Durability of three types of dual active ingredient long-lasting insecticidal net compared to a pyrethroid-only LLIN in Tanzania: methodology for a prospective cohort study nested in a cluster randomized controlled trial

Jackline L Martin, Louisa A Messenger, Franklin W Mosha, Eliud Lukole, Jacklin F Mosha, Manisha Kulkarni, Thomas S Churcher, Ellie Sherrard-Smith, Alphaxard Manjurano, Natacha Protopopoff, Mark Rowland, Jackline L Martin, Louisa A Messenger, Franklin W Mosha, Eliud Lukole, Jacklin F Mosha, Manisha Kulkarni, Thomas S Churcher, Ellie Sherrard-Smith, Alphaxard Manjurano, Natacha Protopopoff, Mark Rowland

Abstract

Background: Progress achieved by long-lasting insecticidal nets (LLINs) against malaria is threatened by widespread selection of pyrethroid resistance among vector populations. LLINs with non-pyrethroid insecticides are urgently needed. This study aims to assess the insecticide and textile durability of three classes of dual-active ingredient (A.I.) LLINs using techniques derived from established WHO LLIN testing methods to set new standards of evaluation.

Methods: A WHO Phase 3 active ingredients and textile durability study will be carried out within a cluster randomized controlled trial in 40 clusters in Misungwi district, Tanzania. The following treatments will be evaluated: (1) Interceptor®G2 combining chlorfenapyr and the pyrethroid alpha-cypermethrin, (2) Royal Guard® treated with pyriproxyfen and alpha-cypermethrin, (3) Olyset™ Plus which incorporates a synergist piperonyl butoxide and the pyrethroid permethrin, and (4) a reference standard alpha-cypermethrin only LLIN (Interceptor®). 750 nets will be followed in 5 clusters per intervention arm at 6, 12, 24 and 36 months post distribution for survivorship and hole index assessment. A second cohort of 1950 nets per net type will be identified in 10 clusters, of which 30 LLINs will be withdrawn for bio-efficacy and chemical analysis every 6 months up to 36 months and another 30 collected for experimental hut trials every year. Bio-efficacy will be assessed using cone bioassays and tunnel tests against susceptible and resistant laboratory strains of Anopheles gambiae sensu stricto. Efficacy of field-collected nets will be compared in six experimental huts. The main outcomes will be Anopheles mortality up to 72 h post exposure, blood feeding and egg maturation using ovary dissection to assess impact on fecundity.

Conclusions: Study findings will help develop bio-efficacy and physical durability criteria for partner A.I., in relation to the cRCT epidemiological and entomological outcomes, and refine preferred product characteristics of each class of LLIN. If suitable, the bioassay and hut outcomes will be fitted to transmission models to estimate correlation with cRCT outcomes.

Trial registration number: NCT03554616.

Keywords: Bio-efficacy; Chlorfenapyr; Experimental hut trial; Insecticide resistance; Interceptor; Interceptor G2; Long-lasting insecticidal net; Malaria vectors; Olyset plus; Piperonyl butoxide; Pyriproxyfen; Royal Guard; Tanzania; Textile durability.

Conflict of interest statement

The authors declare that they have no competing interests.

© 2022. The Author(s).

Figures

Fig. 1
Fig. 1
Map showing cRCT site and experimental hut site
Fig. 2
Fig. 2
Study design flow chart

References

    1. WHO . World Malaria Report. Geneva: World Health Organization; 2018.
    1. Churcher TS, Lissenden N, Griffin JT, Worrall E, Ranson H. The impact of pyrethroid resistance on the efficacy and effectiveness of bednets for malaria control in Africa. Elife. 2016;5:e16090. doi: 10.7554/eLife.16090.
    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;18:1101–1106. doi: 10.3201/eid1807.120218.
    1. Ochomo EO, Bayoh NM, Walker ED, Abongo BO, Ombok MO, Ouma C, et al. The efficacy of long-lasting nets with declining physical integrity may be compromised in areas with high levels of pyrethroid resistance. Malar J. 2013;12:368. doi: 10.1186/1475-2875-12-368.
    1. Pennetier C, Bouraima A, Chandre F, Piameu M, Etang J, Rossignol M, et al. Efficacy of Olyset(R) Plus, a new long-lasting insecticidal net incorporating permethrin and piperonyl-butoxide against multi-resistant malaria vectors [corrected] PLoS ONE. 2013;8:e75134. doi: 10.1371/journal.pone.0075134.
    1. Protopopoff N, Mosha JF, Lukole E, Charlwood JD, Wright A, Mwalimu CD, et al. Effectiveness of a long-lasting piperonyl butoxide-treated insecticidal net and indoor residual spray interventions, separately and together, against malaria transmitted by pyrethroid-resistant mosquitoes: a cluster, randomised controlled, two-by-two factorial design trial. Lancet. 2018;391:1577–1588. doi: 10.1016/S0140-6736(18)30427-6.
    1. Gleave K, Lissenden N, Chaplin M, Choi L, Ranson H. Piperonyl butoxide (PBO) combined with pyrethroids in insecticide-treated nets to prevent malaria in Africa. Cochrane Database Syst Rev. 2021;5:CD012776.
    1. WHO . Conditions for deployment of mosquito nets treated with a pyrethroid and piperonyl butoxide. Geneva: World Health Organization; 2017.
    1. WHO . Guidelines for laboratory and field-testing of long-lasting insecticidal nets. Geneva: World Health Organization; 2013.
    1. WHO . The evaluation process for vector control products. Geneva: World Health Organization; 2017.
    1. Mosha JF, Kulkarni MA, Messenger LA, Rowland M, Matowo N, Pitt C, et al. Protocol for a four parallel-arm, single-blind, cluster-randomised trial to assess the effectiveness of three types of dual active ingredient treated nets compared to pyrethroid-only long-lasting insecticidal nets to prevent malaria transmitted by pyrethroid insecticide-resistant vector mosquitoes in Tanzania. BMJ Open. 2021;11:e046664. doi: 10.1136/bmjopen-2020-046664.
    1. Accrombessi M, Cook J, Ngufor C, Sovi A, Dangbenon E, Yovogan B, et al. Assessing the efficacy of two dual-active ingredients long-lasting insecticidal nets for the control of malaria transmitted by pyrethroid-resistant vectors in Benin: study protocol for a three-arm, single-blinded, parallel, cluster-randomized controlled trial. BMC Infect Dis. 2021;21:194. doi: 10.1186/s12879-021-05879-1.
    1. Malima RC, Magesa SM, Tungu PK, Mwingira V, Magogo FS, Sudi W, et al. An experimental hut evaluation of Olyset® nets against anopheline mosquitoes after seven years use in Tanzanian villages. Malar J. 2008;7:38. doi: 10.1186/1475-2875-7-38.
    1. N'Guessan R, Darriet F, Doannio JM, Chandre F, Carnevale P. Olyset Net efficacy against pyrethroid-resistant Anopheles gambiae and Culex quinquefasciatus after 3 years' field use in C te d'Ivoire. Med Vet Entomol. 2001;15:97–104. doi: 10.1046/j.1365-2915.2001.00284.x.
    1. Killeen GF, Ranson H. Insecticide-resistant malaria vectors must be tackled. Lancet. 2018;391:1551–1552. doi: 10.1016/S0140-6736(18)30844-4.
    1. WHO . Technical consultation on determining non-inferiority of vector control products within an established class: report of a virtual meeting. Geneva: World Health Organization; 2021.
    1. Sherrard-Smith E, Griffin JT, Winskill P, Corbel V, Pennetier C, Djénontin A, et al. Systematic review of indoor residual spray efficacy and effectiveness against Plasmodium falciparum in Africa. Nat Commun. 2018;9:4982. doi: 10.1038/s41467-018-07357-w.
    1. Matowo NS, et al. An increasing role of pyrethroid-resistant Anopheles funestus in malaria transmission in the Lake Zone, Tanzania. Sci Rep. 2021;11:13457. doi: 10.1038/s41598-021-92741-8.
    1. Lorenz LM, Overgaard HJ, Massue DJ, Mageni ZD, Bradley J, Moore JD, et al. Investigating mosquito net durability for malaria control in Tanzania—attrition, bioefficacy, chemistry, degradation and insecticide resistance (ABCDR): study protocol. BMC Public Health. 2014;14:1266. doi: 10.1186/1471-2458-14-1266.
    1. WHO . How to design vector control efficacy trials. Geneva: World Health Organization; 2017.
    1. Azizi S, Snetselaar J, Wright A, Matowo J, Shirima B, Kaaya R, et al. Colonization and authentication of the pyrethroid-resistant Anopheles gambiae s.s. Muleba-Kis strain; an important test system for laboratory screening of new insecticides. Insects. 2021;12:710. doi: 10.3390/insects12080710.
    1. N'Guessan R, Odjo A, Ngufor C, Malone D, Rowland M. A chlorfenapyr mixture net Interceptor® G2 shows high efficacy and wash durability against resistant mosquitoes in West Africa. PLoS ONE. 2016;11:e0165925. doi: 10.1371/journal.pone.0165925.
    1. WHO . Report of the twentieth WHOPES working group meeting: Review of Interceptor G2 LN. Geneva: World Health Organization; 2017.
    1. Djenontin A, Ahoua Alou LP, Koffi A, Zogo B, Duarte E, N'Guessan R, et al. Insecticidal and sterilizing effect of Olyset Duo®, a permethrin and pyriproxyfen mixture net against pyrethroid-susceptible and -resistant strains of Anopheles gambiae s.s.: a release-recapture assay in experimental huts. Parasite. 2015;22:27. doi: 10.1051/parasite/2015027.
    1. Ngufor C, Agbevo A, Fagbohoun J, Fongnikin A, Rowland M. Efficacy of Royal Guard, a new alpha-cypermethrin and pyriproxyfen treated mosquito net, against pyrethroid-resistant malaria vectors. Sci Rep. 2020;10:12227. doi: 10.1038/s41598-020-69109-5.
    1. Toé KH, Mechan F, Tangena JA, Morris M, Solino J, Tchicaya EFS, et al. Assessing the impact of the addition of pyriproxyfen on the durability of permethrin-treated bed nets in Burkina Faso: a compound-randomized controlled trial. Malar J. 2019;18:383. doi: 10.1186/s12936-019-3018-1.
    1. Christophers S. The development of the egg follicle in anophelines. Paludism Simla. 1911;2:73–78.
    1. Koama B, Namountougou M, Sanou R, Ndo S, Ouattara A, Dabire RK, et al. The sterilizing effect of pyriproxyfen on the malaria vector Anopheles gambiae: physiological impact on ovaries development. Malar J. 2015;14:101. doi: 10.1186/s12936-015-0609-3.
    1. Allossogbe M, Gnanguenon V, Yovogan B, Akinro B, Anagonou R, Agossa F, et al. WHO cone bio-assays of classical and new-generation long-lasting insecticidal nets call for innovative insecticides targeting the knock-down resistance mechanism in Benin. Malar J. 2017;16:77. doi: 10.1186/s12936-017-1727-x.
    1. Owusu HF, Müller P. How important is the angle of tilt in the WHO cone bioassay? Malar J. 2016;5:243. doi: 10.1186/s12936-016-1303-9.
    1. Oxborough RM, N’Guessan R, Jones R, Kitau J, Ngufor C, Malone D, et al. The activity of the pyrrole insecticide chlorfenapyr in mosquito bioassay: towards a more rational testing and screening of non-neurotoxic insecticides for malaria vector control. Malar J. 2015;14:124. doi: 10.1186/s12936-015-0639-x.
    1. WHO . Test procedures for insecticide resistance monitoring in malaria vector mosquitoes. Geneva: World Health Organization; 2016.
    1. Smith A, Chabeda PI. A verandah-trap hut for studying the house-frequenting habits of mosquitoes and for assessing insecticides. IV. The effect of tetramethrin on the behaviour and mortality of Anopheles gambiae Giles. Bull Entomol Res. 1969;59(3):457–463. doi: 10.1017/S0007485300003424.
    1. Bayili K, N’do S, Namountougou M, Sanou R, Ouattara A, Dabire RK, et al. Evaluation of efficacy of Interceptor® G2, a long-lasting insecticide net coated with a mixture of chlorfenapyr and alpha-cypermethrin, against pyrethroid resistant Anopheles gambiae s.l. in Burkina Faso. Malar J. 2017;16:190. doi: 10.1186/s12936-017-1846-4.
    1. WHO . Vector Control Technical Export Group report to MPAC September 2013. Estimating functional survival of long-lasting insecticidal nets from field data. Geneva: World Health Organization; 2013.
    1. Tungu P, Messenger LA, Kirby MA, Sudi W, Kisinza W, Rowland M. Phase III evaluation of the insecticidal efficacy and durability of a deltamethrintreated polypropylene long-lasting net LifeNet®, in comparison with long-lasting nets made from polyester and polyethylene: study protocol. Arch Public Health. 2016;74:56. doi: 10.1186/s13690-016-0168-2.
    1. Briet O, Koenker H, Norris L, Wiegand R, Vanden Eng J, Thackeray A, et al. Attrition, physical integrity and insecticidal activity of long-lasting insecticidal nets in sub-Saharan Africa and modelling of their impact on vectorial capacity. Malar J. 2020;19:310. doi: 10.1186/s12936-020-03383-6.
    1. Kilian A, Obi E, Mansiangi P, Abilio AP, Haji KA, Blaufuss S, et al. Variation of physical durability between LLIN products and net use environments: summary of findings from four African countries. Malar J. 2021;20:26. doi: 10.1186/s12936-020-03549-2.

Source: PubMed

Szponzorok és közreműködők

Egészségi állapot

Kábítószer-beavatkozások

3
Iratkozz fel