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Published in: Malaria Journal 1/2016

Open Access 01-12-2016 | Research

Field effectiveness of microbial larvicides on mosquito larvae in malaria areas of Botswana and Zimbabwe

Authors: Mulamuli Mpofu, Piet Becker, Kaka Mudambo, Christiaan de Jager

Published in: Malaria Journal | Issue 1/2016

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Abstract

Background

The successful control of malaria vectors requires the control of both the larval and adult stages. The adult control methods through indoor residual spraying (IRS) and use of long-lasting insecticidal nets (LLINs) continue to be widely used with some high measure of success. Larval control methods are also being used by a number of National Malaria Control Programmes (NMCPs) with limited understanding of its contribution. Larval control might be needed in some areas to move from malaria control to elimination. This experimental study was conducted to assess the field effectiveness of winter larviciding on the larval stages of the mosquito in Botswana and Zimbabwe.

Methods

Two villages were selected in each of the two countries, one as an intervention and the other as the control. Water bodies in the intervention villages were treated using the commercial product VectoBac® WG (Valent BioSciences Corporation, IL, USA) containing the active ingredient Bacillus thuringiensis var. israelensis (Bti), a WHO recommended bio-larvicide, applied at a rate of 300 g per hectare. Random-effects Poisson regression was employed during data analysis to compare intervention with control sites with respect to larval counts.

Results

The average marginal effect of larviciding on the mosquito larvae taking interaction with time (period) into account, was −1.94 (95% CI −2.42 to −1.46) with incidence rate ratio of 0.14, thus an 86% larval reduction attributable to the intervention for both countries combined. There was a 92% and 65% effect for Botswana and Zimbabwe respectively. The effect on the early larval and late stages was 77% (P < 0.001) and 91% (P < 0.001), respectively. Overall, intervention larval sampling points had five more larvae than the control at baseline and 26 less after 16 weeks. The effect on the different species also showed similar trends.

Discussion/conclusion

Larval control using Bti showed a high effect on the population of the mosquito larvae. The reduction of the early and late larval stages can lead to reduced adult mosquito emergence and low adult mosquito densities. Larviciding can be used to control mosquito vector population by suppressing the larval stages thereby reducing adult emergence and malaria risk.
Literature
1.
go back to reference Roll Back Malaria. Roll Back Malaria Partnership. A global malaria action programme. 2008. Roll Back Malaria. Roll Back Malaria Partnership. A global malaria action programme. 2008.
2.
go back to reference Feachem RGA, Phillips AA, Targett GA, (Eds). Shrinking the malaria map: A prospectus on malaria elimination. 2009. Feachem RGA, Phillips AA, Targett GA, (Eds). Shrinking the malaria map: A prospectus on malaria elimination. 2009.
3.
go back to reference WHO. Interim position statement on larvicing in sub-Saharan Africa. Geneva, World Health Organization, 2012. WHO. Interim position statement on larvicing in sub-Saharan Africa. Geneva, World Health Organization, 2012.
5.
go back to reference Fillinger U, Ndenga B, Githeko A, Lindsay SW. Integrated malaria vector control with microbial larvicides and insecticide-treated nets in western Kenya: a controlled trial. Bull World Health Organ. 2009;87:655–65.CrossRefPubMedPubMedCentral Fillinger U, Ndenga B, Githeko A, Lindsay SW. Integrated malaria vector control with microbial larvicides and insecticide-treated nets in western Kenya: a controlled trial. Bull World Health Organ. 2009;87:655–65.CrossRefPubMedPubMedCentral
6.
go back to reference Lines JD, Myamba J, Curtis CF. Experimental hut trials of permethrin-impregnated mosquito nets and eave curtains against malaria vectors in Tanzania. Med Vet Entomol. 1987;1:37–51.CrossRefPubMed Lines JD, Myamba J, Curtis CF. Experimental hut trials of permethrin-impregnated mosquito nets and eave curtains against malaria vectors in Tanzania. Med Vet Entomol. 1987;1:37–51.CrossRefPubMed
7.
go back to reference Jawara M, Pinder M, Cham B, Walraven G, Rowley J. Comparison of deltamethrin tablet formulation with liquid deltamethrin and permethrin for bednet treatment in The Gambia. Trop Med Int Health. 2001;6:309–16.CrossRefPubMed Jawara M, Pinder M, Cham B, Walraven G, Rowley J. Comparison of deltamethrin tablet formulation with liquid deltamethrin and permethrin for bednet treatment in The Gambia. Trop Med Int Health. 2001;6:309–16.CrossRefPubMed
8.
go back to reference Bousema T, Stevenson J, Baidjoe A, Stresman G, Griffin JT, Kleinschmidt I, et al. The impact of hotspot-targeted interventions on malaria transmission: study protocol for a cluster-randomized controlled trial. Trials. 2013;14:36.CrossRefPubMedPubMedCentral Bousema T, Stevenson J, Baidjoe A, Stresman G, Griffin JT, Kleinschmidt I, et al. The impact of hotspot-targeted interventions on malaria transmission: study protocol for a cluster-randomized controlled trial. Trials. 2013;14:36.CrossRefPubMedPubMedCentral
9.
go back to reference Chihanga S, Moakofhi K, Mosweunyane T, Jibril HB, Nkomo B, Motlaleng M, et al. Malaria control in Botswana, 2008–2012: the path towards elimination. Malar J. 2013;12:458.CrossRef Chihanga S, Moakofhi K, Mosweunyane T, Jibril HB, Nkomo B, Motlaleng M, et al. Malaria control in Botswana, 2008–2012: the path towards elimination. Malar J. 2013;12:458.CrossRef
10.
go back to reference WHO. World Malaria Report 2015. Geneva, World Health Organization, 2015. WHO. World Malaria Report 2015. Geneva, World Health Organization, 2015.
11.
go back to reference Mabaso MLH, Sharp B, Lengeler C. Historical review of malarial control in southern African with emphasis on the use of indoor residual house-spraying. Trop Med Int Health. 2004;9:846–56.CrossRefPubMed Mabaso MLH, Sharp B, Lengeler C. Historical review of malarial control in southern African with emphasis on the use of indoor residual house-spraying. Trop Med Int Health. 2004;9:846–56.CrossRefPubMed
12.
go back to reference Le Sueur D, Sharp B, Gouws E, Ngxongo S. Malaria in South Africa. S Afr Med J. 1996;86:936–9.PubMed Le Sueur D, Sharp B, Gouws E, Ngxongo S. Malaria in South Africa. S Afr Med J. 1996;86:936–9.PubMed
13.
go back to reference WHO. Larval source management: a supplementary measure for malaria vector control. Geneva, World Health Organization, 2013. WHO. Larval source management: a supplementary measure for malaria vector control. Geneva, World Health Organization, 2013.
14.
go back to reference Geissbuhler Y, Kannady K, Chaki PP, Emidi B, Govella NJ, Mayagaya V, et al. Microbial larvicide application by a large-scale, community-based program reduces malaria infection prevalence in urban Dar es Salaam, Tanzania. PLoS ONE. 2009;4:e5107.CrossRefPubMedPubMedCentral Geissbuhler Y, Kannady K, Chaki PP, Emidi B, Govella NJ, Mayagaya V, et al. Microbial larvicide application by a large-scale, community-based program reduces malaria infection prevalence in urban Dar es Salaam, Tanzania. PLoS ONE. 2009;4:e5107.CrossRefPubMedPubMedCentral
15.
go back to reference Maheu-Giroux M, Castro MC. Impact of community-based larviciding on the prevalence of malaria infection in Dar es Salaam, Tanzania. PLoS ONE. 2013;8:e71638.CrossRefPubMedPubMedCentral Maheu-Giroux M, Castro MC. Impact of community-based larviciding on the prevalence of malaria infection in Dar es Salaam, Tanzania. PLoS ONE. 2013;8:e71638.CrossRefPubMedPubMedCentral
16.
go back to reference Chaki PP, Govella NJ, Shoo B, Hemed A, Tanner M, Fillinger U, et al. Achieving high coverage of larval-stage mosquito surveillance: challenges for a community-based mosquito control programme in urban Dar es Salaam, Tanzania. Malar J. 2009;8:311.CrossRefPubMedPubMedCentral Chaki PP, Govella NJ, Shoo B, Hemed A, Tanner M, Fillinger U, et al. Achieving high coverage of larval-stage mosquito surveillance: challenges for a community-based mosquito control programme in urban Dar es Salaam, Tanzania. Malar J. 2009;8:311.CrossRefPubMedPubMedCentral
17.
go back to reference Walker K, Lynch M. Contributions of Anopheles larval control to malaria suppression in tropical Africa: review of achievements and potential. Med Vet Entomol. 2007;21:2–21.CrossRefPubMed Walker K, Lynch M. Contributions of Anopheles larval control to malaria suppression in tropical Africa: review of achievements and potential. Med Vet Entomol. 2007;21:2–21.CrossRefPubMed
18.
go back to reference Imbahale SS, Githeko A, Mukabana WR, Takken W. Integrated mosquito larval source management reduces larval numbers in two highland villages in western Kenya. BMC Public Health. 2012;12:362.CrossRefPubMedPubMedCentral Imbahale SS, Githeko A, Mukabana WR, Takken W. Integrated mosquito larval source management reduces larval numbers in two highland villages in western Kenya. BMC Public Health. 2012;12:362.CrossRefPubMedPubMedCentral
19.
go back to reference Tusting LS, Thwing J, Sinclair D, Fillinger U, Gimnig J, Bonner KE, et al. Mosquito larval source management for controlling malaria. Cochrane Database Syst Rev. 2013;8:CD008923.PubMedCentral Tusting LS, Thwing J, Sinclair D, Fillinger U, Gimnig J, Bonner KE, et al. Mosquito larval source management for controlling malaria. Cochrane Database Syst Rev. 2013;8:CD008923.PubMedCentral
20.
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.CrossRefPubMed 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.CrossRefPubMed
21.
go back to reference Cuamba N, Morgan JC, Irving H, Steven A, Wondji CS. High level of pyrethroid resistance in an Anopheles funestus population of the Chokwe District in Mozambique. PLoS ONE. 2010;5:e11010.CrossRefPubMedPubMedCentral Cuamba N, Morgan JC, Irving H, Steven A, Wondji CS. High level of pyrethroid resistance in an Anopheles funestus population of the Chokwe District in Mozambique. PLoS ONE. 2010;5:e11010.CrossRefPubMedPubMedCentral
22.
go back to reference Chandre F, Darrier F, Manga L, Akogbeto M, Faye O, Mouchet J, et al. Status of pyrethroid resistance in Anopheles gambiae sensu lato. Bull World Health Organ. 1999;77:230–4.PubMedPubMedCentral Chandre F, Darrier F, Manga L, Akogbeto M, Faye O, Mouchet J, et al. Status of pyrethroid resistance in Anopheles gambiae sensu lato. Bull World Health Organ. 1999;77:230–4.PubMedPubMedCentral
23.
go back to reference N’Guessan R, Corbel V, Akogbéto 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;13:199–206.CrossRefPubMedPubMedCentral N’Guessan R, Corbel V, Akogbéto 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;13:199–206.CrossRefPubMedPubMedCentral
24.
go back to reference Chandre F, Darriet F, Manguin S, Brengues C, Carnevale P, Guillet P. Pyrethroid cross resistance spectrum among populations of Anopheles gambiae s.s. from Cote d’Ivoire. J Am Mosq Control Assoc. 1999;15:53–9.PubMed Chandre F, Darriet F, Manguin S, Brengues C, Carnevale P, Guillet P. Pyrethroid cross resistance spectrum among populations of Anopheles gambiae s.s. from Cote d’Ivoire. J Am Mosq Control Assoc. 1999;15:53–9.PubMed
25.
go back to reference Muirhead-Thomson RC. The significance of irritability, behaviouristic avoidance and allied phenomena in malaria eradication. Bull World Health Organ. 1960;22:721–34.PubMedPubMedCentral Muirhead-Thomson RC. The significance of irritability, behaviouristic avoidance and allied phenomena in malaria eradication. Bull World Health Organ. 1960;22:721–34.PubMedPubMedCentral
26.
go back to reference Muirhead-Thomson RC. Mosquito behaviour in relation to malaria transmission and control in the tropics. London: Edward Arnold & Co; 1951. Muirhead-Thomson RC. Mosquito behaviour in relation to malaria transmission and control in the tropics. London: Edward Arnold & Co; 1951.
27.
go back to reference Ferguson HM, Dornhaus A, Beeche A, Borgemeister C, Gottlieb M, Mulla MS, et al. Ecology: a prerequisite for malaria elimination and eradication. PLoS Med. 2010;7:e1000303.CrossRefPubMedPubMedCentral Ferguson HM, Dornhaus A, Beeche A, Borgemeister C, Gottlieb M, Mulla MS, et al. Ecology: a prerequisite for malaria elimination and eradication. PLoS Med. 2010;7:e1000303.CrossRefPubMedPubMedCentral
28.
go back to reference malERA Consultative Group on Vector Control. A research agenda for malaria eradication: vector control. PLoS Med. 2011;8:e1000401.CrossRef malERA Consultative Group on Vector Control. A research agenda for malaria eradication: vector control. PLoS Med. 2011;8:e1000401.CrossRef
29.
go back to reference Boete C, Koella JC. A theoretical approach to predicting the success of genetic manipulation of malaria mosquitoes in malaria control. Malar J. 2002;1:3.CrossRefPubMedPubMedCentral Boete C, Koella JC. A theoretical approach to predicting the success of genetic manipulation of malaria mosquitoes in malaria control. Malar J. 2002;1:3.CrossRefPubMedPubMedCentral
30.
go back to reference WHO. Global strategic framework for integrated vector management. Geneva, World Health Organization, 2004. WHO. Global strategic framework for integrated vector management. Geneva, World Health Organization, 2004.
31.
go back to reference WHO. WHOPES-recommended compounds and formulations for control of mosquito larvae. Geneva: World Health Organization, 2012. WHO. WHOPES-recommended compounds and formulations for control of mosquito larvae. Geneva: World Health Organization, 2012.
32.
go back to reference Dambach P, Louis VR, Kaiser A, Ouedraogo S, Sié A, Sauerborn R, Becker N. Efficacy of Bacillus thuringiensis var. israelensis against malaria mosquitoes in northwestern Burkina Faso. Parasit Vectors. 2014;7:371.CrossRefPubMedPubMedCentral Dambach P, Louis VR, Kaiser A, Ouedraogo S, Sié A, Sauerborn R, Becker N. Efficacy of Bacillus thuringiensis var. israelensis against malaria mosquitoes in northwestern Burkina Faso. Parasit Vectors. 2014;7:371.CrossRefPubMedPubMedCentral
33.
go back to reference Fillinger U, Lindsay SW. Suppression of exposure to malaria vectors by an order of magnitude using microbial larvicides in rural Kenya. Trop Med Int Health. 2006;11:1629–42.CrossRefPubMed Fillinger U, Lindsay SW. Suppression of exposure to malaria vectors by an order of magnitude using microbial larvicides in rural Kenya. Trop Med Int Health. 2006;11:1629–42.CrossRefPubMed
34.
go back to reference Lacey LA, Lacey CM. The medical importance of riceland mosquitoes and their control using alternatives to chemical insecticides. J Am Mosq Control Assoc. 1990;2:1–93. Lacey LA, Lacey CM. The medical importance of riceland mosquitoes and their control using alternatives to chemical insecticides. J Am Mosq Control Assoc. 1990;2:1–93.
35.
go back to reference Mittal P. Biolarvicides in vector control: challenges and prospects. J Vec Borne Dis. 2003;40:20. Mittal P. Biolarvicides in vector control: challenges and prospects. J Vec Borne Dis. 2003;40:20.
36.
go back to reference Rishikesh N, Dubitiskij A, Moreau C. Malaria vector control: biological control. Malaria: Principles and practices of malariology; 1988. p. 1227–49. Rishikesh N, Dubitiskij A, Moreau C. Malaria vector control: biological control. Malaria: Principles and practices of malariology; 1988. p. 1227–49.
37.
go back to reference Shililu J, Tewolde G, Brantly E, Githure J, Mbogo C, Beier J, Fusco R, Novak R. Efficacy of Bacillus thuringiensis israelensis, Bacillus sphaericus and temephos for managing Anopheles larvae in Eritrea. J Am Mosq Control Assoc. 2003;19:251–8.PubMed Shililu J, Tewolde G, Brantly E, Githure J, Mbogo C, Beier J, Fusco R, Novak R. Efficacy of Bacillus thuringiensis israelensis, Bacillus sphaericus and temephos for managing Anopheles larvae in Eritrea. J Am Mosq Control Assoc. 2003;19:251–8.PubMed
38.
go back to reference Skovmand O, Bauduin S. Efficacy of a granular formulation of Bacillus sphaericus against Culex quinquefasciatus and Anopheles gambiae in West African countries. J Vec Borne Dis. 1997;22:43–51. Skovmand O, Bauduin S. Efficacy of a granular formulation of Bacillus sphaericus against Culex quinquefasciatus and Anopheles gambiae in West African countries. J Vec Borne Dis. 1997;22:43–51.
39.
go back to reference Barbazan P, Baldet T, Darriet F, Escaffre H, Djoda DH, Hougard J-M. Impact of treatments with Bacillus sphaericus on Anopheles populations and the transmission of malaria in Maroua, a large city in a savannah region of Cameroon. J Am Mosq Control Assoc. 1998;14:33–9.PubMed Barbazan P, Baldet T, Darriet F, Escaffre H, Djoda DH, Hougard J-M. Impact of treatments with Bacillus sphaericus on Anopheles populations and the transmission of malaria in Maroua, a large city in a savannah region of Cameroon. J Am Mosq Control Assoc. 1998;14:33–9.PubMed
40.
go back to reference Karch S, Asidi N, Manzambi Z, Salaun J. Efficacy of Bacillus sphaericus against the malaria vector Anopheles gambiae and other mosquitoes in swamps and rice fields in Zaire. J Am Mosq Control Assoc. 1992;8:376–80.PubMed Karch S, Asidi N, Manzambi Z, Salaun J. Efficacy of Bacillus sphaericus against the malaria vector Anopheles gambiae and other mosquitoes in swamps and rice fields in Zaire. J Am Mosq Control Assoc. 1992;8:376–80.PubMed
41.
go back to reference Fillinger U, Knols BGJ, Becker N. Efficacy and efficiency of new Bacillus thuringiensis var. israelensis and Bacillus sphaericus formulations against Afrotropical anophelines in Western Kenya. Trop Med Int Health. 2003;8:37–47.CrossRefPubMed Fillinger U, Knols BGJ, Becker N. Efficacy and efficiency of new Bacillus thuringiensis var. israelensis and Bacillus sphaericus formulations against Afrotropical anophelines in Western Kenya. Trop Med Int Health. 2003;8:37–47.CrossRefPubMed
42.
go back to reference Majambere S, Pinder M, Fillinger U, Ameh D, Conway DJ, Green C, et al. Is mosquito larval source management appropriate for reducing malaria in areas of extensive flooding in The Gambia? A cross-over intervention trial. J Am J Trop Med Hyg. 2010;82:176–84.CrossRefPubMed Majambere S, Pinder M, Fillinger U, Ameh D, Conway DJ, Green C, et al. Is mosquito larval source management appropriate for reducing malaria in areas of extensive flooding in The Gambia? A cross-over intervention trial. J Am J Trop Med Hyg. 2010;82:176–84.CrossRefPubMed
43.
go back to reference Mulla MS, Federici BA, Darwazeh HA. Larvicidal efficacy of Bacillus thuringiensis serotype H-14 against stagnant-water mosquitoes and its effects on nontarget organisms. Environ Entomol. 1982;11:788–95.CrossRef Mulla MS, Federici BA, Darwazeh HA. Larvicidal efficacy of Bacillus thuringiensis serotype H-14 against stagnant-water mosquitoes and its effects on nontarget organisms. Environ Entomol. 1982;11:788–95.CrossRef
45.
go back to reference Das P, Amalraj DD. Biological control of malaria vectors. Indian J Med Res. 1997;106:174–97.PubMed Das P, Amalraj DD. Biological control of malaria vectors. Indian J Med Res. 1997;106:174–97.PubMed
46.
go back to reference Charles J-F, Nielsen-LeRoux C. Mosquitocidal bacterial toxins: diversity, mode of action and resistance phenomena. Mem Inst Oswaldo Cruz. 2000;95(Suppl 1):201–6.CrossRefPubMed Charles J-F, Nielsen-LeRoux C. Mosquitocidal bacterial toxins: diversity, mode of action and resistance phenomena. Mem Inst Oswaldo Cruz. 2000;95(Suppl 1):201–6.CrossRefPubMed
Metadata
Title
Field effectiveness of microbial larvicides on mosquito larvae in malaria areas of Botswana and Zimbabwe
Authors
Mulamuli Mpofu
Piet Becker
Kaka Mudambo
Christiaan de Jager
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2016
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-016-1642-6

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