Emerg Infect DisEmerging Infect. DisEIDEmerging Infectious Diseases1080-60401080-6059Centers for Disease Control and Prevention21529415332179310-184610.3201/eid1705.101846Letters to the EditorPlasmodium vivax Seroprevalence in Bred Cynomolgus Monkeys, ChinaRunning Head: P. Vivax Seroprevalence in MonkeysLiHai-LongLiuZhen-YongLiJuanAiLinZhouDong-HuiYuanZi-GuoLinRui-QingWengYa-BiaoZhuXing-QuanAuthor affiliations: State Key Laboratory of Veterinary Etiological Biology, Lanzhou Veterinary Research Institute, CAAS, Lanzhou, China (H.-L. Li, Z.-Y. Liu, J. Li, L. Ai, X.-Q. Zhu);South China Agricultural University, Guangzhou, China (H.-L. Li, J. Li, L. Ai, D.-H. Zhou, Z.-G. Yuan, R.-Q. Lin, Y.-B. Weng)Address for correspondence: Xing-Quan Zhu, Department of Parasitology, State Key Laboratory of Veterinary Etiological Biology, Lanzhou Veterinary Research Institute, CAAS, 1 Xujiaping, Yanchangbu, Lanzhou, Gansu Province 730046, People’s Republic of China; email: xingquanzhu1@hotmail.com52011175928929Keywords: Plasmodium vivaxmalariaparasitesseroprevalencecynomolgus monkeysMacaca fascicularisChinaletter

To the Editor: Malaria caused by Plasmodium spp. is one of the most prevalent parasitic diseases in the world, especially in tropical countries. P. vivax represents the second most prevalent of malaria species. Therefore, as measures to control the high death rates in humans caused by P. falciparum become more effective, P. vivax is likely to become the primary malaria threat (1). In P. vivax infection, the main clinical signs and symptoms are fever, chills, nausea and vomiting, generalized body pain and fatigue, toxic shock and pulmonary edema, retinal hemorrhage, renal failure, uremic encephalopathy, and thrombocytopenia (26).

Because of their phylogenetic proximity to humans, nonhuman primates have been used extensively as animal models of human diseases (7). Thousands of workers come in contact with monkeys, but little information about the prevalence of P. vivax in bred cynomolgus monkeys (Macaca fascicularis) is available worldwide. The objective of our investigation was to examine whether P. vivax seroprevalence is present in bred cynomolgus monkeys in the People’s Republic of China.

A total of 328 blood samples were collected by venous puncture during June 2008–September 2009. Of these, 224 blood samples were from 4 nonhuman primate centers in Guangxi Zhuang Nationality Autonomous Region and 108 blood samples were from 2 nonhuman primate centers in Guangdong Province. All of the cynomolgus monkeys were caged. Each cage has 2 rooms, 1 indoors and 1 outdoors. The monkeys spend ≈10 hours in the outdoor room each day during the daytime. The age and sex of monkeys are listed in the Table. Serum samples were separated and stored at –20°C before testing.

Serum samples were tested for P. vivax antibodies by using a commercially available ELISA kit (Tiancheng Yiliu Co., Ltd, Shanghai, China), according to the manufacturer’s instructions. This kit uses biotinylated anti–P. vivax as a coating antigen and is specifically for monkeys. Positive and negative control serum samples were provided in the kit and included in each test. Those samples with doubtful results were retested.

Differences in the seroprevalence of P. vivax in bred cynomolgus monkeys according to sex and area were analyzed by using the χ2 test in SPSS 13.0 standard version for Windows (SPSS Inc., Chicago, IL, USA). The differences were considered to be statistically significant when the p value obtained was <0.05.

The total prevalence of anti–P. vivax antibodies in bred cynomolgus monkeys in southern China was 3.4% (11/328), which was lower than the prevalence of anti–P. vivax antibodies in captured monkeys (Alouatta seniculus, Saguinus midas, and Pithecia pithecia) in French Guiana (8). The prevalence in female monkeys (3.1%, 5/161) was slightly lower than that in male monkeys (3.6%, 6/167); the seroprevalence of 3.6% (8/224) in Guangxi Zhuang Nationality Autonomous Region was slightly higher than that in Guangdong Province (2.9%, 3/104) (Table), but these differences were not significant (p>0.05). A total of 52 monkey serum samples from nonhuman primate center E in Guangdong Province were found seronegative for P. vivax antibodies (Table). The difference in prevalence of P. vivax antibodies in different nonhuman primate centers may be related to differences in ecologic and geographic conditions, climate conditions, as well as in the management practices. All of the nonhuman primate centers are surrounded by hills or paddy fields, and the environment is favorable for Anopheles mosquitoes. The mosquito control measures, including the use of antimosquito insecticides and good drainage facilities for preventing water collection on the ground, were better executed at nonhuman primate center E than at the other nonhuman primate centers.

Prevalence of <italic>Plasmodium vivax</italic> antibodies in serum samples, from bred cynomolgus monkeys in southern China, determined by ELISA, 2008–2009*
Province
Primate
center
Female

Male

Total
Age, y
No. positive/
no. examined
Prevalence, %
Age, y
No. positive/
no. examined
Prevalence, %
No. positive/
no. examined
Prevalence,
%
GX
A3.0–5.00/2003.0–6.51/303.31/502
B3.0–5.00/2903.0–5.51/333.01/621.6
C3.0–5.01/273.73.0–5.52/336.13/605
D2.0–5.02/316.53.0–5.01/214.83/525.8
Subtotal
2.0–5.0
3/107
2.8

3.0–6.5
5/117
4.3

8/224
3.6
GD
E2.5–3.00/1402.5–3.00/1300/270
E7.0–8.00/1208.0–9.00/1300/250
F2.5–3.02/287.12.5–6.01/244.23/525.8
Subtotal
2.5–8.0
2/54
3.7

2.5–9.0
1/50
2

3/104
2.9
Total5/1613.16/1673.611/3283.4

*GX, Guangxi Zhuang Nationality Autonomous Region; GD, Guangdong Province; –, not applicable.

Our survey showed P. vivax seropositivity in 5 of the 6 nonhuman primate centers in southern China, which is a potential health problem for bred cynomolgus monkeys. This finding also indicates the risk for infection with P. vivax for the employees of these nonhuman primate centers. Therefore, studies are warranted that assess the seroprevalence of P. vivax infection in persons who work in these nonhuman primate centers, as well as the seroprevalence of P. vivax infection in wild monkeys.

Suggested citation for this article: Li H-L, Liu Z-Y Li J, Ai L, Zhou D-H, Yuan Z-G, et al. Plasmodium vivax seroprevalence in bred cynomolgus monkeys, China [letter]. Emerg Infect Dis [serial on the Internet]. 2001 May [date cited]. http://dx.doi.org/10.3201/eid1705.101846

This work is supported in part by grants from the National Basic Research Program (973 program) of China (grant no. 2007CB513104), the State Key Laboratory of Veterinary Etiological Biology, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences (SKLVEB2009KFKT014 and SKLVEB2010KFKT010), and the Specialized Research Fund for the Doctoral Program of Higher Education (Grant no. 20094404120016).

ReferencesMendis K, Sina BJ, Marchesini P, Carter R. The neglected burden of Plasmodium vivax malaria. Am J Trop Med Hyg. 2001;64:9710611425182Karahocagil MK, Baran AI, Yaman G, Cicek M, Bilici A, Binici I, Case report: two Plasmodium vivax malaria cases in the Van Province [in Turkish] Turkiye Parazitol Derg. 2009;33:172319598098Song JY, Park CW, Jo YM, Kim JY, Kim JH, Yoon HJ, Two cases of Plasmodium vivax malaria with the clinical picture resembling toxic shock. Am J Trop Med Hyg. 2007;77:6091117978057Lee JH, Chin HS, Chung MH, Moon YS. Retinal hemorrhage in Plasmodium vivax malaria. Am J Trop Med Hyg. 2010;82:21922 10.4269/ajtmh.2010.09-043920133995Das BS. Renal failure in malaria. J Vector Borne Dis. 2008;45:839718592837Kaur D, Wasir V, Gulati S, Bagga A. Unusual presentation of Plasmodium vivax malaria with severe thrombocytopenia and acute renal failure. J Trop Pediatr. 2007;53:2102 10.1093/tropej/fml09217264156Carlsson HE, Schapiro SJ, Farah I, Hau J. Use of primates in research: a global overview. Am J Primatol. 2004;63:22537 10.1002/ajp.2005415300710Volney B, Pouliquen JF, De Thoisy B, Fandeur T. A sero-epidemiological study of malaria in human and monkey populations in French Guiana. Acta Trop. 2002;82:1123 10.1016/S0001-706X(02)00036-011904099