The efficacy of long-lasting nets with declining physical integrity may be compromised in areas with high levels of pyrethroid resistance

Eric O Ochomo, Nabie M Bayoh, Edward D Walker, Bernard O Abongo, Maurice O Ombok, Collins Ouma, Andrew K Githeko, John Vulule, Guiyun Yan, John E Gimnig, Eric O Ochomo, Nabie M Bayoh, Edward D Walker, Bernard O Abongo, Maurice O Ombok, Collins Ouma, Andrew K Githeko, John Vulule, Guiyun Yan, John E Gimnig

Abstract

Background: Long-lasting insecticide-treated mosquito nets (LLINs) are a primary malaria prevention strategy in sub-Saharan Africa. However, emergence of insecticide resistance threatens the effectiveness of LLINs.

Methods: Cross-sectional surveys of LLINs were conducted in houses of seven and four villages in Gem and Bungoma Districts in western Kenya, respectively. Condition (number and area of holes in the nets), number and species of mosquitoes resting inside them, and insecticidal activity of nets were quantified. Mosquitoes collected inside nets were allowed to lay eggs and progeny tested for susceptibility to deltamethrin and permethrin, pyrethoids commonly deployed in LLINs in western Kenya.

Results: In Gem, 83.3% of nets were less than three years old and 32.4% had at least one hole of any size; while in Bungoma, 92% were less than three years old and 48% had at least one hole. No anopheline and five Culex spp. mosquitoes were found resting inside nets in Gem regardless of the number and size of holes, while 552 Anopheles gambiae s.l., five Anopheles funestus s.l. and 137 Culex spp. were in nets in Bungoma. The number of mosquitoes resting inside nets increased with hole areas >50 cm in Bungoma. In WHO resistance assays, f1 offspring of samples collected in nets in Bungoma were 94 and 65% resistant to deltamethrin and permethrin, respectively. Nets from Bungoma retained strong activity against a susceptible laboratory strain, but not against f1 offspring of field-collected An. gambiae s.s. All An. gambiae s.s. samples collected in nets were homozygous for the kdr genotype L1014S.

Conclusions: In areas with pyrethroid resistant vectors, LLINs with modest hole areas permit mosquito entry and feeding, providing little protection against the vectors. LLIN formulations develop large holes within three years of use, diminishing their presupposed lifetime effectiveness.

Figures

Figure 1
Figure 1
Susceptibility status of mosquito populations. Mortality of An. gambiae s.l. mosquito samples when exposed to deltamethrin and permethrin. Bungoma_Nets represents mortality of f1 offspring of mosquitoes collected resting inside nets in Bungoma, Bungoma_larvae represents mortality of samples collected as larvae in Bungoma and reared to adults for exposure while Gem_larvae mortality represents mortality of samples collected as larvae in Gem and reared to adults for exposure.

References

    1. Alonso PL, Lindsay SW, Armstrong JRM. The effect of insecticide-treated bed nets on mortality of Gambian children. Lancet. 1991;12:1499–1502. doi: 10.1016/0140-6736(91)93194-E.
    1. Phillips-Howard PA, Nahlen BL, Kolczak MS, Hightower AW, Kuile FO, Alaii JA, Gimnig JE, Arudo J, Vulule JM, Odhacha A, Kachur SP, Schoute E, Rosen DH, Sexton JD, Oloo AJ, Hawley WA. Efficacy of permethrin-treated bed nets in the prevention of mortality in young children in an area of high perennial malaria transmission in western Kenya. Am J Trop Med Hyg. 2003;12:23–29.
    1. Lengeler C. Cochrane Database of Systematic Reviews. Chichester, UK: John Wiley & Sons, Ltd; 2004. Insecticide-treated bed nets and curtains for preventing malaria; pp. 1–12.
    1. WHO. World malaria report. Geneva: World Health Organization and UNICEF; 2005.
    1. WHO. World malaria report. Geneva: World Health Organization; 2012.
    1. Baume CA, Marin MC. Gains in awareness, ownership and use of insecticide-treated nets in Nigeria, Senegal, Uganda and Zambia. Malar J. 2008;12:153. doi: 10.1186/1475-2875-7-153.
    1. Macintyre K, Littrell M, Keating J, Hamainza B, Miller J, Eisele TP. Determinants of hanging and use of ITNs in the context of near universal coverage in Zambia. Health Policy Plan. 2011. 10.1093/heapol/czr1042.
    1. DOMC. 2010 Kenya MALARIA indicator survey. Nairobi, Kenya: Ministry of Public Health and Sanitation; 2011. pp. 21–22. 47-48.
    1. Okiro EA, Alegana VA, Noor AM, Mutheu JJ, Juma E, Snow RW. Malaria paediatric hospitalization between 1999 and 2008 across Kenya. BMC Med. 2009;12:75. doi: 10.1186/1741-7015-7-75.
    1. Okiro E, Alegana V, Noor A, Snow R. Changing malaria intervention coverage, transmission and hospitalization in Kenya. Malar J. 2010;12:285. doi: 10.1186/1475-2875-9-285.
    1. Curtis CF, Lines JD, Carnevale P, Robert V, CB C. In: Appropriate Technology in Vector Control. Curtis CF, editor. Boca Raton, Florida, USA: CRC Press; 1990. Impregnated nets and curtains against malaria mosquitoes; pp. 5–46.
    1. Irish S, N’Guessan R, Boko P, Metonnou C, Odjo A, Akogbeto M, Rowland M. Loss of protection with insecticide-treated nets against pyrethroid-resistant Culex quinquefasciatus mosquitoes once nets become holed: an experimental hut study. Parasit Vectors. 2008;12:17. doi: 10.1186/1756-3305-1-17.
    1. Miller JE, Lindsay SW, Armstrong JRM. Experimental hut trials of bednets impregnated with synthetic pyrethroid and organophosphate insecticides for Mosquito control in The Gambia. Med Vet Entomol. 1991;12:465–476. doi: 10.1111/j.1365-2915.1991.tb00575.x.
    1. Binka F, Indome F, Smith T. Impact of spatial distribution of permethrin-impregnated bed nets on child mortality in rural northern Ghana. Am J Trop Med Hyg. 1998;12:80–85.
    1. Hawley WA, Phillips-Howard PA, TerKuile FO, Terlouw DJ, Vulule JM, Ombok M, Nahlen BL, Gimnig JE, Kariuki SK, Kolczak MS, Hightower AW. Community-wide effects of permethrin-treated bed nets on child mortality and malaria morbidity in western Kenya. Am J Trop Med Hyg. 2003;12:121–127.
    1. Takken W. Do insecticide treated bednets have an effect on malaria vectors? Trop Med Int Health. 2002;12:1022–1030. doi: 10.1046/j.1365-3156.2002.00983.x.
    1. Choi HW, Breman JG, Teutsch SM, Liu S, Hightower AW, Sexton JD. The effectiveness of insecticide-impregnated bed nets in reducing cases of malaria infection: a meta-analysis of published results. Am J Trop Med Hyg. 1995;12:377–382.
    1. Beier JC, Oster CN, Onyango FK. Plasmodium falciparum incidence relative to entomological inoculation rates at a site proposed for testing malaria vaccines in Western Kenya. Am J Trop Med Hyg. 1994;12:529–536.
    1. Beier JC, Perkins PV, Onyango FK. Characterization of malaria transmission by Anopheles (Diptera: Culicidae) in western Kenya in preparation for malaria vaccine trials. J Med Entomol. 1990;12:570–577.
    1. O’Meara WP, Mangeni JN, Steketee R, Greenwood B. Changes in the burden of malaria in sub-Saharan Africa. Lancet Infect Dis. 2010;12:545–555. doi: 10.1016/S1473-3099(10)70096-7.
    1. Adazu K, Hamel M, Feiken D. Marked decline in childhood mortality in the Western Kenya DSS: evidence from longitudinal data 2003–2007. New Orleans, Louisiana, USA: American Society of Tropical Medicine and Hygiene, 57th Annual Meeting; Dec 7–11; 2008. Abstract #372.
    1. Gimnig J, Kolczak MS, Hightower AW, Vulule JM, Schoute E, Kamau L, Phillips-Howard PA, Kuile FO, Nahlen BL, Hawley WA. Effect of permethrin-treated bed nets on the spatial distribution of malaria vectors in western Kenya. Am J Trop Med Hyg. 2003;12:115–120.
    1. Lindblade KA, Gimnig JE, Kamau L, Hawley WA, Odhiambo F, Olang G, Kuile FOT, Vulule JM, Slutsker L. Impact of sustained use of insecticide-treated bednets on malaria vector species distribution and culicine mosquitoes. J Med Entomol. 2006;12:428–432. doi: 10.1603/0022-2585(2006)043[0428:IOSUOI];2.
    1. Bayoh MN, Mathias DK, Odiere MR, Mutuku FM, Kamau L, Gimnig JE, Vulule JM, Hawley WA, Hamel MJ, Walker ED. Anopheles gambiae: historical population decline associated with regional distribution of insecticide-treated bed nets in western Nyanza Province, Kenya. Malar J. 2010;12:62. doi: 10.1186/1475-2875-9-62.
    1. Zhou G, Afrane YA, Vardo-Zalik AM, Atieli H, Zhong D, Wamae P, Himeidan YE, Minakawa N, Githeko AK, Yan G. Changing patterns of malaria epidemiology between 2002 and 2010 in Western Kenya: the fall and rise of malaria. PLoS ONE. 2011;12:e20318. doi: 10.1371/journal.pone.0020318.
    1. Hamel MJ, Adazu K, Obor D, Sewe M, Vulule J, Williamson JM, Slutsker L, Feikin DR, Laserson KF. A Reversal in reductions of child mortality in Western Kenya, 2003–2009. Am J Trop Med Hyg. 2011;12:597–605. doi: 10.4269/ajtmh.2011.10-0678.
    1. Watsierah CA, Onyango RO, Ombaka JH, Abong’o BO, Ouma C. Provider knowledge of treatment policy and dosing regimen with artemether-lumefantrine and quinine in malaria-endemic areas of western Kenya. Malar J. 2012;12:436. doi: 10.1186/1475-2875-11-436.
    1. Ranson H, N’Guessan R, Lines J, Moiroux N, Nkuni Z, Corbel V. Pyrethroid resistance in African Anopheline mosquitoes: what are the implications for malaria control? Trends Parasitol. 2011;12:91–98. doi: 10.1016/j.pt.2010.08.004.
    1. Adazu K, Lindblade KA, Rosen DH, Odhiambo F, Ofware P, Kwach J, Eijk AMV, Decock KM, Amornkul P, Karanja D, Vulule JM, Slutsker L. Health and demographic surveillance in rural western Kenya: a platform for evaluating interventions to reduce morbidity and mortality from infectious diseases. Am J Trop Med Hyg. 2005;12:1151–1158.
    1. Ochomo E, Bayoh MN, Brogdon WG, Brogdon JE, Gimnig JE, Ouma C, Vulule JM, Walker ED. Pyrethroid resistance in Anopheles gambiae s.s. and Anopheles arabiensis in western Kenya:phenotypic, metabolic and target site characterizations of three populations. Med Vet Entomol. 2013;12:156–164. doi: 10.1111/j.1365-2915.2012.01039.x.
    1. WHO. Guidelines for monitoring the durability of long-lasting insecticidalmosquito nets under operational conditions. WHO/HTM/NTD/WHOPES. Geneva: World Health Organization; 2011.
    1. WHO. Test procedures for insecticide resistance monitoring in malaria vector mosquitoes. Geneva: World Health Organization; 2013. pp. 6–17.
    1. WHO. Report of the fifteenth WHOPES working group meeting. World Health Organization: Geneva; 2012.
    1. Scott JA, Brogdon WG, Collins FH. Identification of single specimens of the Anopheles gambiae complex by polymerase chain reaction. Am J Trop Med Hyg. 1993;12:520–529.
    1. Bass C, Nikou D, Donnelly MJ, Williamson MS, Ranson H, Ball A, Vontas J, Field LM. Detection of knockdown resistance (kdr) mutations in Anopheles gambiae: a comparison of two new high-throughput assays with existing methods. Malar J. 2007;12:111. doi: 10.1186/1475-2875-6-111.
    1. Mathias D, Ochomo E, Atieli F, Ombok M, Bayoh N, Olang G, Muhia D, Kamau L, Vulule JM, Hamel MJ, Walker ED, Gimnig JE. Spatial and temporal variation in the kdr allele L1014S in Anopheles gambiae s.s. and phenotypic variability in susceptibility to insecticides in Western Kenya. Malar J. 2011;12:10. doi: 10.1186/1475-2875-10-10.
    1. Wirtz RA, Zavala F, Charoenvit Y, Campbell GH, Burkot TR, Schneider I, Esser KM, Beaudoin RL, Andre RG. Comparative testing of monoclonal antibodies against Plasmodium falciparum sporozoites for ELISA development. Bull World Health Organ. 1987;12:39–45.
    1. Chandre F, Darriet F, Manga L, Akogbeto M, Faye O, Mouchet J, Guillet P. Status of pyrethroid resistance in Anopheles gambiae sensu lato. Bull World Health Organ. 1999;12:230–234.
    1. Brooke BD, Hunt RH, Koekemoer LL, Doussou-Yovo J, Coetzee M. Evaluation of PCR assay for detection of pyrethroid insecticide resistance in the malaria vector species of the Anopheles gambiae complex (Diptera: Culicidae) J Am Mosqu Control Assoc. 1999;12:565–568.
    1. Diabate A, Baldet T, Chandre F, Akogbeto M, Guiguemde TR, Darriet F, Brengues C, Guillet P, Hemingway J, Small GH, Hougard JM. The role of agricultural use ofinsecticides in resistance to pyrethroids in Anopheles gambiae s.l in Burkina Faso. Am J Trop Med Hyg. 2002;12:617–622.
    1. Henry MC, Assi SB, Rogier C, Dossou-Yovo J, Chandre F, Guillet P, Carnevale P. Protective efficacy of lambda-cyhalothrin treated nets in Anopheles gambiae pyrethroid resistance areas of Cote d’Ivoire. Am J Trop Med Hyg. 2005;12:859–864.
    1. Hargreaves K, Koekemoer LL, Brooke BD, Hunt RH, Mthembu J, Coetzee M. Anopheles funestus resistant to pyrethroid insecticides in South Africa. Med Vet Entomol. 2000;12:181–189. doi: 10.1046/j.1365-2915.2000.00234.x.
    1. Vulule J, Beach R, Atieli F, Roberts J, Mount D, Mwangi R. Reduced susceptibility of Anopheles gambiae to permethrin associated with the use of permethrin-impregnated bednets and curtains in Kenya. Med Vet Entomol. 1994;12:71–75. doi: 10.1111/j.1365-2915.1994.tb00389.x.
    1. Czeher C, Labbo R, Arzika I, Duchemin J. Evidence of increasing leu-phe knockdown resistance mutation in Anopheles gambiae from Niger following a nationwide long-lasting insecticide-treated nets implementation. Malar J. 2008;12:189. doi: 10.1186/1475-2875-7-189.
    1. WHO. Malaria vector control and personal protection. Geneva: World Health Organization; 2006. (WHO Technical Report series 936).
    1. N’Guessan R, Corbel V, Akogbeto M, Rowland M. Reduced efficacy of insecticide-treated nets and indoor residual spraying for malaria control in pyrethroid resistance area, Benin. Emerg Infect Dis. 2007;12:199–206. doi: 10.3201/eid1302.060631.
    1. Asidi A, N’Guessan R, Akogbeto M, Curtis C, Rowland M. Loss of household protection from use of insecticide-treated nets against pyrethroid-resistant mosquitoes, benin. Emerg Infect Dis. 2012;12:1101–1106. doi: 10.3201/eid1807.120218.
    1. Trape JF, 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. Malaria morbidity and pyrethroid resistance after the introduction of insecticide-treated bednets and artemisinin-based combination therapies: a longitudinal study. Lancet Infect Dis. 2011;12:925–932. doi: 10.1016/S1473-3099(11)70194-3.
    1. Wondji CS, Coleman M, Kleinschmidt I, Mzilahowa T, Irving H, Ndula M, Rehman A, Morgan J, Barnes KG, Hemingway J. Impact of pyrethroid resistance on operational malaria control in Malawi. Proc Natl Acad Sci U S A. 2012;12:19063–19070. doi: 10.1073/pnas.1217229109.
    1. Gnanguenon V, Azondekon R, Oke-Agbo F, Sovi A, Osse R, Padonou G, Aikpon R, Akogbeto MC. Evidence of man-vector contact in torn long-lasting insecticide-treated nets. BMC Public Health. 2013;12:751. doi: 10.1186/1471-2458-13-751.
    1. Briet OJ, Penny MA, Hardy D, Awolola TS, Van Bortel W, Corbel V, Dabire RK, Etang J, Koudou BG, Tungu PK, Chitnis N. Effects of pyrethroid resistance on the cost effectiveness of a mass distribution of long-lasting insecticidal nets: a modelling study. Malar J. 2013;12:77. doi: 10.1186/1475-2875-12-77.
    1. Rehman AM, Coleman M, Schwabe C, Baltazar G, Matias A, Gomes IR, Yellott L, Aragon C, Nchama GN, Mzilahowa T, Rowland M, Kleinschmidt I. How much does malaria vector control quality matter: the epidemiological impact of holed nets and inadequate indoor residual spraying. PLoS ONE. 2011;12:e19205. doi: 10.1371/journal.pone.0019205.
    1. Kilian A, Byamukama W, Pigeon O, Atieli F, Duchon S, Phan C. Long-term field performance of a polyester-based long-lasting insecticidal mosquito net in rural Uganda. Malar J. 2008;12:49. doi: 10.1186/1475-2875-7-49.
    1. Wills AB, Smith SC, Anshebo GY, Graves PM, Endeshaw T, Shargie EB, Damte M, Gebre T, Mosher AW, Patterson AE, Tesema YB, Richards FO Jr, Emerson PM. Physical durability of PermaNet 2.0 long-lasting insecticidal nets over three to 32 months of use in Ethiopia. Malar J. 2013;12:242. doi: 10.1186/1475-2875-12-242.
    1. Mutuku FM, Khambira M, Bisanzio D, Mungai P, Mwanzo I, Muchiri EM, King CH, Kitron U. Physical condition and maintenance of mosquito bed nets in Kwale County, coastal Kenya. Malar J. 2013;12:46. doi: 10.1186/1475-2875-12-46.
    1. Githinji S, Herbst S, Kistemann T, Noor AM. Mosquito nets in a rural area of western Kenya: ownership, use and quality. Malar J. 2010;12:250. doi: 10.1186/1475-2875-9-250.
    1. Kilian A, Byamukama W, Pigeon O, Gimnig J, Atieli F, Koekemoer L, Protopopoff N. Evidence for a useful life of more than three years for a polyester-based long-lasting insecticidal mosquito net in Western Uganda. Malar J. 2011;12:299. doi: 10.1186/1475-2875-10-299.
    1. Batisso E, Habte T, Tesfaye G, Getachew D, Tekalegne A, Kilian A, Mpeka B, Lynch C. A stitch in time: a cross-sectional survey looking at long lasting insecticide-treated bed net ownership, utilization and attrition in SNNPR, Ethiopia. Malar J. 2012;12:183. doi: 10.1186/1475-2875-11-183.
    1. Kakko I, Toimela T, Tahti H. Piperonyl butoxide potentiates the synaptosome ATPase inhibiting effect of pyrethrin. Chemosphere. 2000;12:301–305. doi: 10.1016/S0045-6535(99)00264-7.
    1. WHO. Report of the twelfth WHOPES working group meeting. Geneva: World Health Organization; 2009.
    1. Paul A, Harrington LC, Scott JG. Evaluation of novel insecticide for control of dengue vector Aedes aegypti (Diptera:Culicidae) J Med Entomol. 2006;12:55–60.
    1. Achee NL, Bangs MJ, Farlow R, Killeen GF, Lindsay S, Logan JG, Moore SJ, Rowland M, Sweeney K, Torr SJ, Zwiebel LJ, Grieco JP. Spatial repellents: from discovery and development to evidence-based validation. Malar J. 2012;12:164. doi: 10.1186/1475-2875-11-164.
    1. Beier JC, Muller GC, Gu W, Arheart KL, Schlein Y. Attractive toxic sugar bait (ATSB) methods decimate populations of Anopheles malaria vectors in arid environments regardless of the local availability of favoured sugar-source blossoms. Malar J. 2012;12:31. doi: 10.1186/1475-2875-11-31.

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