Absence of Close-Range Excitorepellent Effects in Malaria Mosquitoes Exposed to Deltamethrin-Treated Bed Nets

Jeroen Spitzen Laboratory of Entomology, Wageningen University, Wageningen, The Netherlands; Vestergaard Frandsen SA, Lausanne, Switzerland

Search for other papers by Jeroen Spitzen in
Current site
Google Scholar
PubMed
Close
,
Camille Ponzio Laboratory of Entomology, Wageningen University, Wageningen, The Netherlands; Vestergaard Frandsen SA, Lausanne, Switzerland

Search for other papers by Camille Ponzio in
Current site
Google Scholar
PubMed
Close
,
Constantianus J. M. Koenraadt Laboratory of Entomology, Wageningen University, Wageningen, The Netherlands; Vestergaard Frandsen SA, Lausanne, Switzerland

Search for other papers by Constantianus J. M. Koenraadt in
Current site
Google Scholar
PubMed
Close
,
Helen V. Pates Jamet Laboratory of Entomology, Wageningen University, Wageningen, The Netherlands; Vestergaard Frandsen SA, Lausanne, Switzerland

Search for other papers by Helen V. Pates Jamet in
Current site
Google Scholar
PubMed
Close
, and
Willem Takken Laboratory of Entomology, Wageningen University, Wageningen, The Netherlands; Vestergaard Frandsen SA, Lausanne, Switzerland

Search for other papers by Willem Takken in
Current site
Google Scholar
PubMed
Close
Restricted access

Flight behavior of insecticide-resistant and susceptible malaria mosquitoes approaching deltamethrin-treated nets was examined using a wind tunnel. Behavior was linked to resulting health status (dead or alive) using comparisons between outcomes from free-flight assays and standard World Health Organization (WHO) bioassays. There was no difference in response time, latency time to reach the net, or spatial distribution in the wind tunnel between treatments. Unaffected resistant mosquitoes spent less time close to (< 30 cm) treated nets. Nettings that caused high knockdown or mortality in standard WHO assays evoked significantly less mortality in the wind tunnel; there was no excitorepellent effect in mosquitoes making contact with the nettings in free flight. This study shows a new approach to understanding mosquito behavior near insecticidal nets. The methodology links free-flight behavior to mosquito health status on exposure to nets. The results suggest that behavioral assays can provide important insights for evaluation of insecticidal effects on disease vectors.

Author Notes

* Address correspondence to Willem Takken, Laboratory of Entomology, Wageningen University, PO Box 8031, 6700 EH Wageningen, The Netherlands. E-mail: willem.takken@wur.nl

Financial support: This study received financial support from Vestergaard Frandsen SA and Wageningen University and Research Centre.

Authors' addresses: Jeroen Spitzen, Camille Ponzio, Constantianus J. M. Koenraadt, and Willem Takken, Laboratory of Entomology, Wageningen University, Wageningen, The Netherlands, E-mails: jeroen.spitzen@wur.nl, camillie.ponzio@wur.nl, sander.koenraadt@wur.nl, and willem.takken@wur.nl. Helen V. Pates Jamet, Vestergaard Frandsen SA, Lausanne, Switzerland, E-mail: hpj@vestergaard.com.

  • 1.

    Steketee RW, Campbell CC, 2010. Impact of national malaria control scale-up programmes in Africa: magnitude and attribution of effects. Malar J 9: 299.

    • Search Google Scholar
    • Export Citation
  • 2.

    Lim SS, Fullman N, Stokes A, Ravishankar N, Masiye F, Murray CJL, Gakidou E, 2011. Net benefits: a multicountry analysis of observational data examining associations between insecticide-treated mosquito nets and health outcomes. PLoS Med 8: e1001091.

    • Search Google Scholar
    • Export Citation
  • 3.

    Lengeler C, 2004. Insecticide-treated bed nets and curtains for preventing malaria. Cochrane Database Syst Rev 2: CD000363.

  • 4.

    Lengeler C, 2004. Insecticide-treated nets for malaria control: real gains. Bull World Health Organ 82: 84.

  • 5.

    Phillips-Howard PA, ter Kuile FO, Nahlen BL, Alaii JA, Gimnig JE, Kolczak MS, Terlouw DJ, Kariuki SK, Shi YP, Kachur SP, Hightower AW, Vulule JM, Hawley WA, 2003. The efficacy of permethrin-treated bed nets on child mortality and morbidity in western Kenya. II. Study design and methods. Am J Trop Med Hyg 68: 1015.

    • Search Google Scholar
    • Export Citation
  • 6.

    Binka FN, Kubale A, Adjuik M, Williams LA, Lengeler C, Maude GH, Armah GE, Kajihara B, Adiamah JH, Smith PG, 1996. Impact of permethrin impregnated bednets on child mortality in Kassena-Nankana district, Ghana: a randomized controlled trial. Trop Med Int Health 1: 147154.

    • Search Google Scholar
    • Export Citation
  • 7.

    Kongmee M, Boonyuan W, Achee NL, Prabaripai A, Lerdthusnee K, Chareonviriyaphap T, 2012. Irritant and repellent responses of Anopheles harrisoni and Anopheles minimus upon exposure to bifenthrin or deltamethrin using an excito-repellency system and a live host. J Am Mosq Control Assoc 28: 2029.

    • Search Google Scholar
    • Export Citation
  • 8.

    Singh K, Rahman SJ, Joshi GC, 1989. Village scale trial of deltamethrin against mosquitoes. J Commun Dis 21: 339353.

  • 9.

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

    • Search Google Scholar
    • Export Citation
  • 10.

    Curtis CF, 1991. Control of Disease Vectors in the Community. London, UK: Wolfe Publishing Ltd., 233.

  • 11.

    Mosha FW, Lyimo IN, Oxborough RM, Matowo J, Malima R, Feston E, Mndeme R, Tenu F, Kulkarni M, Maxwell CA, Magesa SM, Rowland MW, 2008. Comparative efficacies of permethrin-, deltamethrin- and alpha-cypermethrin-treated nets, against Anopheles arabiensis and Culex quinquefasciatus in northern Tanzania. Ann Trop Med Parasitol 102: 367376.

    • Search Google Scholar
    • Export Citation
  • 12.

    Darriet F, Robert V, Tho Vien N, Carnevale P, 1984. Evaluation of the Efficacy of Permethrin-Impregnated Intact and Perforated Mosquito Nets against Vectors of Malaria. WHO Bulletin WHO/VBC 84. Geneva: World Health Organization.

    • Search Google Scholar
    • Export Citation
  • 13.

    Lindsay SW, Adiamah JH, Miller JE, Armstrong JR, 1991. Pyrethroid-treated bednet effects on mosquitoes of the Anopheles gambiae complex in The Gambia. Med Vet Entomol 5: 477483.

    • Search Google Scholar
    • Export Citation
  • 14.

    Koudou BG, Koffi AA, Malone D, Hemingway J, 2011. Efficacy of PermaNet® 2.0 and PermaNet® 3.0 against insecticide-resistant Anopheles gambiae in experimental huts in Côte d'Ivoire. Malar J 10: 172.

    • Search Google Scholar
    • Export Citation
  • 15.

    Miller JE, Lindsay SW, Armstrong JR, 1991. Experimental hut trials of bednets impregnated with synthetic pyrethroid or organophosphate insecticide for mosquito control in The Gambia. Med Vet Entomol 5: 465476.

    • Search Google Scholar
    • Export Citation
  • 16.

    Mathenge EM, Gimnig JE, Kolczak M, Ombok M, Irungu LW, Hawley WA, 2001. Effect of permethrin-impregnated nets on exiting behavior, blood feeding success, and time of feeding of malaria mosquitoes (Diptera: Culicidae) in western Kenya. J Med Entomol 38: 531536.

    • Search Google Scholar
    • Export Citation
  • 17.

    Killeen GF, Smith TA, 2007. Exploring the contributions of bed nets, cattle, insecticides, and excitorepellency to malaria control: a deterministic model of mosquito host-seeking behaviour and mortality. Trans R Soc Trop Med Hyg 101: 867880.

    • Search Google Scholar
    • Export Citation
  • 18.

    Cooperband MF, Allan SA, 2009. Effects of different pyrethroids on landing behavior of female Aedes aegypti, Anopheles quadrimaculatus, and Culex quinquefasciatus mosquitoes (Diptera: Culicidae). J Med Entomol 46: 292306.

    • Search Google Scholar
    • Export Citation
  • 19.

    Roberts DR, Alecrim WD, Hshieh P, Grieco JP, Bangs M, Andre RG, Chareonviriphap T, 2000. A probability model of vector behavior: effects of DDT repellency, irritancy, and toxicity in malaria control. J Vector Ecol 25: 4861.

    • Search Google Scholar
    • Export Citation
  • 20.

    Achee NL, Sardelis MR, Dusfour I, Chauhan KR, Grieco JP, 2009. Characterization of spatial repellent, contact irritant, and toxicant chemical actions of standard vector control compounds. J Am Mosq Control Assoc 25: 156167.

    • Search Google Scholar
    • Export Citation
  • 21.

    White GB, 2006. Terminology of insect repellents. Debboun MF, Strickman D, eds. Insect Repellents: Principles, Methods and Uses. Boca Raton, FL: CRC Press, 3146.

    • Search Google Scholar
    • Export Citation
  • 22.

    Itoh T, Shinjo G, Kurihara T, 1986. Studies on wide mesh netting impregnated with insecticides against Culex mosquitos. J Am Mosq Control Assoc 2: 503506.

    • Search Google Scholar
    • Export Citation
  • 23.

    Bogh C, Pedersen EM, Mukoko DA, Ouma JH, 1998. Permethrin-impregnated bednet effects on resting and feeding behaviour of lymphatic filariasis vector mosquitoes in Kenya. Med Vet Entomol 12: 5259.

    • Search Google Scholar
    • Export Citation
  • 24.

    Grieco JP, Achee NL, Andre RG, Roberts DR, 2000. A comparison study of house entering and exiting behavior of Anopheles vestitipennis (Diptera: Culicidae) using experimental huts sprayed with DDT or Deltamethrin in the Southern District of Toledo, Belize, C. A. J Vector Ecol 25: 6273.

    • Search Google Scholar
    • Export Citation
  • 25.

    Okumu FO, Moore J, Mbeyela E, Sherlock M, Sangusangu R, Ligamba G, Russell T, Moore SJ, 2012. A modified experimental hut design for studying responses of disease-transmitting mosquitoes to indoor interventions: the Ifakara experimental huts. PLoS ONE 7: e30967.

    • Search Google Scholar
    • Export Citation
  • 26.

    WHO, 2005. Guidelines for Laboratory and Field Testing of Long-Lasting Insecticidal Mosquito Nets. Geneva: World Health Organization, 18.

    • Search Google Scholar
    • Export Citation
  • 27.

    Mboera LEG, Takken W, 1999. Odour-mediated host preference of Culex quinquefasciatus in Tanzania. Entomol Exp Appl 92: 8388.

  • 28.

    Smallegange RC, Knols BGJ, Takken W, 2010. Effectiveness of synthetic versus natural human volatiles as attractants for Anopheles gambiae (Diptera: Culicidae) sensu stricto. J Med Entomol 47: 338344.

    • Search Google Scholar
    • Export Citation
  • 29.

    Spitzen JS, Smallegange CR, Takken W, 2008. Effect of human odours and positioning of CO2 release point on trap catches of the malaria mosquito Anopheles gambiae s.s. in an olfactometer. Physiol Entomol 33: 116122.

    • Search Google Scholar
    • Export Citation
  • 30.

    WHO, 2006. Guidelines for Testing Mosquito Adulticides for Indoor Residual Spraying and Treatment of Mosquito Nets. Geneva: World Health Organization, 70.

    • Search Google Scholar
    • Export Citation
  • 31.

    Carnevale P, Bitsindou P, Diomande L, Robert V, 1992. Insecticide impregnation can restore the efficiency of torn bed nets and reduce man-vector contact in malaria endemic areas. Trans R Soc Trop Med Hyg 86: 362364.

    • Search Google Scholar
    • Export Citation
  • 32.

    Darriet F, Chandre F, 2011. Combining piperonyl butoxide and dinotefuran restores the efficacy of deltamethrin mosquito nets against resistant Anopheles gambiae (Diptera: Culicidae). J Med Entomol 48: 952955.

    • Search Google Scholar
    • Export Citation
  • 33.

    N'Guessan R, Asidi A, Boko P, Odjo A, Akogbeto M, Pigeon O, Rowland M, 2010. An experimental hut evaluation of PermaNet® 3.0, a deltamethrin-piperonyl butoxide combination net, against pyrethroid-resistant Anopheles gambiae and Culex quinquefasciatus mosquitoes in southern Benin. Trans R Soc Trop Med Hyg 104: 758765.

    • Search Google Scholar
    • Export Citation
  • 34.

    Hougard JM, Corbel V, N'Guessan R, Darriet F, Chandre F, Akogbeto M, Baldet T, Guillet P, Carnevale P, Traore-Lamizana M, 2003. Efficacy of mosquito nets treated with insecticide mixtures or mosaics against insecticide resistant Anopheles gambiae and Culex quinquefasciatus (Diptera: Culicidae) in Cote d'Ivoire. Bull Entomol Res 93: 491498.

    • Search Google Scholar
    • Export Citation
  • 35.

    Lines JD, Myamba J, Curtis CF, 1987. Experimental hut trials of permethrin-impregnated mosquito nets and eave curtains against malaria vectors in Tanzania. Med Vet Entomol 1: 3751.

    • Search Google Scholar
    • Export Citation
  • 36.

    Malima RC, Oxborough RM, Tungu PK, Maxwell C, Lyimo I, Mwingira V, Mosha FW, Matowo J, Magesa SM, Rowland MW, 2009. Behavioural and insecticidal effects of organophosphate-, carbamate- and pyrethroid-treated mosquito nets against African malaria vectors. Med Vet Entomol 23: 317325.

    • Search Google Scholar
    • Export Citation
  • 37.

    Takken W, Knols BGJ, 1999. Odor-mediated behavior of afrotropical malaria mosquitoes. Annu Rev Entomol 44: 131157.

  • 38.

    Corbel V, Chabi J, Dabire RK, Etang J, Nwane P, Pigeon O, Akogbeto M, Hougard JM, 2010. Field efficacy of a new mosaic long-lasting mosquito net (PermaNet (R) 3.0) against pyrethroid-resistant malaria vectors: a multi centre study in Western and Central Africa. Malar J 9: 113.

    • Search Google Scholar
    • Export Citation
  • 39.

    Fane M, Cisse O, Traore CSF, Sabatier P, 2012. Anopheles gambiae resistance to pyrethroid-treated nets in cotton versus rice areas in Mali. Acta Trop 122: 16.

    • Search Google Scholar
    • Export Citation
  • 40.

    Magesa SM, Wilkes TJ, Mnzava AE, Njunwa KJ, Myamba J, Kivuyo MD, Hill N, Lines JD, Curtis CF, 1991. Trial of pyrethroid impregnated bednets in an area of Tanzania holoendemic for malaria. Part 2. Effects on the malaria vector population. Acta Trop 49: 97108.

    • Search Google Scholar
    • Export Citation
  • 41.

    Schreck CE, Kline DL, 1983. Area protection by use of repellent-treated netting against culicoides biting midges. Mosq News 43: 338342.

  • 42.

    Ruigt GSF, 1985. Pyrethroids. Kerkut GA, Gilbert LI, eds. Comprehensive Insect Physiology Biochemistry and Pharmacology, Vol 12. Oxford, UK: Pergamon, 183262.

    • Search Google Scholar
    • Export Citation
  • 43.

    Sawicki R, 1962. Insecticidal activity of pyrethrum extract and its four insecticidal constituents against house flies. III. Knock-down and recovery of flies treated with pyrethrum extract with and without piperonyl butoxide. J Sci Food Agric 13: 283292.

    • Search Google Scholar
    • Export Citation
  • 44.

    Alzogaray RA, Zerba EN, 1997. Incoordination, paralysis and recovery after pyrethroid treatment on nymphs III of Triatoma infestans (Hemiptera: Reduviidae). Mem Inst Oswaldo Cruz 92: 431435.

    • Search Google Scholar
    • Export Citation
  • 45.

    Bernard CB, Philogene BJR, 1993. Insecticide synergists: role, importance, and perspectives. J Toxicol Environ Health 38: 199223.

  • 46.

    Moores G, Bingham G, Gunning R, 2005. Use of 'temporal synergism' to overcome insecticide resistance. Outlook Pest Manag 16: 79.

  • 47.

    Ahmad M, Denholm I, Bromilow RH, 2006. Delayed cuticular penetration and enhanced metabolism of deltamethrin in pyrethroid-resistant strains of Helicoverpa armigera from China and Pakistan. Pest Manag Sci 62: 805810.

    • Search Google Scholar
    • Export Citation
  • 48.

    Young SJ, Gunning RV, Moores GD, 2006. Effect of pretreatment with piperonyl butoxide on pyrethroid efficacy against insecticide-resistant Helicoverpa armigera (Lepidoptera: Noctuidae) and Bemisia tabaci (Sternorrhyncha: Aleyrodidae). Pest Manag Sci 62: 114119.

    • Search Google Scholar
    • Export Citation
  • 49.

    Bingham G, Strode C, Tran L, Khoa PT, Jamet HP, 2011. Can piperonyl butoxide enhance the efficacy of pyrethroids against pyrethroid-resistant Aedes aegypti? Trop Med Int Health 16: 492500.

    • Search Google Scholar
    • Export Citation
  • 50.

    Spitzen J, Spoor CW, Grieco F, ter Braak C, Beeuwkes J, van Brugge SP, Kranenbarg S, Noldus LP, van Leeuwen JL, Takken W, 2013. A 3D analysis of flight behavior of Anopheles gambiae sensu stricto malaria mosquitoes in response to human odor and heat. PLoS ONE 8: e62995.

    • Search Google Scholar
    • Export Citation
  • 51.

    Achee NL, Bangs MJ, Farlow R, Killeen GF, Lindsay S, Logan JG, Moore SJ, Rowland M, Sweeney K, Torr SJ, Zwiebel L, Grieco JP, 2012. Spatial repellents: from discovery and development to evidence-based validation. Malar J 11: 164.

    • Search Google Scholar
    • Export Citation
Past two years Past Year Past 30 Days
Abstract Views 10 10 5
Full Text Views 420 111 1
PDF Downloads 113 17 1
 
Membership Banner
 
 
 
Affiliate Membership Banner
 
 
Research for Health Information Banner
 
 
CLOCKSS
 
 
 
Society Publishers Coalition Banner
Save