Skip to main content
Top
Published in: Malaria Journal 1/2015

Open Access 01-12-2015 | Case study

Design of a study to determine the impact of insecticide resistance on malaria vector control: a multi-country investigation

Authors: Immo Kleinschmidt, Abraham Peter Mnzava, Hmooda Toto Kafy, Charles Mbogo, Adam Ismail Bashir, Jude Bigoga, Alioun Adechoubou, Kamaraju Raghavendra, Tessa Bellamy Knox, Elfatih M Malik, Zinga José Nkuni, Nabie Bayoh, Eric Ochomo, Etienne Fondjo, Celestin Kouambeng, Herman Parfait Awono-Ambene, Josiane Etang, Martin Akogbeto, Rajendra Bhatt, Dipak K Swain, Teresa Kinyari, Kiambo Njagi, Lawrence Muthami, Krishanthi Subramaniam, John Bradley, Philippa West, Achile Massougbodji, Mariam Okê-Sopoh, Aurore Hounto, Khalid Elmardi, Neena Valecha, Luna Kamau, Evan Mathenge, Martin James Donnelly

Published in: Malaria Journal | Issue 1/2015

Login to get access

Abstract

Background

Progress in reducing the malaria disease burden through the substantial scale up of insecticide-based vector control in recent years could be reversed by the widespread emergence of insecticide resistance. The impact of insecticide resistance on the protective effectiveness of insecticide-treated nets (ITN) and indoor residual spraying (IRS) is not known. A multi-country study was undertaken in Sudan, Kenya, India, Cameroon and Benin to quantify the potential loss of epidemiological effectiveness of ITNs and IRS due to decreased susceptibility of malaria vectors to insecticides. The design of the study is described in this paper.

Methods

Malaria disease incidence rates by active case detection in cohorts of children, and indicators of insecticide resistance in local vectors were monitored in each of approximately 300 separate locations (clusters) with high coverage of malaria vector control over multiple malaria seasons. Phenotypic and genotypic resistance was assessed annually. In two countries, Sudan and India, clusters were randomly assigned to receive universal coverage of ITNs only, or universal coverage of ITNs combined with high coverage of IRS. Association between malaria incidence and insecticide resistance, and protective effectiveness of vector control methods and insecticide resistance were estimated, respectively.

Results

Cohorts have been set up in all five countries, and phenotypic resistance data have been collected in all clusters. In Sudan, Kenya, Cameroon and Benin data collection is due to be completed in 2015. In India data collection will be completed in 2016.

Discussion

The paper discusses challenges faced in the design and execution of the study, the analysis plan, the strengths and weaknesses, and the possible alternatives to the chosen study design.
Literature
1.
go back to reference WHO (2013) World malaria report 2013. World Health Organization, Geneva WHO (2013) World malaria report 2013. World Health Organization, Geneva
2.
go back to reference WHO (2014) World malaria report 2014. World Health Organization, Geneva WHO (2014) World malaria report 2014. World Health Organization, Geneva
3.
go back to reference WHO (2012) Global plan for insecticide resistance management in malaria vectors. World Health Organization, Geneva WHO (2012) Global plan for insecticide resistance management in malaria vectors. World Health Organization, Geneva
4.
go back to reference Sharp BL, Kleinschmidt I, Streat E, Maharaj R, Barnes KI, Durrheim DN et al (2007) Seven years of regional malaria control collaboration—Mozambique, South Africa, and Swaziland. Am J Trop Med Hyg 76:42–47PubMedCentralPubMed Sharp BL, Kleinschmidt I, Streat E, Maharaj R, Barnes KI, Durrheim DN et al (2007) Seven years of regional malaria control collaboration—Mozambique, South Africa, and Swaziland. Am J Trop Med Hyg 76:42–47PubMedCentralPubMed
5.
go back to reference Kleinschmidt I, Sharp B, Benavente LE, Schwabe C, Torrez M, Kuklinski J et al (2006) Reduction in infection with Plasmodium falciparum one year after the introduction of malaria control interventions on Bioko Island, Equatorial Guinea. Am J Trop Med Hyg 74:972–978PubMed Kleinschmidt I, Sharp B, Benavente LE, Schwabe C, Torrez M, Kuklinski J et al (2006) Reduction in infection with Plasmodium falciparum one year after the introduction of malaria control interventions on Bioko Island, Equatorial Guinea. Am J Trop Med Hyg 74:972–978PubMed
6.
go back to reference Chanda E, Coleman M, Kleinschmidt I, Hemingway J, Hamainza B, Masaninga F et al (2012) Impact assessment of malaria vector control using routine surveillance data in Zambia: implications for monitoring and evaluation. Malar J 11:437PubMedCentralPubMedCrossRef Chanda E, Coleman M, Kleinschmidt I, Hemingway J, Hamainza B, Masaninga F et al (2012) Impact assessment of malaria vector control using routine surveillance data in Zambia: implications for monitoring and evaluation. Malar J 11:437PubMedCentralPubMedCrossRef
7.
go back to reference Edi CVA, Koudou BG, Jones CM, Weetman D, Ranson H (2012) Multiple-insecticide resistance in Anopheles gambiae mosquitoes, Southern Cote d’Ivoire. Emerg Infect Dis 18:1508–1511PubMedCentralPubMedCrossRef Edi CVA, Koudou BG, Jones CM, Weetman D, Ranson H (2012) Multiple-insecticide resistance in Anopheles gambiae mosquitoes, Southern Cote d’Ivoire. Emerg Infect Dis 18:1508–1511PubMedCentralPubMedCrossRef
8.
go back to reference Mitchell S, Stevenson B, Müller P, Wilding C, Yawson A, Field S et al (2012) Identification and validation of a gene causing cross-resistance between insecticide classes in Anopheles gambiae from Ghana. Proc Natl Acad Sci USA 109:6147–6152PubMedCentralPubMedCrossRef Mitchell S, Stevenson B, Müller P, Wilding C, Yawson A, Field S et al (2012) Identification and validation of a gene causing cross-resistance between insecticide classes in Anopheles gambiae from Ghana. Proc Natl Acad Sci USA 109:6147–6152PubMedCentralPubMedCrossRef
9.
go back to reference Mitchell SN, Rigden DJ, Dowd AJ, Lu F, Wilding CS, Weetman D et al (2014) Metabolic and target-site mechanisms combine to confer strong DDT resistance in Anopheles gambiae. PLoS One 9:e92662PubMedCentralPubMedCrossRef Mitchell SN, Rigden DJ, Dowd AJ, Lu F, Wilding CS, Weetman D et al (2014) Metabolic and target-site mechanisms combine to confer strong DDT resistance in Anopheles gambiae. PLoS One 9:e92662PubMedCentralPubMedCrossRef
10.
go back to reference Maharaj R, Mthembu DJ, Sharp BL (2005) Impact of DDT re-introduction on malaria transmission in KwaZulu-Natal. S Afr Med J 95:871–874PubMed Maharaj R, Mthembu DJ, Sharp BL (2005) Impact of DDT re-introduction on malaria transmission in KwaZulu-Natal. S Afr Med J 95:871–874PubMed
11.
go back to reference Hargreaves K, Koekemoer LL, Brooke BD, Hunt RH, Mthembu J, Coetzee M (2000) Anopheles funestus resistant to pyrethroid insecticides in South Africa. Med Vet Entomol 14:181–189PubMedCrossRef Hargreaves K, Koekemoer LL, Brooke BD, Hunt RH, Mthembu J, Coetzee M (2000) Anopheles funestus resistant to pyrethroid insecticides in South Africa. Med Vet Entomol 14:181–189PubMedCrossRef
12.
go back to reference Barnes KI, Chanda P, Ab Barnabas G (2009) Impact of the large-scale deployment of artemether/lumefantrine on the malaria disease burden in Africa: case studies of South Africa, Zambia and Ethiopia. Malar J 8(Suppl 1):S8PubMedCentralPubMedCrossRef Barnes KI, Chanda P, Ab Barnabas G (2009) Impact of the large-scale deployment of artemether/lumefantrine on the malaria disease burden in Africa: case studies of South Africa, Zambia and Ethiopia. Malar J 8(Suppl 1):S8PubMedCentralPubMedCrossRef
13.
go back to reference Sharp BL, Ridl FC, Govender D, Kuklinski J, Kleinschmidt I (2007) Malaria vector control by indoor residual insecticide spraying on the tropical island of Bioko, Equatorial Guinea. Malar J 6:52PubMedCentralPubMedCrossRef Sharp BL, Ridl FC, Govender D, Kuklinski J, Kleinschmidt I (2007) Malaria vector control by indoor residual insecticide spraying on the tropical island of Bioko, Equatorial Guinea. Malar J 6:52PubMedCentralPubMedCrossRef
14.
go back to reference Hemingway J, Vontas J, Poupardin R, Raman J, Lines J, Schwabe C et al (2013) Country-level operational implementation of the Global Plan for Insecticide Resistance Management. Proc Natl Acad Sci USA 110:9397–9402PubMedCentralPubMedCrossRef Hemingway J, Vontas J, Poupardin R, Raman J, Lines J, Schwabe C et al (2013) Country-level operational implementation of the Global Plan for Insecticide Resistance Management. Proc Natl Acad Sci USA 110:9397–9402PubMedCentralPubMedCrossRef
15.
go back to reference Strode C, Donegan S, Garner P, Enayati AA, Hemingway J (2014) The impact of pyrethroid resistance on the efficacy of insecticide-treated bed nets against African anopheline mosquitoes: systematic review and meta-analysis. PLoS Med 11:e1001619PubMedCentralPubMedCrossRef Strode C, Donegan S, Garner P, Enayati AA, Hemingway J (2014) The impact of pyrethroid resistance on the efficacy of insecticide-treated bed nets against African anopheline mosquitoes: systematic review and meta-analysis. PLoS Med 11:e1001619PubMedCentralPubMedCrossRef
16.
go back to reference WHO (2013) WHO recommendations for achieving universal coverage with long-lasting insecticidal nets in malaria control. World Health Organization, Geneva WHO (2013) WHO recommendations for achieving universal coverage with long-lasting insecticidal nets in malaria control. World Health Organization, Geneva
17.
go back to reference Hawley WA, Phillips-Howard PA, ter Kuile FO, Terlouw DJ, Vulule JM, Ombok M et al (2003) Community-wide effects of permethrin-treated bed nets on child mortality and malaria morbidity in western Kenya. Am J Trop Med Hyg 68:121–127PubMed Hawley WA, Phillips-Howard PA, ter Kuile FO, Terlouw DJ, Vulule JM, Ombok M et al (2003) Community-wide effects of permethrin-treated bed nets on child mortality and malaria morbidity in western Kenya. Am J Trop Med Hyg 68:121–127PubMed
18.
go back to reference Hayes RJ, Moulton LH (2009) Cluster randomised trials. CRC Press, Boca RatonCrossRef Hayes RJ, Moulton LH (2009) Cluster randomised trials. CRC Press, Boca RatonCrossRef
19.
go back to reference Roll Back Malaria Monitoring and Evaluation Reference Group (2005) Malaria Indicator Survey: HH Questionnaire, vol 2011. Roll Back Malaria Monitoring and Evaluation Reference Group Roll Back Malaria Monitoring and Evaluation Reference Group (2005) Malaria Indicator Survey: HH Questionnaire, vol 2011. Roll Back Malaria Monitoring and Evaluation Reference Group
20.
go back to reference Walsh PS, Metzger DA, Higushi R (2013) Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 54:134–139PubMed Walsh PS, Metzger DA, Higushi R (2013) Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 54:134–139PubMed
21.
go back to reference WHO (2013) Test procedures for insecticide resistance monitoring in malaria vector mosquitoes. World Health Organization, Geneva WHO (2013) Test procedures for insecticide resistance monitoring in malaria vector mosquitoes. World Health Organization, Geneva
22.
go back to reference Bagi J, Grisales N, Corkill R, Morgan JC, N’Fale S, Brogdon WG et al (2015) When a discriminating dose assay is not enough: measuring the intensity of insecticide resistance in malaria vectors. Malar J 14:210PubMedCentralPubMedCrossRef Bagi J, Grisales N, Corkill R, Morgan JC, N’Fale S, Brogdon WG et al (2015) When a discriminating dose assay is not enough: measuring the intensity of insecticide resistance in malaria vectors. Malar J 14:210PubMedCentralPubMedCrossRef
23.
go back to reference Toe KH, Jones CM, N’Fale S, Ismail HM, Dabire RK, Ranson H (2014) Increased pyrethroid resistance in malaria vectors and decreased bed net effectiveness, Burkina Faso. Emerg Infect Dis 20:1691–1696PubMedCentralPubMedCrossRef Toe KH, Jones CM, N’Fale S, Ismail HM, Dabire RK, Ranson H (2014) Increased pyrethroid resistance in malaria vectors and decreased bed net effectiveness, Burkina Faso. Emerg Infect Dis 20:1691–1696PubMedCentralPubMedCrossRef
24.
go back to reference Muller P, Warr E, Stevenson BJ, Pignatelli PM, Morgan JC, Steven A et al (2008) Field-caught permethrin-resistant Anopheles gambiae overexpress CYP6P3, a P450 that metabolises pyrethroids. PLoS Genet 4:e1000286PubMedCentralPubMedCrossRef Muller P, Warr E, Stevenson BJ, Pignatelli PM, Morgan JC, Steven A et al (2008) Field-caught permethrin-resistant Anopheles gambiae overexpress CYP6P3, a P450 that metabolises pyrethroids. PLoS Genet 4:e1000286PubMedCentralPubMedCrossRef
26.
go back to reference 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 27:91–98PubMedCrossRef 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 27:91–98PubMedCrossRef
27.
go back to reference Etang J, Fondjo E, Chandre F, Morlais I, Brengues C, Nwane P et al (2006) First report of knockdown mutations in the malaria vector Anopheles gambiae from Cameroon. Am J Trop Med Hyg 74:795–797PubMed Etang J, Fondjo E, Chandre F, Morlais I, Brengues C, Nwane P et al (2006) First report of knockdown mutations in the malaria vector Anopheles gambiae from Cameroon. Am J Trop Med Hyg 74:795–797PubMed
28.
go back to reference Nwane P, Etang J, Chouasmall yi UM, Toto JC, Koffi A, Mimpfoundi R et al (2013) Multiple insecticide resistance mechanisms in Anopheles gambiae s.l. populations from Cameroon, Central Africa. Parasit Vectors 6:41PubMedCentralPubMedCrossRef Nwane P, Etang J, Chouasmall yi UM, Toto JC, Koffi A, Mimpfoundi R et al (2013) Multiple insecticide resistance mechanisms in Anopheles gambiae s.l. populations from Cameroon, Central Africa. Parasit Vectors 6:41PubMedCentralPubMedCrossRef
29.
go back to reference Nwane P, Etang J, Chouasmall yi UM, Toto JC, Mimpfoundi R, Simard F (2011) Kdr-based insecticide resistance in Anopheles gambiae s.s populations in. BMC Res Notes 4:463PubMedCentralPubMedCrossRef Nwane P, Etang J, Chouasmall yi UM, Toto JC, Mimpfoundi R, Simard F (2011) Kdr-based insecticide resistance in Anopheles gambiae s.s populations in. BMC Res Notes 4:463PubMedCentralPubMedCrossRef
30.
go back to reference Gething PW, Patil AP, Smith DL, Guerra CA, Elyazar IR, Johnston GL et al (2011) A new world malaria map: Plasmodium falciparum endemicity in 2010. Malar J 10:378PubMedCentralPubMedCrossRef Gething PW, Patil AP, Smith DL, Guerra CA, Elyazar IR, Johnston GL et al (2011) A new world malaria map: Plasmodium falciparum endemicity in 2010. Malar J 10:378PubMedCentralPubMedCrossRef
31.
go back to reference Sismanidis C, Moulton LH, Ayles H, Fielding K, Schaap A, Beyers N et al (2008) Restricted randomization of ZAMSTAR: a 2 × 2 factorial cluster randomized trial. Clin Trials 5:316–327PubMedCrossRef Sismanidis C, Moulton LH, Ayles H, Fielding K, Schaap A, Beyers N et al (2008) Restricted randomization of ZAMSTAR: a 2 × 2 factorial cluster randomized trial. Clin Trials 5:316–327PubMedCrossRef
32.
go back to reference Rao JNK, Scott AJ (1981) The analysis of categorical data from complex sample surveys: Chi squared tests for goodness of fit and independence in two-way tables. J Am Stat Assoc 76:221–230CrossRef Rao JNK, Scott AJ (1981) The analysis of categorical data from complex sample surveys: Chi squared tests for goodness of fit and independence in two-way tables. J Am Stat Assoc 76:221–230CrossRef
33.
go back to reference Stata Corporation (2011) Stata survey data reference manual: release 12. Stata Press, College Station Stata Corporation (2011) Stata survey data reference manual: release 12. Stata Press, College Station
34.
go back to reference McCarroll L, Hemingway J (2002) Can insecticide resistance status affect parasite transmission in mosquitoes? Insect Biochem Mol Biol 32:1345–1351PubMedCrossRef McCarroll L, Hemingway J (2002) Can insecticide resistance status affect parasite transmission in mosquitoes? Insect Biochem Mol Biol 32:1345–1351PubMedCrossRef
36.
go back to reference Davey Smith G, Shipley MJ, Batty GD, Morris JN, Marmot M (2000) Physical activity and cause-specific mortality in the Whitehall study. Public Health 114:308–315PubMedCrossRef Davey Smith G, Shipley MJ, Batty GD, Morris JN, Marmot M (2000) Physical activity and cause-specific mortality in the Whitehall study. Public Health 114:308–315PubMedCrossRef
37.
38.
go back to reference Mawejje HD, Wilding CS, Rippon EJ, Hughes A, Weetman D, Donnelly MJ (2013) Insecticide resistance monitoring of field-collected Anopheles gambiae s.l. populations from Jinja, eastern Uganda, identifies high levels of pyrethroid resistance. Med Vet Entomol 27:276–283PubMedCentralPubMedCrossRef Mawejje HD, Wilding CS, Rippon EJ, Hughes A, Weetman D, Donnelly MJ (2013) Insecticide resistance monitoring of field-collected Anopheles gambiae s.l. populations from Jinja, eastern Uganda, identifies high levels of pyrethroid resistance. Med Vet Entomol 27:276–283PubMedCentralPubMedCrossRef
39.
go back to reference Lengeler C (2004) Insecticide-treated bed nets and curtains for preventing malaria. Cochrane Database Syst Rev 2:CD000363PubMed Lengeler C (2004) Insecticide-treated bed nets and curtains for preventing malaria. Cochrane Database Syst Rev 2:CD000363PubMed
Metadata
Title
Design of a study to determine the impact of insecticide resistance on malaria vector control: a multi-country investigation
Authors
Immo Kleinschmidt
Abraham Peter Mnzava
Hmooda Toto Kafy
Charles Mbogo
Adam Ismail Bashir
Jude Bigoga
Alioun Adechoubou
Kamaraju Raghavendra
Tessa Bellamy Knox
Elfatih M Malik
Zinga José Nkuni
Nabie Bayoh
Eric Ochomo
Etienne Fondjo
Celestin Kouambeng
Herman Parfait Awono-Ambene
Josiane Etang
Martin Akogbeto
Rajendra Bhatt
Dipak K Swain
Teresa Kinyari
Kiambo Njagi
Lawrence Muthami
Krishanthi Subramaniam
John Bradley
Philippa West
Achile Massougbodji
Mariam Okê-Sopoh
Aurore Hounto
Khalid Elmardi
Neena Valecha
Luna Kamau
Evan Mathenge
Martin James Donnelly
Publication date
01-12-2015
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2015
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-015-0782-4

Other articles of this Issue 1/2015

Malaria Journal 1/2015 Go to the issue
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.