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Published in: Malaria Journal 1/2020

01-12-2020 | Malaria | Research

Risk factors for malaria infection prevalence and household vector density between mass distribution campaigns of long-lasting insecticidal nets in North-western Tanzania

Authors: Jacklin F. Mosha, Eliud Lukole, J. Derek Charlwood, Alexandra Wright, Mark Rowland, Olivia Bullock, Alphaxard Manjurano, William Kisinza, Franklin W. Mosha, Immo Kleinschmidt, Natacha Protopopoff

Published in: Malaria Journal | Issue 1/2020

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Abstract

Background

Long-lasting insecticidal nets (LLINs) are the most widely deployed vector control intervention in sub-Saharan Africa to prevent malaria. Recent reports indicate selection of pyrethroid insecticide resistance is widespread in mosquito vectors. This paper explores risk factors associated with malaria infection prevalence and vector density between mass distribution campaigns, changes in net coverage, and loss of protection in an area of high pyrethroid resistance in Northwest Tanzania.

Methods

A cross sectional malaria survey of 3456 children was undertaken in 2014 in Muleba district, Kagera region west of Lake Victoria. Vector density was assessed using indoor light traps and outdoor tent traps. Anophelines were identified to species using PCR and tested for Plasmodium falciparum circumsporozoite protein. Logistic regression was used to identify household and environmental factors associated with malaria infection and regression binomial negative for vector density.

Results

LLIN use was 27.7%. Only 16.9% of households had sufficient nets to cover all sleeping places. Malaria infection was independently associated with access to LLINs (OR: 0.57; 95% CI 0.34–0.98). LLINs less than 2 years old were slightly more protective than older LLINs (53 vs 65% prevalence of infection); however, there was no evidence that LLINs in good condition (hole index < 65) were more protective than LLINs, which were more holed. Other risk factors for malaria infection were age, group, altitude and house construction quality. Independent risk factors for vector density were consistent with malaria outcomes and included altitude, wind, livestock, house quality, open eaves and LLIN usage. Indoor collections comprised 4.6% Anopheles funestus and 95.4% Anopheles gambiae of which 4.5% were Anopheles arabiensis and 93.5% were Anopheles gambiae sensu stricto.

Conclusion

Three years after the mass distribution campaign and despite top-ups, LLIN usage had declined considerably. While children living in households with access to LLINs were at lower risk of malaria, infection prevalence remained high even among users of LLINs in good condition. While effort should be made to maintain high coverage between campaigns, distribution of standard pyrethroid-only LLINs appears insufficient to prevent malaria transmission in this area of intense pyrethroid resistance.
Literature
1.
go back to reference Bhatt S, Weiss DJ, Cameron E, Bisanzio D, Mappin B, Dalrymple U, et al. The effect of malaria control on Plasmodium falciparum in Africa between 2000 and 2015. Nature. 2015;526:207–11.PubMedPubMedCentralCrossRef Bhatt S, Weiss DJ, Cameron E, Bisanzio D, Mappin B, Dalrymple U, et al. The effect of malaria control on Plasmodium falciparum in Africa between 2000 and 2015. Nature. 2015;526:207–11.PubMedPubMedCentralCrossRef
2.
go back to reference WHO. World Malaria Report 2018. Geneva: World Health Organization; 2018. WHO. World Malaria Report 2018. Geneva: World Health Organization; 2018.
3.
go back to reference National Bureau of Statistics. Demographic and health survey and malaria indicator survey 2015–2016. Tanzania: Dar Es Salaam; 2016. National Bureau of Statistics. Demographic and health survey and malaria indicator survey 2015–2016. Tanzania: Dar Es Salaam; 2016.
4.
go back to reference Bonner K, Mwita A, McElroy PD, Omari S, Mzava A, Lengeler C, et al. Design, implementation and evaluation of a national campaign to distribute nine million free LLINs to children under five years of age in Tanzania. Malar J. 2011;10:73.PubMedPubMedCentralCrossRef Bonner K, Mwita A, McElroy PD, Omari S, Mzava A, Lengeler C, et al. Design, implementation and evaluation of a national campaign to distribute nine million free LLINs to children under five years of age in Tanzania. Malar J. 2011;10:73.PubMedPubMedCentralCrossRef
5.
go back to reference Renggli S, Mandike R, Kramer K, Patrick F, Brown NJ, McElroy PD, et al. Design, implementation and evaluation of a national campaign to deliver 18 million free long-lasting insecticidal nets to uncovered sleeping spaces in Tanzania. Malar J. 2013;12:85.PubMedPubMedCentralCrossRef Renggli S, Mandike R, Kramer K, Patrick F, Brown NJ, McElroy PD, et al. Design, implementation and evaluation of a national campaign to deliver 18 million free long-lasting insecticidal nets to uncovered sleeping spaces in Tanzania. Malar J. 2013;12:85.PubMedPubMedCentralCrossRef
6.
go back to reference Levitz L, Janko M, Mwandagalirwa K, Thwai KL, Likwela JL, Tshefu AK, et al. Effect of individual and community-level bed net usage on malaria prevalence among under-fives in the Democratic Republic of Congo. Malar J. 2018;17:39.PubMedPubMedCentralCrossRef Levitz L, Janko M, Mwandagalirwa K, Thwai KL, Likwela JL, Tshefu AK, et al. Effect of individual and community-level bed net usage on malaria prevalence among under-fives in the Democratic Republic of Congo. Malar J. 2018;17:39.PubMedPubMedCentralCrossRef
7.
go back to reference Koenker HM, Yukich JO, Mkindi A, Mandike R, Brown N, Kilian A, Lengeler C. Analysing and recommending options for maintaining universal coverage with long-lasting insecticidal nets: the case of Tanzania in 2011. Malar J. 2013;12:150.PubMedPubMedCentralCrossRef Koenker HM, Yukich JO, Mkindi A, Mandike R, Brown N, Kilian A, Lengeler C. Analysing and recommending options for maintaining universal coverage with long-lasting insecticidal nets: the case of Tanzania in 2011. Malar J. 2013;12:150.PubMedPubMedCentralCrossRef
8.
go back to reference Kramer K, Mandike R, Nathan R, Mohamed A, Lynch M, Brown N, et al. Effectiveness and equity of the Tanzania National Voucher Scheme for mosquito nets over 10 years of implementation. Malar J. 2017;16:255.PubMedPubMedCentralCrossRef Kramer K, Mandike R, Nathan R, Mohamed A, Lynch M, Brown N, et al. Effectiveness and equity of the Tanzania National Voucher Scheme for mosquito nets over 10 years of implementation. Malar J. 2017;16:255.PubMedPubMedCentralCrossRef
9.
go back to reference Acosta A, Obi E, Ato Selby R, Ugot I, Lynch M, Maire M, et al. Design, implementation, and evaluation of a school insecticide-treated net distribution program in Cross River State. Nigeria Glob Health Sci Pract. 2018;6:272–87.PubMedCrossRef Acosta A, Obi E, Ato Selby R, Ugot I, Lynch M, Maire M, et al. Design, implementation, and evaluation of a school insecticide-treated net distribution program in Cross River State. Nigeria Glob Health Sci Pract. 2018;6:272–87.PubMedCrossRef
10.
go back to reference Gnanguenon V, Azondekon R, Oke-Agbo F, Beach R, Akogbeto M. Durability assessment results suggest a serviceable life of two, rather than three, years for the current long-lasting insecticidal (mosquito) net (LLIN) intervention in Benin. BMC Infect Dis. 2014;14:69.PubMedPubMedCentralCrossRef Gnanguenon V, Azondekon R, Oke-Agbo F, Beach R, Akogbeto M. Durability assessment results suggest a serviceable life of two, rather than three, years for the current long-lasting insecticidal (mosquito) net (LLIN) intervention in Benin. BMC Infect Dis. 2014;14:69.PubMedPubMedCentralCrossRef
11.
go back to reference 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;27:91–8.PubMedCrossRef 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;27:91–8.PubMedCrossRef
12.
go back to reference Kabula B, Tungu P, Malima R, Rowland M, Minja J, Wililo R, et al. Distribution and spread of pyrethroid and DDT resistance among the Anopheles gambiae complex in Tanzania. Med Vet Entomol. 2014;28:244–52.PubMedCrossRef Kabula B, Tungu P, Malima R, Rowland M, Minja J, Wililo R, et al. Distribution and spread of pyrethroid and DDT resistance among the Anopheles gambiae complex in Tanzania. Med Vet Entomol. 2014;28:244–52.PubMedCrossRef
13.
go back to reference 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
14.
go back to reference 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;18:1101–6.PubMedCrossRef 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;18:1101–6.PubMedCrossRef
15.
go back to reference 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;391:1577–88.PubMedPubMedCentralCrossRef 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;391:1577–88.PubMedPubMedCentralCrossRef
16.
go back to reference West PA, Protopopoff N, Rowland MW, Kirby MJ, Oxborough RM, Mosha FW, et al. Evaluation of a national universal coverage campaign of long-lasting insecticidal nets in a rural district in north-west Tanzania. Malar J. 2012;11:273.PubMedPubMedCentralCrossRef West PA, Protopopoff N, Rowland MW, Kirby MJ, Oxborough RM, Mosha FW, et al. Evaluation of a national universal coverage campaign of long-lasting insecticidal nets in a rural district in north-west Tanzania. Malar J. 2012;11:273.PubMedPubMedCentralCrossRef
17.
go back to reference West PA, Protopopoff N, Wright A, Kivaju Z, Tigererwa R, Mosha FW, et al. Enhanced protection against malaria by indoor residual spraying in addition to insecticide treated nets: is it dependent on transmission intensity or net usage? PLoS ONE. 2015;10:e0115661.PubMedPubMedCentralCrossRef West PA, Protopopoff N, Wright A, Kivaju Z, Tigererwa R, Mosha FW, et al. Enhanced protection against malaria by indoor residual spraying in addition to insecticide treated nets: is it dependent on transmission intensity or net usage? PLoS ONE. 2015;10:e0115661.PubMedPubMedCentralCrossRef
18.
go back to reference Protopopoff N, Matowo J, Malima R, Kavishe R, Kaaya R, Wright A, et al. High level of resistance in the mosquito Anopheles gambiae to pyrethroid insecticides and reduced susceptibility to bendiocarb in north-western Tanzania. Malar J. 2013;12:149.PubMedPubMedCentralCrossRef Protopopoff N, Matowo J, Malima R, Kavishe R, Kaaya R, Wright A, et al. High level of resistance in the mosquito Anopheles gambiae to pyrethroid insecticides and reduced susceptibility to bendiocarb in north-western Tanzania. Malar J. 2013;12:149.PubMedPubMedCentralCrossRef
19.
go back to reference Protopopoff N, Wright A, West PA, Tigererwa R, Mosha FW, Kisinza W, et al. Combination of Insecticide treated nets and indoor residual spraying in Northern Tanzania provides additional reduction in vector population density and malaria transmission rates compared to insecticide treated nets alone: a randomised control trial. PLoS ONE. 2015;10:e0142671.PubMedPubMedCentralCrossRef Protopopoff N, Wright A, West PA, Tigererwa R, Mosha FW, Kisinza W, et al. Combination of Insecticide treated nets and indoor residual spraying in Northern Tanzania provides additional reduction in vector population density and malaria transmission rates compared to insecticide treated nets alone: a randomised control trial. PLoS ONE. 2015;10:e0142671.PubMedPubMedCentralCrossRef
20.
go back to reference WHO. Guidelines for monitoring the durability of long-lasting insecticidal mosquito nets under operational conditions. Geneva: World Health Organization; 2011. WHO. Guidelines for monitoring the durability of long-lasting insecticidal mosquito nets under operational conditions. Geneva: World Health Organization; 2011.
21.
go back to reference 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. 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.
22.
23.
go back to reference Gillies MT, Coetzee M. A supplement to the Anophelinae of Africa south of the Sahara (Afrotropical Region). Publ South Afr Inst Med Res. 1987;55:1–143. Gillies MT, Coetzee M. A supplement to the Anophelinae of Africa south of the Sahara (Afrotropical Region). Publ South Afr Inst Med Res. 1987;55:1–143.
24.
go back to reference Wirtz RA, Zavala F, Charoenvit Y, Campbell GH, Burkot TR, Schneider I, et al. Comparative testing of monoclonal antibodies against Plasmodium falciparum sporozoites for ELISA development. Bull World Health Organ. 1987;65:39–45.PubMedPubMedCentral Wirtz RA, Zavala F, Charoenvit Y, Campbell GH, Burkot TR, Schneider I, et al. Comparative testing of monoclonal antibodies against Plasmodium falciparum sporozoites for ELISA development. Bull World Health Organ. 1987;65:39–45.PubMedPubMedCentral
25.
go back to reference Bass C, Williamson MS, Field LM. Development of a multiplex real-time PCR assay for identification of members of the Anopheles gambiae species complex. Acta Trop. 2008;107:50–3.PubMedCrossRef Bass C, Williamson MS, Field LM. Development of a multiplex real-time PCR assay for identification of members of the Anopheles gambiae species complex. Acta Trop. 2008;107:50–3.PubMedCrossRef
26.
go back to reference Koekemoer LL, Kamau L, Hunt RH, Coetzee M. A cocktail polymerase chain reaction assay to identify members of the Anopheles funestus (Diptera: Culicidae) group. Am J Trop Med Hyg. 2002;66:804–11.PubMedCrossRef Koekemoer LL, Kamau L, Hunt RH, Coetzee M. A cocktail polymerase chain reaction assay to identify members of the Anopheles funestus (Diptera: Culicidae) group. Am J Trop Med Hyg. 2002;66:804–11.PubMedCrossRef
27.
go back to reference Koenker H, Kilian A, Zegers de Beyl C, Onyefunafoa EO, Selby RA, Abeku T, et al. What happens to lost nets: a multi-country analysis of reasons for LLIN attrition using 14 household surveys in four countries. Malar J. 2014;13:464.PubMedPubMedCentralCrossRef Koenker H, Kilian A, Zegers de Beyl C, Onyefunafoa EO, Selby RA, Abeku T, et al. What happens to lost nets: a multi-country analysis of reasons for LLIN attrition using 14 household surveys in four countries. Malar J. 2014;13:464.PubMedPubMedCentralCrossRef
28.
go back to reference Graves PM, Richards FO, Ngondi J, Emerson PM, Shargie EB, Endeshaw T, et al. Individual, household and environmental risk factors for malaria infection in Amhara, Oromia and SNNP regions of Ethiopia. Trans R Soc Trop Med Hyg. 2009;103:1211–20.PubMedCrossRef Graves PM, Richards FO, Ngondi J, Emerson PM, Shargie EB, Endeshaw T, et al. Individual, household and environmental risk factors for malaria infection in Amhara, Oromia and SNNP regions of Ethiopia. Trans R Soc Trop Med Hyg. 2009;103:1211–20.PubMedCrossRef
29.
go back to reference West PA, Protopopoff N, Rowland M, Cumming E, Rand A, Drakeley C, et al. Malaria risk factors in North West Tanzania: the effect of spraying, nets and wealth. PLoS ONE. 2013;8:e65787.PubMedPubMedCentralCrossRef West PA, Protopopoff N, Rowland M, Cumming E, Rand A, Drakeley C, et al. Malaria risk factors in North West Tanzania: the effect of spraying, nets and wealth. PLoS ONE. 2013;8:e65787.PubMedPubMedCentralCrossRef
30.
go back to reference Essendi WM, Vardo-Zalik AM, Lo E, Machani MG, Zhou G, Githeko AK, et al. Epidemiological risk factors for clinical malaria infection in the highlands of Western Kenya. Malar J. 2019;18:211.PubMedPubMedCentralCrossRef Essendi WM, Vardo-Zalik AM, Lo E, Machani MG, Zhou G, Githeko AK, et al. Epidemiological risk factors for clinical malaria infection in the highlands of Western Kenya. Malar J. 2019;18:211.PubMedPubMedCentralCrossRef
31.
go back to reference Mmbando BP, Vestergaard LS, Kitua AY, Lemnge MM, Theander TG, Lusingu JP. A progressive declining in the burden of malaria in north-eastern Tanzania. Malar J. 2010;9:216.PubMedPubMedCentralCrossRef Mmbando BP, Vestergaard LS, Kitua AY, Lemnge MM, Theander TG, Lusingu JP. A progressive declining in the burden of malaria in north-eastern Tanzania. Malar J. 2010;9:216.PubMedPubMedCentralCrossRef
32.
go back to reference Bødker R, Akida J, Shayo D, Kisinza W, Msangeni HA, Pedersen EM, et al. Relationship between altitude and intensity of malaria transmission in the Usambara Mountains. Tanzania J Med Entomol. 2003;40:706–17.PubMedCrossRef Bødker R, Akida J, Shayo D, Kisinza W, Msangeni HA, Pedersen EM, et al. Relationship between altitude and intensity of malaria transmission in the Usambara Mountains. Tanzania J Med Entomol. 2003;40:706–17.PubMedCrossRef
33.
go back to reference Lwetoijera DW, Kiware SS, Mageni ZD, Dongus S, Harris C, Devine GJ, et al. A need for better housing to further reduce indoor malaria transmission in areas with high bed net coverage. Parasit Vectors. 2013;6:57.PubMedPubMedCentralCrossRef Lwetoijera DW, Kiware SS, Mageni ZD, Dongus S, Harris C, Devine GJ, et al. A need for better housing to further reduce indoor malaria transmission in areas with high bed net coverage. Parasit Vectors. 2013;6:57.PubMedPubMedCentralCrossRef
34.
go back to reference Tusting LS, Ippolito MM, Willey BA, Kleinschmidt I, Dorsey G, Gosling RD, et al. The evidence for improving housing to reduce malaria: a systematic review and meta-analysis. Malar J. 2015;14:209.PubMedPubMedCentralCrossRef Tusting LS, Ippolito MM, Willey BA, Kleinschmidt I, Dorsey G, Gosling RD, et al. The evidence for improving housing to reduce malaria: a systematic review and meta-analysis. Malar J. 2015;14:209.PubMedPubMedCentralCrossRef
35.
go back to reference Lindsay SW, Jawara M, Paine K, Pinder M, Walraven GEL, Emerson PM. Changes in house design reduce exposure to malaria mosquitoes. Trop Med Int Health. 2003;8:512–7.PubMedCrossRef Lindsay SW, Jawara M, Paine K, Pinder M, Walraven GEL, Emerson PM. Changes in house design reduce exposure to malaria mosquitoes. Trop Med Int Health. 2003;8:512–7.PubMedCrossRef
37.
go back to reference Noor AM, Kirui VC, Brooker SJ, Snow RW. The use of insecticide treated nets by age: implications for universal coverage in Africa. BMC Public Health. 2009;9:369.PubMedPubMedCentralCrossRef Noor AM, Kirui VC, Brooker SJ, Snow RW. The use of insecticide treated nets by age: implications for universal coverage in Africa. BMC Public Health. 2009;9:369.PubMedPubMedCentralCrossRef
38.
go back to reference Nankabirwa J, Brooker SJ, Clarke SE, Fernando D, Gitonga CW, Schellenberg D, et al. Malaria in school-age children in Africa: an increasingly important challenge. Trop Med Int Health. 2014;19:1294–309.PubMedPubMedCentralCrossRef Nankabirwa J, Brooker SJ, Clarke SE, Fernando D, Gitonga CW, Schellenberg D, et al. Malaria in school-age children in Africa: an increasingly important challenge. Trop Med Int Health. 2014;19:1294–309.PubMedPubMedCentralCrossRef
39.
go back to reference Mayagaya VS, Nkwengulila G, Lyimo IN, Kihonda J, Mtambala H, Ngonyani H, et al. The impact of livestock on the abundance, resting behaviour and sporozoite rate of malaria vectors in southern Tanzania. Malar J. 2015;21(14):17.CrossRef Mayagaya VS, Nkwengulila G, Lyimo IN, Kihonda J, Mtambala H, Ngonyani H, et al. The impact of livestock on the abundance, resting behaviour and sporozoite rate of malaria vectors in southern Tanzania. Malar J. 2015;21(14):17.CrossRef
40.
go back to reference Kitau J, Oxborough RM, Tungu PK, Matowo J, Malima RC, Magesa SM, et al. Species shifts in the Anopheles gambiae complex: do LLINs successfully control Anopheles arabiensis? PLoS ONE. 2012;7:e31481.PubMedPubMedCentralCrossRef Kitau J, Oxborough RM, Tungu PK, Matowo J, Malima RC, Magesa SM, et al. Species shifts in the Anopheles gambiae complex: do LLINs successfully control Anopheles arabiensis? PLoS ONE. 2012;7:e31481.PubMedPubMedCentralCrossRef
Metadata
Title
Risk factors for malaria infection prevalence and household vector density between mass distribution campaigns of long-lasting insecticidal nets in North-western Tanzania
Authors
Jacklin F. Mosha
Eliud Lukole
J. Derek Charlwood
Alexandra Wright
Mark Rowland
Olivia Bullock
Alphaxard Manjurano
William Kisinza
Franklin W. Mosha
Immo Kleinschmidt
Natacha Protopopoff
Publication date
01-12-2020
Publisher
BioMed Central
Keyword
Malaria
Published in
Malaria Journal / Issue 1/2020
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-020-03369-4

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