal J Med Health Sci. 17(SUPP2): 85-88. eISSN: 2636-9346
Levecke B, Dorny P, Vercammen F, Visser LG, Van Esbroeck M, Vercruysse J, Verweij JJ. 2015. Transmission of Entamoeba nuttalli and Trichuris trichiura from nonhuman primates to humans. Emerging Infectious Diseasease 21:1871–1872. DOI: 10.3201/eid2110.141456
Levecke B, Dreesen L, Dorny P, Verweij JJ, Vercammen F, Casaert S, Vercruysse J, Geldhof P. 2010. Molecular identi?cation of Entamoeba spp. in captive nonhuman primates. Journal of Clinical Microbiology 48:2988–2990. DOI:https://doi.org/10.1128/JCM.00013-10
Li, J., Wang, Z., Karim, M.R. et al. Detection of human intestinal protozoan parasites in vegetables and fruits: a review. Parasites Vectors. 2020; 13: 380. DOI: https://doi.org/10.1186/s13071-020-04255-3
Madden GR, Shirley DA, Townsend G, Moonah S. 2019. Case report: lower gastrointestinal bleeding due to Entamoeba histolytica detected early by multiplex PCR: case report and review of the laboratory diagnosis of amebiasis. Am J Trop Med Hyg.101(6):1380–3. doi:10.4269/ajtmh.19-0237
Matsubayashi M, Murakoshi N, Komatsu T, Sasai K, and Shibahara T. 2019. Retrospective and Histopathological Studies of Entamoeba spp. and Other Pathogens Associated with Diarrhea and Wasting in Pigs in Aichi Prefecture, Japan. Japan Agricultural Research Quarterly 53(1):59-67.
Nunn CL and Altizer SM.2006. Infectious diseases in primates: behavior, ecology and evolution. Oxford University Press. Oxford Scholarship Online. DOI: 10.1093/acprof:oso/9780198565857.001.000
Parija SC and Khairnar K.2005. Entamoeba moshkovskii and Entamoeba dispar-associated infections in Pondicherry, India. Journal of Health, Population and Nutrition 23: 292–295.PMID: 16262027
Pu LH, Li Z, Wu J, Zhang YL, Chen J, Yang JF and Zou F. 2020. Prevalence, molecular epidemiology and zoonotic risk of Entamoeba spp. from experimental macaques in Yunnan Province, southwestern China. Parasitology Research, 119(8), pp.2733-2740. DOI:https://doi.org/10.1007/s00436-020-06762-9
Putra AAWK, Wandia IN, Dwinata IM.2020. Prevalence and Identification of Gastrointestinal Protozoa In LongTail Monkey in Nusa Penida Island. Buletin Veteriner Udayana 12 (1): 80-85. DOI: https://doi.org/10.24843/bulvet.2020.v12.i01.p14
Regan CS, Yon L, Hossain M, Elsheikha HM. 2014. Prevalence of Entamoeba species in captive primates in zoological gardens in the UK. PeerJ. 2:e492. DOI: 10.7717/peerj.492
Robertson, L., Clark, C., Debenham, J., Dubey, J., Kvá?, M., Li, J., Ponce-Gordo, F., Ryan, U., Schares, G., Su, C. and Tsaousis, A., 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, pp.323-341. doi: 10.1016/j.ijppaw.2019.01.010
Singh A, Banerjee T, Khan U, Shukla SK. 2021. Epidemiology of clinically relevant Entamoeba spp. (E. histolytica/dispar/moshkovskii/ bangladeshi): A cross sectional study from North India. PLoS Negl Trop Dis. 15(9): e0009762. DOI: https://doi.org/10.1371/journal.pntd.0009762
Skappak C, Akierman S, Belga S, Novak K, Chadee K, Urbanski SJ, Church D, Beck PL. 2014. Invasive amoebiasis: a review of Enta-moeba infections highlighted with case reports. Canadian Journal of Gastroenterology and Hepatology. 28: 355-359. DOI: https://doi.org/10.1155/2014/745130
Tachibana H. 2016. Identi?cation of Entamoeba polecki with Unique 18S rRNA Gene Sequences from Celebes Crested Macaques and Pigs in Tangkoko Nature Reserve, North Sulawesi, Indonesia. Journal of Eukaryotic Microbiology. 1–6. DOI: https://doi.org/10.1111/jeu.12304
Tharmaratnam T, Kumanan T, Iskandar MA, D'Urzo K, Gopee-Ramanan P, Loganathan M, Tabobondung T, Tabobondung TA, Sivagurunathan S, Patel M & Tobbia I. 2020. Entamoeba histolytica and amoebic liver abscess in northern Sri Lanka: a public health problem. Tropical medicine and health. 48: 2. DOI: https://doi.org/10.1186/s41182-020-0193-2
Verweij JJ, Polderman AM, Clark CG. 2001. Genetic variation among human isolates of uninucleated cyst-producing Entamoeba species. Journal of Clinical Microbiology 39: 1644–1646. DOI: https://doi.org/10.1128/JCM.39.4.1644-1646.2001
Yakoob J, Abbas Z, Beg MA, Naz S, Khan R, Jafri W. 2012. Entamoeba species associated with chronic diarrhoea in Pakistan. Epidemiology and Infection 140(2):323 – 328. DOI:10.1017/S0950268811000215
Zhang Q, Liu K, Wang C, Luo J, Lu J, He H.2019. Molecular characterization of Entamoeba spp. in wild Taihangshan macaques (Macaca mulatta tcheliensis) in China. Acta Parasitologica.64:228–231.DOI: https://doi.org/10.2478/s11686-019-00026-y

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