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Prevalence, molecular epidemiology and zoonotic risk of Entamoeba spp. from experimental macaques in Yunnan Province, southwestern China

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Abstract

Amebiasis is a worldwide parasitic zoonosis, with symptoms of abdominal discomfort, indigestion, diarrhea, and even death. However, limited information about the prevalence of Entamoeba spp. in experimental nonhuman primates (NHPs) in southwestern China is available. The objective of the current study was to investigate the frequency and species identity of Entamoeba to evaluate potential zoonotic risk factors for Entamoeba spp. infection in experimental NHPs. A total of 505 fecal samples were collected from NHPs (macaques) and analyzed by PCR analysis the small subunit rRNA (SSU rRNA) gene of Entamoeba spp. Forty-seven specimens were positive for Entamoeba spp., and the prevalence of Entamoeba spp. was 9.31% (47/505). Significant differences in the prevalence rates among the three breeds (P = 0.002 < 0.01, df = 2, χ2 = 12.33) and feed types (P = 0.001 < 0.01, df = 1, χ2 = 10.12) were observed. Altogether, four Entamoeba species, including E. dispar (57.44%), E. chattoni (29.78%), E. histolytica (6.38%), and E. coli (6.38%), were identified by DNA sequence analysis. The results suggested a low prevalence but high diversity of Entamoeba species in experimental NHPs in Yunnan Province, southwestern China. Results of this study contribute to the knowledge of the genetic characteristics of Entamoeba spp. in NHPs.

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Data availability

The datasets supporting the conclusions in this article are included within the article. All the sequences of the obtained SSU rRNA genes were deposited in GenBank, with the following accession nos: MK559460–MK559471.

References

  • Ali IK, Hossain MB, Roy S, Ayeh-Kumi PF, Petri WA Jr, Haque R, Clark CG (2003) Entamoeba moshkovskii infections in children, Bangladesh. Emerg Infect Dis 9:580–584

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Altshuler D, Pollara VJ, Cowles CR, Van Etten WJ, Baldwin J, Linton L, Lander ES (2000) An SNP map of the human genome generated by reduced representation shotgun sequencing. Nature 407:513–516

    Article  CAS  PubMed  Google Scholar 

  • Apetrei C, Robertson DL, Marx PA (2004) The history of SIVS and AIDS: epidemiology, phylogeny and biology of isolates from naturally SIV infected non-human primates (NHP) in Africa. Front Biosci 9:225–254

    Article  CAS  PubMed  Google Scholar 

  • Berrilli F, Prisco C, Friedrich KG, Di Cerbo P, Di Cave D, De Liberato C (2011) Giardia duodenalis assemblages and Entamoeba species infecting non-human primates in an Italian zoological garden: zoonotic potential and management traits. Parasit Vectors 4:199

    Article  PubMed  PubMed Central  Google Scholar 

  • Chihi A, Stensvold CR, Ben-Abda I, Ben-Romdhane R, Aoun K, Siala E, Bouratbine A (2019) Development and evaluation of molecular tools for detecting and differentiating intestinal amoebae in healthy individuals. Parasitology 146:821–827

    Article  CAS  PubMed  Google Scholar 

  • Clark CG, Diamond LS (1991) The Laredo strain and other 'Entamoeba histolytica-like' amoebae are Entamoeba moshkovskii. Mol Biochem Parasitol 46:11–18

    Article  CAS  PubMed  Google Scholar 

  • 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. Int J Parasitol Parasites Wildl 6:29–34

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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. Infect Genet Evol 54:216–220

    Article  PubMed  Google Scholar 

  • Elsheikha HM, Regan CS, Clark CG (2018) Novel Entamoeba findings in nonhuman primates. Trends Parasitol 34:283–294

    Article  PubMed  Google Scholar 

  • 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. Parasitol Res 109:1093–1097

    Article  PubMed  Google Scholar 

  • Feng M, Yanagi T, Putaporntip C, Pattanawong U, Cheng X, Jongwutiwes S, Tachibana H (2019) Correlation between genotypes and geographic distribution of Entamoeba nuttalli isolates from wild long-tailed macaques in Central Thailand. Infect Genet Evol 70:114–122

    Article  PubMed  Google Scholar 

  • Folch J, Busquets O, Ettcheto M, Sanchez-Lopez E, Pallas M, Beas-Zarate C, Marin M, Casadesus G, Olloquequi J, Auladell C, Camins A (2018) Experimental models for aging and their potential for novel drug discovery. Curr Neuropharmacol 16:1466–1483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Karere GM, Munene E (2002) Some gastro-intestinal tract parasites in wild De Brazza's monkeys (Cercopithecus neglectus) in Kenya. Vet Parasitol 110:153–157

    Article  CAS  PubMed  Google Scholar 

  • Kebede A, Verweij JJ, Petros B, Polderman AM (2004) Short communication: misleading microscopy in amoebiasis. Tropical Med Int Health 9:651–652

    Article  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Levecke B, Dorny P, Geurden T, Vercammen F, Vercruysse J (2007) Gastrointestinal protozoa in non-human primates of four zoological gardens in Belgium. Vet Parasitol 148:236–246

    Article  PubMed  Google Scholar 

  • Levecke B, Dreesen L, Dorny P, Verweij JJ, Vercammen F, Casaert S, Vercruysse J, Geldhof P (2010) Molecular identification of Entamoeba spp. in captive nonhuman primates. J Clin Microbiol 48:2988–2990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li M, Zhao B, Li B, Wang Q, Niu L, Deng J, Gu X, Peng X, Wang T, Yang G (2015) Prevalence of gastrointestinal parasites in captive non-human primates of twenty-four zoological gardens in China. J Med Primatol 44:168–173

    Article  PubMed  PubMed Central  Google Scholar 

  • Li J, Dong H, Wang R, Yu F, Wu Y, Chang Y, Wang C, Qi M, Zhang L (2017) An investigation of parasitic infections and review of molecular characterization of the intestinal protozoa in nonhuman primates in China from 2009 to 2015. Int J Parasitol Parasites Wildl 6:8–15

    Article  PubMed  PubMed Central  Google Scholar 

  • Li WC, Geng JZ, Chen C, Qian L, Zhang T, Liu JL, Luo JX, Gu YF (2018) First report on the occurance of intestinal Entamoeba spp. in pigs in China. Acta Trop 185:385–390

    Article  PubMed  Google Scholar 

  • Lozano R, Naghavi M, Foreman K, Lim S, Shibuya K, Aboyans V, Abraham J, Adair T, Aggarwal R, Ahn SY, AlMazroa MA, Alvarado M, Anderson HR, Anderson LM, Andrews KG, Atkinson C, Baddour LM, Barker-Collo S, Bartels DH, Bell ML, Benjamin EJ, Bennett D, Bhalla K, Bikbov B, Abdulhak AB, Birbeck G, Blyth F, Bolliger I, Boufous S, Bucello C, Burch M, Burney P, Carapetis J, Chen H, Chou D, Chugh SS, Coffeng LE, Colan SD, Colquhoun S, Colson KE, Condon J, Connor MD, Cooper LT, Corriere M, Cortinovis M, de Vaccaro KC, Couser W, Cowie BC, Criqui MH, Cross M, Dabhadkar KC, Dahodwala N, de Leo D, Degenhardt L, Delossantos A, Denenberg J, Des Jarlais DC, Dharmaratne SD, Dorsey ER, Driscoll T, Duber H, Ebel B, Erwin PJ, Espindola P, Ezzati M, Feigin V, Flaxman AD, Forouzanfar MH, Fowkes FGR, Franklin R, Fransen M, Freeman MK, Gabriel SE, Gakidou E, Gaspari F, Gillum RF, Gonzalez-Medina D, Halasa YA, Haring D, Harrison JE, Havmoeller R, Hay RJ, Hoen B, Hotez PJ, Hoy D, Jacobsen KH, James SL, Jasrasaria R, Jayaraman S, Johns N, Karthikeyan G, Kassebaum N, Keren A, Khoo JP, Knowlton LM, Kobusingye O, Koranteng A, Krishnamurthi R, Lipnick M, Lipshultz SE, Ohno SL, Mabweijano J, MacIntyre MF, Mallinger L, March L, Marks GB, Marks R, Matsumori A, Matzopoulos R, Mayosi BM, McAnulty JH, McDermott MM, McGrath J, Memish ZA, Mensah GA, Merriman TR, Michaud C, Miller M, Miller TR, Mock C, Mocumbi AO, Mokdad AA, Moran A, Mulholland K, Nair MN, Naldi L, Narayan KMV, Nasseri K, Norman P, O'Donnell M, Omer SB, Ortblad K, Osborne R, Ozgediz D, Pahari B, Pandian JD, Rivero AP, Padilla RP, Perez-Ruiz F, Perico N, Phillips D, Pierce K, Pope CA III, Porrini E, Pourmalek F, Raju M, Ranganathan D, Rehm JT, Rein DB, Remuzzi G, Rivara FP, Roberts T, de León FR, Rosenfeld LC, Rushton L, Sacco RL, Salomon JA, Sampson U, Sanman E, Schwebel DC, Segui-Gomez M, Shepard DS, Singh D, Singleton J, Sliwa K, Smith E, Steer A, Taylor JA, Thomas B, Tleyjeh IM, Towbin JA, Truelsen T, Undurraga EA, Venketasubramanian N, Vijayakumar L, Vos T, Wagner GR, Wang M, Wang W, Watt K, Weinstock MA, Weintraub R, Wilkinson JD, Woolf AD, Wulf S, Yeh PH, Yip P, Zabetian A, Zheng ZJ, Lopez AD, Murray CJL (2012) Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the global burden of disease study 2010. Lancet 380:2095–2128

    Article  PubMed  Google Scholar 

  • Mi-Ichi F, Miyake Y, Tam VK, Yoshida H (2018) A flow Cytometry method for dissecting the cell differentiation process of Entamoeba Encystation. Front Cell Infect Microbiol 8:250

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Munene E, Otsyula M, Mbaabu DA, Mutahi WT, Muriuki SM, Muchemi GM (1998) Helminth and protozoan gastrointestinal tract parasites in captive and wild-trapped African non-human primates. Vet Parasitol 78:195–201

    Article  CAS  PubMed  Google Scholar 

  • Nath J, Ghosh SK, Singha B, Paul J (2015) Molecular epidemiology of Amoebiasis: a cross-sectional study among north east Indian population. PLoS Negl Trop Dis 9:e0004225

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Parkar U, Traub RJ, Vitali S, Elliot A, Levecke B, Robertson I, Geurden T, Steele J, Drake B, Thompson RC (2010) Molecular characterization of Blastocystis isolates from zoo animals and their animal-keepers. Vet Parasitol 169:8–17

    Article  CAS  PubMed  Google Scholar 

  • Petri WA Jr, Haque R, Lyerly D, Vines RR (2000) Estimating the impact of amebiasis on health. Parasitol Today 16:320–321

    Article  PubMed  Google Scholar 

  • Pourrut X, Diffo JL, Somo RM, Bilong Bilong CF, Delaporte E, LeBreton M, Gonzalez JP (2011) Prevalence of gastrointestinal parasites in primate bushmeat and pets in Cameroon. Vet Parasitol 175:187–191

    Article  CAS  PubMed  Google Scholar 

  • Pullan RL, Sturrock HJ, Soares Magalhaes RJ, Clements AC, Brooker SJ (2012) Spatial parasite ecology and epidemiology: a review of methods and applications. Parasitology 139:1870–1887

    Article  PubMed  Google Scholar 

  • Ragazzo LJ, Zohdy S, Velonabison M, Herrera J, Wright PC, Gillespie TR (2018) Entamoeba histolytica infection in wild lemurs associated with proximity to humans. Vet Parasitol 249:98–101

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Rivera WL, Kanbara H (1999) Detection of Entamoeba dispar DNA in macaque feces by polymerase chain reaction. Parasitol Res 85:493–495

    Article  CAS  PubMed  Google Scholar 

  • Rivera WL, Yason JA, Adao DE (2010) Entamoeba histolytica and E. dispar infections in captive macaques (Macaca fascicularis) in the Philippines. Primates 51:69–74

    Article  PubMed  Google Scholar 

  • Saidin S, Othman N, Noordin R (2019) Update on laboratory diagnosis of amoebiasis. Eur J Clin Microbiol Infect Dis 38:15–38

    Article  PubMed  Google Scholar 

  • Standley CJ, Mugisha L, Dobson AP, Stothard JR (2012) Zoonotic schistosomiasis in non-human primates: past, present and future activities at the human-wildlife interface in Africa. J Helminthol 86:131–140

    Article  CAS  PubMed  Google Scholar 

  • t Hart BA, Laman JD, Kap YS (2018) Merits and complexities of modeling multiple sclerosis in non-human primates: implications for drug discovery. Expert Opin Drug Discov 13:387–397

    Article  CAS  Google Scholar 

  • Tachibana H, Cheng XJ, Kobayashi S, Matsubayashi N, Gotoh S, Matsubayashi K (2001) High prevalence of infection with Entamoeba dispar, but not E. histolytica, in captive macaques. Parasitol Res 87:14–17

    Article  CAS  PubMed  Google Scholar 

  • Tachibana H, Yanagi T, Akatsuka A, Kobayashi S, Kanbara H, Tsutsumi V (2009) Isolation and characterization of a potentially virulent species Entamoeba nuttalli from captive Japanese macaques. Parasitology 136:1169–1177

    Article  CAS  PubMed  Google Scholar 

  • Tachibana H, Yanagi T, Feng M, Bandara KB, Kobayashi S, Cheng X, Hirayama K, Rajapakse RP (2016) Isolation and molecular characterization of Entamoeba nuttalli strains showing novel Isoenzyme patterns from wild toque macaques in Sri Lanka. J Eukaryot Microbiol 63:171–180

    Article  CAS  PubMed  Google Scholar 

  • Takano J, Narita T, Tachibana H, Shimizu T, Komatsubara H, Terao K, Fujimoto K (2005) Entamoeba histolytica and Entamoeba dispar infections in cynomolgus monkeys imported into Japan for research. Parasitol Res 97:255–257

    Article  PubMed  Google Scholar 

  • Thomas E, Liang TJ (2016) Experimental models of hepatitis B and C - new insights and progress. Nat Rev Gastroenterol Hepatol 13:362–374

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tuda J, Feng M, Imada M, Kobayashi S, Cheng X, Tachibana H (2016) Identification of Entamoeba polecki with unique 18S rRNA gene sequences from Celebes crested macaques and pigs in Tangkoko Nature Reserve, North Sulawesi, Indonesia. J Eukaryot Microbiol 63:572–577

    Article  CAS  PubMed  Google Scholar 

  • Verweij JJ, Polderman AM, Clark CG (2001) Genetic variation among human isolates of uninucleated cyst-producing Entamoeba species. J Clin Microbiol 39:1644–1646

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Verweij JJ, Vermeer J, Brienen EA, Blotkamp C, Laeijendecker D, van Lieshout L, Polderman AM (2003) Entamoeba histolytica infections in captive primates. Parasitol Res 90:100–103

    Article  PubMed  Google Scholar 

  • Visser LG, Verweij JJ, Van Esbroeck M, Edeling WM, Clerinx J, Polderman AM (2006) Diagnostic methods for differentiation of Entamoeba histolytica and Entamoeba dispar in carriers: performance and clinical implications in a non-endemic setting. Int J Med Microbiol 296:397–403

    Article  CAS  PubMed  Google Scholar 

  • Zanzani SA, Gazzonis AL, Epis S, Manfredi MT (2016) Study of the gastrointestinal parasitic fauna of captive non-human primates (Macaca fascicularis). Parasitol Res 115:307–312

    Article  PubMed  Google Scholar 

  • 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 Parasitol 64:228–231

    Article  PubMed  Google Scholar 

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Funding

Project support was provided by the Subject Construction ESI Promotion Plan Fund of Yunnan Agricultural University, China (grant No. 2019YNAUESIMS03), and the Open Funds of the State Key Laboratory of Veterinary Etiological Biology, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences (grant No. SKLVEB2017KFKT008).

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  1. Li-Hua Pu, Zhao Li and Jie Wu contributed equally to this work.

Authors and Affiliations

  1. Key Laboratory of Veterinary Public Health of Yunnan Province, College of Veterinary Medicine, Yunnan Agricultural University, Kunming, 650201, Yunnan Province, People’s Republic of China

    Li-Hua Pu, Zhao Li, Jie Wu, Jian-Fa Yang & Feng-Cai Zou

  2. Kunming Primate Research Center of the Chinese Academy of Sciences, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, 650223, Yunnan Province, People’s Republic of China

    Yu-Lin Zhang & Jia-Qi Chen

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  1. Li-Hua Pu
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  2. Zhao Li
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  3. Jie Wu
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  4. Yu-Lin Zhang
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Correspondence to Jian-Fa Yang or Feng-Cai Zou.

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The protocol of the present study has been reviewed and approved by the Animal Ethical and Welfare Committee of Yunnan Agricultural University. Fecal samples were collected from experimental NHPs accordance with the Animal Ethics Procedures and Guidelines of the People’s Republic of China.

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Pu, LH., Li, Z., Wu, J. et al. Prevalence, molecular epidemiology and zoonotic risk of Entamoeba spp. from experimental macaques in Yunnan Province, southwestern China. Parasitol Res 119, 2733–2740 (2020). https://doi.org/10.1007/s00436-020-06762-9

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