Anopheles population belonging to Barbirostris complex in Narathiwat Province and its vectorial status for human and simian malaria

Authors

  • Surasuk Yanmanee Faculty of Medicine, Chulalongkorn University, Bangkok, Thailand and Faculty of Science, Naresuan University, Pitsanulok, Thailand
  • Sunee Seethamchai Faculty of Science, Naresuan University, Pitsanulok, Thailand
  • Napaporn Kuamsab Faculty of Medicine, Chulalongkorn University, Bangkok, Thailand and Faculty of Health Science and Technology, Southern College of Technology, Nakhorn Si Thammarat, Thailand
  • Taweesak Tia Faculty of Medicine, Chulalongkorn University, Bangkok, Thailand
  • Somchai Jongwutiwes Faculty of Medicine, Chulalongkorn University, Bangkok, Thailand
  • Chaturong Putaporntip Faculty of Medicine, Chulalongkorn University, Bangkok, Thailand

Keywords:

Anopheles barbirostris, internal transcribed spacer 2, malaria vector, primate malaria

Abstract

Background: Besides well-perceived species of Plasmodium infecting humans, at least four simian malaria species including P. knowlesi, P. cynomolgi, P. inui and P. fieldi have been incriminated in human infections in Thailand. The vectors of simian malaria in this country have been recently identified as Anopheles latens and An. introlatus.

Objectives: To address whether mosquitoes in Barbirostris complex could be potential vectors of simian malaria and to analyze species composition of Anopheles in this complex from the sampled population.

Methods: During 2018 and 2019, a total of 115 female Anopheles collected by human-landing catches from Sukhirin and Waeng Districts in Narathiwat Province morphologically assigned to Barbirostris complex were included for analysis. Deoxyribonucleic acid (DNA) was extracted from salivary gland samples of individual mosquitoes. Molecular identification of mosquito members of Barbirostris complex was performed by polymerase chain reaction (PCR) amplification of the internal transcribed spacer 2 (ITS2) region and its partial flanking sequences of Anopheles ribosomal ribonucleic acid (rRNA) cistron, followed by sequencing. Analysis of individual salivary gland samples was performed by species-specific nested PCR targeting mitochondrial cytochrome oxidase I of four human Plasmodium species, P. knowlesi, P. cynomolgi, P. inui and P. fieldi.

Results: Two amplicon lengths comprising ~1.9 and ~1 kb fragments were observed in 72 and 43 mosquitoes, respectively. Sequence analysis of the 5’ portion of ITS2 from 21 randomly selected mosquitoes has shown two distinct phylogenetic clades. All 12 mosquitoes bearing 1.9-kb amplicons displayed perfect sequence identity across samples and were placed in a clade related to but distinct from An. saeungae. Nine specimens with 1-kb amplicons were clustered within An. barbirostris species A3. All salivary gland samples gave negative results for malarial DNA.

Conclusion: Two genetically distinct lineages have been identified in Barbirostris complex in Narathiwat Province. None of these carried malarial DNA in their salivary glands, suggesting that they might not be vectors of simian malaria.

Downloads

Download data is not yet available.

References

World Health Organization. World malaria report 2022.Geneva: WHO; 2022.

Coatney GR, Collins WE, Warren M, Contacos PG. Theprimate malarias [CD-ROM]. Atlanta: Centers forDisease Control and Prevention; 2003.

Jongwutiwes S, Putaporntip C, Iwasaki T, Sata T,Kanbara H. Naturally acquired Plasmodium knowlesimalaria in human, Thailand. Emerg Infect Dis2004;10:2211-3. https://doi.org/10.3201/eid1012.040293 PMid:15663864 PMCid:PMC3323387

Putaporntip C, Hongsrimuang T, Seethamchai S,Kobasa T, Limkittikul K, Cui L, et al. Differentialprevalence of Plasmodium infections and crypticPlasmodium knowlesi malaria in humans in Thailand.J Infect Dis 2009;199:1143-50. https://doi.org/10.1086/597414 PMid:19284284 PMCid:PMC8817623

Putaporntip C, Kuamsab N, Pattanawong U, YanmaneeS, Seethamchai S, Jongwutiwes S. Plasmodiumcynomolgi co-infections among symptomatic malariapatients, Thailand. Emerg Infect Dis 2021;27:590-3. https://doi.org/10.3201/eid2702.191660 PMid:33496236 PMCid:PMC7853550

Putaporntip C, Kuamsab N, Seethamchai S,Pattanawong U, Rojrung R, Yanmanee S, et al. CrypticPlasmodium inui and Plasmodium fieldi infectionsamong symptomatic malaria patients in Thailand.Clin Infect Dis 2022;75:805-12. https://doi.org/10.1093/cid/ciab1060 PMid:34971372

Singh B, Daneshvar C. Human infections and detection306 of Plasmodium knowlesi. Clin Microbiol Rev2013;26:165-84. https://doi.org/10.1128/CMR.00079-12 PMid:23554413 PMCid:PMC3623376

Cox-Singh J, Davis TM, Lee KS, Shamsul SS, MatusopA, Ratnam S, et al. Plasmodium knowlesi malaria inhumans is widely distributed and potentially lifethreatening. Clin Infect Dis 2008;46:165-71. https://doi.org/10.1086/524888 PMid:18171245 PMCid:PMC2533694

Nakaviroj S, Kobasa T, Teeranaipong P, PutaporntipC, Jongwutiwes S. An autochthonous case of severePlasmodium knowlesi malaria in Thailand. Am J TropMed Hyg 2015;92:569-72. https://doi.org/10.4269/ajtmh.14-0610 PMid:25535314 PMCid:PMC4350551

Ministry of Public Health of Thailand, Division ofVector Bourne Diseases. Malaria Online. Bangkok:MPH: 2023.

Jongwutiwes S, Buppan P, Kosuvin R, Seethamchai S,Pattanawong U, Sirichaisinthop J, et al. Plasmodiumknowlesi malaria in humans and macaques, Thailand.Emerg Infect Dis 2011;17:1799-806. https://doi.org/10.3201/eid1710.110349 PMid:22000348 PMCid:PMC3310673

Scanlon JE, Peyton EL, Gould DJ. The anopheles(cellia ) leucosphyrus donitz 1901 group in Thailand.Proc Pap Annu Conf Calif Mosq Control Assoc1967;35:78-83.

Rattanarithikul R, Linthicum KJ, Konishi E. Seasonalabundance and parity rates of Anopheles species insouthern Thailand. J Am Mosq Control Assoc1996;12:75-83.

Yanmanee S, Seethamchai S, Kuamsab N, Karaphan S,Suwonkerd W, Jongwutiwes S, et al. Natural vectorsfor Plasmodium knowlesi and other primate, avian andungulate malaria parasites in Narathiwat Province,Southern Thailand. Sci Rep 2023;13:8875. https://doi.org/10.1038/s41598-023-36017-3 PMid:37264067 PMCid:PMC10235068

Ang JXD, Kadir KA, Mohamad DSA, Matusop A,Divis PCS, Yaman K, et al. New vectors in northernSarawak, Malaysian Borneo, for the zoonotic malariaparasite, Plasmodium knowlesi. Parasit Vectors2020;13:472. https://doi.org/10.1186/s13071-020-04345-2 PMid:32933567 PMCid:PMC7490903

Sinka ME, Bangs MJ, Manguin S, ChareonviriyaphapT, Patil AP, Temperley WH, et al. The dominantAnopheles vectors of human malaria in the Asia-Pacificregion: occurrence data, distribution maps andbionomic précis. Parasit Vectors 2011;4:89. https://doi.org/10.1186/1756-3305-4-89 PMid:21612587 PMCid:PMC3127851

Putaporntip C, Jongwutiwes S, Thongaree S,Seethamchai S, Grynberg P, Hughes AL. Ecology ofmalaria parasites infecting Southeast Asian macaques:evidence from cytochrome b sequences. Mol Ecol2010;19:3466-76. https://doi.org/10.1111/j.1365-294X.2010.04756.x PMid:20646216 PMCid:PMC2921002

Edgar RC. MUSCLE: multiple sequence alignment withhigh accuracy and high throughput. Nucleic AcidsRes 2004;32:1792-7. https://doi.org/10.1093/nar/gkh340 PMid:15034147 PMCid:PMC390337

Tamura K, Stecher G, Peterson D, Filipski A, Kumar S.MEGA6: Molecular Evolutionary Genetics Analysisversion 6.0. Mol Biol Evol 2013;30:2725-9. https://doi.org/10.1093/molbev/mst197 PMid:24132122 PMCid:PMC3840312

Sum JS, Lee WC, Amir A, Braima KA, Jeffery J, Abdul-Aziz NM, et al. Phylogenetic study of six species ofAnopheles mosquitoes in Peninsular Malaysia basedon inter- transcribed spacer region 2 (ITS2) of ribosomalDNA. Parasit Vectors 2014;7:309. https://doi.org/10.1186/1756-3305-7-309 PMid:24993022 PMCid:PMC4094596

Van Bortel W, Harbach RE, Trung HD, Roelants P,Backeljau T, Coosemans M. Confirmation of Anophelesvaruna in vietnam, previously misidentified andmistargeted as the malaria vector Anopheles minimus.Am J Trop Med Hyg 2001;65:729-32. https://doi.org/10.4269/ajtmh.2001.65.729 PMid:11791965

Limrat D, Rojruthai B, Apiwathnasorn C, Samung Y,Prommongkol S. Anopheles barbirostris/campestrisas a probable vector of malaria in Aranyaprathet,Sa Kaeo Province. Southeast Asian J Trop Med PublicHealth 2001;32:739-44.

Apiwathnasorn C, Prommongkol S, Samung Y, LimratD, Rojruthai B. Potential for Anopheles campestris(Diptera: Culicidae) to transmit malaria parasites inPa Rai subdistrict (Aranyaprathet, Sa Kaeo Province),Thailand. J Med Entomol 2002; 39: 583-6 https://doi.org/10.1603/0022-2585-39.4.583 PMid:12144288

Wolfe ND, Escalante AA, Karesh WB, Kilbourn A,Spielman A, Lal AA. Wild primate populations inemerging infectious disease research: the missing link?Emerg Infect Dis 1998;4:149-58. https://doi.org/10.3201/eid0402.980202 PMid:9621185 PMCid:PMC2640138

Vythilingam I, Chua TH, Liew JWK, Manin BO,Ferguson HM. The vectors of Plasmodium knowlesiand other simian malarias Southeast Asia: challengesin malaria elimination.Adv Parasitol 2021;113:131-89. https://doi.org/10.1016/bs.apar.2021.08.005 PMid:34620382

De Ang JX, Yaman K, Kadir KA, Matusop A, Singh B.New vectors that are early feeders for Plasmodiumknowlesi and other simian malaria parasites in Sarawak,Malaysian Borneo. Sci Rep 2021;11:7739. https://doi.org/10.1038/s41598-021-86107-3 PMid:33833272 PMCid:PMC8032675

Hawkes FM, Manin BO, Cooper A, Daim SRH, Jelip J,Husin T, et al. Vector compositions change acrossforested to deforested ecotones in emerging areas ofzoonotic malaria transmission in Malaysia. Sci Rep2019;9:13312. https://doi.org/10.1038/s41598-019-49842-2 PMid:31527622 PMCid:PMC6746737

Vidhya PT, Sunish IP, Maile A, Zahid AK. Anophelessundaicus mosquitoes as vector for Plasmodiumknowlesi, Andaman and Nicobar Islands, India. EmergInfect Dis 2019;25:817-20. https://doi.org/10.3201/eid2504.181668 PMid:30882328 PMCid:PMC6433020

Reid JA, Weitz B. Anopheline mosquitoes as vectorsof animal malaria in Malaya. Ann Trop Med Parasitol1961;55:180-6. https://doi.org/10.1080/00034983.1961.11686034 PMid:13740488

Reid JA, Harrison BA, Atmosoedjono S. Variation andvector status in Anopheles barbirostris. Mosq Syst1979;11:235-51.

Amerasinghe PH, Amerasinghe FP. Multiple hostfeeding in field populations of Anopheles culicifaciesand An. subpictus in Sri Lanka. Med Vet Entomol1999;13:124-31. https://doi.org/10.1046/j.1365-2915.1999.00160.x PMid:10484158

Brosseau L, Udom C, Sukkanon C, ChareonviriyaphapT, Bangs MJ, Saeung A, et al. A multiplex PCR assayfor the identification of five species of the Anophelesbarbirostris complex in Thailand. Parasit Vectors2019;12:223. https://doi.org/10.1186/s13071-019-3494-8 PMid:31088534 PMCid:PMC6515612

Chaiphongpachara T, Changbunjong T, Laojun S,Sumruayphol S, Suwandittakul N, Kuntawong K, et al.Geometric morphometric and molecular techniques for307discriminating among three cryptic species of theAnopheles barbirostris complex (Diptera: Culicidae)in Thailand. Heliyon 2022;8:e11261 https://doi.org/10.1016/j.heliyon.2022.e11261 PMid:36339998 PMCid:PMC9634016

Baker EZ, Beier JC, Meek SR, Wirtz RA. Detection andquantification of Plasmodium falciparum and P. vivaxinfections in Thai-Kampuchean Anopheles (Diptera:Culicidae) by enzyme-linked immunosorbent assay.J Med Entomol 1987;24:536-41. https://doi.org/10.1093/jmedent/24.5.536 PMid:3312607

Rattanarithikul R, Konishi E, Linthicum KJ. Detectionof Plasmodium vivax and Plasmodium falciparumcircumsporozoite antigen in anopheline mosquitoescollected in southern Thailand. Am J Trop Med Hyg1996;54:114-21. https://doi.org/10.4269/ajtmh.1996.54.114 PMid:8619432

Frances SP, Klein TA, Wirtz RA, Eamsila C, PilakasiriC, Linthicum KJ. Plasmodium falciparum and P. vivaxcircumsporozoite proteins in anophelines (Diptera:Culicidae) collected in eastern Thailand. J Med Entomol1996;33:990-1. https://doi.org/10.1093/jmedent/33.6.990 PMid:8961653

Sriwichai P, Samung Y, Sumruayphol S, Kiattibutr K,Kumpitak C, Payakkapol A, et al. Natural humanPlasmodium infections in major Anopheles mosquitoesin western Thailand. Parasit Vectors 2016;9:17.38. Cooper RD, Edstein MD, Frances SP, Beebe NW.Malaria vectors of Timor-Leste. Malar J 2010;9:40.308 https://doi.org/10.1186/s13071-016-1295-x PMid:26762512 PMCid:PMC4712558

Downloads

Published

2023-09-13

How to Cite

1.
Yanmanee S, Seethamchai S, Kuamsab N, Tia T, Jongwutiwes S, Putaporntip C. Anopheles population belonging to Barbirostris complex in Narathiwat Province and its vectorial status for human and simian malaria. Chula Med J [Internet]. 2023 Sep. 13 [cited 2024 Dec. 22];67(4):297-308. Available from: https://he05.tci-thaijo.org/index.php/CMJ/article/view/711

Similar Articles

You may also start an advanced similarity search for this article.