Implications of insecticide resistance for malaria vector control with long-lasting insecticidal nets: trends in pyrethroid resistance during a WHO-coordinated multicountry prospective study

Jackie Cook; Sean Tomlinson; Immo Kleinschmidt; Martin Donnelly; Martin Akogbeto; Alioun Adechoubou; Achile Massougbodji; Mariam Okê-Sopoh; Vincent Corbel; Sylvie Cornelie; Aurore Hounto; Josiane Etang; Herman Parfait Awono-Ambene; Jude Bigoga; Stanislas Elysée Mandeng; Boris Njeambosay; Raymond Tabue; Celestin Kouambeng; Etienne Fondjo; Kamaraju Raghavendra; Rajendra M. Bhatt; Mehul Kumar Chourasia; Dipak K. Swain; Sreehari Uragayala; Neena Valecha; Charles Mbogo; Nabie Bayoh; Teresa Kinyari; Kiambo Njagi; Lawrence Muthami; Luna Kamau; Evan Mathenge; Eric Ochomo; Hmooda Toto Kafy; Adam Ismail Bashir; Elfatih M. Malik; Khalid Elmardi; Jihad Eltaher Sulieman; Mujahid Abdin; Krishanthi Subramaniam; Brent Thomas; Philippa West; John Bradley; Tessa Bellamy Knox; Abraham Peter Mnzava; Jonathan Lines; Michael Macdonald; Zinga José Nkuni

doi:10.1186/s13071-018-3101-4

Implications of insecticide resistance for malaria vector control with long-lasting insecticidal nets: trends in pyrethroid resistance during a WHO-coordinated multicountry prospective study

Jackie Cook, Sean Tomlinson, Immo Kleinschmidt, Martin Donnelly, Martin Akogbeto, Alioun Adechoubou, Achile Massougbodji, Mariam Okê-Sopoh, Vincent Corbel, Sylvie Cornelie, Aurore Hounto, Josiane Etang, Herman Parfait Awono-Ambene, Jude Bigoga, Stanislas Elysée Mandeng, Boris Njeambosay, Raymond Tabue, Celestin Kouambeng, Etienne Fondjo, Kamaraju RaghavendraRajendra M. Bhatt, Mehul Kumar Chourasia, Dipak K. Swain, Sreehari Uragayala, Neena Valecha, Charles Mbogo, Nabie Bayoh, Teresa Kinyari, Kiambo Njagi, Lawrence Muthami, Luna Kamau, Evan Mathenge, Eric Ochomo, Hmooda Toto Kafy, Adam Ismail Bashir, Elfatih M. Malik, Khalid Elmardi, Jihad Eltaher Sulieman, Mujahid Abdin, Krishanthi Subramaniam, Brent Thomas, Philippa West, John Bradley, Tessa Bellamy Knox, Abraham Peter Mnzava, Jonathan Lines, Michael Macdonald, Zinga José Nkuni

Vector Biology

London School of Hygiene and Tropical Medicine

Research output: Contribution to journal › Article › peer-review

34 Citations (Scopus)

Abstract

Background: Increasing pyrethroid resistance has been an undesirable correlate of the rapid increase in coverage of insecticide-treated nets (ITNs) since 2000. Whilst monitoring of resistance levels has increased markedly over this period, longitudinal monitoring is still lacking, meaning the temporal and spatial dynamics of phenotypic resistance in the context of increasing ITN coverage are unclear.

Methods: As part of a large WHO-co-ordinated epidemiological study investigating the impact of resistance on malaria infection, longitudinal monitoring of phenotypic resistance to pyrethroids was undertaken in 290 clusters across Benin, Cameroon, India, Kenya and Sudan.

Mortality in response to pyrethroids in the major anopheline vectors in each location was recorded during consecutive years using standard WHO test procedures. Trends in mosquito mortality were examined using generalised linear mixed-effect models.

Results: Insecticide resistance (using the WHO definition of mortality < 90%) was detected in clusters in all countries across the study period. The highest mosquito mortality (lowest resistance frequency) was consistently reported from India, in an area where ITNs had only

recently been introduced. Substantial temporal and spatial variation was evident in mortality measures in all countries. Overall, a trend of decreasing mosquito mortality (increasing resistance frequency) was recorded (Odds Ratio per year: 0.79 per year (95% CI: 0.79–0.81,

P < 0.001). There was also evidence that higher net usage was associated with lower mosquito mortality in some countries.

Discussion: Pyrethroid resistance increased over the study duration in four out of five countries. Insecticide-based vector control may be compromised as a result of ever higher resistance frequencies.

Original language	English
Article number	550
Journal	Parasites and Vectors
Volume	11
Issue number	1
Early online date	22 Oct 2018
DOIs	https://doi.org/10.1186/s13071-018-3101-4
Publication status	E-pub ahead of print - 22 Oct 2018

Keywords

Bednets
Bioassay
Insecticide resistance
Malaria
Trends
Vector control

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

Access to Document

10.1186/s13071-018-3101-4Licence: CC BY

PARV-D-18-00506 R2 acceptedAccepted author manuscript, 1.42 MBLicence: CC BY-ND

Cite this

Cook, J., Tomlinson, S., Kleinschmidt, I., Donnelly, M., Akogbeto, M., Adechoubou, A., Massougbodji, A., Okê-Sopoh, M., Corbel, V., Cornelie, S., Hounto, A., Etang, J., Awono-Ambene, H. P., Bigoga, J., Mandeng, S. E., Njeambosay, B., Tabue, R., Kouambeng, C., Fondjo, E., ... Nkuni, Z. J. (2018). Implications of insecticide resistance for malaria vector control with long-lasting insecticidal nets: trends in pyrethroid resistance during a WHO-coordinated multicountry prospective study. Parasites and Vectors, 11(1), Article 550. Advance online publication. https://doi.org/10.1186/s13071-018-3101-4

@article{42ed09a4263243fab565ab6207136a49,

title = "Implications of insecticide resistance for malaria vector control with long-lasting insecticidal nets: trends in pyrethroid resistance during a WHO-coordinated multicountry prospective study",

abstract = "Background: Increasing pyrethroid resistance has been an undesirable correlate of the rapid increase in coverage of insecticide-treated nets (ITNs) since 2000. Whilst monitoring of resistance levels has increased markedly over this period, longitudinal monitoring is still lacking, meaning the temporal and spatial dynamics of phenotypic resistance in the context of increasing ITN coverage are unclear.Methods: As part of a large WHO-co-ordinated epidemiological study investigating the impact of resistance on malaria infection, longitudinal monitoring of phenotypic resistance to pyrethroids was undertaken in 290 clusters across Benin, Cameroon, India, Kenya and Sudan.Mortality in response to pyrethroids in the major anopheline vectors in each location was recorded during consecutive years using standard WHO test procedures. Trends in mosquito mortality were examined using generalised linear mixed-effect models.Results: Insecticide resistance (using the WHO definition of mortality < 90\%) was detected in clusters in all countries across the study period. The highest mosquito mortality (lowest resistance frequency) was consistently reported from India, in an area where ITNs had onlyrecently been introduced. Substantial temporal and spatial variation was evident in mortality measures in all countries. Overall, a trend of decreasing mosquito mortality (increasing resistance frequency) was recorded (Odds Ratio per year: 0.79 per year (95\% CI: 0.79–0.81,P < 0.001). There was also evidence that higher net usage was associated with lower mosquito mortality in some countries.Discussion: Pyrethroid resistance increased over the study duration in four out of five countries. Insecticide-based vector control may be compromised as a result of ever higher resistance frequencies.",

keywords = "Bednets, Bioassay, Insecticide resistance, Malaria, Trends, Vector control",

author = "Jackie Cook and Sean Tomlinson and Immo Kleinschmidt and Martin Donnelly and Martin Akogbeto and Alioun Adechoubou and Achile Massougbodji and Mariam Ok{\^e}-Sopoh and Vincent Corbel and Sylvie Cornelie and Aurore Hounto and Josiane Etang and Awono-Ambene, \{Herman Parfait\} and Jude Bigoga and Mandeng, \{Stanislas Elys{\'e}e\} and Boris Njeambosay and Raymond Tabue and Celestin Kouambeng and Etienne Fondjo and Kamaraju Raghavendra and Bhatt, \{Rajendra M.\} and Chourasia, \{Mehul Kumar\} and Swain, \{Dipak K.\} and Sreehari Uragayala and Neena Valecha and Charles Mbogo and Nabie Bayoh and Teresa Kinyari and Kiambo Njagi and Lawrence Muthami and Luna Kamau and Evan Mathenge and Eric Ochomo and Kafy, \{Hmooda Toto\} and Bashir, \{Adam Ismail\} and Malik, \{Elfatih M.\} and Khalid Elmardi and Sulieman, \{Jihad Eltaher\} and Mujahid Abdin and Krishanthi Subramaniam and Brent Thomas and Philippa West and John Bradley and Knox, \{Tessa Bellamy\} and Mnzava, \{Abraham Peter\} and Jonathan Lines and Michael Macdonald and Nkuni, \{Zinga Jos{\'e}\}",

year = "2018",

month = oct,

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doi = "10.1186/s13071-018-3101-4",

language = "English",

volume = "11",

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issn = "1756-3305",

publisher = "BioMed Central Ltd",

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Cook, J, Tomlinson, S, Kleinschmidt, I, Donnelly, M, Akogbeto, M, Adechoubou, A, Massougbodji, A, Okê-Sopoh, M, Corbel, V, Cornelie, S, Hounto, A, Etang, J, Awono-Ambene, HP, Bigoga, J, Mandeng, SE, Njeambosay, B, Tabue, R, Kouambeng, C, Fondjo, E, Raghavendra, K, Bhatt, RM, Chourasia, MK, Swain, DK, Uragayala, S, Valecha, N, Mbogo, C, Bayoh, N, Kinyari, T, Njagi, K, Muthami, L, Kamau, L, Mathenge, E, Ochomo, E, Kafy, HT, Bashir, AI, Malik, EM, Elmardi, K, Sulieman, JE, Abdin, M, Subramaniam, K, Thomas, B, West, P, Bradley, J, Knox, TB, Mnzava, AP, Lines, J, Macdonald, M & Nkuni, ZJ 2018, 'Implications of insecticide resistance for malaria vector control with long-lasting insecticidal nets: trends in pyrethroid resistance during a WHO-coordinated multicountry prospective study', Parasites and Vectors, vol. 11, no. 1, 550. https://doi.org/10.1186/s13071-018-3101-4

Implications of insecticide resistance for malaria vector control with long-lasting insecticidal nets: trends in pyrethroid resistance during a WHO-coordinated multicountry prospective study. / Cook, Jackie; Tomlinson, Sean; Kleinschmidt, Immo et al.
In: Parasites and Vectors, Vol. 11, No. 1, 550, 22.10.2018.

Research output: Contribution to journal › Article › peer-review

TY - JOUR

T1 - Implications of insecticide resistance for malaria vector control with long-lasting insecticidal nets: trends in pyrethroid resistance during a WHO-coordinated multicountry prospective study

AU - Cook, Jackie

AU - Tomlinson, Sean

AU - Kleinschmidt, Immo

AU - Donnelly, Martin

AU - Akogbeto, Martin

AU - Adechoubou, Alioun

AU - Massougbodji, Achile

AU - Okê-Sopoh, Mariam

AU - Corbel, Vincent

AU - Cornelie, Sylvie

AU - Hounto, Aurore

AU - Etang, Josiane

AU - Awono-Ambene, Herman Parfait

AU - Bigoga, Jude

AU - Mandeng, Stanislas Elysée

AU - Njeambosay, Boris

AU - Tabue, Raymond

AU - Kouambeng, Celestin

AU - Fondjo, Etienne

AU - Raghavendra, Kamaraju

AU - Bhatt, Rajendra M.

AU - Chourasia, Mehul Kumar

AU - Swain, Dipak K.

AU - Uragayala, Sreehari

AU - Valecha, Neena

AU - Mbogo, Charles

AU - Bayoh, Nabie

AU - Kinyari, Teresa

AU - Njagi, Kiambo

AU - Muthami, Lawrence

AU - Kamau, Luna

AU - Mathenge, Evan

AU - Ochomo, Eric

AU - Kafy, Hmooda Toto

AU - Bashir, Adam Ismail

AU - Malik, Elfatih M.

AU - Elmardi, Khalid

AU - Sulieman, Jihad Eltaher

AU - Abdin, Mujahid

AU - Subramaniam, Krishanthi

AU - Thomas, Brent

AU - West, Philippa

AU - Bradley, John

AU - Knox, Tessa Bellamy

AU - Mnzava, Abraham Peter

AU - Lines, Jonathan

AU - Macdonald, Michael

AU - Nkuni, Zinga José

PY - 2018/10/22

Y1 - 2018/10/22

N2 - Background: Increasing pyrethroid resistance has been an undesirable correlate of the rapid increase in coverage of insecticide-treated nets (ITNs) since 2000. Whilst monitoring of resistance levels has increased markedly over this period, longitudinal monitoring is still lacking, meaning the temporal and spatial dynamics of phenotypic resistance in the context of increasing ITN coverage are unclear.Methods: As part of a large WHO-co-ordinated epidemiological study investigating the impact of resistance on malaria infection, longitudinal monitoring of phenotypic resistance to pyrethroids was undertaken in 290 clusters across Benin, Cameroon, India, Kenya and Sudan.Mortality in response to pyrethroids in the major anopheline vectors in each location was recorded during consecutive years using standard WHO test procedures. Trends in mosquito mortality were examined using generalised linear mixed-effect models.Results: Insecticide resistance (using the WHO definition of mortality < 90%) was detected in clusters in all countries across the study period. The highest mosquito mortality (lowest resistance frequency) was consistently reported from India, in an area where ITNs had onlyrecently been introduced. Substantial temporal and spatial variation was evident in mortality measures in all countries. Overall, a trend of decreasing mosquito mortality (increasing resistance frequency) was recorded (Odds Ratio per year: 0.79 per year (95% CI: 0.79–0.81,P < 0.001). There was also evidence that higher net usage was associated with lower mosquito mortality in some countries.Discussion: Pyrethroid resistance increased over the study duration in four out of five countries. Insecticide-based vector control may be compromised as a result of ever higher resistance frequencies.

AB - Background: Increasing pyrethroid resistance has been an undesirable correlate of the rapid increase in coverage of insecticide-treated nets (ITNs) since 2000. Whilst monitoring of resistance levels has increased markedly over this period, longitudinal monitoring is still lacking, meaning the temporal and spatial dynamics of phenotypic resistance in the context of increasing ITN coverage are unclear.Methods: As part of a large WHO-co-ordinated epidemiological study investigating the impact of resistance on malaria infection, longitudinal monitoring of phenotypic resistance to pyrethroids was undertaken in 290 clusters across Benin, Cameroon, India, Kenya and Sudan.Mortality in response to pyrethroids in the major anopheline vectors in each location was recorded during consecutive years using standard WHO test procedures. Trends in mosquito mortality were examined using generalised linear mixed-effect models.Results: Insecticide resistance (using the WHO definition of mortality < 90%) was detected in clusters in all countries across the study period. The highest mosquito mortality (lowest resistance frequency) was consistently reported from India, in an area where ITNs had onlyrecently been introduced. Substantial temporal and spatial variation was evident in mortality measures in all countries. Overall, a trend of decreasing mosquito mortality (increasing resistance frequency) was recorded (Odds Ratio per year: 0.79 per year (95% CI: 0.79–0.81,P < 0.001). There was also evidence that higher net usage was associated with lower mosquito mortality in some countries.Discussion: Pyrethroid resistance increased over the study duration in four out of five countries. Insecticide-based vector control may be compromised as a result of ever higher resistance frequencies.

KW - Bednets

KW - Bioassay

KW - Insecticide resistance

KW - Malaria

KW - Trends

KW - Vector control

U2 - 10.1186/s13071-018-3101-4

DO - 10.1186/s13071-018-3101-4

M3 - Article

SN - 1756-3305

VL - 11

JO - Parasites and Vectors

JF - Parasites and Vectors

IS - 1

M1 - 550

ER -

Implications of insecticide resistance for malaria vector control with long-lasting insecticidal nets: trends in pyrethroid resistance during a WHO-coordinated multicountry prospective study

Abstract

Keywords

UN SDGs

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