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Natural Plasmodium vivax infections in Anopheles mosquitoes in a malaria endemic area of northeastern Thailand

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Abstract

There was recently an outbreak of malaria in Ubon Ratchathani Province, northeastern Thailand. In the absence of information on malaria vector transmission dynamics, this study aimed to identify the anopheline vectors and their role in malaria transmission. Adult female Anopheles mosquitoes were collected monthly by human-landing catch in Na Chaluai District of Ubon Ratchathani Province during January 2014−December 2015. Field-captured mosquitoes were identified to species using morphology-based keys and molecular assays (allele-specific polymerase chain reaction, AS-PCR), and analysed for the presence of Plasmodium falciparum and Plasmodium vivax using an enzyme-linked immunosorbent assay (ELISA) for the detection of circumsporozoite proteins (CSP). A total of 1,229 Anopheles females belonging to 13 species were collected. Four anopheline taxa were most abundant: Members of the Anopheles barbirostris complex, comprising 38% of the specimens, species of the Anopheles hyrcanus group (18%), Anopheles nivipes (17%) and Anopheles philippinensis (12%). The other nine species comprised 15% of the collections. Plasmodium infections were detected in two of 668 pooled samples of heads/thoraces, Anopheles dirus (1/29) and An. philippinensis (1/97). The An. dirus pool had a mixed infection of P. vivax-210 and P. vivax-247, whereas the An. philippinensis pool was positive only for the latter protein variant. Both positive ELISA samples were confirmed by nested PCR. This study is the first to incriminate An. dirus and An. philippinensis as natural malaria vectors in the area where the outbreak occurred. This information can assist in designing and implementing a more effective malaria control programme in the province.

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References

  • Alam MS, Chakma S, Khan WA, Glass GE, Mohon AN, Elahi R, Norris LC, Podder MP, Ahmed S, Haque R, Sack DA, Sullivan DJ Jr, Norris DE (2012) Diversity of anopheline species and their Plasmodium infection status in rural Bandarban, Bangladesh. Parasit Vectors 5:150

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arez AP, Lopes D, Pinto J, Franco AS, Snounou G, do Rosário VE (2000) Plasmodium sp.: optimal protocols for PCR detection of low parasite numbers from mosquito (Anopheles sp.) samples. Exp Parasitol 94:269−272

    Article  CAS  PubMed  Google Scholar 

  • Baimai V, Kijchalao U, Sawadwongporn P, Green CA (1988) Geographic distribution and biting behaviour of four species of the Anopheles dirus complex (Diptera: Culicidae) in Thailand. Southeast Asian J Trop Med Public Health 19:151−161

    CAS  PubMed  Google Scholar 

  • Bashar K, Tuno N (2014) Seasonal abundance of Anopheles mosquitoes and their association with meteorological factors and malaria incidence in Bangladesh. Parasit Vectors 7:442

    Article  PubMed  PubMed Central  Google Scholar 

  • Bureau of Vector Borne Diseases (2014) Annual Report 2014, Bureau of Vector Borne Diseases, Ministry of Public Health

  • Bureau of Vector Borne Diseases (2015) Annual Report 2015, Bureau of Vector Borne Diseases, Ministry of Public Health

  • Coleman RE, Sithiprasasna R, Kankaew P, Kiaattiut C, Ratanawong S, Khuntirat B, Sattabongkot J (2002) Naturally occurring infection of Plasmodium vivax VK210 and P. vivax VK247 in Anopheles mosquitoes (Diptera: Culicidae) in western Thailand. J Med Entomol 39:556–559

    Article  PubMed  Google Scholar 

  • Corbel V, Nosten F, Thanispong K, Luxemburger C, Kongmee M, Chareonviriyaphap T (2013) Challenges and prospects for dengue and malaria control in Thailand, Southeast Asia. Trends Parasitol 29:623–633

    Article  PubMed  Google Scholar 

  • Durnez L, Van Bortel W, Denis L, Roelants P, Veracx A, Trung HD, Sochantha T, Coosemans M (2011) False positive circumsporozoite protein ELISA: a challenge for the estimation of the entomological inoculation rate of malaria and for vector incrimination. Malar J 10:195

    Article  PubMed  PubMed Central  Google Scholar 

  • Frances SP, Klein TA, Wirtz RA, Eamsila C, Linthicum KJ (1996) Plasmodium falciparum and Plasmodium vivax circumsporozoite antigen in Anopheles collected in eastern Thailand. J Med Entomol 33:990–991

    Article  CAS  PubMed  Google Scholar 

  • Gingrich J, Weatherhead A, Sattabongkot J, Pilakasiri C, Wirtz RA (1990) Hyperendemic malaria in Thai village: dependence of year-round transmission on focal and seasonally circumscribed mosquito (Diptera: Culicidae) habitats. J Med Entomol 27:1016–1126

    Article  CAS  PubMed  Google Scholar 

  • Harbach RE (2017) Anopheles classification. Mosquito taxonomic inventory. http://mosquito-taxonomic-inventory.info/. Accessed 20 May 2017

  • Harbach RE, Gingrich JB, Pang LW (1987) Some entomological observations on malaria transmission in a remote village in northwestern Thailand. J Am Mosq Control Assoc 3:296–301

    CAS  PubMed  Google Scholar 

  • Harbach RE, Rattanarithikul R, Harrison BA (2017) Anopheles prachongae, a new species of the Gigas complex of subgenus Anopheles (Diptera: Culicidae) in Thailand, contrasted with known forms of the complex. Zootaxa 4236(1):65–81

    Article  Google Scholar 

  • Harrison BA, Scanlon JE (1975) Medical entomology studies II. The subgenus Anopheles in Thailand (Diptera: Culicidae). Contrib Am Entomol Inst 12(1):iv + 1–307

    Google Scholar 

  • Imwong M, Jindakhad T, Kunasol C, Sutawong K, Vejakama P, Dondorp AM (2015) An outbreak of artemisinin resistant falciparum malaria in eastern Thailand. Sci Rep 5:17412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Junkum A, Pitasawat B, Tuetun B, Saeung A, Rattanachanpichai E, Jariyapan N, Komalamisra N, Mogi M, Chaithong U, Choochote W (2007) Seasonal abundance and biting activity of Anopheles aconitus (Diptera: Culicidae) in Chiang Mai, northern Thailand. Southeast Asian J Trop Med Public Health 38(Suppl 1):215–223

    Google Scholar 

  • Kimura M, Kawamoto F (2000) PCR diagnosis of four human malaria parasites. The Toyota Foundation mini-symposium on malaria, Faculty of Tropical Medicine, Mahidol University, Bangkok

    Google Scholar 

  • Cui L, Yan G, Sattabongkot J, Cao Y, Chen B, Chen X, Fan Q, Fang Q, Jongwutiwes S, Parker D, Sirichaisinthop J, Kyaw MP, Su XZ, Yang H, Yang Z, Wang B, Xu J, Zheng B, Zhong D, Zhou G (2012) Malaria in the greater Mekong subregion: heterogeneity and complexity. Acta Trop 121:227–239

    Article  PubMed  Google Scholar 

  • Lyttleton C (2016) Deviance and resistance: malaria elimination in the greater Mekong subregion. Soc Sci Med 150:144–152

    Article  PubMed  Google Scholar 

  • Manguin S, Garros C, Dusfour I, Harbach RE, Coosemans M (2008) Bionomics, taxonomy, and distribution of the major malaria vector taxa of Anopheles subgenus Cellia in Southeast Asia: an updated review. Infect Genet Evol 8:489–503

    Article  CAS  PubMed  Google Scholar 

  • Obsomer V, Defourny P, Coosemans M (2007) The Anopheles dirus complex: spatial distribution and environmental drivers. Malar J 6:26

    Article  PubMed  PubMed Central  Google Scholar 

  • Petney T, Sithithaworn P, Satrawaha R, Grundy-Warr C, Andrews WYC, Feng CC (2009) Potential malaria reemergence, northeastern Thailand. Emerg Infect Dis 15:1330

    Article  PubMed  PubMed Central  Google Scholar 

  • Peyton EL, Harrison BA (1979) Anopheles (Cellia) dirus, a new species of the Leucosphyrus Group from Thailand (Diptera: Culicidae). Mosq Syst 11:40–52

    Google Scholar 

  • Prakash A, Walton C, Bhattacharyya DR, Mohapatra PK, Mahanta J (2006) Characterization of ITS2 rDNA of Anopheles philippinensis and Anopheles nivipes (Diptera: Culicidae) from north-east India. Southeast Asian J Trop Med Public Health 37:1134–1138

    CAS  PubMed  Google Scholar 

  • Rattanarithikul R, Harrison BA, Harbach RE, Panthusiri P, Coleman RE (2006) Illustrated keys to the mosquitoes of Thailand IV. Anopheles. Southeast Asian J Trop Med Public Health 37:1–128

    Google Scholar 

  • Rattanarithikul R, Konishi E, Linthicum KJ (1996) Detection of Plasmodium vivax and Plasmodium falciparum circumsporozoite antigen in anopheline mosquitoes collected in southern Thailand. Am J Trop Med Hyg 54:114–121

    Article  CAS  PubMed  Google Scholar 

  • Reid JA (1968) Anopheline mosquitoes of Malaya and Borneo. Stud Inst Med Res Malaya 31:1–520

    Google Scholar 

  • Rosenberg R, Andre RG (1985) Highly efficient, dry season transmission of malaria in eastern Thailand. Southeast Asian J Trop Med Public Health 16:188–189

    Google Scholar 

  • Rosenberg R, Andre RG, Somchit L (1990) Highly efficient dry season transmission of malaria in Thailand. Trans R Soc Trop Med Hyg 84:22–28

    Article  CAS  PubMed  Google Scholar 

  • Scanlon JE, Sandhinand J (1965) The distribution and biology of Anopheles balabacensis in Thailand (Diptera: Culicidae). J Med Entomol 2:61–69

    Article  CAS  PubMed  Google Scholar 

  • Sinka ME, Bangs MJ, Manguin S, Chareonviriyaphap T, Patil AP, Temperley WH, Gething PW, Elyazar IR, Kabaria CW, Harbach RE, Hay SI (2011) The dominant Anopheles vectors of human malaria in the Asia-Pacific region: occurrence data, distribution maps and bionomic précis. Parasit Vectors 4:89

    Article  PubMed  PubMed Central  Google Scholar 

  • Snounou G, Viriyakosol S, Zhu XP, Jarra W, Pinheiro L, do Rosario VE, Thaithong S, Brown KN (1993) High sensitivity of detection of human malaria parasites by the use of nested polymerase chain reaction. Mol Biochem Parasitol 61:315–320

    Article  CAS  PubMed  Google Scholar 

  • Somboon P, Rattanarithikul R (2013) Mosquito surveys, rearing, preservation of mosquito specimens and identification of Anopheles in Thailand. Bureau of Vector Borne Disease, Ministry of Public Health

  • Somboon P, Suwonkerd W, Lines JD (1994) Susceptibility of Thai zoophilic anophelines and suspected malaria vectors to local strains of human malaria parasites. Southeast Asian J Trop Med Public Health 25:766–770

    CAS  PubMed  Google Scholar 

  • Sriwichai P, Samung Y, Sumruayphol S, Kiattibutr K, Kumpitak C, Payakkapol A, Kaewkungwal J, Yan G, Cui L, Sattabongkot J (2016) Natural human Plasmodium infections in major Anopheles mosquitoes in western Thailand. Parasit Vectors 9:17

    Article  PubMed  PubMed Central  Google Scholar 

  • Sungvornyothin S, Kongmee M, Muenvorn V, Polsomboon S, Bangs MJ, Prabaripai A, Tantakom S, Chareonviriyaphap T (2009) Seasonal abundance and bloodfeeding activity of Anopheles dirus sensu lato in western Thailand. J Am Mosq Control Assoc 25:425–430

  • Tainchum K, Kongmee M, Manguin S, Bangs MJ, Chareonviriyaphap T (2015) Anopheles species diversity and distribution of the malaria vectors of Thailand. Trends Parasitol 31:109–119

    Article  PubMed  Google Scholar 

  • Tainchum K, Ritthison W, Chuaycharoensuk T, Bangs MJ, Manguin S, Chareonviriyaphap T (2014) Diversity of Anopheles species and trophic behavior of putative malaria vectors in two malaria endemic areas of northwestern Thailand. J Vector Ecol 39:424–436

    Article  PubMed  Google Scholar 

  • Tananchai C, Tisgratog R, Juntarajumnong W, Grieco JR, Manguin S, Prabaripai A, Chareonviriyaphap T (2012) Species diversity and biting activity of Anopheles dirus and Anopheles baimaii (Diptera: Culicidae) in a malaria prone area of western Thailand. Parasit Vectors 5:211

    Article  PubMed  PubMed Central  Google Scholar 

  • Thongsahuan S, Baimai V, Junkum A, Saeung A, Min GS, Joshi D, Park MH, Somboon P, Suwonkerd W, Tippawangkosol P, Jariyapan N, Choochote W (2011) Susceptibility of Anopheles campestris-like and Anopheles barbirostris species complexes to Plasmodium falciparum and Plasmodium vivax in Thailand. Mem Inst Oswaldo Cruz 106:105–112

    Article  PubMed  Google Scholar 

  • Tisgratog R, Tananchai C, Juntarajumnong W, Tuntakom S, Bangs MJ, Corbel V, Chareonviriyaphap T (2012) Host feeding patterns and preference of Anopheles minimus (Diptera: Culicidae) in a malaria endemic area of western Thailand: baseline site description. Parasit Vectors 5:114

    Article  PubMed  PubMed Central  Google Scholar 

  • Trung HD, Van Bortel W, Sochantha T, Keokenchanh K, Quang NT, Cong LD, Coosemans M (2004) Malaria transmission and major malaria vectors in different geographical areas of Southeast Asia. Tropical Med Int Health 9:230–237

    Article  CAS  Google Scholar 

  • Walton C, Handley JM, Kuvangkadilok C, Collins FH, Harbach RE, Baimai V, Butlin RK (1999) Identification of five species of the Anopheles dirus complex from Thailand, using allele-specific polymerase chain reaction. Med Vet Entomol 13:24–32

    Article  CAS  PubMed  Google Scholar 

  • Walton C, Somboon P, Harbach RE, Zhang S, Weerasinghe I, O'Loughlin SM, Phompida S, Sochantha T, Tun-Lin W, Chen B, Butlin RK (2007) Molecular identification of mosquito species in the Anopheles annularis group in southern Asia. Med Vet Entomol 21:30–35

    Article  CAS  PubMed  Google Scholar 

  • WHO (2016) World malaria report 2016. WHO Global Malaria Programme

  • Wilkinson RN, Miller TA, Esah S (1970) Anthropophilic mosquitoes in central Thailand, with notes on Anopheles balabacensis Baisas and malaria. Mosq News 30:146–148

    Google Scholar 

  • Wirtz RA, Sattabongkot J, Hall T, Burkot TR, Rosenberg R (1992) Development and evaluation of an enzyme-linked immunosorbent assay for Plasmodium vivax-VK247 sporozoites. J Med Entomol 29:854–857

    Article  CAS  PubMed  Google Scholar 

  • Yasuoka J, Levins R (2007) Impact of deforestation and agricultural development on anopheline ecology and malaria epidemiology. Am J Trop Med Hyg 76:450–460

    PubMed  Google Scholar 

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Correspondence to Atiporn Saeung.

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Poolphol, P., Harbach, R.E., Sriwichai, P. et al. Natural Plasmodium vivax infections in Anopheles mosquitoes in a malaria endemic area of northeastern Thailand. Parasitol Res 116, 3349–3359 (2017). https://doi.org/10.1007/s00436-017-5653-1

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