• View in gallery
    Figure 1.

    The location of the mosquito collection in Hainan Province, China. The black circles in the right map indicate the eight collection sites.

  • View in gallery
    Figure 2.

    The relationship between the mortality of dichlorodiphenyltrichloroethane (DDT) and that of deltamethrin in Anopheles sinensis population. The equation (Y = 0.543x + 14.40) is the linear correlation equation of mortalities of An. sinensis to DDT and deltamethrin. R2 is the square of correlation coefficient.

  • 1.

    Sheng H, Zhou S, Gu Z, Zheng X, 2003. Malaria situation in the People’s Republic of China in 2002. Chin J Parasitol Parasit Dis 21: 193196.

  • 2.

    Sun DW, Wang F, Wang SQ, Hu XM, Wang GZ, Zeng LH, Li SG, Cai HL, Lin SX, Liu Y, 2012. Distribution of anopheline mosquitoes (Diptera: Culicidae) in five cities/counties of Hainan Province. China Trop Med 12: 160162.

    • Search Google Scholar
    • Export Citation
  • 3.

    Bortel VW, Trung HD, Thuanle K, Sochantha T, Socheat D, Sumrandee C, Baimai V, Keokenchanh K, Samlane P, Roelants P, Denis L, Verhaeghen K, Obsomer V, Coosemans M, 2008. The insecticide resistance status of malaria vectors in the Mekong region. Malar J 7: 102.

    • Search Google Scholar
    • Export Citation
  • 4.

    Sun DW, Du JW, Wang GZ, Li YC, He CH, Xue RD, Wang SQ, Hu XM, 2015. A Cost-effectiveness analysis of Plasmodium falciparum malaria elimination in Hainan Province, 2002–2012. Am J Trop Med Hyg 93: 12401248.

    • Search Google Scholar
    • Export Citation
  • 5.

    Cai XZ, 2009. Residual spraying of DDT to be an effectively interventional measure in malaria control. China Trop Med 9: 19571960.

  • 6.

    Cai XZ, 1993. Anti-malaria in Hainan from 1952–1992. Hainan Med 4: 1–3, 6263.

  • 7.

    Dai YH, Huang XD, Cheng P, Liu LJ, Wang HF, Qang HW, Kou JX, 2015. Development of insecticide resistance in malaria vector Anopheles sinensis populations from Shandong Province in China. Malar J 14: 62.

    • Search Google Scholar
    • Export Citation
  • 8.

    Ministry of Health Disease Prevention and Control Bureau, 2007: Handbook for Malaria Control and Prevention. Beijing, China: People’s Hygiene Publishing House Press, 6370.

    • Search Google Scholar
    • Export Citation
  • 9.

    World Health Organization, 2013: Test Procedures for Insecticide Resistance Monitoring in Malaria Vector Mosquitoes. Geneva, Switzerland: World Health Organization.

    • Search Google Scholar
    • Export Citation
  • 10.

    Miller TA, 1988. Mechanisms of resistance to pyrethroid insecticides. Parasitol Today 4: 813.

  • 11.

    Etang J, Manga L, Chandre F, Guillet P, Fondjo E, Mimpfoundi R, Toto JC, Fontenille D, 2003. Insecticide susceptibility status of Anopheles gambiae s.l. (Diptera: Culicidae) in the Republic of Cameroon. J Med Entomol 40: 491497.

    • Search Google Scholar
    • Export Citation
  • 12.

    Etang J, Fondjo E, Chandre F, Eorlais I, Brengues C, Nwane P, Chouaibou M, Ndjemal H, Simard F, 2006. First report of knockdown mutations in the malaria vector Anopheles gambiae from Cameroon. Am J Trop Med Hyg 74: 795797.

    • Search Google Scholar
    • Export Citation
  • 13.

    Nwane P, Etang J, Chouaibou M, Toto JC, Kerah-Hinzoumbé C, Mimpfoundi R, Awono-Ambene HP, Simard F, 2009. Trends in DDT and pyrethroid resistance in Anopheles gambiae s.s. populations from urban and agro-industrial settings in southern Cameroon. BMC Infect Dis 9: 163.

    • Search Google Scholar
    • Export Citation
  • 14.

    Abdalla H, Matambo TS, Koekemoer LL, 2008. Insecticide susceptibility and vector status of natural populations of Anopheles arabiensis from Sudan. Trans R Soc Trop Med Hyg 102: 263271.

    • Search Google Scholar
    • Export Citation
  • 15.

    Wang DQ, Xia ZG, Zhou SS, Zhou XN, Wang RB, Zhang QF, 2013. A potential threat to malaria elimination: extensive deltamethrin and DDT resistance to Anopheles sinensis from the malaria-endemic areas in China. Malar J 12: 164.

    • Search Google Scholar
    • Export Citation
  • 16.

    Perera MDB, Hemingway J, Karunaratne SHPP, 2008. Multiple insecticide resistance mechanisms involving metabolic changes and insensitive target sites selected in anopheline vectors of malaria in Sri Lanka. Malar J 7: 168.

    • Search Google Scholar
    • Export Citation
  • 17.

    Mzilahowa T, Ball AJ, Bass C, Morgan JC, Nyoni B, Steen K, Donnelly MJ, Wilding CS, 2008. Reduced susceptibility to DDT in field populations of Anopheles quadriannulatus and Anopheles arabiensis in Malawi: evidence for larval selection. Med Vet Entomol 22: 258263.

    • Search Google Scholar
    • Export Citation
  • 18.

    Diabate A, Baldet T, Chandre F, Akogbeto M, Guiguemde TR, Darriet F, Brengues C, Guillet P, Hemingway J, Small GJ, Hougard JM, 2002. The role of agricultural use of insecticide in resistance to pyrethroids in Anopheles gambiae s.l. in Burkina Faso. Am J Trop Med Hyg 67: 617622.

    • Search Google Scholar
    • Export Citation
  • 19.

    Hua XM, Shan ZJ, 1996. The production and application of pesticides and factor analysis of their pollution in environment in China. Adv Environ Sci 4: 3345.

    • Search Google Scholar
    • Export Citation
  • 20.

    Hemingway J, Hawkes NJ, McCarroll L, Ranson H, 2004. The molecular basis of insecticide resistance in mosquitoes. Insect Biochem Mol Biol 34: 653665.

    • Search Google Scholar
    • Export Citation
  • 21.

    Qin Q, Li J, Zhong D, Zhou N, Chang X, Li C, Cui L, Yan G, Chen X, 2014. Insecticide resistance of Anopheles sinensis and An. vagus in Hainan Island, a malaria-endemic area of China. Parasit Vectors 7: 92.

    • Search Google Scholar
    • Export Citation
  • 22.

    Zeng LH, Wang SQ, Sun DW, Zhao W, Li SG, Yang X, 2011. Resistance assay of malaria vector to four kinds of common insecticides in some endemic areas of Hainan Province. Chin J Parasitol Parasit Dis 29: 200203.

    • Search Google Scholar
    • Export Citation
  • 23.

    Utzinger J, Tozan Y, Singer BH, 2001. Efficacy and cost-effectiveness of environmental management for malaria control. Trop Med Int Health 6: 677687.

    • Search Google Scholar
    • Export Citation
  • 24.

    Yang W, Xu GJ, Chen HL, Yan JC, Feng SZ, Liu SP, Xu ZZ, 2003. Investigation of impact of the ecologic environmental and social economic factors on malaria in areas with Anopheles anthropophagus as vector in Sichuan. China Trop Med 3: 8688.

    • Search Google Scholar
    • Export Citation
  • 25.

    Ogoma SB, Kannady K, Sikulu M, Chaki PP, Govella NJ, Mukabana WR, Killeen GF, 2009. Window screening, ceilings and closed eaves as sustainable ways to control malaria in Dar es Salaam, Tanzania. Malar J 8: 221.

    • Search Google Scholar
    • Export Citation
  • 26.

    Blanford S, Jenkins NE, Christian R, Chan BHK, Nardini L, Osae M, Koekemoer L, Coetzee M, Read AF, Thomas MB, 2012. Storage and persistence of a candidate fungal biopesticide for use against adult malaria vectors. Malar J 11: 354.

    • Search Google Scholar
    • Export Citation
  • 27.

    Fu MY, Wang Y, Yu SS, Zhong M, Ai GP, Zhao Q, 2014. Killing effect of Bacillus thuringiensis israelensis on larvae of Anopheles stephensi. China Trop Med 14: 10311034.

    • Search Google Scholar
    • Export Citation
  • 28.

    Wilke ABB, Marrelli MT, 2015. Paratransgenesis: a promising new strategy for mosquito vector control. Parasit Vectors 8: 342.

Past two years Past Year Past 30 Days
Abstract Views 0 0 0
Full Text Views 268 106 11
PDF Downloads 85 40 7
 
 
 
 
 
 
 
 
 
 
 
 
 
 

 

 

 

Extensive Resistance of Anopheles sinensis to Insecticides in Malaria-Endemic Areas of Hainan Province, China

Ding-wei SunDepartment of Parasitic Control and Prevention, Hainan Provincial Center for Disease Control and Prevention, Haikou, People’s Republic of China

Search for other papers by Ding-wei Sun in
Current site
Google Scholar
PubMed
Close
,
Guang-ze WangDepartment of Parasitic Control and Prevention, Hainan Provincial Center for Disease Control and Prevention, Haikou, People’s Republic of China

Search for other papers by Guang-ze Wang in
Current site
Google Scholar
PubMed
Close
,
Lin-hai ZengDepartment of Parasitic Control and Prevention, Hainan Provincial Center for Disease Control and Prevention, Haikou, People’s Republic of China

Search for other papers by Lin-hai Zeng in
Current site
Google Scholar
PubMed
Close
,
Shan-gan LiDepartment of Parasitic Control and Prevention, Hainan Provincial Center for Disease Control and Prevention, Haikou, People’s Republic of China

Search for other papers by Shan-gan Li in
Current site
Google Scholar
PubMed
Close
,
Chang-hua HeDepartment of Parasitic Control and Prevention, Hainan Provincial Center for Disease Control and Prevention, Haikou, People’s Republic of China

Search for other papers by Chang-hua He in
Current site
Google Scholar
PubMed
Close
,
Xi-min HuDepartment of Parasitic Control and Prevention, Hainan Provincial Center for Disease Control and Prevention, Haikou, People’s Republic of China

Search for other papers by Xi-min Hu in
Current site
Google Scholar
PubMed
Close
, and
Shan-qing WangDepartment of Parasitic Control and Prevention, Hainan Provincial Center for Disease Control and Prevention, Haikou, People’s Republic of China

Search for other papers by Shan-qing Wang in
Current site
Google Scholar
PubMed
Close

Anopheles sinensis is one of the major malaria vectors and among the dominant species in Hainan Province, China. The resistance of An. sinensis to insecticides is an important threat to malaria control. However, few reports on insecticide resistance of An. sinensis were reported in this area. Eight districts in Hainan Province were selected as the study areas. Insecticide susceptibility bioassays were tested on wild-caught female mosquitoes of An. sinensis to 4% dichlorodiphenyltrichloroethane (DDT), 0.05% deltamethrin, and 5% malathion by using the World Health Organization standard resistance tube assay procedure. All the tested An. sinensis mosquitoes demonstrated resistance to 4% DDT, with less than 72% mortality in the standard assay. The populations from Baisha and Qiongzhong demonstrated possible resistance to 0.05% deltamethrin, with 94–95% mortality, whereas the populations from other districts demonstrated resistance to 0.05% deltamethrin in the standard assay. The populations from Baisha, Qiongzhong, and Dongfang demonstrated susceptibility to 5% malathion, but the populations from other districts demonstrated resistance. These results facilitate the improvement of effective control strategies for malaria vector mosquitoes in Hainan.

INTRODUCTION

Anopheles sinensis, Anopheles fluviatilis, Anopheles candidiensis, Anopheles philippinensis, Anopheles minimus, and Anopheles dirus are the main malaria vectors in Hainan, a tropic island that had the highest morbidity of malaria in China before 2002.1 One of the most widely distributed malaria vectors in this area is An. sinensis.2 Vector control is one of the key measures used to control malaria in endemic areas.3 The use of insecticide-treated bed nets and indoor residual spraying (IRS) were the main methods to control anopheline mosquitoes. Malaria was successfully under control after the implementation of these control strategies. The population of malaria vectors was decreased2 and no locally acquired malaria cases were reported from 2012 to 2014 in Hainan Province.4 In 2010, a plan of action for the elimination of malaria was launched by the Chinese government and the government decided to achieve this goal across China by 2020.

Organochlorines, such as dichlorodiphenyltrichloroethane (DDT), have been widely used for malaria vector control since the 1950s in China.5 In the 1980s, DDT was replaced by more specific and less toxic chemicals, such as pyrethroids.6 With the approval of the World Health Organization (WHO), pyrethroids, such as deltamethrin, have been extensively used for IRS and impregnated bed nets for malaria vector control.7 However, abusive application of chemical insecticides not only leads to environmental pollution, but also to emergence of resistance in malaria vector.

Numbers of reports about the resistance of An. sinensis to insecticides were reported in China, but the information on malaria vector resistance in recent years lacked of comprehensive and systematic standards, especially in the malaria-endemic areas of Hainan Province.

MATERIALS AND METHODS

Study area.

One sentinel site in each of eight cities or counties from different malaria-endemic areas was chosen for this study (Figure 1

Figure 1.
Figure 1.

The location of the mosquito collection in Hainan Province, China. The black circles in the right map indicate the eight collection sites.

Citation: The American Society of Tropical Medicine and Hygiene 97, 1; 10.4269/ajtmh.16-0723

). The selected sites were chosen in highly endemic malaria villages where insecticides were used for malaria vectors, and near the rice fields or small streams, where it is suitable for breeding of An. sinensis.

Sampling collection.

Wild-caught female An. sinensis mosquitoes were used for the bioassays directly. From 2011 to 2014, female mosquitoes were attracted to and fed on cattle in the sentinel sites. All wild-caught female mosquitoes were fed sugar and identified morphologically using taxonomic keys.8 The next day, the identified female mosquitoes of An. sinensis were used for resistance tests.

Resistance tests.

Three insecticides were tested at discriminating concentrations recommended by the WHO: 0.05% deltamethrin, 5% malathion, and 4% DDT. Insecticide-impregnated papers were obtained from the National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention. At least 100 female mosquitoes (4–5 replicates of approximately 25 mosquitoes) were exposed to the insecticide-impregnated paper for 60 minutes. Mortality was recorded 24 hours postexposure. A minimum of 50 mosquitoes (two replicates of approximately 25 mosquitoes) were used as controls, and exposed to papers impregnated with carrier oil only in a single bioassay test. The control mosquitoes were tested at the same time under the same conditions to estimate a base mortality during the test. The observed mortality was corrected using the Abbott formula when control mortality was between 5% and 20%. The bioassay results were categorized in three resistance levels as defined by WHO9: susceptible (mortality between 98% and 100%), possible resistant (mortality between 90% and 98%), and resistant (mortality lower than 90%).

RESULTS

No correction was required as less than 3.92% mortality was observed in control groups.

Wild-caught female An. sinensis mosquitoes in Sanya, Lingshui, Baoting, Dongfang, Ledong, and Haikou demonstrated resistance to 0.05% deltamethrin, with mortality ranging from 17.00% to 68.93%, whereas mosquitoes tested in the other two sites demonstrated possible resistance to deltamethrin, with mortality ranging from 94.12% to 95.00% in the standard assay. The mortality was significantly different among different areas, and the highest percentage of mosquitoes surviving the WHO diagnostic doses was observed in the agricultural districts of Lingshui, whereas the lowest was observed in Qiongzhong.

A higher frequency of resistance was observed with all the tested An. sinensis exposed to 4% DDT, with 24% (in Lingshui) to 72% (in Baisha) mortality in the standard assay.

In the standard assay, An. sinensis populations in Qiongzhong, Dongfang, and Baisha were susceptible when exposed to 5% malathion, with higher than 98.00% mortality, whereas the populations from Sanya, Lingshui, Baoting, Ledong, and Haikou were obviously resistant, with 16.00–73.00% mortality in the standard assay.

Our results showed that An. sinensis mosquitoes in Hainan Province demonstrated resistance or possible resistance to these common insecticides (Table 1

Table 1

Resistance of wild-caught female mosquitoes of Anopheles sinensis to the tested insecticides in Hainan Province

City/countyDeltamethrin (0.05% w/v)*
DDT (4% w/v)*
Malathion (5% w/v)*
Total(%) MortalityResistance statusControl
Total(%) MortalityResistance statusControl
Total(%) MortalityResistance statusControl
Total(%) MortalityTotal(%) MortalityTotal(%) Mortality
Sanya10125.74R50010027.00R51010016.00R520
Lingshui10017.00R511.9610024.00R50210041.00R500
Qiongzhong10095.00M50010560.95R500121100.00S513.92
Baoting10368.93R523.8510053.00R521.9210073.00R511.96
Dongfang10049.00R502.0010031.00R50010199.01S500
Baisha10294.12M502.0010072.00R51010399.03S500
Ledong10038.00R513.9210041.00R531.8910056.00R521.92
Haikou10035.00R50010036.00R502.0010039.00R510

DDT = dichlorodiphenyltrichloroethane.

World Health Organization diagnostic concentration.

S = susceptible; M = possible resistant; R = resistant.

), especially to DDT.

DISCUSSION

The results from this study show that field populations of An. sinensis females from Hainan Province developed high resistance to the tested insecticides, especially to DDT. The resistance to DDT is extremely prevalent, as less than 72% mortality was observed in the standard assay, and in some cases up to 76% of the mosquitoes survived at the diagnostic dose. Obviously the resistance to DDT still exists in An. sinensis populations, although they have not been treated with DDT for more than 30 years in Hainan.

Pyrethroid insecticides are neurotoxins and share many characteristics with DDT, they both target insect sodium channels, have a negative temperature coefficient, and have a rapid knockdown effect followed by a lethal effect.10 Also, resistance to one is likely to create cross-resistance to the other. In our study, we observed an obvious correlation between deltamethrin and DDT in mortality rates of An. sinensis (Figure 2

Figure 2.
Figure 2.

The relationship between the mortality of dichlorodiphenyltrichloroethane (DDT) and that of deltamethrin in Anopheles sinensis population. The equation (Y = 0.543x + 14.40) is the linear correlation equation of mortalities of An. sinensis to DDT and deltamethrin. R2 is the square of correlation coefficient.

Citation: The American Society of Tropical Medicine and Hygiene 97, 1; 10.4269/ajtmh.16-0723

). The higher mortality to deltamethrin with a higher mortality to DDT indicated a positive correlation between the levels of resistance to both insecticides in the tested population. Similar results were also reported on Anopheles gambiae populations from Cameroon,1113 Anopheles arabiensis populations from Sudan,14 and An. sinensis populations from other provinces in China.15 The mode of action of malathion to mosquitoes is different from DDT and deltamethrin, as it is an inhibitor of acetylcholinesterase activity.16 No correlation was observed between malathion and DDT/deltamethrin in this study.

Anopheles sinensis prefers large bodies of water, such as rice fields. As a consequence, insecticides used in agriculture will put a selective pressure on the larvae of An. sinensis.17 Reports from Diabate and others18 showed that the resistance of An. gambiae to insecticides was related to the use of insecticides in agronomy. No information on pesticide use at the household or communal level was collected in our study. However, about 8.3 × 107 kg of pyrethroids insecticide per year has been used in China since 1997.19 Extensive abuse of pyrethroids in agriculture and public health probably lead to the extensive resistance in An. sinensis.

Reduced target site sensitivity and increased metabolic detoxification are two proven insecticide resistance mechanisms in mosquitoes. Mutations in the para-type sodium channel gene can decrease the affinity of these insecticides to insect sodium channels and cause target site resistance to DDT and deltamethrin.20 Target resistance to malathion was different from DDT and deltamethrin because it was a mutation of the acetylcholinesterase (ace-1) gene.16 Metabolic resistance to insecticides is caused by the increased activity of detoxification enzymes, including cytochrome P450 monooxygenases (P450s), glutathione S-transferases, and carboxylesterases.16 A report from Qin and others21 showed that target-site insensitivity and metabolic resistance both play important roles in insecticide resistance in An. sinensis in Hainan Island.

Historically, DDT was widely used for IRS to control malaria vector in Hainan Province since the 1950s. Since the 1980s, pyrethroid insecticides, such as deltamethrin and cyfluthrin, have been widely used for insecticide-treated nets or long-lasting insecticide-treated nets for malaria vector control.22 Resistance to deltamethrin in our study was related to the long-term use of these insecticides. Although DDT had not been used for malaria vector control for many years, vector resistance to DDT still exists. Maybe DDT and pyrethroid insecticides have similar mechanisms of action in malaria vectors, which could explain the observed cross-resistance between DDT and pyrethroid insecticides in our study. The larvae of An. sinensis prefer to develop in large bodies of water, such as rice fields. Organophosphorus insecticides, such as malathion, are not the main insecticides used for malaria vector control in Hainan Province, but they are widely used for rice pest control. Selective pressure from pesticide exposure will inevitably result in resistance to malathion in the larvae of An. sinensis.

Resistance of malaria vector to insecticides is a common threat to public health all over the world, especially resistance to pyrethroids. For this reason, the choice of insecticides to control mosquitoes is limited. Fortunately, chemicals are not the only choice. Integrated vector management is a sustainable way to control malaria vectors. Effective and economical interventions should be used for mosquito control, such as environmental manipulation or management,23,24 house modification,25 biopesticides,26,27 and paratransgenesis.28

In our study, we detected that different levels of insecticide resistance in An. sinensis populations in Hainan Province demonstrated possible resistance or resistance to deltamethrin, resistance to DDT, and sensitivity or resistance to malathion. For effective and economical use of insecticides in malaria vector control, it is necessary to set up networks to systematically and continuously monitor the resistance levels of malaria vectors to insecticides. More research should be done to clarify the resistance mechanisms and screen more effective insecticides.

Acknowledgments:

We would like to thank Sanya CDC, Lingshui CDC, Qiongzhong CDC, Baoting CDC, Dongfang CDC, Baisha CDC, Ledong CDC, and Haikou CDC for their excellent cooperation. We also thank Daniel Dixon who edited the manuscript.

REFERENCES

  • 1.

    Sheng H, Zhou S, Gu Z, Zheng X, 2003. Malaria situation in the People’s Republic of China in 2002. Chin J Parasitol Parasit Dis 21: 193196.

  • 2.

    Sun DW, Wang F, Wang SQ, Hu XM, Wang GZ, Zeng LH, Li SG, Cai HL, Lin SX, Liu Y, 2012. Distribution of anopheline mosquitoes (Diptera: Culicidae) in five cities/counties of Hainan Province. China Trop Med 12: 160162.

    • Search Google Scholar
    • Export Citation
  • 3.

    Bortel VW, Trung HD, Thuanle K, Sochantha T, Socheat D, Sumrandee C, Baimai V, Keokenchanh K, Samlane P, Roelants P, Denis L, Verhaeghen K, Obsomer V, Coosemans M, 2008. The insecticide resistance status of malaria vectors in the Mekong region. Malar J 7: 102.

    • Search Google Scholar
    • Export Citation
  • 4.

    Sun DW, Du JW, Wang GZ, Li YC, He CH, Xue RD, Wang SQ, Hu XM, 2015. A Cost-effectiveness analysis of Plasmodium falciparum malaria elimination in Hainan Province, 2002–2012. Am J Trop Med Hyg 93: 12401248.

    • Search Google Scholar
    • Export Citation
  • 5.

    Cai XZ, 2009. Residual spraying of DDT to be an effectively interventional measure in malaria control. China Trop Med 9: 19571960.

  • 6.

    Cai XZ, 1993. Anti-malaria in Hainan from 1952–1992. Hainan Med 4: 1–3, 6263.

  • 7.

    Dai YH, Huang XD, Cheng P, Liu LJ, Wang HF, Qang HW, Kou JX, 2015. Development of insecticide resistance in malaria vector Anopheles sinensis populations from Shandong Province in China. Malar J 14: 62.

    • Search Google Scholar
    • Export Citation
  • 8.

    Ministry of Health Disease Prevention and Control Bureau, 2007: Handbook for Malaria Control and Prevention. Beijing, China: People’s Hygiene Publishing House Press, 6370.

    • Search Google Scholar
    • Export Citation
  • 9.

    World Health Organization, 2013: Test Procedures for Insecticide Resistance Monitoring in Malaria Vector Mosquitoes. Geneva, Switzerland: World Health Organization.

    • Search Google Scholar
    • Export Citation
  • 10.

    Miller TA, 1988. Mechanisms of resistance to pyrethroid insecticides. Parasitol Today 4: 813.

  • 11.

    Etang J, Manga L, Chandre F, Guillet P, Fondjo E, Mimpfoundi R, Toto JC, Fontenille D, 2003. Insecticide susceptibility status of Anopheles gambiae s.l. (Diptera: Culicidae) in the Republic of Cameroon. J Med Entomol 40: 491497.

    • Search Google Scholar
    • Export Citation
  • 12.

    Etang J, Fondjo E, Chandre F, Eorlais I, Brengues C, Nwane P, Chouaibou M, Ndjemal H, Simard F, 2006. First report of knockdown mutations in the malaria vector Anopheles gambiae from Cameroon. Am J Trop Med Hyg 74: 795797.

    • Search Google Scholar
    • Export Citation
  • 13.

    Nwane P, Etang J, Chouaibou M, Toto JC, Kerah-Hinzoumbé C, Mimpfoundi R, Awono-Ambene HP, Simard F, 2009. Trends in DDT and pyrethroid resistance in Anopheles gambiae s.s. populations from urban and agro-industrial settings in southern Cameroon. BMC Infect Dis 9: 163.

    • Search Google Scholar
    • Export Citation
  • 14.

    Abdalla H, Matambo TS, Koekemoer LL, 2008. Insecticide susceptibility and vector status of natural populations of Anopheles arabiensis from Sudan. Trans R Soc Trop Med Hyg 102: 263271.

    • Search Google Scholar
    • Export Citation
  • 15.

    Wang DQ, Xia ZG, Zhou SS, Zhou XN, Wang RB, Zhang QF, 2013. A potential threat to malaria elimination: extensive deltamethrin and DDT resistance to Anopheles sinensis from the malaria-endemic areas in China. Malar J 12: 164.

    • Search Google Scholar
    • Export Citation
  • 16.

    Perera MDB, Hemingway J, Karunaratne SHPP, 2008. Multiple insecticide resistance mechanisms involving metabolic changes and insensitive target sites selected in anopheline vectors of malaria in Sri Lanka. Malar J 7: 168.

    • Search Google Scholar
    • Export Citation
  • 17.

    Mzilahowa T, Ball AJ, Bass C, Morgan JC, Nyoni B, Steen K, Donnelly MJ, Wilding CS, 2008. Reduced susceptibility to DDT in field populations of Anopheles quadriannulatus and Anopheles arabiensis in Malawi: evidence for larval selection. Med Vet Entomol 22: 258263.

    • Search Google Scholar
    • Export Citation
  • 18.

    Diabate A, Baldet T, Chandre F, Akogbeto M, Guiguemde TR, Darriet F, Brengues C, Guillet P, Hemingway J, Small GJ, Hougard JM, 2002. The role of agricultural use of insecticide in resistance to pyrethroids in Anopheles gambiae s.l. in Burkina Faso. Am J Trop Med Hyg 67: 617622.

    • Search Google Scholar
    • Export Citation
  • 19.

    Hua XM, Shan ZJ, 1996. The production and application of pesticides and factor analysis of their pollution in environment in China. Adv Environ Sci 4: 3345.

    • Search Google Scholar
    • Export Citation
  • 20.

    Hemingway J, Hawkes NJ, McCarroll L, Ranson H, 2004. The molecular basis of insecticide resistance in mosquitoes. Insect Biochem Mol Biol 34: 653665.

    • Search Google Scholar
    • Export Citation
  • 21.

    Qin Q, Li J, Zhong D, Zhou N, Chang X, Li C, Cui L, Yan G, Chen X, 2014. Insecticide resistance of Anopheles sinensis and An. vagus in Hainan Island, a malaria-endemic area of China. Parasit Vectors 7: 92.

    • Search Google Scholar
    • Export Citation
  • 22.

    Zeng LH, Wang SQ, Sun DW, Zhao W, Li SG, Yang X, 2011. Resistance assay of malaria vector to four kinds of common insecticides in some endemic areas of Hainan Province. Chin J Parasitol Parasit Dis 29: 200203.

    • Search Google Scholar
    • Export Citation
  • 23.

    Utzinger J, Tozan Y, Singer BH, 2001. Efficacy and cost-effectiveness of environmental management for malaria control. Trop Med Int Health 6: 677687.

    • Search Google Scholar
    • Export Citation
  • 24.

    Yang W, Xu GJ, Chen HL, Yan JC, Feng SZ, Liu SP, Xu ZZ, 2003. Investigation of impact of the ecologic environmental and social economic factors on malaria in areas with Anopheles anthropophagus as vector in Sichuan. China Trop Med 3: 8688.

    • Search Google Scholar
    • Export Citation
  • 25.

    Ogoma SB, Kannady K, Sikulu M, Chaki PP, Govella NJ, Mukabana WR, Killeen GF, 2009. Window screening, ceilings and closed eaves as sustainable ways to control malaria in Dar es Salaam, Tanzania. Malar J 8: 221.

    • Search Google Scholar
    • Export Citation
  • 26.

    Blanford S, Jenkins NE, Christian R, Chan BHK, Nardini L, Osae M, Koekemoer L, Coetzee M, Read AF, Thomas MB, 2012. Storage and persistence of a candidate fungal biopesticide for use against adult malaria vectors. Malar J 11: 354.

    • Search Google Scholar
    • Export Citation
  • 27.

    Fu MY, Wang Y, Yu SS, Zhong M, Ai GP, Zhao Q, 2014. Killing effect of Bacillus thuringiensis israelensis on larvae of Anopheles stephensi. China Trop Med 14: 10311034.

    • Search Google Scholar
    • Export Citation
  • 28.

    Wilke ABB, Marrelli MT, 2015. Paratransgenesis: a promising new strategy for mosquito vector control. Parasit Vectors 8: 342.

Author Notes

Address correspondence to Xi-min Hu or Shan-qing Wang, Department of Parasitic Control and Prevention, Hainan Provincial Center for Disease Control and Prevention, Haifu Road 44, Haikou, Hainan Province 570203, People’s Republic of China. E-mails: hxm.168@163.com or wangsqkevin@hotmail.com
These authors contributed equally to this work.

Financial support: This work has been supported by National Natural Science Funds of China 81460520, and Provincial Natural Science Funds of Hainan 813251, 309074.

Authors’ addresses: Ding-wei Sun, Guang-ze Wang, Lin-hai Zeng, Shan-gan Li, Chang-hua He, Xi-min Hu, and Shan-qing Wang, Department of Parasitic Control and Prevention, Hainan Provincial Center for Disease Control and Prevention, Haikou, People’s Republic of China, E-mails: sdw_bmjc@163.com, wangguangze63@126.com, hnzlh09@163.com, lishgan@163.com, hechanghua2006@126.com, hxm.168@163.com, and wangsqkevin@hotmail.com.

Save