Abstract
Non-human primates are natural virus reservoirs, whether wild or domestic. In this study, we determined the seroprevalence of common viruses by ELISA in a northern pig-tailed macaque (Macaca leonina) colony derived from Ho Chi Minh City, Vietnam. A total of 20 types of virus which are commonly selected as target microorganisms for specific-pathogen-free colonies, or which have zoonotic potential were included in this study. The results showed only 2 in 90 northern pig-tailed macaques were seronegative for all the detected viruses, and at least 16 out of the total 20 types of virus tested were prevalent in this colony, so these macaques were commonly infected by various viruses. These macaques should be carefully assessed for viral seroprevalence in order to prevent zoonotic diseases from being transferred to human beings.
Similar content being viewed by others
References
Brown DW (1997) Threat to humans from virus infections of non-human primates. Rev Med Virol 7:239–246
Gao F, Bailes E, Robertson DL, Chen Y, Rodenburg CM, Michael SF, Cummins LB, Arthur LO, Peeters M, Shaw GM, Sharp PM, Hahn BH (1999) Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes. Nature 397:436–441
Gautret P, Blanton J, Dacheux L, Ribadeau-Dumas F, Brouqui P, Parola P, Esposito DH, Bourhy H (2014) Rabies in nonhuman primates and potential for transmission to humans: a literature review and examination of selected French national data. PLoS Negl Trop Dis 8:e2863
Gippoliti S (2001) Notes on the taxonomy of Macaca nemestrina leonina Blyth, 1863 (Primates: Cercopithecidae). Hystrix It J Mamm 12(1):51–54
Hatziioannou T, Evans DT (2012) Animal models for HIV/AIDS research. Nat Rev Microbiol 10:852–867
Hatziioannou T, Del Prete GQ, Keele BF, Estes JD, McNatt MW, Bitzegeio J, Raymond A, Rodriguez A, Schmidt F, Mac Trubey C, Smedley J, Piatak M, KewalRamani VN, Lifson JD, Bieniasz PD (2014) HIV-1-induced AIDS in monkeys. Science 344:1401–1405
Hirsch VM, Olmsted RA, Murphey-Corb M, Purcell RH, Johnson PR (1989) An African primate lentivirus (SIVsm) closely related to HIV-2. Nature 339:389–392
Huff JL, Barry PA (2003) B-virus (Cercopithecine herpesvirus 1) infection in humans and macaques: potential for zoonotic disease. Emerg Infect Dis 9:246–250
Khabbaz RF, Heneine W, George JR, Parekh B, Rowe T, Woods T, Switzer WM, McClure HM, Murphey-Corb M, Folks TM (1994) Brief report: infection of a laboratory worker with simian immunodeficiency virus. N Engl J Med 330:172–177
Kuang YQ, Tang X, Liu FL, Jiang XL, Zhang YP, Gao G, Zheng YT (2009) Genotyping of TRIM5 locus in northern pig-tailed macaques (Macaca leonina), a primate species susceptible to human immunodeficiency virus type 1 infection. Retrovirology 6:58
Lanford RE, Chavez D, Brasky KM, Burns RB 3rd, Rico-Hesse R (1998) Isolation of a hepadnavirus from the woolly monkey, a New World primate. Proc Natl Acad Sci USA 95:5757–5761
Lerche NW, Osborn KG (2003) Simian retrovirus infections: potential confounding variables in primate toxicology studies. Toxicol Pathol 31(Suppl):103–110
Liao CH, Kuang YQ, Liu HL, Zheng YT, Su B (2007) A novel fusion gene, TRIM5-cyclophilin A in the pig-tailed macaque determines its susceptibility to HIV-1 infection. AIDS 21(Suppl 8):S19–S26
Machado GP, Antunes JM, Uieda W, Biondo AW, Cruvinel TM, Kataoka AP, Martorelli LF, de Jong D, Amaral JM, Hoppe EG, Guerra Neto G, Megid J (2012) Exposure to rabies virus in a population of free-ranging capuchin monkeys (Cebus apella nigritus) in a fragmented, environmentally protected area in southeastern Brazil. Primates 53:227–231
Makuwa M, Souquiere S, Telfer P, Bourry O, Rouquet P, Kazanji M, Roques P, Simon F (2006) Hepatitis viruses in non-human primates. J Med Primatol 35:384–387
Mavalankar D, Shastri P, Raman P (2007) Chikungunya epidemic in India: a major public-health disaster. Lancet Infect Dis 7:306–307
Montiel NA (2010) An updated review of simian betaretrovirus (SRV) in macaque hosts. J Med Primatol 39:303–314
Moss JA, Malone AM, Smith TJ, Butkyavichene I, Cortez C, Gilman J, Kennedy S, Kopin E, Nguyen C, Sinha P, Hendry RM, Guenthner P, Holder A, Martin A, McNicholl J, Mitchell J, Pau CP, Srinivasan P, Smith JM, Baum MM (2012) Safety and pharmacokinetics of intravaginal rings delivering tenofovir in pig-tailed macaques. Antimicrob Agents Chemother 56:5952–5960
Nakamura S, Tsuchiya H, Okahara N, Nakagawa T, Ohara N, Yamamoto H, Li TC, Takeda N, Ogasawara K, Torii R (2012) Epidemiology of hepatitis E virus in indoor-captive cynomolgus monkey colony. J Vet Med Sci 74:279–283
Nakgoi K, Nitatpattana N, Wajjwalku W, Pongsopawijit P, Kaewchot S, Yoksan S, Siripolwat V, Souris M, Gonzalez JP (2014) Dengue, Japanese encephalitis and chikungunya virus antibody prevalence among captive monkey (Macaca nemestrina) colonies of Northern Thailand. Am J Primatol 76:97–102
Pang W, Lu LB, Wang Y, Li G, Huang DT, Lei AH, Zhang GH, Zheng YT (2013) Measurement and analysis of hematology and blood chemistry parameters in northern pig-tailed macaques (Macaca leonina). Zool Res 34:89–96
Promadej-Lanier N, Srinivasan P, Curtis K, Adams DR, Kim C, Luo W, Jia H, Subbarao S, Otten RA, Butera S (2008) Systemic and mucosal immunological responses during repeated mucosal SHIV(162P3) challenges prior to and following infection in pigtailed macaques. Virology 375:492–503
Rosenblum LL, Supriatna J, Melnick DJ (1997) Phylogeographic analysis of pigtail macaque populations (Macaca nemestrina) inferred from mitochondrial DNA. Am J Phys Anthropol 104:35–45
Rudd RJ, Appler KA, Wong SJ (2013) Presence of cross-reactions with other viral encephalitides in the indirect fluorescent-antibody test for diagnosis of rabies. J Clin Microbiol 51:4079–4082
Saito A, Nomaguchi M, Iijima S, Kuroishi A, Yoshida T, Lee YJ, Hayakawa T, Kono K, Nakayama EE, Shioda T, Yasutomi Y, Adachi A, Matano T, Akari H (2011) Improved capacity of a monkey-tropic HIV-1 derivative to replicate in cynomolgus monkeys with minimal modifications. Microbes Infect 13:58–64
Saito A, Nomaguchi M, Kono K, Iwatani Y, Yokoyama M, Yasutomi Y, Sato H, Shioda T, Sugiura W, Matano T, Adachi A, Nakayama EE, Akari H (2013) TRIM5 genotypes in cynomolgus monkeys primarily influence inter-individual diversity in susceptibility to monkey-tropic human immunodeficiency virus type 1. J Gen Virol 94(Pt 6):1318–1324
Sa-nguanmoo P, Thawornsuk N, Rianthavorn P, Sommanustweechai A, Ratanakorn P, Poovorawan Y (2010) High prevalence of antibodies against hepatitis A virus among captive nonhuman primates. Primates 51:167–170
Simmons JH (2010) Herpesvirus infections of laboratory macaques. J Immunotoxicol 7:102–113
Yasutomi Y (2010) Establishment of specific pathogen-free macaque colonies in Tsukuba Primate Research Center of Japan for AIDS research. Vaccine 28(Suppl 2):B75–B77
Zhang XL, Pang W, Deng DY, Lv LB, Feng Y, Zheng YT (2014a) Analysis of immunoglobulin, complements and CRP levels in serum of captive northern pig-tailed macaques (Macaca leonina). Zool Res 35:196–203
Zhang XL, Pang W, Hu XT, Li JL, Yao YG, Zheng YT (2014b) Experimental primates and non-human primate (NHP) models of human diseases in China: current status and progress. Zool Res 35:447–464
Zheng HY, Zhang MX, Zhang LT, Zhang XL, Pang W, Lyu LB, Zheng YT (2014) Flow cytometric characterizations of leukocyte subpopulations in the peripheral blood of northern pig-tailed macaques (Macaca leonina). Zool Res 35:465–473
Zhu L, Lei AH, Zheng HY et al (2015) Longitudinal analysis reveals characteristic of high proportions of bacterial vaginosis-related bacteria and temporal variability of vaginal microbiota in northern pig-tailed macaques (Macaca leonina). Zool Res 2015(36):285–298
Acknowledgments
This work was supported partly by the National Basic Research Program of China (2012CBA01305), the National Natural Science Foundation of China (81172876, 81273251, U1202228), the Knowledge Innovation Program of CAS (KSCX2-EW-R-13, KJZD-EW-L10-02), and the Key Scientific and Technological Program of China (2012ZX10001-007, 2013ZX10001-002). We thank Mr. Long-Bao Lv, and all the members from Kunming Primate Research Center, Kunming Institute of Zoology, CAS who provided assistance with the sample collection. We thank Prof. Muhammad Shahzad and Dr. Xin Chen for their assistance with editing. We complied with the ethical standards in the treatment of the animals with the guidelines laid down by NIH (US).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that there is no conflict of interests regarding the publication of this article.
Electronic supplementary material
Below is the link to the electronic supplementary material.
10329_2016_531_MOESM1_ESM.tif
Supplementary Fig. 1. OD values of different viruses in each age group. The OD values are shown as mean. The abbreviation in this figure is the same as in Table 2. 1 (TIFF 75431 kb)
About this article
Cite this article
Zhang, MX., Zheng, HY., Jiang, J. et al. Viral seroprevalence in northern pig-tailed macaques (Macaca leonina) derived from Ho Chi Minh City, Vietnam. Primates 57, 413–419 (2016). https://doi.org/10.1007/s10329-016-0531-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10329-016-0531-5