Co-infections of Plasmodium knowlesi, P. falciparum, and P. vivax among Humans and Anopheles dirus Mosquitoes, Southern Vietnam

Ron P Marchand, Richard Culleton, Yoshimasa Maeno, Nguyen Tuyen Quang, Shusuke Nakazawa, Ron P Marchand, Richard Culleton, Yoshimasa Maeno, Nguyen Tuyen Quang, Shusuke Nakazawa

Abstract

A single Anopheles dirus mosquito carrying sporozoites of Plasmodium knowlesi, P. falciparum, and P. vivax was recently discovered in Khanh Phu, southern Vietnam. Further sampling of humans and mosquitoes in this area during 2009-2010 showed P. knowlesi infections in 32 (26%) persons with malaria (n = 125) and in 31 (43%) sporozoite-positive An. dirus mosquitoes (n = 73). Co-infections of P. knowlesi and P. vivax were predominant in mosquitoes and humans, while single P. knowlesi infections were found only in mosquitoes. P. knowlesi-co-infected patients were largely asymptomatic and were concentrated among ethnic minority families who commonly spend nights in the forest. P. knowlesi carriers were significantly younger than those infected with other malaria parasite species. These results imply that even if human malaria could be eliminated, forests that harbor An. dirus mosquitoes and macaque monkeys will remain a reservoir for the zoonotic transmission of P. knowlesi.

Figures

Figure 1
Figure 1
Results and interpretation of the PCR analyses of sporozoite-positive salivary glands of Anopheles dirus mosquitoes in Khanh Phu forest, Vietnam. CSP, circumsporozoite protein; ssu, small subunit; shaded cells, PCR products present; F, Plasmodium falciparum; V, P. vivax; K, P. knowlesi; M, P. malariae; ?, unknown.
Figure 2
Figure 2
Dynamics of biting density and sporozoite positive salivary glands (including Plasmodium knowlesi) of Anopheles dirus mosquitoes in Khanh Phu forest, Vietnam. The solid red line connects the points of mean monthly An. dirus density (bites/person-night). Bars indicate the monthly number of sporozoite-positive salivary glands: white, P. knowlesi; gray, other species. The first mosquito found with P. knowlesi in August 2008 was described in Nakazawa et al. (11).
Figure 3
Figure 3
Age analysis of persons tested for Plasmodium knowlesi infection, Khanh Phu, Vietnam. A) Age groups of P. knowlesi–positive persons (n = 32; mean age 15.8 y) compared with P. knowlesi–negative persons (n = 179; mean age 26.2 y); p = 0.0004 (significant) by 2-tailed t test with unequal variance. B) Age groups of P. knowlesi–positive persons compared with ages of those positive for other parasites (n = 93; mean age 24.5 y); p = 0.004 (significant) by 2 tailed t test with unequal variance. C) Age groups of P. falciparum–positive persons (n = 95; mean age 23.4 y) compared with P. falciparum–negative persons (n = 116; mean age 25.6 y); p = 036 (not significant) by 2-tailed t test with unequal variance.
Figure 4
Figure 4
Frequency of single and co-infections among 124 human blood samples (A) and 73 mosquito salivary glands (B) positive for Plasmodium spp. infection by PCR. P. malariae was discarded. Gray bars indicate P. knowlesi infection or co-infection. F, P. falciparum; V, P. vivax; K, P. knowlesi.

References

    1. Viet Nam National Institute of Malariology. Parasitology and Entomology (NIMPE). Annual reports of the National Malaria Control Program in Vietnam: 2003–2008. Hanoi: The Institute; 2008.
    1. Erhart A, Thang ND, Hung NQ, Toi LV, Hung LX, Tuy TQ, et al. Forest malaria in Vietnam: a challenge for control. Am J Trop Med Hyg. 2004;70:110–8.
    1. Marchand RP. The Khanh Phu malaria research project: an overview 1994–2004. 2005. [cited 2010 Sep 4].
    1. Erhart A, Ngo DT, Phan VK, Ta TT, Van Overmeir C, Speybroeck N, et al. Epidemiology of forest malaria in central Vietnam: a large scale cross-sectional survey. Malar J. 2005;4:58. 10.1186/1475-2875-4-58
    1. Singh B, Kim Sung L, Matusop A, Radhakrishnan A, Shamsul SS, Cox-Singh J, et al. A large focus of naturally acquired Plasmodium knowlesi infections in human beings. Lancet. 2004;363:1017–24. 10.1016/S0140-6736(04)15836-4
    1. Putaporntip C, Hongsrimuang T, Seethamchai S, Kobasa T, Limkittikul K, Cui L, et al. Differential prevalence of Plasmodium infections and cryptic Plasmodium knowlesi malaria in humans in Thailand. J Infect Dis. 2009;199:1143–50. 10.1086/597414
    1. Luchavez J, Espino F, Curameng P, Espina R, Bell D, Chiodini P, et al. Human infections with Plasmodium knowlesi, the Philippines. Emerg Infect Dis. 2008;14:811–3. 10.3201/eid1405.071407
    1. Vythilingam I, Noorazian YM, Huat TC, Jiram AI, Yusri YM, Azahari AH, et al. Plasmodium knowlesi in humans, macaques and mosquitoes in peninsular Malaysia. Parasit Vectors. 2008;1:26. 10.1186/1756-3305-1-26
    1. Cox-Singh J, Singh B. Knowlesi malaria: newly emergent and of public health importance? Trends Parasitol. 2008;24:406–10. 10.1016/j.pt.2008.06.001
    1. Jiang N, Chang Q, Sun X, Lu H, Yin J, Zhang Z, et al. Co-infections with Plasmodium knowlesi and other malaria parasites, Myanmar. Emerg Infect Dis. 2010;16:1476–8. 10.3201/eid1609.100339
    1. Nakazawa S, Marchand RP, Quang NT, Culleton R, Manh ND, Maeno Y. Anopheles dirus co-infection with human and monkey malaria parasites in Vietnam. Int J Parasitol. 2009;39:1533–7. 10.1016/j.ijpara.2009.08.005
    1. Garros C, Marchand RP, Quang NT, Hai NS, Manguin S. First record of Anopheles minimus C and significant decrease of An. minimus A in central Vietnam. J Am Mosq Control Assoc. 2005;21:139–43. 10.2987/8756-971X(2005)21[139:FROAMC];2
    1. Vietnam National Institute of Malariology. Parasitology and Entomology. Identification key for Anophelinae in Vietnam. Hanoi (Vietnam): Medical Publishing House; 2008.
    1. Trung HD, Van Bortel W, Sochantha T, Keokenchanh K, Quang NT, Cong LD, et al. Malaria transmission and major malaria vectors in different geographical areas of Southeast Asia. Trop Med Int Health. 2004;9:230–7. 10.1046/j.1365-3156.2003.01179.x
    1. Obsomer V, Defourny P, Coosemans M. The Anopheles dirus complex: spatial distribution and environmental drivers. Malar J. 2007;6:26. 10.1186/1475-2875-6-26
    1. Maeno Y, Nakazawa S, Dao le D, Yamamoto N, Giang ND, Van Hanh T, et al.. A dried blood sample on filter paper is suitable for detecting Plasmodium falciparum gametocytes by reverse transcription polymerase chain reaction. Acta Trop. 2008;107:121–7. 10.1016/j.actatropica.2008.05.001
    1. Singh B, Bobogare A, Cox-Singh J, Snounou G, Abdullah MS, Rahman HA. A genus- and species-specific nested polymerase chain reaction malaria detection assay for epidemiologic studies. Am J Trop Med Hyg. 1999;60:687–92.
    1. Imwong M, Tanomsing N, Pukrittayakamee S, Day NP, White NJ, Snounou G. Spurious amplification of a Plasmodium vivax small-subunit RNA gene by use of primers currently used to detect P. knowlesi. J Clin Microbiol. 2009;47:4173–5. 10.1128/JCM.00811-09
    1. Tan CH, Vythilingam I, Matusop A, Chan ST, Singh B. Bionomics of Anopheles latens in Kapit, Sarawak, Malaysian Borneo in relation to the transmission of zoonotic simian malaria parasite Plasmodium knowlesi. Malar J. 2008;7:52. 10.1186/1475-2875-7-52
    1. Jongwutiwes S, Putaporntip C, Iwasaki T, Sata T, Kanbara H. Naturally acquired Plasmodium knowlesi malaria in human, Thailand. Emerg Infect Dis. 2004;10:2211–3.
    1. Daneshvar C, Davis TME, Cox-Singh J, Rafe’ee MZ, Zakaria SK, Divis PCS, et al. Clinical and laboratory features of human Plasmodium knowlesi infection. Clin Infect Dis. 2009;49:852–60. 10.1086/605439
    1. Cox-Singh J, Hiu J, Lucas SB, Divis PC, Zulkarnaen M, Chandran P, et al. Severe malaria—a case of fatal Plasmodium knowlesi infection with post-mortem findings: a case report. Malar J. 2010;9:10. 10.1186/1475-2875-9-10
    1. Van den Eede P, Van HN, Van Overmeir C, Vythilingam I, Duc TN, Hung LX, et al. Human Plasmodium knowlesi infections in young children in central Vietnam. Malar J. 2009;8:249. 10.1186/1475-2875-8-249
    1. Escalante AA, Cornejo OE, Freeland DE, Poe AC, Durrego E, Collins WE, et al. A monkey's tale: the origin of Plasmodium vivax as a human malaria parasite. Proc Natl Acad Sci U S A. 2005;102:1980–5. 10.1073/pnas.0409652102
    1. Hayakawa T, Culleton R, Otani H, Horii T, Tanabe K. Big bang in the evolution of extant malaria parasites. Mol Biol Evol. 2008;25:2233–9. 10.1093/molbev/msn171
    1. Duarte AM, Malafronte RS, Cerutti C Jr, Curado I, de Paiva BR, Maeda AY, et al. Natural Plasmodium infections in Brazilian wild monkeys: reservoirs for human infections? Acta Trop. 2008;107:179–85. 10.1016/j.actatropica.2008.05.020
    1. Prugnolle F, Durand P, Neel C, Ollomo B, Ayala FJ, Arnathau C, et al. African great apes are natural hosts of multiple related malaria species, including Plasmodium falciparum. Proc Natl Acad Sci U S A. 2010;107:1458–63. 10.1073/pnas.0914440107
    1. Garamszegi LZ. Patterns of co-speciation and host switching in primate malaria parasites. Malar J. 2009;8:110. 10.1186/1475-2875-8-110
    1. Liu W, Li Y, Learn GH, Rudicell RS, Robertson JD, Keele BF, et al. Origin of the human malaria parasite Plasmodium falciparum in gorillas. Nature. 2010;467:420–5. 10.1038/nature09442

Source: PubMed

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