Anopheles sinensis mosquito insecticide resistance: comparison of three mosquito sample collection and preparation methods and mosquito age in resistance measurements

Particle and Fibre Toxicology

Bin Zheng²  Guiyun Yan¹  Fengyang Fu³  Xuelian Chang⁴  Linhua Tang²  Daibin Zhong¹  Tielong Xu² 

[1] Program in Public Health, College of Health Sciences, University of California at Irvine, Irvine, CA 92697, USA;National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, and WHO Collaborating Center for Malaria, Schistosomiasis and Filariasis, Ministry of Public Health, Shanghai, China;Institute of Entomology and Molecular Biology, College of Life Sciences, Chongqing Normal University, Chongqing, China;Department of Pathogen Biology, Bengbu Medical College, Anhui, China

关键词: Mosquito preparation methods;    Pyrethroid resistance;    Anopheles sinensis;   

Others  :  822970
DOI  :  10.1186/1756-3305-7-54

 received in 2013-06-14, accepted in 2014-01-17,  发布年份 2014

【 摘 要 】

Background

Insecticide resistance monitoring in malaria mosquitoes is essential for guiding the rational use of insecticides in vector control programs. Resistance bioassay is the first step for insecticide monitoring and it lays an important foundation for molecular examination of resistance mechanisms. In the literature, various mosquito sample collection and preparation methods have been used, but how mosquito sample collection and preparation methods affect insecticide susceptibility bioassay results is largely unknown. The objectives of this study were to determine whether mosquito sample collection and preparation methods affected bioassay results, which may cause incorrect classification of mosquito resistance status.

Methods

The study was conducted in Anopheles sinensis mosquitoes in two study sites in central China. Three mosquito sample collection and preparation methods were compared for insecticide susceptibility, kdr frequencies and metabolic enzyme activities: 1) adult mosquitoes collected from the field; 2) F1 adults from field collected, blood-fed mosquitoes; and 3) adult mosquitoes reared from field collected larvae.

Results

Mosquito sample collection and preparation methods significantly affected mortality rates in the standard WHO tube resistance bioassay. Mortality rate of field-collected female adults was 10-15% higher than in mosquitoes reared from field-collected larvae and F1 adults from field collected blood-fed females. This pattern was consistent in mosquitoes from the two study sites. High kdr mutation frequency (85-95%) with L1014F allele as the predominant mutation was found in our study populations. Field-collected female adults consistently exhibited the highest monooxygenase and GST activities. The higher mortality rate observed in the field-collected female mosquitoes may have been caused by a mixture of mosquitoes of different ages, as older mosquitoes were more susceptible to deltamethrin than younger mosquitoes.

Conclusions

Female adults reared from field-collected larvae in resistance bioassays are recommended to minimize the effect of confounding factors such as mosquito age and blood feeding status so that more reliable and reproducible mortality may be obtained.

【 授权许可】

   
2014 Xu et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

【 参考文献 】

• [1]WHO: Global Malaria Program: Use of indoor residual spraying for scaling up global malaria control and elimination. WHO position statement. Geneva: World Health Organization; 2006. Available at: http://whqlibdoc.who.int/hq/2006/WHO_HTM_MAL_2006.1112_eng.pdf?ua=1 webcite. Accessed January 17, 2014
• [2]WHO: Malaria control today: current WHO recommendations. Geneva: Working document March, World Health Organization; 2005.
• [3]Hunt R, Edwardes M, Coetzee M: Pyrethroid resistance in southern African Anopheles funestusextends to Likoma Island in Lake Malawi. Parasit Vectors 2010, 3:122. BioMed Central Full Text
• [4]Raghavendra K, Verma V, Srivastava HC, Gunasekaran K, Sreehari U, Dash AP: Persistence of DDT, malathion& deltamethrin resistance in Anopheles culicifacies after their sequential withdrawal from indoor residual spraying in Surat district, India. Indian J Med Res 2010, 132:260-264.
• [5]Tikar SN, Mendki MJ, Sharma AK, Sukumaran D, Veer V, Prakash S, Parashar BD: Resistance status of the malaria vector mosquitoes, Anopheles stephensi and Anopheles subpictus towards adulticides and larvicides in arid and semi-arid areas of India. J Insect Sci 2011, 11:85.
• [6]Antonio-Nkondjio C, Fossog BT, Ndo C, Djantio BM, Togouet SZ, Awono-Ambene P, Costantini C, Wondji CS, Ranson H: Anopheles gambiae distribution and insecticide resistance in the cities of Douala and Yaounde (Cameroon): influence of urban agriculture and pollution. Malaria J 2011, 10:154. BioMed Central Full Text
• [7]Chandre F, Darrier F, Manga L, Akogbeto M, Faye O, Mouchet J, Guillet P: Status of pyrethroid resistance in Anopheles gambiaesensulato. B World Health Organ 1999, 77(3):230-234.
• [8]Ranson H, Abdallah H, Badolo A, Guelbeogo WM, Kerah-Hinzoumbe C, Yangalbe-Kalnone E, Sagnon N, Simard F, Coetzee M: Insecticide resistance in Anopheles gambiae: data from the first year of a multi-country study highlight the extent of the problem. Malaria J 2009, 8:299. BioMed Central Full Text
• [9]Morgan JC, Irving H, Okedi LM, Steven A, Wondji CS: Pyrethroid resistance in an Anopheles funestus population from Uganda. PloS One 2010, 5(7):e11872.
• [10]Perera MD, Hemingway J, Karunaratne SP: Multiple insecticide resistance mechanisms involving metabolic changes and insensitive target sites selected in anopheline vectors of malaria in Sri Lanka. Malaria J 2008, 7:168. BioMed Central Full Text
• [11]WHO: Test procedures for insecticide resistance monitoring in malaria vector mosquitoes. Geneva, Switaerland: World Health Organization; 2013.
• [12]Chen H, Githeko AK, Githure JI, Mutunga J, Zhou G, Yan G: Monooxygenase levels and knockdown resistance (kdr) allele frequencies in Anopheles gambiae and Anopheles arabiensis in Kenya. J Med Entomol 2008, 45(2):242-250.
• [13]Enayati AA, Vatandoost H, Ladonni H, Townson H, Hemingway J: Molecular evidence for a kdr-like pyrethroid resistance mechanism in the malaria vector mosquito Anopheles stephensi. Med Vet Entomol 2003, 17(2):138-144.
• [14]Kim HBJ, Lee W-J, Lee SH: Frequency detection of pyrethroid resistance allele in Anopheles sinensis populations by real-time PCR amplification of specific allele (rtPASA). Pestic Biochem Phys 2007, 87:54-61.
• [15]Ranson H, Jensen B, Vulule JM, Wang X, Hemingway J, Collins FH: Identification of a point mutation in the voltage-gated sodium channel gene of Kenyan Anopheles gambiae associated with resistance to DDT and pyrethroids. Insect MolBiol 2000, 9(5):491-497.
• [16]Singh OP, Dykes CL, Lather M, Agrawal OP, Adak T: Knockdown resistance (kdr)-like mutations in the voltage-gated sodium channel of a malaria vector Anopheles stephensi and PCR assays for their detection. Malaria J 2011, 10:59. BioMed Central Full Text
• [17]Syafruddin D, Hidayati AP, Asih PB, Hawley WA, Sukowati S, Lobo NF: Detection of 1014 F kdr mutation in four major Anophelinemalaria vectors in Indonesia. Malaria J 2010, 9:315. BioMed Central Full Text
• [18]Verhaeghen K, Van Bortel W, Roelants P, Backeljau T, Coosemans M: Detection of the East and West African kdr mutation in Anopheles gambiae and Anopheles arabiensis from Uganda using a new assay based on FRET/Melt Curve analysis. Malaria J 2006, 5:16. BioMed Central Full Text
• [19]Verhaeghen K, Van Bortel W, Trung HD, Sochantha T, Keokenchanh K, Coosemans M: Knockdown resistance in Anopheles vagus, An. sinensis, An. paraliaeandAn. peditaeniatuspopulations of the Mekong region. Parasit Vectors 2010, 3(1):59. BioMed Central Full Text
• [20]Jamroz RC, Guerrero FD, Kammlah DM, Kunz SE: Role of the kdr and super-kdr sodium channel mutations in pyrethroid resistance: correlation of allelic frequency to resistance level in wild and laboratory populations of horn flies (Haematobiairritans). Insect Biochem Molec 1998, 28(12):1031-1037.
• [21]Williamson MS, Martinez-Torres D, Hick CA, Devonshire AL: Identification of mutations in the housefly para-type sodium channel gene associated with knockdown resistance (kdr) to pyrethroid insecticides. Mol Gen Genet 1996, 252(1–2):51-60.
• [22]Cuamba N, Morgan JC, Irving H, Steven A, Wondji CS: High level of pyrethroid resistance in an Anopheles funestus population of the Chokwe District in Mozambique. PloS One 2010, 5(6):e11010.
• [23]Munhenga G, Masendu HT, Brooke BD, Hunt RH, Koekemoer LK: Pyrethroid resistance in the major malaria vector Anopheles arabiensis from Gwave, a malaria-endemic area in Zimbabwe. Malaria J 2008, 7:247. BioMed Central Full Text
• [24]Hunt RH, Brooke BD, Pillay C, Koekemoer LL, Coetzee M: Laboratory selection for and characteristics of pyrethroid resistance in the malaria vector Anopheles funestus. Med Vet Entomol 2005, 19(3):271-275.
• [25]Wang LPJS, Cao WC: The Analysis of Spatio-temporal Character of Malaria Epidemic Situation and Its Determinants. Beijing: Chinese center for disease control and prevention; 2008.
• [26]Cui F, Tan Y, Qiao CL: Filariasis vector in China: insecticide resistance and population structure of mosquito Culex pipiens complex. Pest Manag Sci 2007, 63(5):453-458.
• [27]Finney DJ: Statisical logic in the monitoring of reactions to therapeutic drugs. Meth Inform Med 1971, 10(4):237-245.
• [28]Brengues C, Hawkes NJ, Chandre F, McCarroll L, Duchon S, Guillet P, Manguin S, Morgan JC, Hemingway J: Pyrethroid and DDT cross-resistance in Aedesaegypti is correlated with novel mutations in the voltage-gated sodium channel gene. Med Vet Entomol 2003, 17(1):87-94.
• [29]Penilla RP, Rodriguez AD, Hemingway J, Torres JL, Arredondo-Jimenez JI, Rodriguez MH: Resistance management strategies in malaria vector mosquito control. Baseline data for a large-scale field trial against Anopheles albimanusin Mexico. Med Vet Entomol 1998, 12(3):217-233.
• [30]Joshi D, Park MH, Saeung A, Choochote W, Min GS: Multiplex assay to identify Korean vectors of malaria. Mol Ecol Resour 2010, 10(4):748-750.
• [31]Zhong D, Chang X, Zhou G, He Z, Fu F, Yan Z, Zhu G, Xu T, Bonizzoni M, Wang M, et al.: Relationship between Knockdown Resistance (kdr), Metabolic Detoxification and Organismal Resistance to Pyrethroids in Anopheles sinensis. PloS One 2013, 8(2):e55475.
• [32]China mohotpsro: Action Plan of China Malaria Elimination (2010–2020). Beijing: ministry of health of the people's republic of China; 2010. Available at: http://whothailand.healthrepository.org/bitstream/123456789/1460/1/Action%20Plan%20of%20China%20%20Malaria%20Elimination%20_2010-2020_.pdf webcite. Accessed January 17, 2014.
• [33]Glunt KD, Thomas MB, Read AF: The effects of age, exposure history and malaria infection on the susceptibility of Anopheles mosquitoes to low concentrations of pyrethroid. PloS One 2011, 6(9):e24968.
• [34]Lines JD, Nassor NS: DDT resistance in Anopheles gambiae declines with mosquito age. Med Vet Entomol 1991, 5(3):261-265.
• [35]Spillings BL, Coetzee M, Koekemoer LL, Brooke BD: The effect of a single blood meal on the phenotypic expression of insecticide resistance in the major malaria vector Anopheles funestus. Malaria J 2008, 7:226. BioMed Central Full Text