Skip to main content
SpringerLink
Log in

Study of the gastrointestinal parasitic fauna of captive non-human primates (Macaca fascicularis)

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

The aim of this study was to examine helminths and protozoans in cynomolgus macaques (Macaca fascicularis) imported from registered breeding facilities in China and their relation to health risks for non-human primate handlers in biomedical research centers and in breeding facilities. Fresh fecal samples were collected from a total of 443 M. fascicularis and analyzed by copromicroscopical analysis, immunoenzymatic, or molecular assays. As to helminths, whose eggs were shed in 2.03% of the samples, Trichuris and Oesophagostomum were the only two taxa found, with low prevalence and low eggs per gram (EPG) values. Protozoans were more frequently detected (87.40%), with Entamoeba coli (85.19%) and Endolimax nana (79.26%) as the most prevalent species shed. Other parasites found by fecal smear examination were uninucleated-cyst-producing Entamoebas (78.52%), Iodamoeba bütschlii (42.96%), and Chilomastix mesnili (24.44%), while cysts of Balantidium coli (22.2%) were only observed by sedimentation. No coproantigens of Giardia duodenalis, Cryptosporidium spp., and Entamoeba histolytica complex were detected. Blastocystis sp. infection was noticed in 87.63% of macaques by PCR. These cynomolgus monkeys were infected with many subtypes (ST1, ST2, ST3, ST5, and ST7), where the predominant Blastocystis sp. subtypes were ST2 (77.5%), followed by ST1 (63.5%). Data collected confirmed the presence of potentially zoonotic parasites and a high parasite diversity, suggesting the need for appropriate and sensitive techniques to adequately control them and related health risks for handlers of non-human primates in biomedical research centers and in breeding facilities.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Abbott DP, Majeed SK (1984) A survey of parasitic lesions in wild-caught, laboratory-maintained primates: (rhesus, cynomolgus, and baboon). Vet Pathol 21:198–207

    CAS  PubMed  Google Scholar 

  • Abe N, Nagoshi M, Takami K, Sawano Y, Yoshikawa H (2002) A survey of Blastocystis sp. in livestock, pets, and zoo animals in Japan. Vet Parasitol 106:203–212

    Article  PubMed  Google Scholar 

  • Alfellani MA, Aner-Mulla D, Jacob AS, Atim Imeede C, Yoshikawa H, Stensvold CR, Clark CG (2013a) Genetic diversity of Blastocystis in livestock and zoo animals. Protist 164:497–509

    Article  CAS  PubMed  Google Scholar 

  • Alfellani MA, Jacob AS, Ortíz Perea N, Krecek RC, Taner-Mulla D, Verweij JJ, Levecke B, Tannich E, Clark CG, Stensvold CR (2013b) Diversity and distribution of Blastocystis sp. subtypes in non-human primates. Parasitology 140:966–971

    Article  CAS  PubMed  Google Scholar 

  • Bezubik B, Furmaga S (1960) The parasites in Macaca cynomolgous from Indonesia. Acta Parasitol 8:335–344

    Google Scholar 

  • Boorom KF, Smith H, Nimri L, Viscogliosi E, Spanakos G, Parkar U, Li LH, Zhou XN, Ok ÜZ, Leelayoova S, Jones MS (2008) Oh my aching gut: irritable bowel syndrome, Blastocystis, and asymptomatic infection. Parasite Vector 1:40

    Article  Google Scholar 

  • Broadhurst MJ, Ardeshir A, Kanwar B, Mirpuri J, Gundra UM, Leung JM, Wiens KE, Vujkovic-Cvijin I, Kim CC, Yarovinsky F, Lerche NW, McCune JM, Loke P (2012) Therapeutic helminth infection of macaques with idiopathic chronic diarrhea alters the inflammatory signature and mucosal microbiota of the colon. PLoS Pathog 8:e1003000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cekin AH, Cekin Y, Adakan Y, Tasdemir E, Koclar FG, Yolcular BO (2012) Blastocystosis in patients with gastrointestinal symptoms: a case-control study. BMC Gastroenterol 12:122

    Article  PubMed  PubMed Central  Google Scholar 

  • da Silva Barbosa A, Pissinatti A, Verdan Dib L, Perlingeiro de Siqueira M, Lessa Cardozo M, Monteiro Fonseca AB, de Barros OA, Alves da Silva F, Antunes Uchȏa CM, Machado Pereira Bastos O, Reis Amendoeira MR (2015) Balantidium coli and other gastrointestinal parasites in captives non-human primates of the Rio de Janeiro, Brazil. J Med Primatol 44:18–26

    Article  PubMed  Google Scholar 

  • Dinh SV (2002) Intestinal parasites of Macaca fascicularis in a Mangrove Forest, Ho Chi Minh City, Vietnam. Laboratory Primate Newsletter 41:9–10

    Google Scholar 

  • Emikpe BO, Ayoade GO, Ohore OG, Olaniyan OO, Akusu MO (2002) Fatal trichuriosis in a captive baboon (Papio anubis) in Ibadan Nigeria: a case report. Trop Vet 20:36–39

    Article  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 

  • Honjo S, Muto K, Fujiwara T, Suzuki Y, Imaizumi K (1963) Significance of the natural infection of Oesophagostomum sp. in cynomolgus monkeys (Macaca irus) used as experimental animals. Jpn J Med Sci Biol 16:225–227

    Article  CAS  PubMed  Google Scholar 

  • Janagi TS (1981) A report of gastro-intestinal helminth parasites found in Macaca fascicularis in peninsular Malaysia. Malaysia Applied Biol 10:99–100

    Google Scholar 

  • Lane KE, Holley C, Hollocher H, Fuentes A (2011) The anthropogenic environment lessens the intensity and prevalence of gastrointestinal parasites in Balinese long-tailed macaques (Macaca fascicularis). Primates 52:117–128

    Article  PubMed  Google Scholar 

  • Lee JI, Kang SJ, Kim NA, Lee CW, Ahn K, Kwon H, Park C, Kim S (2010) Investigation of helminths and protozoans infecting old world monkeys: captive vervet, cynomolgus, and rhesus monkeys. Korean J Vet Res 50:273–277

    Google Scholar 

  • Lee RV, Prowten AW, Anthone S, Satchidanand SK, Fisher JE, Anthone R (1990) Typhlitis due to Balantidium coli in captive lowland gorillas. Rev Infect Dis 12:1052–1059

    Article  CAS  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 non-human primates. J Clin Microbiol 48:2988

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu YW, Suzuki S, Kashima M, Tokado H, Fukuzaki K, Miyajima H (2008) Clinical pathology data from cynomolgus monkeys from China in which diarrhea was observed during quarantine. Exp Anim 57:139–143

    Article  PubMed  Google Scholar 

  • Loomis M (1983) Hepatic and gastric amebiasis in black and white colobus monkeys. J Am Vet Med Assoc 183:1188–1191

    CAS  PubMed  Google Scholar 

  • Loomis MR, Wright JF (1986) Gastric trichuriasis in a black and white colobus monkey. J Am Vet Med Assoc 189:1214–1215

    CAS  PubMed  Google Scholar 

  • Matsubayashi K, Gotoh S, Kawamoto Y, Watanabe T, Nozawa K, Takasaka M, Narita T, Griffiths O, Stanley MA (1992) Clinical examinations on crab-eating macaques in Mauritius. Primates 33:281–288

    Article  Google Scholar 

  • MacIntosh AJJ, Hernandez AD, Huffman MA (2010) Host age, sex, and reproductive seasonality affect nematode parasitism in wild Japanese macaques. Primates 51:353–364

    Article  PubMed  Google Scholar 

  • Melfi V, Poyser F (2007) Trichuris burdens in zoo-housed Colobus guereza. Int J Primatol 28:1449–1456

    Article  Google Scholar 

  • Meloni D, Poirier P, Mantini C, Noël C, Gantois N, Wawrzyniak I, Delbac F, Chabé M, Delhaes L, Dei-Cas E, Fiori PL, El Alaoui H, Viscogliosi E (2012) Mixed human intra- and inter-subtype infections with the parasite Blastocystis sp. Parasitol Int 61:719–722

    Article  PubMed  Google Scholar 

  • Muriuki SMK, Farah IO, Agwiria RM, Chai DC, Njamunge G, Suleman M, Olobo JO (1997) The presence of Cryptosporidium oocysts in stools of clinically diarrhoeic and normal non-human primates in Kenya. Vet Parasitol 72:141–147

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Nakauchi K (1999) The prevalence of Balantidium coli infection in fifty-six mammalian species. J Vet Med Sci 61:63–65

    Article  CAS  PubMed  Google Scholar 

  • Pedersen AB, Altizer S, Poss M, Cunningham AA, Nunn CL (2005) Patterns of host specificity and transmission among parasites of wild primates. Int J Parasitol 35:647–657

    Article  PubMed  Google Scholar 

  • Phillippi KM, Clarke MR (1992) Survey of parasites of rhesus monkeys housed in small social groups. Am J Primatol 27:293–302

    Article  Google Scholar 

  • Pomajbíkova K, Oborník M, Horák A, Petrzálková KJ, Grim JN, Levecke B, Todd A, Mulama M, Kiyang J, Modr D (2013) Novel Insights into the genetic diversity of Balantidium and Balantidium-like cyst-forming ciliates. PLoS Neglect Trop D 7:e2140

    Article  Google Scholar 

  • Regan CS, Yon L, Hossain M, Elsheikha HM (2014) Prevalence of Entamoeba species in captive primates in zoological gardens in the UK. Peer J 2:e492

    Article  PubMed  PubMed Central  Google Scholar 

  • Reichard MV, Wolf RF, Carey DW, Garrett JJ, Briscoe HA (2007) Efficacy of fenbendazole and milbemycin oxime for treating baboons (Papio cynocephalus anubis) infected with Trichuris trichiura. J Am Ass Lab Anim 46:42–45

    CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Roperto F, Quesada A, Pandolfi F, Izzi R (1985) Oesophagostomiasis in monkeys imported from Senegal. Atti della Societa Italiana delle Scienze Veterinarie 38:603–5

    Google Scholar 

  • Sano M, Kino H, de Guzman TS, Ishii AI, Kino J, Tanaka T, Tsuruta M (1980) Studies on the examination of imported laboratory monkey, Macaca fascicularis for E. histolytica and other intestinal parasites. Int J Zoonoses 7:34–39

    CAS  PubMed  Google Scholar 

  • Santín M, Gómez-Muñoz MT, Solano-Aguilar G, Fayer R (2011) Development of a new PCR protocol to detect and subtype Blastocystis spp. from humans and animals. Parasitol Res 109:205–212

    Article  PubMed  Google Scholar 

  • Scanlan PD, Stensvold CR, Cotter PD (2015) Development and application of a Blastocystis subtype-specific pcr assay reveals that mixed-subtype infections are common in a healthy human population. Appl Environ Microbiol 81:4071–6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scanlan PD, Stensvold CR, Rajilić-Stojanović M, Heilig HG, De Vos WM, O’Toole PW, Cotter PD (2014) The microbial eukaryote Blastocystis is a prevalent and diverse member of the healthy human gut microbiota. FEMS Microbiol Ecol 90:326–30

    Article  CAS  PubMed  Google Scholar 

  • Schuster FL, Ramirez-Avila L (2008) Current world status of Balantidium coli. Clin Microbiol Rev 21:626–638

    Article  PubMed  PubMed Central  Google Scholar 

  • Stensvold CR (2013) Comparison of sequencing (Barcode Region) and sequence-tagged-site PCR for Blastocystis subtyping. J Clin Microbiol 51:190–194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stensvold CR, Alfellani M, Clark CG (2012) Levels of genetic diversity vary dramatically between Blastocystis subtypes. Infect Genet Evol 12:263–273

    Article  PubMed  Google Scholar 

  • Stensvold CR, Lebbad M, Victory EL, Verweij JJ, Tannich E, Alfellani M, Legarraga P, Clark CG (2011) Increased sampling reveals novel lineages of Entamoeba: consequences of genetic diversity and host specificity for taxonomy and molecular detection. Protist 162:525–541

    Article  PubMed  Google Scholar 

  • Tachibana H, Cheng X, 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 

  • 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 

  • Taylor L, Lessnau RG, Lehman SM (1994) Prevalence of whipworm (Trichuris) ova in two free-ranging populations of rhesus macaques (Macaca mulatta) in the Florida Keys. Florida Scientist 57:102–107

    Google Scholar 

  • Vogel P, Zaucha G, Goodwin D, Kuehl K, Fritz D (1996) Rapid postmortem invasion of cecal mucosa of macaques by non pathogenic Entamoeba chattoni. Am J Trop Med Hyg 55:595–602

    CAS  PubMed  Google Scholar 

  • Wong MM, Conrad HD (1978) Prevalence of metazoan parasite infections in five species of Asian macaques. Lab Anim Sci 28:412–416

    CAS  PubMed  Google Scholar 

  • Ye J, Xiao L, Li J, Huang W, Amer SE, Guo Y, Roellig D, Feng Y (2014) Occurrence of human-pathogenic Enterocytozoon bieneusi, Giardia duodenalis and Cryptosporidium genotypes in laboratory macaques in Guangxi, China. Parasitol Int 63:132–137

    Article  PubMed  Google Scholar 

  • Yoshikawa H, Wu Z, Kimata I, Iseki M, Ali IK, Hossain MB, Zaman V, Haque R, Takahashi Y (2004) Polymerase chain reaction-based genotype classification among human Blastocystis hominis populations isolated from different countries. Parasitol Res 92:22–29

    Article  PubMed  Google Scholar 

  • Yoshikawa H, Wu Z, Pandey K, Pandey BD, Sherchand JB, Yanagi T, Kanbara H (2009) Molecular characterization of Blastocystis isolates from children and rhesus monkeys in Kathmandu, Nepal. Vet Parasitol 160:295–300

    Article  CAS  PubMed  Google Scholar 

  • Zanzani S, Epis S, Bandi C, Manfredi MT (2014) What is your diagnosis? Fecal smear stained with Lugol’s solution and Giemsa from a cynomolgus macaque (Macaca fascicularis) presenting with liquid diarrhea. Vet Clin Path 43:293–294

    Article  Google Scholar 

Download references

Acknowledgments

The authors are grateful to Ms Gigliola Canepa, University of Milan, for her support in editing our manuscript.

Conflict of interests

The authors declare that they have no competing interests.

Author information

Authors and Affiliations

  1. Department of Veterinary Science and Public Health, Università degli Studi di Milano, via Celoria 10, 20133, Milan, Italy

    Sergio Aurelio Zanzani, Alessia Libera Gazzonis, Sara Epis & Maria Teresa Manfredi

Authors
  1. Sergio Aurelio Zanzani
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alessia Libera Gazzonis
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sara Epis
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Maria Teresa Manfredi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maria Teresa Manfredi.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zanzani, S.A., Gazzonis, A.L., Epis, S. et al. Study of the gastrointestinal parasitic fauna of captive non-human primates (Macaca fascicularis). Parasitol Res 115, 307–312 (2016). https://doi.org/10.1007/s00436-015-4748-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-015-4748-9

Keywords

Search

Navigation