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Synergistic insecticidal and repellent effects of combined pyrethroid and repellent-impregnated bed nets using a novel long-lasting polymer-coating multi-layer technique

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Abstract

New and improved strategies for malaria control and prevention are urgently needed. As a contribution to an optimized personal protection strategy, a novel long-lasting insecticide and repellent-treated net (LLIRN) has been designed by binding combinations of permethrin plus N,N-diethyl-m-toluamide (DEET), or insect repellent 3535 (IR3535), and etofenprox plus DEET, onto fibres of bed net fabric employing a new multi-layer polymer-coating technique. Protective repellent efficacy, toxicological effectiveness and residual activity of 12 LLIRN types have been evaluated by laboratory testing against adult Aedes aegypti. The novel multi-layer LLIRN design allowed simultaneous embedding at concentrations up to 5,930 mg/m2 for DEET, 3,408 mg/m2 for IR3535, 2,296 mg/m2 for permethrin and 2,349 mg/m2 for etofenprox, respectively. IR3535 layers prevented co-binding of additional pyrethroid-containing polymer layers, thus making pyrethroids plus DEET LLIRNs an ideal combination. All LLIRNs revealed synergistic insecticidal effects which, when measured against concentration controls of the isolated compounds, were significant in all LLIRN types designed. DEET in DEET plus permethrin LLIRNs significantly (p < 0.0001) reduced the concentration-dependent permethrin 100 % knockdown (KD) time from 55 to 75 %, the corresponding 100 % kill time (p < 0.0001) from 55 to 64 %. DEET in DEET plus etofenprox LLIRNs reduced the dose-specific 100 % knockdown (KD) time of etofenprox from 42 to 50 % (p = 0.004), the 100 % kill time from 25 to 38 % (p < 0.0001). Permethrin or etofenprox did not influence spatial repellency of DEET or IR3535 on LLIRNs. Vice versa, DEET and IR3535 increased spatial and excitatory repellency and reduced landing and probing frequency on LLIRNs resulting in strongly enhanced biting protection, even at low concentrations. One hundred percent biting and probing protection of stored LLIRNs was preserved for 83 weeks with the 5,930 mg/m2 DEET and 2,139 mg/m2 etofenprox LLIRN, for 72 weeks with the 5,002 mg/m2 DEET and 2,349 mg/m2 etofenprox LLIRN, for 63 weeks with the 3,590 mg/m2 DEET and 1,208 mg/m2 permethrin LLRN, and for 61 weeks with the 4,711 mg/m2 DEET and 702 mg/m2 etofenprox LLIRN. Because 100 % bite protection with up to 75 % quicker contact toxicity of pyrethroids were documented, synergistic toxicological and repellent effects of multi-layer polymer-coating LLIRNs may overcome LLIN-triggered selection pressure for development of new kdr- and metabolic pyrethroid resistances while simultaneously increasing protective efficacy also against kdr- and metabolic pyrethroid-resistant mosquitoes substantially due to the repellent-induced effects of LLIRNs thus indicating that this approach is a promising new candidate for future bed net, curtain, and window screen impregnation aiming at optimized prevention from mosquito-borne diseases.

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References

  • Anyanwu EC, Ehiri JE, Kanu I, Merrick J (2006) Health effects of long-term exposure to insecticide-treated mosquito nets in the control of malaria in endemic regions, revised. Sci World J 15:1631–1641

    Article  Google Scholar 

  • 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(4):492–500

    Article  PubMed  CAS  Google Scholar 

  • Boeckh J, Breer H, Geier M, Hoever F-P, Krüger B-W, Nentwig G, Sass H (1996) Acylated 1,3-aminopropanols as repellents against bloodsucking arthropods. Pestic Sci 48:359–373

    Article  CAS  Google Scholar 

  • Bonnet J, Pennetier C, Duchon S, Lapied B, Corbel V (2009) Multi-function oxidases are responsible for the synergistic interactions occurring between repellents and insecticides in mosquitoes. Parasit Vectors 16:17–23

    Article  Google Scholar 

  • Calvete C, Estrada R, Miranda MA, Del Rio R, Borras D, Beldron F, Martinez A, Calvo A, Lucientes J (2010) Protection of livestock against bluetongue virus vector Culicoides imicola using insecticide-treated netting in open areas. Med Vet Entomol 24:169–175

    Article  PubMed  CAS  Google Scholar 

  • Chandre F, Darriet F, Duchon S, Finot L, Manguin S, Carnevale P, Guillet P (2000) Modifications of pyrethroid effects associated with kdr mutation in Anopheles gambiae. Med Vet Entomol 14:81–88

    Article  PubMed  CAS  Google Scholar 

  • Chapin G, Wasserstrom R (1981) Agricultural production and malaria resurgence in Central America and India. Nature 293:181–185

    Article  PubMed  CAS  Google Scholar 

  • Cooperband MF, Allan SA (2009) Effects of different pyrethroids on landing behaviour of female Aedes aegypti, Anopheles quadrimaculatus, and Culex quinquefasciatus mosquitoes (Diptera: Culicidae). J Med Entomol 46:292–306

    Article  PubMed  CAS  Google Scholar 

  • Curtis CF, Jana-Kara B, Maxwell CA (2003) Insecticide treated nets: impact on vector populations and relevance of initial intensity of transmission and permethrin resistance. J Vector Borne Dis 40:1–8

    PubMed  CAS  Google Scholar 

  • 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 in Burkina Faso. AmJTrop Med Hyg 67:617–622

    CAS  Google Scholar 

  • Dieng H, Saifur RGM, Hassan AA, Salmah MRC, Boots M, Satho T, Jaal Z, AbuBakar S (2010) Indoor breeding of Aedes albopictus in northern peninsular Malaysia and its potential epidemiological implications. PLoS One 5(7):e11790

    Article  PubMed  Google Scholar 

  • Emami MM, Yazdi M, Guillet P (2009) Efficacy of Olyset long-lasting bednets to control transmission of cutaneous leishmaniasis in Iran. East Mediterr Health J 15:1075–1083

    PubMed  CAS  Google Scholar 

  • Enayati AA, Hemingway J (2006) Pyrethroid insecticide resistance and treated bed nets efficacy in malaria control. Pestic Biochem Physiol 84:116–126

    Article  CAS  Google Scholar 

  • Farenhorst M, Hilhorst A, Thomas MB, Knols BGJ (2011) Development of fungal applications on netting substrates for malaria vector control. J Med Entomol 48:305–313

    Article  PubMed  Google Scholar 

  • Faulde M (2010) Insektizide, Akarizide und Repellenzien. In: Aspöck H (ed) Krankheiten durch Arthropoden. Denisia-Verlag, Wien. Denisia 30:109–122

  • Faulde MK, Uedelhoven WM, Robbins RG (2003) Contact toxicity and residual activity of different permethrin-based fabric impregnation methods for Aedes aegypti (Diptera: Culicidae), Ixodes ricinus (Acari: Ixodidae), and Lepisma saccharina (Thysanura: Lepismatidae). J Med Entomol 40:935–941

    Article  PubMed  CAS  Google Scholar 

  • Faulde M, Albiez G, Nehring O (2010) Insecticidal, acaricidal and repellent effects of DEET- and IR3535-impregnated bed nets using a novel long-lasting polymer-coating technique. Parasitol Res 106:957–965

    Article  PubMed  Google Scholar 

  • Faulde M, Albiez G, Nehring O (2012) Novel long-lasting impregnation technique transferred from clothing to bednets: extended efficacy and residual activity of different pyrethroids against Aedes aegypti as shown by EN ISO 6330-standardized machine laundering. Parasitol Res. doi:10.1007/s00436-011-2769-6, Vol. 18

  • Fradin MS, Day JF (2002) Comparative efficacy of insect repellents against mosquito bites. N Engl J Med 347:13–18

    Article  PubMed  CAS  Google Scholar 

  • Griffin BA, Lagakos SW (2008) Design and analysis of arm-in-cage experiments: inference for three-state progressive disease models with common periodic observation times. Biometrics 64:337–344

    Article  PubMed  CAS  Google Scholar 

  • Hamel MJ, Otieno P, Bayoh N, Kariuki S, Were V, Marwanga D, Laserson KF, Williamson J, Slutsker L, Gimnig J (2011) The combination of indoor residual spraying and insecticide-treated nets provides added protection against malaria compared with insecticide-treated nets alone. AmJTrop Med Hyg 85:1080–1086

    Article  Google Scholar 

  • Hodjati MH, Curtis CF (1997) Dosage differential effects of permethrin impregnated into bednets on pyrethroid resistant and susceptible genotypes of the mosquito Anopheles stephensi. Med Vet Entomol 11:368–372

    Article  PubMed  CAS  Google Scholar 

  • Hoffmann G (1995) Wirkung, Einsatzgebiete und Erfordernis der Anwendung von Pyrethroiden im nicht-agrarischen Bereich. Bundesgesundheitsblatt 38:294–303

    Google Scholar 

  • Kasili S, Kutima H, Mwandawiro C, Ngumbi PM, Anjili CO, Enayati AA (2010) Laboratory and semi-field evaluation of long-lasting insecticidal nets against leishmaniasis vector, Phlebotomus (Phlebotomus) duboscqi in Kenya. J Vector Borne Dis 47:1–10

    PubMed  Google Scholar 

  • Kayedi MH, Lines JD, Haghdoost AA, Najafi S (2007) A randomized and controlled comparison of the wash-resistances and insecticidal efficacies of four types of deltamethrin-treated nets, over a 6-month period of domestic use with washing every 2 weeks, in a rural area of Iran. Ann Trop Med Parasitol 101:519–528

    Article  PubMed  CAS  Google Scholar 

  • 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 101:867–880

    Article  PubMed  Google Scholar 

  • Kolaczinski JH, Curtis CF (2000) Comparison of two alpha-cyano pyrethroids when impregnated into bednets against a pyrethroid resistant and susceptible strain of Anopheles stephensi (Diptera: Culicidae) and their F1 progeny. Bull Entomol Res 90:119–123

    PubMed  CAS  Google Scholar 

  • 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):1–10

    Google Scholar 

  • Licciardi S, Herve JP, Darriet F, Hougard J-M, Corbel V (2006) Lethal and behavioural effects of three synthetic repellents (DEET, IR3535 and KBR 3023) on Aedes aegypti mosquitoes in laboratory assays. Med Vet Entomol 20:288–293

    Article  PubMed  CAS  Google Scholar 

  • Masetti A, Maini S (2006) Arm in cage tests to compare skin repellents against bites of Aedes albopictus. Bull Insectol 59:157–160

    Google Scholar 

  • Miot HA, Ferreira DP, Mendes FG, Carrenho FRH, de Olivera AI, Carneiro CAS, Madeira NG (2008) Efficacy of topical permethrin as repellent against Aedes aegypti's bites. Dermatol Online J 14(7):1–6

    PubMed  Google Scholar 

  • Mondal D, Alam MS, Karim Z, Haque R, Boelaert M, Kroeger A (2008) Present situation of vector-control management in Bangladesh: a wake up call. Health Policy 87:369–376

    Article  PubMed  Google Scholar 

  • Muller O, Ido K, Traore C (2002) Evaluation of a prototype long-lasting insecticide-treated mosquito net under field conditions in rural Burkina Faso. Trans R Soc Trop Med Hyg 96:483–484

    Article  PubMed  CAS  Google Scholar 

  • Norris LC, Norris DE (2011) Efficacy of long-lasting insecticidal nets in use in Macha, Zambia, against the local Anopheles arabiensis population. Malar J 10:254

    Article  PubMed  Google Scholar 

  • Overgaard HJ, Sandve SR, Suwonkerd W (2005) Evidence of anopheline mosquito resistance to agrochemicals in northern Thailand. Southeast Asian J Trop Med Pub Health 36:148–153

    Google Scholar 

  • Pennetier C, Corbel V, Hougard JM (2005) Combination of a non-pyrethroid insecticide and a repellent: a new approach for controlling knockdown-resistant mosquitoes. AmJTrop Med Hyg 72:739–744

    CAS  Google Scholar 

  • Peterson RKD, Barber LM, Schleier JJ III (2011) Net risk: a risk assessment of long-lasting insecticide bed nets used for malaria management. Am Soc Trop Med Hyg 84:951–956

    Article  Google Scholar 

  • Pridgeon JW, Bernier UR, Becnel JJ (2009) Toxicity comparison of eight repellents against four species of female mosquitoes. J Am Mosq Control Assoc 25:168–173

    Article  PubMed  CAS  Google Scholar 

  • Raghavendra K, Barik TK, Reddy BPN, Sharma P, Dash AP (2011) Malaria vector control: from past to future. Parasitol Res 108:757–779

    Article  PubMed  Google Scholar 

  • Ranson H, N'Guessan R, Lines J, Moiroux N, Nkuni Z, Corbel V (2011) Pyrethroid resistance in African anopheline mosquitoes: what are the implications for malaria control? Trends Parasitol 27:91–98

    Article  PubMed  CAS  Google Scholar 

  • Rozendaal JA (1997) Vector control: methods for use by individuals and communities. World Health Organization, Geneva. ISBN 92-4-154494-5

    Google Scholar 

  • Rutledge LC, Gupta RK, Piper GN, Lowe CA (1994) Studies on the inheritance of repellent tolerance in Aedes aegypti. J Am Mosq Contr 10:93–100

    CAS  Google Scholar 

  • Sharma VP (1996) Re-emergence of malaria in India. Indian J Med Res 103:26–45

    PubMed  CAS  Google Scholar 

  • Stanczyk NM, Brookfield JFY, Ignell R, Logan JG, Field LM (2010) Behavioral insensitivity to DEET in Aedes aegypti is a genetically determined trait residing in changes in sensillum function. PNAS 107:8575–8580

    Article  PubMed  CAS  Google Scholar 

  • Takken W (2002) Do insecticide-treated bed nets have an effect on malaria vectors? Trop Med Int Health 7:1022–1030

    Article  PubMed  CAS  Google Scholar 

  • Tandon N, Ray S (2000) Breeding habitats and larval indices of Aedes aegypti and Ae. albopictus in the residential areas of Calcutta City. J Commun Dis 32:180–184

    PubMed  CAS  Google Scholar 

  • Trape J-F, Tall A, Diagne N, Ndiath O, Ly AB, Faye J, Dieye-Ba F, Roucher C, Bouganali C, Badiane A, Sarr FD, Mazenot C, Touré-Baldé A, Raoult D, Druilhe P, Mercereau-Puijalon O, Rogier C, Sokhna C (2011) Malaria morbidity and pyrethroid resistance after the introduction of insecticide-treated bednets and artemisinin-based combination therapies: a longitudinal study. Lancet Infect Dis 11(12):925–932

    Article  PubMed  CAS  Google Scholar 

  • White MT, Griffin JT, Churcher TS, Ferguson NM, Basanez M-G, Ghani AC (2011) Modelling the impact of vector control interventions on Anopheles gambiae population dynamics. Parasites Vectors 4:153–166

    Article  PubMed  Google Scholar 

  • WHO (1989) The use of impregnated bed nets and other materials for vector-borne disease control. World Health Organization, Geneva, document WHO/VBC, 89.981

    Google Scholar 

  • WHO (2001a) Vectors of diseases: hazards and risks for travellers. Part I. WER 26:189–194

    Google Scholar 

  • WHO (2001b) Vectors of diseases: hazards and risks for travellers. Part II. WER 26:201–203

    Google Scholar 

  • WHO (2005) Guidelines for laboratory and field testing of long-lasting insecticidal mosquito nets. World Health Organization, Geneva, document WHO/CDS/WHOPES/GCDPP/2005.11

    Google Scholar 

  • WHO (2010) International travel and health. World Health Organization, Geneva. ISBN 9789241580458

    Google Scholar 

  • WHO (2011a) Global insecticide use for vector-borne disease control. http://whqlibdoc.who.int/publications/2011/9789241502153_eng.pdf. Accessed 26 Dec 2011

  • WHO (2011b) Insecticide-treated mosquito nets: a WHO position statement. www.who.int/malaria/publications/atoz/itnspospaperfinal.pdf. Accessed 6 Dec 2011

  • WHO (2011c) WHO recommended long-lasting insecticidal mosquito nets. www.who.int/whopes/Long_lasting_insecticidal_nets_Jul_2011.pdf. Accessed 6 Dec 2011

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Acknowledgments

The authors thank Mr. Jacques Casteur, UTEXBEL, Ronse, Belgium for producing and providing impregnated netting material as well as Mrs. Anke Crecelius, Mr. Bernd Bocklet, Mr. Simon Leineweber and Mr. Sascha Franke for technical laboratory support. We also are grateful to Dr. Jerrold Scharninghausen for kindly reviewing and commenting on this manuscript. This manuscript represents, in part, the thesis of Mr. Oliver Nehring.

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Correspondence to Michael K. Faulde.

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Faulde, M.K., Nehring, O. Synergistic insecticidal and repellent effects of combined pyrethroid and repellent-impregnated bed nets using a novel long-lasting polymer-coating multi-layer technique. Parasitol Res 111, 755–765 (2012). https://doi.org/10.1007/s00436-012-2896-8

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