Effect of different habitat types on abundance and biting times of Anopheles balabacensis Baisas (Diptera: Culicidae) in Kudat district of Sabah, Malaysia

Parasites and Vectors - Tập 12 - Trang 1-13 - 2019
Tock H. Chua1, Benny O. Manin1, Indra Vythilingam2, Kimberly Fornace3, Chris J. Drakeley3
1Department of Pathobiology and Medical Diagnostics, Faculty of Medicine and Health Sciences, Universiti Malaysia Sabah, Sabah, Malaysia
2Department of Parasitology, Faculty of Medicine, University of Malaya, Kuala Lumpur, Malaysia
3Faculty of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, UK

Tóm tắt

We investigated the effect of five common habitat types on the diversity and abundance of Anopheles spp. and on the biting rate and time of Anopheles balabacensis (currently the only known vector for Plasmodium knowlesi in Sabah) at Paradason village, Kudat, Sabah. The habitats were forest edge, playground area, longhouse, oil palm plantation and shrub-bushes area. Sampling of Anopheles was done monthly using the human landing catch method in all habitat types for 14 months (October 2013 to December 2014, excluding June 2014). The Anopheles species were morphologically identified and subjected to PCR assay for the detection of Plasmodium parasites. Generalised linear mixed models (GLMM) were applied to test the variation in abundance and biting rates of An. balabacensis in different habitat types. A total of 1599 Anopheles specimens were collected in the village, of which about 90% were An. balabacensis. Anopheles balabacensis was present throughout the year and was the dominant Anopheles species in all habitat types. The shrub bushes habitat had the highest Anopheles species diversity while forest edge had the greatest number of Anopheles individuals caught. GLMM analysis indicated that An. balabacensis abundance was not affected by the type of habitats, and it was more active during the early and late night compared to predawn and dawn. PCR assay showed that 1.61% of the tested An. balabacensis were positive for malaria parasites, most of which were caught in oil palm estates and infected with one to two Plasmodium species. The identification of infected vectors in a range of habitats, including agricultural and farming areas, illustrates the potential for humans to be exposed to P. knowlesi outside forested areas. This finding contributes to a growing body of evidence implicating environmental changes due to deforestation, expansion of agricultural and farming areas, and development of human settlements near to forest fringes in the emergence of P. knowlesi in Sabah.

Tài liệu tham khảo

Gaveau DLA, Sheil D, Husnayaen A, Salim MA, Arjasakusuma S, Ancrenaz M, et al. Rapid conversions and avoided deforestation: examining four decades of industrial plantation expansion in Borneo. Sci Rep. 2016;6:32017. Yasuoka J, Levins R. Impact of deforestation and agricultural development on anopheline ecology and malaria epidemiology. Am J Trop Med Hyg. 2007;76:450–60. Gaveau DLA, Sloan S, Molidena E, Yaen H, Sheil D, Abram NK, et al. Four decades of forest persistence, clearance and logging on Borneo. PLoS ONE. 2014;9:e101654. Imai N, White MT, Ghani AC, Drakeley CJ. Transmission and control of Plasmodium knowlesi: a mathematical modelling study. PLoS Negl Trop Dis. 2014;8:e2978. Gunggut H, Saufi K, Zaaba Z, Liu MSM. Where have all the forests gone Deforestation in land below the wind. Procedia Soc Behav Sci. 2014;153:363–9. Millar SB, Cox-Singh J. Human infections with Plasmodium knowlesi—zoonotic malaria. Clin Microbiol Infect. 2015;21:640–8. World Health Organization Malaria Policy Advisory Committee. Outcomes from the evidence review group on Plasmodium knowlesi. 2017. http://www.who.int/malaria/mpac/mpac-mar2017-plasmodium-knowlesi-presentation. Accessed 7 Apr 2018. Fornace KM, Abidin TR, Alexander N, Brock P, Grigg MJ, Murphy A, et al. Association between landscape factors and spatial patterns of Plasmodium knowlesi infections in Sabah, Malaysia. Emerg Infect Dis. 2016;22:201–8. Morgan K, Somboon P, Walton C. Understanding Anopheles diversity in Southeast Asia. Rijeka: InTech; 2013. p. 327–55. Sinka ME, Bangs MJ, Manguin S, Chareonviriyaphap T, Patil AP, Temperley WH, et al. The dominant Anopheles vectors of human malaria in the Asia-Pacific region: occurrence data, distribution maps and bionomic précis. Parasit Vectors. 2011;4:89. Bortel WV, Harbach RE, Trung HD, Roelants P, Backeljau T, Coosemans M. Confirmation of Anopheles varuna in Vietnam, previously misidentified and mistargeted as the malaria vector Anopheles minimus. Am J Trop Med Hyg. 2001;65:729–32. Saeung A. Anopheles (Diptera: Culicidae) species complex in Thailand: identification, distribution, bionomics and malaria-vector importance. Int J Parasitol Res. 2012;4:75–82. Vythilingam I, Tan CH, Asmad M, Chan ST, Lee KS, Singh B. Natural transmission of Plasmodium knowlesi to humans by Anopheles latens in Sarawak, Malaysia. Trans R Soc Trop Med Hyg. 2006;100:1087–8. Wong ML, Chua TH, Leong CS, Khaw LT, Fornace K, Wan-Sulaiman WY, et al. Seasonal and spatial dynamics of the primary vector of Plasmodium knowlesi within a major transmission focus in Sabah, Malaysia. PLoS Negl Trop Dis. 2015;9:e0004135. Vythilingam I, Wong ML, Wan-Yussof WS. Current status of Plasmodium knowlesi vectors: a public health concern? Parasitology. 2018;145:32–40. Jeslyn WPS, Huat TC, Vernon L, Irene LMZ, Sung LK, Jarrod LP, et al. Molecular epidemiological investigation of Plasmodium knowlesi in humans and macaques in Singapore. Vector Borne Zoonotic Dis. 2011;11:131–5. Singh B, Sung LK, Matusop A, Radhakrishnan A, Shamsul SSG, Cox-Singh J, et al. A large focus of naturally acquired Plasmodium knowlesi infections in human beings. Lancet. 2004;363:1017–24. Lee KS, Cox-Singh J, Singh B. Morphological features and differential counts of Plasmodium knowlesi parasites in naturally acquired human infections. Malar J. 2009;8:73. Barber BE, William T, Dhararah P, Anderios F, Grigg M, Yeo TW, et al. Epidemiology of Plasmodium knowlesi malaria in north-east Sabah, Malaysia: family clusters and wide age distributions. Malar J. 2012;11:401. Barber BE, William T, Grigg MJ, Menon J, Auburn S, Marfurt J, et al. A prospective comparative study of knowlesi, falciparum, and vivax malaria in Sabah, Malaysia: high proportion with severe disease from Plasmodium knowlesi and Plasmodium vivax but no mortality with early referral and artesunate therapy. Clin Infect Dis. 2013;56:383–97. Goh XT, Lim YA, Vythilingam I, Chew CH, Lee PC, Ngui R, et al. Increased detection of Plasmodium knowlesi in Sandakan division, Sabah as revealed by PlasmoNex™. Malar J. 2013;12:264. Jiram AI, Hisam S, Reuben H, Husin SZ, Roslan A, Ismail WRW. Submicroscopic evidence of the simian malaria parasite, Plasmodium knowlesi, in an orang asli community. SE Asian J Trop Med Public Health. 2016;47:591–9. Lee WC, Chin PW, Lau YL, Chin LC, Fong MY, Yap CJ, et al. Hyperparasitaemic human Plasmodium knowlesi infection with atypical morphology in peninsular Malaysia. Malar J. 2013;12:88. Yusof R, Lau YL, Mahmud R, Fong MY, Jelip J, Ngian HU, et al. High proportion of knowlesi malaria in recent malaria cases in Malaysia. Malar J. 2014;13:168. Figtree M, Lee R, Bain L, Kennedy T, Mackertich S, Urban M, et al. Plasmodium knowlesi in human, Indonesian Borneo. Emerging. Infect Dis. 2010;16:672–4. Setiadi W, Sudoyo H, Trimarsanto H, Sihite BA, Saragih RJ, Juliawaty R, et al. A zoonotic human infection with simian malaria, Plasmodium knowlesi, in central Kalimantan. Indonesia. Malar J. 2016;15:218. Lubis IND, Wijaya H, Lubis M, Lubis CP, Divis PCS, Beshir KB, et al. Contribution of Plasmodium knowlesi to multispecies human malaria infections in North Sumatera, Indonesia. J Infect Dis. 2017;215:1148–55. Ramaswami A, Pisharam JK, Aung H, Ghazala K, Maboud K, Chong VH, et al. Co-incidental Plasmodium knowlesi and mucormycosis infections presenting with acute kidney injury and lower gastrointestinal bleeding. Am J Case Rep. 2013;14:103–5. 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. Jongwutiwes S, Buppan P, Kosuvin R, Seethamchai S, Pattanawong U, Sirichaisinthop J, et al. Plasmodium knowlesi malaria in humans and macaques, Thailand. Emerg Infect Dis. 2011;17:1799–806. Marchand RP, Culleton R, Maeno Y, Quang NT, Nakazawa S. Co-infections of Plasmodium knowlesi, P. falciparum, and P. vivax among humans and Anopheles dirus mosquitoes, Southern Vietnam. Emerg Infect Dis. 2011;17:1232–8. Van den Eede P, Van HN, Overmeir CV, Vythilingam I, Duc TN, Hung LX, et al. Human Plasmodium knowlesi infections in young children in central Vietnam. Malar J. 2009;8:249. Ng OT, Ooi EE, Lee CC, Lee PJ, Ng LC, Wong PS, et al. Naturally acquired human Plasmodium knowlesi infection, Singapore. Emerg Infect Dis. 2008;14:814–6. 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. 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. Khim N, Siv S, Kim S, Mueller T, Fleischmann E, Singh B, et al. Plasmodium knowlesi infection in humans, Cambodia, 2007–2010. Emerg Infect Dis. 2011;17:1900–2. Iwagami M, Nakatsu M, Khattignavong P, Soundala P, Lorphachan L, Keomalaphet S, et al. First case of human infection with Plasmodium knowlesi in Laos. PLoS Negl Trop Dis. 2018;12:e0006244. Hii JLK, Kan S, Vun YS, Chin KF, Tambakau S, Chan MKC, et al. Transmission dynamics and estimates of malaria vectorial capacity for Anopheles balabacensis and An. flavirostris (Diptera: Culicidae) on Banggi island, Sabah, Malaysia. Ann Trop Med Parasitol. 1988;82:91–101. Sabah State Department of Health. 2016 Annual Report of Unit for Control of Vector Borne Diseases (RKPBV), Division of Public Health, Sabah, Malaysia; 2016 (Jabatan Kesihatan Negeri Sabah. Laporan Tahunan RKPBV 2016. Unit Rancangan Kawalan Penyakit Bawaan Vektor, Bahagian Kesihatan Awam, JKNS; 2016). Fornace KM, Herman LS, Abidin TR, Chua TH, Daim S, Lorenzo PJ, et al. Exposure and infection to Plasmodium knowlesi in case study communities in northern Sabah, Malaysia and Palawan, The Philippines. PLoS Negl Trop Dis. 2018;12:e0006432. Cagampang-Ramos A, Darsie Jr RF. Illustrated keys to the Anopheles mosquitoes of the Philippine Islands. Malaria Eradication Training Center, Technical Report 70-1, USAF Fifth Epidemiological Flight. Manila: PACAF; 1970. Rattanarithikul R, Harrison B, Harbach RE, Panthusiri P, Coleman RE. Illustrated keys to the mosquitoes of Thailand IV. Anopheles. Southeast Asian J Trop Med Public Health. 2006;37(2):1–128. Reid JA. Anopheline mosquitoes of Malaya and Borneo. Kuala Lumpur: Government of Malaysia; 1968. Sallum MAM, Peyton EL, Harrison BA, Wilkerson RC. Revision of the Leucosphyrus group of Anopheles (Cellia) (Diptera, Culicidae). Rev Bras Entomol. 2005;49:1–152. Shannon CE, Weaver W. The mathematical theory of communication. Urbana: University of Illinois Press; 1963. Phillips A, Simon C. Simple, efficient, and nondestructive DNA extraction protocols for arthropods. Ann Entomol Soc Am. 1995;88:281–3. 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. Hawkes F, Manin BO, Ng SH, Torr SJ, Drakeley C, Chua TH, Ferguson HM. Evaluation of electric nets as means to sample mosquito vectors host seeking on humans and primates. Parasit Vectors. 2017;10:338. Rohani A, Chan ST, Abdullah AG, Tanrang H, Lee HL. Species composition of mosquito fauna in Ranau, Sabah, Malaysia. Trop Biomed. 2008;25:232–6. Vythilingam I, Chan ST, Shanmugratnam C, Tanrang H, Chooi KH. The impact of development and malaria control activities on its vectors in the Kinabatangan area of Sabah, East Malaysia. Acta Trop. 2005;96:24–30. Hii JLK, Vun YS. A study of dispersal, survival and adult population estimates of the malaria vector, Anopheles balabacensis Baisas (Diptera: Culicidae) in Sabah, Malaysia. Trop Biomed. 1985;2:121–31. McArthur. The control of Anopheles leucospyrus. Malaria conference for the Western Pacific and Southeast Asia Regions, Taipei, 15–27 November 1954. Bryan JE, Shearman PL, Asner GP, Knapp DE, Aoro G, Lokes B. Extreme differences in forest degradation in Borneo: comparing practices in Sarawak, Sabah, and Brunei. PLoS ONE. 2013;8:e69679. Jiram AI, Vythilingam I, NoorAzian YM, Yusof YM, Azahari AH, Fong MY. Entomologic investigation of Plasmodium knowlesi vectors in Kuala Lipis, Pahang, Malaysia. Malar J. 2012;11:213. Rosenberg R, Andre RG, Somchit L. Highly efficient dry season transmission of malaria in Thailand. Trans R Soc Trop Med Hyg. 1990;84:22–8. Dewald JR, Fuller DO, Müller GC, Beier JC. A novel method for mapping village-scale outdoor resting microhabitats of the primary African malaria vector, Anopheles gambiae. Malar J. 2016;15:489. Stark DJ, Fornace KM, Brock PM, Abidin TR, Gilhooly L, Jalius C, et al. Long-tailed macaque response to deforestation in a Plasmodium knowlesi-endemic area. EcoHealth. 2019. https://doi.org/10.1007/s10393-019-01403-9. Akter R, Vythilingam I, Khaw LT, Qvist R, Lim YAL, Sitam FT, et al. Simian malaria in wild macaques: first report from Hulu Selangor district, Selangor, Malaysia. Malar J. 2015;14:386. Lee K, Divis PCS, Zakaria SK, Matusop A, Julin RA, Conway DJ, et al. Plasmodium knowlesi: reservoir hosts and tracking the emergence in humans and macaques. PLoS Pathog. 2011;7:e1002015. 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. Grigg MJ, Cox J, William T, Jelip J, Fornace KM, Brock PM, et al. Individual-level factors associated with the risk of acquiring human Plasmodium knowlesi malaria in Malaysia: a case-control study. Lancet Planet Health. 2017;1:e97–104. Verdonschot PFM, Besse-Lototskaya AA. Flight distance of mosquitoes (Culicidae): a metadata analysis to support the management of barrier zones around rewetted and newly constructed wetlands. Limnologica. 2014;45:69–79. Brant HL, Ewers RM, Vythilingam I, Drakeley C, Benedick S. Vertical stratification of adult mosquitoes (Diptera: Culicidae) within a tropical rainforest in Sabah, Malaysia. Malar J. 2016;15:370. Manin BO, Ferguson HM, Vythilingam I, Fornace K, William T, Torr SJ, et al. Investigating the contribution of peri-domestic transmission to risk of zoonotic malaria infection in humans. PLoS Negl Trop Dis. 2016;10:e0005064. Basseri H, Raeisi A, Khakha MJ, Pakarai A, Abdolghafar H. Seasonal abundance and host-feeding patterns of anopheline vectors in malaria endemic area of Iran. J Parasitol Res. 2010. https://doi.org/10.1155/2010/671291. Freire MG, Schweigmann NJ, Svagelj WS, Loetti MV, Jensen O, Burroni NE. Relationship between environmental conditions and host-seeking activity of Ochlerotatus albifasciatus (Diptera: Culicidae) in an agroecosystem and in an urban area in Chubut, central Patagonia, Argentina. J Nat Hist. 2016;50:1369–80. Stone C, Chitnis N, Gross K. Environmental influences on mosquito foraging and integrated vector management can delay the evolution of behavioral resistance. Evol Appl. 2015. https://doi.org/10.1111/eva.12354. William T, Jelip J, Menon MY, Anderios F, Mohammad R, Mohammad TAAM, et al. Changing epidemiology of malaria in Sabah, Malaysia: increasing incidence of Plasmodium knowlesi. Malar J. 2014;13:390. 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. Coatney GR, Chin W, Contacos PG, King HK. Plasmodium inui, a quartan-type malaria parasite of old world monkeys transmissible to man. J Parasitol. 1966;52:660–3. Imwong M, Madmanee W, Suwannasin K, Kunasol C, Peto TJ, Tripura R, et al. Asymptomatic natural human infections with the simian malaria parasites Plasmodium cynomolgi and Plasmodium knowlesi. J Infect Dis. 2018. https://doi.org/10.1093/infdis/jiy519. Ta TH, Hisam S, Lanza M, Jiram AI, Ismail N, Rubio JM. First case of naturally acquired human infection with Plasmodium cynomolgi. Malar J. 2014;13:68.