Outdoor malaria transmission in forested villages of Cambodia

Lies Durnez, Sokny Mao, Leen Denis, Patricia Roelants, Tho Sochantha, Marc Coosemans, Lies Durnez, Sokny Mao, Leen Denis, Patricia Roelants, Tho Sochantha, Marc Coosemans

Abstract

Background: Despite progress in malaria control, malaria remains an important public health concern in Cambodia, mostly linked to forested areas. Large-scale vector control interventions in Cambodia are based on the free distribution of long-lasting insecticidal nets (LLINs), targeting indoor- and late-biting malaria vectors only. The present study evaluated the vector density, early biting activity and malaria transmission of outdoor-biting malaria vectors in two forested regions in Cambodia.

Methods: In 2005 two entomological surveys were conducted in 12 villages and their related forest plots in the east and west of Cambodia. Mosquitoes were collected outdoors by human landing collections and subjected to enzyme-linked immunosorbent assay (ELISA) to detect Plasmodium sporozoites after morphological identification. Blood samples were collected in the same villages for serological analyses. Collected data were analysed by the classification and regression tree (CART) method and linear regression analysis.

Results: A total of 11,826 anophelines were recorded landing in 787 man-night collections. The majority (82.9%) were the known primary and secondary vectors. Most of the variability in vector densities and early biting rates was explained by geographical factors, mainly at village level. Vector densities were similar between forest and village sites. Based on ELISA results, 29% out of 17 Plasmodium-positive bites occurred before sleeping time, and 65% in the forest plots. The entomological inoculation rates of survey 1 were important predictors of the respective seroconversion rates in survey 2, whereas the mosquito densities were not.

Discussion: In Cambodia, outdoor malaria transmission in villages and forest plots is important. In this context, deforestation might result in lower densities of the primary vectors, but also in higher densities of secondary vectors invading deforested areas. Moreover, higher accessibility of the forest could result in a higher man-vector contact. Therefore, additional vector control measures should be developed to target outdoor- and early-biting vectors.

Figures

Figure 1
Figure 1
Overview of Cambodia with the four districts indicated. Pailin and Pursat are located in the west, O’chum and Borkeo are located in the north-east. (Google Maps).
Figure 2
Figure 2
Meteorological data in Ratanakkiri province (A), Pursat province (B) and Pailin province (C) in 2005. This includes the monthly rainfall in mm (left axis) and the minimum and maximum temperature in degrees Celsius (right axis). The timing of survey 1 (S1) and survey 2 (S2) are indicated by arrows.
Figure 3
Figure 3
Average man biting rate of the most abundant anopheline species in the different districts. Surveys (S1 = survey 1, S2 = survey 2) and collection sites (Fo = forest, Vi = village).
Figure 4
Figure 4
Early biting rate for the different vector species complexes per collection site. (F = forest, V = village), districts (B = Borkeo, O = O’Chum, P = Pailin, V = Pursat), and region (E = east, W = west).
Figure 5
Figure 5
Regression tree representing the important determinants for Anopheles dirus s.l. early biting proportion (EBP), expressed as percentage of vectors biting before 22.00. The selected splitter variables (village, survey, district, site) are shown in the nodes.
Figure 6
Figure 6
Cumulative number of infected Anopheles mosquitoes (n = 17) during the night outdoors (all data pooled). The approximate time for bed net use is between 22.00 and 05.00 (marked by arrows).

References

    1. Delacollette C, D’Souza C, Christophel E, Thimasarn K, Abdur R, Bell D, Dai TC, Gopinath D, Lu S, Mendoza R, Ortega L, Rastogi R, Tantinimitkul C, Ehrenberg J. Malaria trends and challenges in the Greater Mekong Subregion. Southeast Asian J Trop Med Public Health. 2009;40:674–691.
    1. WHO. World Malaria Report 2011. Geneva: World Health Organization; 2012. p. 278.
    1. WHO. Malaria in the Greater Mekong Subregion: Regional and Country Profiles. Geneva: World Health Organization; 2010. p. 58.
    1. SCW. “The School Atlas of Cambodia”. Phnom Penh, Cambodia: Save Cambodia’s Wildlife; 2006.
    1. Guerra CA, Snow RW, Hay SI. A global assessment of closed forests, deforestation and malaria risk. Ann Trop Med Parasitol. 2006;100:189–204. doi: 10.1179/136485906X91512.
    1. Meek SR. Vector control in some countries of Southeast Asia: comparing the vectors and the strategies. Ann Trop Med Parasitol. 1995;89:135–147.
    1. Coosemans M, Van Bortel W. Proceedings of the International Conferece Hubs, Harbours and Deltas in Southeast Asia. Phnom Penh; 2006–2007. Malaria vectors in the Mekong Countries : a complex interaction between vectors, environment and human behaviour; pp. 6–8.
    1. Sanh NH, Van Dung N, Thanh NX, Trung TN, Van Co T, Cooper RD. Forest malaria in central Vietnam. Am J Trop Med Hyg. 2008;79:652–654.
    1. Obsomer V, Dufrene M, Defourny P, Coosemans M. Anopheles species associations in Southeast Asia: indicator species and environmental influences. Parasit Vectors. 2013;6:136. doi: 10.1186/1756-3305-6-136.
    1. Trung HD, Van BW, Sochantha T, Keokenchanh K, Briët OJT, Coosemans M. Behavioural heterogeneity of Anopheles species in ecologically different localities in Southeast Asia: a challenge for vector control. Trop Med Int Health. 2005;10:251–262. doi: 10.1111/j.1365-3156.2004.01378.x.
    1. Van Bortel W, Trung HD, Hoi LX, Van Ham N, Van Chut N, Luu ND, Roelants P, Denis L, Speybroeck N, D’Alessandro U, Coosemans M. Malaria transmission and vector behaviour in a forested malaria focus in central Vietnam and the implications for vector control. Malar J. 2010;9:373. doi: 10.1186/1475-2875-9-373.
    1. Tananchai C, Tisgratog R, Juntarajumnong W, Grieco JP, Manguin S, Prabaripai A, Chareonviriyaphap T. Species diversity and biting activity of Anopheles dirus and Anopheles baimaii (Diptera: Culicidae) in a malaria prone area of western Thailand. Parasit Vectors. 2012;5:211. doi: 10.1186/1756-3305-5-211.
    1. Tisgratog R, Tananchai C, Juntarajumnong W, Tuntakom S, Bangs MJ, Corbel V, Chareonviriyaphap T. Host feeding patterns and preference of Anopheles minimus (Diptera: Culicidae) in a malaria endemic area of western Thailand: baseline site description. Parasit Vectors. 2012;5:114. doi: 10.1186/1756-3305-5-114.
    1. Sochantha T, Van Bortel W, Savonnaroth S, Marcotty T, Speybroeck N, Coosemans M. Personal protection by long-lasting insecticidal hammocks against the bites of forest malaria vectors. Trop Med Int Health. 2010;15:336–341. doi: 10.1111/j.1365-3156.2009.02457.x.
    1. Durnez L, Coosemans M. In: Anopheles mosquitoes - New insights into malaria vectors. Manguin S, editor. 2013. Residual transmission of malaria: an old issue for new approaches; pp. 671–704. .
    1. Ministry of Health Cambodia. National strategy for malaria elimination in Cambodia. Phnom Penh: Ministry of Health Cambodia; 2011.
    1. Cook J, Reid H, Iavro J, Kuwahata M, Taleo G, Clements A, McCarthy J, Vallely A, Drakeley C. Using serological measures to monitor changes in malaria transmission in Vanuatu. Malar J. 2010;9:169. doi: 10.1186/1475-2875-9-169.
    1. Corran P, Coleman P, Riley E, Drakeley C. Serology: a robust indicator of malaria transmission intensity? Trends Parasitol. 2007;23:575–582. doi: 10.1016/j.pt.2007.08.023.
    1. Cook J, Speybroeck N, Sochanta T, Somony H, Sokny M, Claes F, Lemmens K, Theisen M, Soares IS, D’Alessandro U, Coosemans M, Erhart A. Sero-epidemiological evaluation of changes in Plasmodium falciparum and Plasmodium vivax transmission patterns over the rainy season in Cambodia. Malar J. 2012;11:86. doi: 10.1186/1475-2875-11-86.
    1. IMPE. Key for identification of Anopheles in Vietnam (adults, pupae and larvae) Hanoi; 1987.
    1. Durnez L, Van Bortel W, Denis L, Roelants P, Veracx A, Trung HD, Sochantha T, Coosemans M. False positive circumsporozoite protein ELISA: a challenge for the estimation of the entomological inoculation rate of malaria and for vector incrimination. Malar J. 2011;10:195. doi: 10.1186/1475-2875-10-195.
    1. Van Bortel W, Trung HD, Roelants P, Harbach RE, Backeljau T, Coosemans M. Molecular identification of Anopheles minimus s.l. beyond distinguishing the members of the species complex. Insect Mol Biol. 2000;9:335–340. doi: 10.1046/j.1365-2583.2000.00192.x.
    1. Walton C, Handley JM, Kuvangkadilok C, Collins FH, Harbach RE, Baimai V, Butlin RK. Identification of five species of the Anopheles dirus complex from Thailand, using allele-specific polymerase chain reaction. Med Vet Entomol. 1999;13:24–32. doi: 10.1046/j.1365-2915.1999.00142.x.
    1. Beebe NW, Saul A. Discrimination of all members of the Anopheles punctulatus complex by polymerase chain reaction--restriction fragment length polymorphism analysis. Am J Trop Med Hyg. 1995;53:478–481.
    1. Walton C, Somboon P, O’Loughlin SM, Zhang S, Harbach RE, Linton Y-M, Chen B, Nolan K, Duong S, Fong M-Y, Vythilingum I, Mohammed ZD, Trung HD, Butlin RK. Genetic diversity and molecular identification of mosquito species in the Anopheles maculatus group using the ITS2 region of rDNA. Infect Genet Evol. 2007;7:93–102. doi: 10.1016/j.meegid.2006.05.001.
    1. Protopopoff N, Van Bortel W, Speybroeck N, Van Geertruyden J-P, Baza D, D’Alessandro U, Coosemans M. Ranking malaria risk factors to guide malaria control efforts in African highlands. PloS One. 2009;4:e8022. doi: 10.1371/journal.pone.0008022.
    1. The malERA Consultative Group on Vector Control. A research agenda for malaria eradication: vector control. PLoS Med. 2011;8:e1000401.
    1. Muenworn V, Sungvornyothin S, Kongmee M, Polsomboon S, Bangs MJ, Akrathanakul P, Tanasinchayakul S, Prabaripai A, Chareonviriyaphap T. Biting activity and host preference of the malaria vectors Anopheles maculatus and Anopheles sawadwongporni (Diptera: Culicidae) in Thailand. J Vector Ecol. 2009;34:62–69.
    1. Obsomer V, Defourny P, Coosemans M. The Anopheles dirus complex: spatial distribution and environmental drivers. Malar J. 2007;6:26. doi: 10.1186/1475-2875-6-26.
    1. Eyles DE, Wharton RH, Cheong WH, Warren M. Studies on malaria and Anopheles balabacensis in Cambodia. Bull World Health Organ. 1964;30:7–21.
    1. Hai NS, Marchand RP, VIen NT, Quang NT, Hung VV, Hinh TD, Do PC, Al E. Vectorial role of An. dirus in deep forest in Khanh Phu. Journal of malaria and parasite diseases control. 2003;4:61–67.
    1. Chambers M, Thuy TQ, Farrar J, Hien TT, Hung NQ. Malaria transmission and occupational risk factors in rural south western Vietnam. In Proceedings of the 5th Vietnam national conference on entomology. Hanoi. 2005;710b–710c:11–12. 710.
    1. Sinka ME, Bangs MJ, Manguin S, Chareonviriyaphap T, Patil AP, Temperley WH, Gething PW, Elyazar IRF, Kabaria CW, Harbach RE, Hay SI. The dominant Anopheles vectors of human malaria in the Asia-Pacific region: occurrence data, distribution maps and bionomic précis. Parasit Vectors. 2011;4:89. doi: 10.1186/1756-3305-4-89.
    1. Trung HD, Van Bortel W, Sochantha T, Keokenchanh K, Quang NT, Cong LD, Coosemans M. Malaria transmission and major malaria vectors in different geographical areas of Southeast Asia. Trop Med Int Health. 2004;9:230–237. doi: 10.1046/j.1365-3156.2003.01179.x.
    1. Dysoley L, Kaneko A, Eto H, Mita T, Socheat D, Börkman A, Kobayakawa T. Changing patterns of forest malaria among the mobile adult male population in Chumkiri District Cambodia. Acta Trop. 2008;106:207–212. doi: 10.1016/j.actatropica.2007.01.007.
    1. Peeters-Grietens K, Nguyen Xuan X, Muela-Ribera J, Ngo-Duc T, Van Bortel W, Truong Ba N, Pham Van K, Le Xuan H, D’Alessandro U, Erhart A. Social determinants of long lasting insecticidal hammock use among the Ra-glai ethnic minority in Vietnam: implications for forest malaria control. PloS One. 2012;7:e29991. doi: 10.1371/journal.pone.0029991.
    1. Russell TL, Govella NJ, Azizi S, Drakeley CJ, Kachur SP, Killeen GF. Increased proportions of outdoor feeding among residual malaria vector populations following increased use of insecticide-treated nets in rural Tanzania. Malar J. 2011;10:80. doi: 10.1186/1475-2875-10-80.
    1. CNM. Cambodia Malaria Survey 2010. CNM: Phnom Penh; 2011.
    1. Lien JC, Atmosoedjono S, Usfinit AU, Gundelfinger BF. Observations on natural plasmodial infections in mosquitoes and a brief survey of mosquito fauna in Belu Regency, Indonesian Timor. J Med Entomol. 1975;12:333–337.
    1. Lien JC, Kawengian BA, Partono F, Lami B, Cross JH. A brief survey of the mosquitoes of South Sulawesi, Indonesia, with special reference to the identity of Anopheles barbirostris (Diptera: Culicidae) from the Margolembo area. J Med Entomol. 1977;13:719–727.
    1. Amerasinghe PH, Amerasinghe FP, Konradsen F, Fonseka KT, Wirtz RA. Malaria vectors in a traditional dry zone village in Sri Lanka. Am J Trop Med Hyg. 1999;60:421–429.
    1. Rattanarithikul R, Konishi E, Linthicum KJ. Detection of Plasmodium vivax and Plasmodium falciparum circumsporozoite antigen in anopheline mosquitoes collected in southern Thailand. Am J Trop Med Hyg. 1996;54:114–121.
    1. Limrat D, Rojruthai B, Apiwathnasorn C, Samung Y, Prommongkol S. Anopheles barbirostris/campestris as a probable vector of malaria in Aranyaprathet, Sa Kaeo Province. Southeast Asian J Trop Med Public Health. 2001;32:739–744.
    1. Do MC, Beebe NW, Van VNT, Le QT, Lein CT, Van ND, Xuan TN, Le NA, Cooper RD. Vectors and malaria transmission in deforested, rural communities in north-central Vietnam. Malar J. 2010;9:259. doi: 10.1186/1475-2875-9-259.
    1. Mouchet J, Carnevale P, Manguin S. Biodiversity of Malaria in the World. John Libbey Eurotext. 2008;427:427.
    1. Rwegoshora TR, Sharpe RG, Baisley KJ, Kittayapong P. Biting behavior and seasonal variation in the abundance of Anopheles minimus species A and C in Thailand. Southeast Asian J Trop Med Public Health. 2002;33:694–701.
    1. Kiware SS, Chitnis N, Devine GJ, Moore SJ, Majambere S, Killeen GF. Biologically meaningful coverage indicators for eliminating malaria transmission. Biol Lett. 2012;8:874–877. doi: 10.1098/rsbl.2012.0352.

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