Skip to main content
Top
Published in: Malaria Journal 1/2019

Open Access 01-12-2019 | Malaria | Research

Dynamics and monitoring of insecticide resistance in malaria vectors across mainland Tanzania from 1997 to 2017: a systematic review

Authors: Deokary Joseph Matiya, Anitha B. Philbert, Winifrida Kidima, Johnson J. Matowo

Published in: Malaria Journal | Issue 1/2019

Login to get access

Abstract

Background

Malaria still claims substantial lives of individuals in Tanzania. Insecticide-treated nets (ITNs) and indoor residual spray (IRS) are used as major malaria vector control tools. These tools are facing great challenges from the rapid escalating insecticide resistance in malaria vector populations. This review presents the information on the dynamics and monitoring of insecticide resistance in malaria vectors in mainland Tanzania since 1997. The information is important to policy-makers and other vector control stakeholders to reflect and formulate new resistance management plans in the country.

Methods

Reviewed articles on susceptibility and mechanisms of resistance in malaria vectors to insecticides across mainland Tanzania were systematically searched from the following databases: PubMed, Google scholar, HINARI and AGORA. The inclusion criteria were articles published between 2000 and 2017, reporting susceptibility of malaria vectors to insecticides, mechanisms of resistance in the mainland Tanzania, involving field collected adult mosquitoes, and mosquitoes raised from the field collected larvae. Exclusion criteria were articles reporting insecticide resistance in larval bio-assays, laboratory strains, and unpublished data. Reviewed information include year of study, malaria vectors, insecticides, and study sites. This information was entered in the excel sheet and analysed.

Results

A total of 30 articles met the selection criteria. The rapid increase of insecticide resistance in the malaria vectors across the country was reported since year 2006 onwards. Insecticide resistance in Anopheles gambiae sensu lato (s.l.) was detected in at least one compound in each class of all recommended insecticide classes. However, the Anopheles funestus s.l. is highly resistant to pyrethroids and DDT. Knockdown resistance (kdr) mechanism in An. gambiae s.l. is widely studied in the country. Biochemical resistance by detoxification enzymes (P450s, NSE and GSTs) in An. gambiae s.l. was also recorded. Numerous P450s genes associated with metabolic resistance were over transcribed in An. gambiae s.l. collected from agricultural areas. However, no study has reported mechanisms of insecticide resistance in the An. funestus s.l. in the country.

Conclusion

This review has shown the dynamics and monitoring of insecticide resistance in malaria vector populations across mainland Tanzanian. This highlights the need for devising improved control approaches of the malaria vectors in the country.
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.PubMedPubMedCentral 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.PubMedPubMedCentral
2.
go back to reference WHO. World malaria report. Geneva, Switzerland: World Health Organization; 2017. WHO. World malaria report. Geneva, Switzerland: World Health Organization; 2017.
4.
go back to reference WHO. Global plan for insecticide resistance management in malaria vectors. Geneva: World Health Organization; 2012. WHO. Global plan for insecticide resistance management in malaria vectors. Geneva: World Health Organization; 2012.
6.
go back to reference Kulkarni MA, Malima R, Mosha FW, Msangi S, Mrema E, Kabula B, et al. Efficacy of pyrethroid-treated nets against malaria vectors and nuisance-biting mosquitoes in Tanzania in areas with long-term insecticide-treated net use: pyrethroid-treated nets against malaria vectors and nuisance-biting mosquitoes. Trop Med Int Health. 2007;12:1061–73.PubMed Kulkarni MA, Malima R, Mosha FW, Msangi S, Mrema E, Kabula B, et al. Efficacy of pyrethroid-treated nets against malaria vectors and nuisance-biting mosquitoes in Tanzania in areas with long-term insecticide-treated net use: pyrethroid-treated nets against malaria vectors and nuisance-biting mosquitoes. Trop Med Int Health. 2007;12:1061–73.PubMed
7.
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.PubMedPubMedCentral 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.PubMedPubMedCentral
8.
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 s.l. to pyrethroid insecticides and reduced susceptibility to bendiocarb in north-western Tanzania. Malar J. 2013;12:149.PubMedPubMedCentral Protopopoff N, Matowo J, Malima R, Kavishe R, Kaaya R, Wright A, et al. High level of resistance in the mosquito Anopheles gambiae s.l. to pyrethroid insecticides and reduced susceptibility to bendiocarb in north-western Tanzania. Malar J. 2013;12:149.PubMedPubMedCentral
9.
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.PubMedPubMedCentral 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.PubMedPubMedCentral
10.
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.PubMedPubMedCentral 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.PubMedPubMedCentral
11.
go back to reference Kisinza WN, Nkya TE, Kabula B, Overgaard HJ, Massue DJ, Mageni Z, et al. Multiple insecticide resistance in Anopheles gambiae from Tanzania: a major concern for malaria vector control. Malar J. 2017;16:439.PubMedPubMedCentral Kisinza WN, Nkya TE, Kabula B, Overgaard HJ, Massue DJ, Mageni Z, et al. Multiple insecticide resistance in Anopheles gambiae from Tanzania: a major concern for malaria vector control. Malar J. 2017;16:439.PubMedPubMedCentral
12.
go back to reference Kabula B, Tungu P, Matowo J, Kitau J, Mweya C, Emidi B, et al. Susceptibility status of malaria vectors to insecticides commonly used for malaria control in Tanzania. Trop Med Int Health. 2012;17:742–50.PubMed Kabula B, Tungu P, Matowo J, Kitau J, Mweya C, Emidi B, et al. Susceptibility status of malaria vectors to insecticides commonly used for malaria control in Tanzania. Trop Med Int Health. 2012;17:742–50.PubMed
13.
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 in Tanzania: insecticide resistance in An. gambiae. Med Vet Entomol. 2013;28:244–52.PubMed 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 in Tanzania: insecticide resistance in An. gambiae. Med Vet Entomol. 2013;28:244–52.PubMed
15.
go back to reference Nkya TE, Akhouayri I, Poupardin R, Batengana B, Mosha F, Magesa S, et al. Insecticide resistance mechanisms associated with different environments in the malaria vector Anopheles gambiae : a case study in Tanzania. Malar J. 2014;13:28.PubMedPubMedCentral Nkya TE, Akhouayri I, Poupardin R, Batengana B, Mosha F, Magesa S, et al. Insecticide resistance mechanisms associated with different environments in the malaria vector Anopheles gambiae : a case study in Tanzania. Malar J. 2014;13:28.PubMedPubMedCentral
17.
go back to reference Okumu FO, Chipwaza B, Madumla EP, Mbeyela E, Lingamba G, Moore J, et al. Implications of bio-efficacy and persistence of insecticides when indoor residual spraying and long-lasting insecticide nets are combined for malaria prevention. Malar J. 2012;11:378.PubMedPubMedCentral Okumu FO, Chipwaza B, Madumla EP, Mbeyela E, Lingamba G, Moore J, et al. Implications of bio-efficacy and persistence of insecticides when indoor residual spraying and long-lasting insecticide nets are combined for malaria prevention. Malar J. 2012;11:378.PubMedPubMedCentral
18.
go back to reference Ngufor C, Tungu P, Malima R, Kirby M, Kisinza W, Rowland M. Insecticide-treated net wall hangings for malaria vector control: an experimental hut study in north-eastern Tanzania. Malar J. 2014;13:366.PubMedPubMedCentral Ngufor C, Tungu P, Malima R, Kirby M, Kisinza W, Rowland M. Insecticide-treated net wall hangings for malaria vector control: an experimental hut study in north-eastern Tanzania. Malar J. 2014;13:366.PubMedPubMedCentral
19.
go back to reference Matowo J, Kitau J, Kaaya R, Kavishe R, Wright A, Kisinza W, et al. Trends in the selection of insecticide resistance in Anopheles gambiae s.l. mosquitoes in northwest Tanzania during a community randomized trial of long lasting insecticidal nets and indoor residual spraying: Selection of insecticide resistance in An. gambiae. Med Vet Entomol. 2015;29:51–9.PubMed Matowo J, Kitau J, Kaaya R, Kavishe R, Wright A, Kisinza W, et al. Trends in the selection of insecticide resistance in Anopheles gambiae s.l. mosquitoes in northwest Tanzania during a community randomized trial of long lasting insecticidal nets and indoor residual spraying: Selection of insecticide resistance in An. gambiae. Med Vet Entomol. 2015;29:51–9.PubMed
20.
go back to reference Nnko EJ, Kihamia C, Tenu F, Premji Z, Kweka EJ. Insecticide use pattern and phenotypic susceptibility of Anopheles gambiae sensu lato to commonly used insecticides in Lower Moshi, northern Tanzania. BMC Res Notes. 2017;10:443.PubMedPubMedCentral Nnko EJ, Kihamia C, Tenu F, Premji Z, Kweka EJ. Insecticide use pattern and phenotypic susceptibility of Anopheles gambiae sensu lato to commonly used insecticides in Lower Moshi, northern Tanzania. BMC Res Notes. 2017;10:443.PubMedPubMedCentral
21.
go back to reference Kabula B, Tungu P, Rippon EJ, Steen K, Kisinza W, Magesa S, et al. A significant association between deltamethrin resistance, Plasmodium falciparum infection and the Vgsc-1014S resistance mutation in Anopheles gambiae highlights the epidemiological importance of resistance markers. Malar J. 2016;15:289.PubMedPubMedCentral Kabula B, Tungu P, Rippon EJ, Steen K, Kisinza W, Magesa S, et al. A significant association between deltamethrin resistance, Plasmodium falciparum infection and the Vgsc-1014S resistance mutation in Anopheles gambiae highlights the epidemiological importance of resistance markers. Malar J. 2016;15:289.PubMedPubMedCentral
22.
go back to reference Lwetoijera DW, Harris C, Kiware SS, Dongus S, Devine GJ, McCall PJ, et al. Increasing role of Anopheles funestus s.l. and Anopheles arabiensis in malaria transmission in the Kilombero Valley, Tanzania. Malar J. 2014;13:331.PubMedPubMedCentral Lwetoijera DW, Harris C, Kiware SS, Dongus S, Devine GJ, McCall PJ, et al. Increasing role of Anopheles funestus s.l. and Anopheles arabiensis in malaria transmission in the Kilombero Valley, Tanzania. Malar J. 2014;13:331.PubMedPubMedCentral
23.
go back to reference Kweka EJ, Lyaruu LJ, Mahande AM. Efficacy of PermaNet® 3.0 and PermaNet® 2.0 nets against laboratory-reared and wild Anopheles gambiae sensu lato populations in northern Tanzania. Infect Dis Poverty. 2017;6:11.PubMedPubMedCentral Kweka EJ, Lyaruu LJ, Mahande AM. Efficacy of PermaNet® 3.0 and PermaNet® 2.0 nets against laboratory-reared and wild Anopheles gambiae sensu lato populations in northern Tanzania. Infect Dis Poverty. 2017;6:11.PubMedPubMedCentral
24.
go back to reference Philbert A, Lyantagaye SL, Pradel G, Ngwa CJ, Nkwengulila G. Pyrethroids and DDT tolerance of Anopheles gambiae s.l. from Sengerema District, an area of intensive pesticide usage in north-western Tanzania. Trop Med Int Health. 2017;22:388–98.PubMed Philbert A, Lyantagaye SL, Pradel G, Ngwa CJ, Nkwengulila G. Pyrethroids and DDT tolerance of Anopheles gambiae s.l. from Sengerema District, an area of intensive pesticide usage in north-western Tanzania. Trop Med Int Health. 2017;22:388–98.PubMed
25.
go back to reference Mbepera S, Nkwengulila G, Peter R, Mausa EA, Mahande AM, Coetzee M, et al. The influence of age on insecticide susceptibility of Anopheles arabiensis during dry and rainy seasons in rice irrigation schemes of Northern Tanzania. Malar J. 2017;16:364.PubMedPubMedCentral Mbepera S, Nkwengulila G, Peter R, Mausa EA, Mahande AM, Coetzee M, et al. The influence of age on insecticide susceptibility of Anopheles arabiensis during dry and rainy seasons in rice irrigation schemes of Northern Tanzania. Malar J. 2017;16:364.PubMedPubMedCentral
26.
go back to reference Kweka EJ, Lee M-C, Mwang’onde BJ, Tenu F, Munga S, Kimaro EE, et al. Bio-efficacy of deltamethrin based durable wall lining against wild populations of Anopheles gambiae sl in Northern Tanzania. BMC Res Notes. 2017;10:92.PubMedPubMedCentral Kweka EJ, Lee M-C, Mwang’onde BJ, Tenu F, Munga S, Kimaro EE, et al. Bio-efficacy of deltamethrin based durable wall lining against wild populations of Anopheles gambiae sl in Northern Tanzania. BMC Res Notes. 2017;10:92.PubMedPubMedCentral
27.
go back to reference Emidi B, Kisinza WN, Kaaya RD, Malima R, Mosha FW. Insecticide susceptibility status of human biting mosquitoes in Muheza, Tanzania. Tanzan J Health Res. 2017;19:1–10. Emidi B, Kisinza WN, Kaaya RD, Malima R, Mosha FW. Insecticide susceptibility status of human biting mosquitoes in Muheza, Tanzania. Tanzan J Health Res. 2017;19:1–10.
28.
go back to reference Matowo NS, Munhenga G, Tanner M, Coetzee M, Feringa WF, Ngowo HS, et al. Fine-scale spatial and temporal heterogeneities in insecticide resistance profiles of the malaria vector, Anopheles arabiensis in rural south-eastern Tanzania. Wellcome Open Res. 2017;2:96.PubMedPubMedCentral Matowo NS, Munhenga G, Tanner M, Coetzee M, Feringa WF, Ngowo HS, et al. Fine-scale spatial and temporal heterogeneities in insecticide resistance profiles of the malaria vector, Anopheles arabiensis in rural south-eastern Tanzania. Wellcome Open Res. 2017;2:96.PubMedPubMedCentral
29.
go back to reference Kaindoa EW, Matowo NS, Ngowo HS, Mkandawile G, Mmbando A, Finda M, et al. Interventions that effectively target Anopheles funestus s.l. mosquitoes could significantly improve control of persistent malaria transmission in south–eastern Tanzania. PLOS ONE. 2017;12:e0177807.PubMedPubMedCentral Kaindoa EW, Matowo NS, Ngowo HS, Mkandawile G, Mmbando A, Finda M, et al. Interventions that effectively target Anopheles funestus s.l. mosquitoes could significantly improve control of persistent malaria transmission in south–eastern Tanzania. PLOS ONE. 2017;12:e0177807.PubMedPubMedCentral
30.
go back to reference Matowo J, Kitau JA, Kabula B, Kavishe R, Oxborough RM, Kaaya R, et al. Dynamics of insecticide resistance and the frequency of kdr mutation in the primary malaria vector Anopheles arabiensis in rural villages of Lower Moshi, North Eastern Tanzania. J Parasitol Vector Biol. 2014;6:31–41. Matowo J, Kitau JA, Kabula B, Kavishe R, Oxborough RM, Kaaya R, et al. Dynamics of insecticide resistance and the frequency of kdr mutation in the primary malaria vector Anopheles arabiensis in rural villages of Lower Moshi, North Eastern Tanzania. J Parasitol Vector Biol. 2014;6:31–41.
31.
go back to reference WHO. Test procedures for insecticide resistance monitoring in malaria vector mosquitoes. 2nd ed. Geneva: World Health Organization; 2016. WHO. Test procedures for insecticide resistance monitoring in malaria vector mosquitoes. 2nd ed. Geneva: World Health Organization; 2016.
32.
go back to reference Kulkarni MA, Rowland M, Alifrangis M, Mosha FW, Matowo J, Malima R, et al. Occurrence of the leucine-to-phenylalanine knockdown resistance (kdr) mutation in Anopheles arabiensis populations in Tanzania, detected by a simplified high-throughput SSOP-ELISA method. Malar J. 2006;75:6. Kulkarni MA, Rowland M, Alifrangis M, Mosha FW, Matowo J, Malima R, et al. Occurrence of the leucine-to-phenylalanine knockdown resistance (kdr) mutation in Anopheles arabiensis populations in Tanzania, detected by a simplified high-throughput SSOP-ELISA method. Malar J. 2006;75:6.
33.
go back to reference Mahande AM, Dusfour I, Matias JR, Kweka EJ. Knockdown resistance, rdl alleles, and the annual entomological inoculation rate of wild mosquito populations from lower Moshi, Northern Tanzania. J Glob Infect Dis. 2012;4:114.PubMedPubMedCentral Mahande AM, Dusfour I, Matias JR, Kweka EJ. Knockdown resistance, rdl alleles, and the annual entomological inoculation rate of wild mosquito populations from lower Moshi, Northern Tanzania. J Glob Infect Dis. 2012;4:114.PubMedPubMedCentral
34.
go back to reference Matowo J, Kulkarni MA, Mosha FW, Oxborough RM, Kitau JA, Tenu F, et al. Biochemical basis of permethrin resistance in Anopheles arabiensis from Lower Moshi, north-eastern Tanzania. Malar J. 2010;9:193.PubMedPubMedCentral Matowo J, Kulkarni MA, Mosha FW, Oxborough RM, Kitau JA, Tenu F, et al. Biochemical basis of permethrin resistance in Anopheles arabiensis from Lower Moshi, north-eastern Tanzania. Malar J. 2010;9:193.PubMedPubMedCentral
35.
go back to reference Malima RC, Oxborough RM, Tungu PK, Maxwell C, Lyimo I, Mwingira V, et al. Behavioural and insecticidal effects of organophosphate-, carbamate- and pyrethroid-treated mosquito nets against African malaria vectors. Med Vet Entomol. 2009;23:317–25.PubMed Malima RC, Oxborough RM, Tungu PK, Maxwell C, Lyimo I, Mwingira V, et al. Behavioural and insecticidal effects of organophosphate-, carbamate- and pyrethroid-treated mosquito nets against African malaria vectors. Med Vet Entomol. 2009;23:317–25.PubMed
36.
go back to reference Kabula B, Kisinza W, Tungu P, Ndege C, Batengana B, Kollo D, et al. Co-occurrence and distribution of East (L1014S) and West (L1014F) African knock-down resistance in Anopheles gambiae sensu lato population of Tanzania. Trop Med Int Health. 2014;19:1–11.PubMedCentral Kabula B, Kisinza W, Tungu P, Ndege C, Batengana B, Kollo D, et al. Co-occurrence and distribution of East (L1014S) and West (L1014F) African knock-down resistance in Anopheles gambiae sensu lato population of Tanzania. Trop Med Int Health. 2014;19:1–11.PubMedCentral
37.
go back to reference Matowo J, Jones CM, Kabula B, Ranson H, Steen K, Mosha F, et al. Genetic basis of pyrethroid resistance in a population of Anopheles arabiensis, the primary malaria vector in Lower Moshi, north-eastern Tanzania. Parasit Vectors. 2014;7:274.PubMedPubMedCentral Matowo J, Jones CM, Kabula B, Ranson H, Steen K, Mosha F, et al. Genetic basis of pyrethroid resistance in a population of Anopheles arabiensis, the primary malaria vector in Lower Moshi, north-eastern Tanzania. Parasit Vectors. 2014;7:274.PubMedPubMedCentral
38.
go back to reference Maliti D, Ranson H, Magesa S, Kisinza W, Mcha J, Haji K, et al. Islands and stepping-stones: comparative population structure of Anopheles gambiae sensu stricto and Anopheles arabiensis in Tanzania and implications for the spread of insecticide resistance. PLoS ONE. 2014;9:e110910.PubMedPubMedCentral Maliti D, Ranson H, Magesa S, Kisinza W, Mcha J, Haji K, et al. Islands and stepping-stones: comparative population structure of Anopheles gambiae sensu stricto and Anopheles arabiensis in Tanzania and implications for the spread of insecticide resistance. PLoS ONE. 2014;9:e110910.PubMedPubMedCentral
39.
go back to reference Nkya TE, Poupardin R, Laporte F, Akhouayri I, Mosha F, Magesa S, et al. Impact of agriculture on the selection of insecticide resistance in the malaria vector Anopheles gambiae: a multigenerational study in controlled conditions. Parasit Vectors. 2014;7:480.PubMedPubMedCentral Nkya TE, Poupardin R, Laporte F, Akhouayri I, Mosha F, Magesa S, et al. Impact of agriculture on the selection of insecticide resistance in the malaria vector Anopheles gambiae: a multigenerational study in controlled conditions. Parasit Vectors. 2014;7:480.PubMedPubMedCentral
41.
go back to reference Liu N. Insecticide resistance in mosquitoes: impact, mechanisms, and research directions. Annu Rev Entomol. 2015;60:537–59.PubMed Liu N. Insecticide resistance in mosquitoes: impact, mechanisms, and research directions. Annu Rev Entomol. 2015;60:537–59.PubMed
42.
go back to reference Nardini L, Christian RN, Coetzer N, Ranson H, Coetzee M, Koekemoer LL. Detoxification enzymes associated with insecticide resistance in laboratory strains of Anopheles arabiensis of different geographic origin. Parasit Vectors. 2012;5:113.PubMedPubMedCentral Nardini L, Christian RN, Coetzer N, Ranson H, Coetzee M, Koekemoer LL. Detoxification enzymes associated with insecticide resistance in laboratory strains of Anopheles arabiensis of different geographic origin. Parasit Vectors. 2012;5:113.PubMedPubMedCentral
43.
go back to reference Feyereisen R. Insect P450 inhibitors and insecticides: challenges and opportunities. Pest Manag Sci. 2015;71:793–800.PubMed Feyereisen R. Insect P450 inhibitors and insecticides: challenges and opportunities. Pest Manag Sci. 2015;71:793–800.PubMed
44.
go back to reference David J-P, Ismail HM, Chandor-Proust A, Paine MJI. Role of cytochrome P450 s in insecticide resistance: impact on the control of mosquito-borne diseases and use of insecticides on Earth. Philos Trans R Soc B Biol Sci. 2013;368:20120429. David J-P, Ismail HM, Chandor-Proust A, Paine MJI. Role of cytochrome P450 s in insecticide resistance: impact on the control of mosquito-borne diseases and use of insecticides on Earth. Philos Trans R Soc B Biol Sci. 2013;368:20120429.
45.
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.PubMed 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.PubMed
46.
go back to reference Russell TL, Govella NJ, Azizi S, Drakeley CJ, Kachur SP, Killeen GF. Increased proportions of outdoor feeding among residual malaria vector populations following increased use of insecticide-treated nets in rural Tanzania. Malar J. 2011;10:80.PubMedPubMedCentral Russell TL, Govella NJ, Azizi S, Drakeley CJ, Kachur SP, Killeen GF. Increased proportions of outdoor feeding among residual malaria vector populations following increased use of insecticide-treated nets in rural Tanzania. Malar J. 2011;10:80.PubMedPubMedCentral
47.
go back to reference Müller P, Chouaïbou M, Pignatelli P, Etang J, Walker ED, Donnelly MJ, et al. Pyrethroid tolerance is associated with elevated expression of antioxidants and agricultural practice in Anopheles arabiensis sampled from an area of cotton fields in Northern Cameroon. Mol Ecol. 2007;17:1145–55.PubMed Müller P, Chouaïbou M, Pignatelli P, Etang J, Walker ED, Donnelly MJ, et al. Pyrethroid tolerance is associated with elevated expression of antioxidants and agricultural practice in Anopheles arabiensis sampled from an area of cotton fields in Northern Cameroon. Mol Ecol. 2007;17:1145–55.PubMed
48.
go back to reference Müller P, Warr E, Stevenson BJ, Pignatelli PM, Morgan JC, Steven A, et al. Field-caught permethrin-resistant Anopheles gambiae overexpress CYP6P3, a P450 that metabolises pyrethroids. PLoS Genet. 2008;4:e1000286.PubMedPubMedCentral Müller P, Warr E, Stevenson BJ, Pignatelli PM, Morgan JC, Steven A, et al. Field-caught permethrin-resistant Anopheles gambiae overexpress CYP6P3, a P450 that metabolises pyrethroids. PLoS Genet. 2008;4:e1000286.PubMedPubMedCentral
49.
go back to reference Djouaka RF, Bakare AA, Coulibaly ON, Akogbeto MC, Ranson H, Hemingway J, et al. Expression of the cytochrome P450s, CYP6P3 and CYP6M2 are significantly elevated in multiple pyrethroid resistant populations of Anopheles gambiae ss from Southern Benin and Nigeria. BMC Genomics. 2008;9:538.PubMedPubMedCentral Djouaka RF, Bakare AA, Coulibaly ON, Akogbeto MC, Ranson H, Hemingway J, et al. Expression of the cytochrome P450s, CYP6P3 and CYP6M2 are significantly elevated in multiple pyrethroid resistant populations of Anopheles gambiae ss from Southern Benin and Nigeria. BMC Genomics. 2008;9:538.PubMedPubMedCentral
50.
go back to reference Vontas J, Grigoraki L, Morgan J, Tsakireli D, Fuseini G, Segura L, et al. Rapid selection of a pyrethroid metabolic enzyme CYP9K1 by operational malaria control activities. Proc Natl Acad Sci USA. 2018;115:4619–24.PubMed Vontas J, Grigoraki L, Morgan J, Tsakireli D, Fuseini G, Segura L, et al. Rapid selection of a pyrethroid metabolic enzyme CYP9K1 by operational malaria control activities. Proc Natl Acad Sci USA. 2018;115:4619–24.PubMed
51.
go back to reference Yahouédo GA, Chandre F, Rossignol M, Ginibre C, Balabanidou V, Mendez NGA, et al. Contributions of cuticle permeability and enzyme detoxification to pyrethroid resistance in the major malaria vector Anopheles gambiae. Sci Rep. 2017;7:11091.PubMedPubMedCentral Yahouédo GA, Chandre F, Rossignol M, Ginibre C, Balabanidou V, Mendez NGA, et al. Contributions of cuticle permeability and enzyme detoxification to pyrethroid resistance in the major malaria vector Anopheles gambiae. Sci Rep. 2017;7:11091.PubMedPubMedCentral
52.
go back to reference Yahouédo GA, Cornelie S, Djègbè I, Ahlonsou J, Aboubakar S, Soares C, et al. Dynamics of pyrethroid resistance in malaria vectors in southern Benin following a large scale implementation of vector control interventions. Parasit Vectors. 2016;9:385.PubMedPubMedCentral Yahouédo GA, Cornelie S, Djègbè I, Ahlonsou J, Aboubakar S, Soares C, et al. Dynamics of pyrethroid resistance in malaria vectors in southern Benin following a large scale implementation of vector control interventions. Parasit Vectors. 2016;9:385.PubMedPubMedCentral
53.
go back to reference Toé KH, N’Falé S, Dabiré RK, Ranson H, Jones CM. The recent escalation in strength of pyrethroid resistance in Anopheles coluzzi in West Africa is linked to increased expression of multiple gene families. BMC Genomics. 2015;16:146.PubMedPubMedCentral Toé KH, N’Falé S, Dabiré RK, Ranson H, Jones CM. The recent escalation in strength of pyrethroid resistance in Anopheles coluzzi in West Africa is linked to increased expression of multiple gene families. BMC Genomics. 2015;16:146.PubMedPubMedCentral
54.
go back to reference Kihampa C, Mato R. Distribution of pesticide residues in soil due to point source pollution at old Korogwe, Tanzania. Int J Biol Chem Sci. 2009;3:422–30. Kihampa C, Mato R. Distribution of pesticide residues in soil due to point source pollution at old Korogwe, Tanzania. Int J Biol Chem Sci. 2009;3:422–30.
55.
go back to reference Kishimba M. The status of pesticide pollution in Tanzania. Talanta. 2004;64:48–53.PubMed Kishimba M. The status of pesticide pollution in Tanzania. Talanta. 2004;64:48–53.PubMed
57.
go back to reference Zacharia JT, Kishimba MA, Masahiko H. Biota uptake of pesticides by selected plant species; the case study of Kilombero sugarcane plantations in Morogoro Region, Tanzania. Pestic Biochem Physiol. 2010;97:71–5. Zacharia JT, Kishimba MA, Masahiko H. Biota uptake of pesticides by selected plant species; the case study of Kilombero sugarcane plantations in Morogoro Region, Tanzania. Pestic Biochem Physiol. 2010;97:71–5.
58.
go back to reference Kishimba M, Mihale M. Levels of pesticide residues and metabolites in soil at Vikuge farm, Kibaha district, Tanzania—a classic case of soil contamination by obsolete pesticides. Tanzan J Sci. 2009;30:77–86. Kishimba M, Mihale M. Levels of pesticide residues and metabolites in soil at Vikuge farm, Kibaha district, Tanzania—a classic case of soil contamination by obsolete pesticides. Tanzan J Sci. 2009;30:77–86.
59.
go back to reference Henry L, Kishimba M. Levels of pesticide residues in water, soil and sediments from southern Lake Victoria and its basin. Tanzan J Sci. 2004;29:77–89. Henry L, Kishimba M. Levels of pesticide residues in water, soil and sediments from southern Lake Victoria and its basin. Tanzan J Sci. 2004;29:77–89.
60.
go back to reference Elfvendahl S, Mihale M, Kishimba MA, Kylin H. Pesticide pollution remains severe after cleanup of a stockpile of obsolete pesticides at Vikuge, Tanzania. AMBIO J Hum Environ. 2004;33:503–8. Elfvendahl S, Mihale M, Kishimba MA, Kylin H. Pesticide pollution remains severe after cleanup of a stockpile of obsolete pesticides at Vikuge, Tanzania. AMBIO J Hum Environ. 2004;33:503–8.
61.
go back to reference Hellar H, Kishimba M. Pesticide residues in water from TPC sugarcane plantations and environs, Kilimanjaro region, Tanzania. Tanzan J Sci. 2005;31:1–22. Hellar H, Kishimba M. Pesticide residues in water from TPC sugarcane plantations and environs, Kilimanjaro region, Tanzania. Tanzan J Sci. 2005;31:1–22.
62.
go back to reference Ngowi AV. Health impact of exposure to pesticides in agriculture in Tanzania. Tampere: Tampere University Press: Taju; 2002. Ngowi AV. Health impact of exposure to pesticides in agriculture in Tanzania. Tampere: Tampere University Press: Taju; 2002.
63.
go back to reference Kiwango P, Kassim N, Kimanya M. Pesticide residues in vegetables: practical interventions to minimize the risk of human exposure in Tanzania. Curr J Appl Sci Technol. 2018;26:1–18. Kiwango P, Kassim N, Kimanya M. Pesticide residues in vegetables: practical interventions to minimize the risk of human exposure in Tanzania. Curr J Appl Sci Technol. 2018;26:1–18.
65.
go back to reference Kapeleka JA, Lekei EE, Hagali T. Pesticides exposure and biological monitoring of Ache activity among commercial farm workers in Tanzania: a case of tea estates. Int J Sci Res. 2013;6:1708–13. Kapeleka JA, Lekei EE, Hagali T. Pesticides exposure and biological monitoring of Ache activity among commercial farm workers in Tanzania: a case of tea estates. Int J Sci Res. 2013;6:1708–13.
66.
go back to reference Stadlinger N, Mmochi AJ, Dobo S, Gyllbäck E, Kumblad L. Pesticide use among smallholder rice farmers in Tanzania. Environ Dev Sustain. 2011;13:641–56. Stadlinger N, Mmochi AJ, Dobo S, Gyllbäck E, Kumblad L. Pesticide use among smallholder rice farmers in Tanzania. Environ Dev Sustain. 2011;13:641–56.
67.
go back to reference Kariathi V, Kassim N, Kimanya M. Pesticide exposure from fresh tomatoes and its relationship with pesticide application practices in Meru district. Cogent Food Agric. 2016;2:1196808. Kariathi V, Kassim N, Kimanya M. Pesticide exposure from fresh tomatoes and its relationship with pesticide application practices in Meru district. Cogent Food Agric. 2016;2:1196808.
68.
go back to reference Mrema EJ, Ngowi AV, Kishinhi SS, Mamuya SH. Pesticide exposure and health problems among female horticulture workers in Tanzania. Environ Health Insights. 2017;11:117863021771523. Mrema EJ, Ngowi AV, Kishinhi SS, Mamuya SH. Pesticide exposure and health problems among female horticulture workers in Tanzania. Environ Health Insights. 2017;11:117863021771523.
69.
go back to reference Ngowi AVF, Mbise TJ, Ijani ASM, London L, Ajayi OC. Pesticides use by smallholder farmers in vegetable production in Northern Tanzania. Crop Prot Guildf Survey. 2007;26:1617–24. Ngowi AVF, Mbise TJ, Ijani ASM, London L, Ajayi OC. Pesticides use by smallholder farmers in vegetable production in Northern Tanzania. Crop Prot Guildf Survey. 2007;26:1617–24.
70.
go back to reference Kariathi V, Neema K, Martin K. Risk of exposures of pesticide residues from tomato in Tanzania. Afr J Food Sci. 2017;11:255–62. Kariathi V, Neema K, Martin K. Risk of exposures of pesticide residues from tomato in Tanzania. Afr J Food Sci. 2017;11:255–62.
71.
go back to reference Lema E, Machunda R, Njau K. Agrochemicals use in horticulture industry in Tanzania and their potential impact to water resources. Int J Biol Chem Sci. 2014;8:831. Lema E, Machunda R, Njau K. Agrochemicals use in horticulture industry in Tanzania and their potential impact to water resources. Int J Biol Chem Sci. 2014;8:831.
72.
go back to reference Reid MC, McKenzie FE. The contribution of agricultural insecticide use to increasing insecticide resistance in African malaria vectors. Malar J. 2016;15:107.PubMedPubMedCentral Reid MC, McKenzie FE. The contribution of agricultural insecticide use to increasing insecticide resistance in African malaria vectors. Malar J. 2016;15:107.PubMedPubMedCentral
73.
go back to reference Kihampa C, Ram Mato R, Mohamed H. Levels of pesticide residues in irrigation effluent from tomato fields in Owiro Estate, Tanzania. Int J Biol Chem Sci. 2010;4:601–7. Kihampa C, Ram Mato R, Mohamed H. Levels of pesticide residues in irrigation effluent from tomato fields in Owiro Estate, Tanzania. Int J Biol Chem Sci. 2010;4:601–7.
74.
go back to reference Kihampa C, Ram Mato R, Mohamed H. Residues of organochlorinated pesticides in soil from tomato fields, Ngarenanyuki, Tanzania. J Appl Sci Environ Manag. 2010;14:37–40. Kihampa C, Ram Mato R, Mohamed H. Residues of organochlorinated pesticides in soil from tomato fields, Ngarenanyuki, Tanzania. J Appl Sci Environ Manag. 2010;14:37–40.
75.
go back to reference Lekei EE, Ngowi AV, London L. Farmers’ knowledge, practices and injuries associated with pesticide exposure in rural farming villages in Tanzania. BMC Public Health. 2014;14:389.PubMedPubMedCentral Lekei EE, Ngowi AV, London L. Farmers’ knowledge, practices and injuries associated with pesticide exposure in rural farming villages in Tanzania. BMC Public Health. 2014;14:389.PubMedPubMedCentral
76.
go back to reference Lekei EE, Ngowi AV, London L. Pesticide retailers’ knowledge and handling practices in selected towns of Tanzania. Environ Health. 2014;13:79.PubMedPubMedCentral Lekei EE, Ngowi AV, London L. Pesticide retailers’ knowledge and handling practices in selected towns of Tanzania. Environ Health. 2014;13:79.PubMedPubMedCentral
77.
go back to reference Sattler MA, Mtasiwa D, Kiama M, Premji Z, Tanner M, Killeen GF, et al. Habitat characterization and spatial distribution of Anopheles sp. mosquito larvae in Dar es Salaam (Tanzania) during an extended dry period. Malar J. 2005;4:4.PubMedPubMedCentral Sattler MA, Mtasiwa D, Kiama M, Premji Z, Tanner M, Killeen GF, et al. Habitat characterization and spatial distribution of Anopheles sp. mosquito larvae in Dar es Salaam (Tanzania) during an extended dry period. Malar J. 2005;4:4.PubMedPubMedCentral
78.
go back to reference Emidi B, Kisinza WN, Mmbando BP, Malima R, Mosha FW. Effect of physicochemical parameters on Anopheles and Culex mosquito larvae abundance in different breeding sites in a rural setting of Muheza, Tanzania. Parasit Vectors. 2017;10:304.PubMedPubMedCentral Emidi B, Kisinza WN, Mmbando BP, Malima R, Mosha FW. Effect of physicochemical parameters on Anopheles and Culex mosquito larvae abundance in different breeding sites in a rural setting of Muheza, Tanzania. Parasit Vectors. 2017;10:304.PubMedPubMedCentral
79.
go back to reference Awolola TS, Oduola AO, Obansa JB, Chukwurar NJ, Unyimadu JP. Anopheles gambiae s.s. breeding in polluted water bodies in urban Lagos, southwestern Nigeria. J Vector Borne Dis. 2007;44:241–4.PubMed Awolola TS, Oduola AO, Obansa JB, Chukwurar NJ, Unyimadu JP. Anopheles gambiae s.s. breeding in polluted water bodies in urban Lagos, southwestern Nigeria. J Vector Borne Dis. 2007;44:241–4.PubMed
80.
go back to reference Oliver SV, Brooke BD. The effect of metal pollution on the life history and insecticide resistance phenotype of the major malaria vector Anopheles arabiensis (Diptera: Culicidae). PLoS ONE. 2018;13:e0192551.PubMedPubMedCentral Oliver SV, Brooke BD. The effect of metal pollution on the life history and insecticide resistance phenotype of the major malaria vector Anopheles arabiensis (Diptera: Culicidae). PLoS ONE. 2018;13:e0192551.PubMedPubMedCentral
81.
go back to reference Kabula BI, Attah PK, Wilson MD, Boakye DA. Characterization of Anopheles gambiae s.l. and insecticide resistance profile relative to physicochemical properties of breeding habitats within Accra Metropolis. Ghana. Tanzania J Health Res. 2011;13:25. Kabula BI, Attah PK, Wilson MD, Boakye DA. Characterization of Anopheles gambiae s.l. and insecticide resistance profile relative to physicochemical properties of breeding habitats within Accra Metropolis. Ghana. Tanzania J Health Res. 2011;13:25.
82.
83.
go back to reference Imam A, Deeni Y. Larval productivity, and detoxification enzymes profile in response to physico-chemical environmental factors of Anopheles gambiae breeding ecologies in Nigeria. Br J Appl Sci Technol. 2015;5:595–612. Imam A, Deeni Y. Larval productivity, and detoxification enzymes profile in response to physico-chemical environmental factors of Anopheles gambiae breeding ecologies in Nigeria. Br J Appl Sci Technol. 2015;5:595–612.
84.
go back to reference Djouaka RF, Bakare AA, Bankole HS, Doannio JM, Coulibaly ON, Kossou H, et al. Does the spillage of petroleum products in Anopheles breeding sites have an impact on the pyrethroid resistance? Malar J. 2007;6:159.PubMedPubMedCentral Djouaka RF, Bakare AA, Bankole HS, Doannio JM, Coulibaly ON, Kossou H, et al. Does the spillage of petroleum products in Anopheles breeding sites have an impact on the pyrethroid resistance? Malar J. 2007;6:159.PubMedPubMedCentral
85.
go back to reference Nkya TE, Akhouayri I, Kisinza W, David J-P. Impact of environment on mosquito response to pyrethroid insecticides: facts, evidences and prospects. Insect Biochem Mol Biol. 2013;43:407–16.PubMed Nkya TE, Akhouayri I, Kisinza W, David J-P. Impact of environment on mosquito response to pyrethroid insecticides: facts, evidences and prospects. Insect Biochem Mol Biol. 2013;43:407–16.PubMed
86.
go back to reference Tene Fossog B, Antonio-Nkondjio C, Kengne P, Njiokou F, Besansky NJ, Costantini C. Physiological correlates of ecological divergence along an urbanization gradient: differential tolerance to ammonia among molecular forms of the malaria mosquito Anopheles gambiae. BMC Ecol. 2013;13:1.PubMedPubMedCentral Tene Fossog B, Antonio-Nkondjio C, Kengne P, Njiokou F, Besansky NJ, Costantini C. Physiological correlates of ecological divergence along an urbanization gradient: differential tolerance to ammonia among molecular forms of the malaria mosquito Anopheles gambiae. BMC Ecol. 2013;13:1.PubMedPubMedCentral
87.
go back to reference Antonio-Nkondjio C, Youmsi-Goupeyou M, Kopya E, Tene-Fossog B, Njiokou F, Costantini C, et al. Exposure to disinfectants (soap or hydrogen peroxide) increases tolerance to permethrin in Anopheles gambiae populations from the city of Yaoundé, Cameroon. Malar J. 2014;13:296.PubMedPubMedCentral Antonio-Nkondjio C, Youmsi-Goupeyou M, Kopya E, Tene-Fossog B, Njiokou F, Costantini C, et al. Exposure to disinfectants (soap or hydrogen peroxide) increases tolerance to permethrin in Anopheles gambiae populations from the city of Yaoundé, Cameroon. Malar J. 2014;13:296.PubMedPubMedCentral
88.
go back to reference Tene Fossog B, Kopya E, Ndo C, Menze-Djantio B, Costantini C, Njiokou F, et al. Water quality and Anopheles gambiae larval tolerance to pyrethroids in the Cities of Douala and Yaoundé (Cameroon). J Trop Med. 2012;2012:1–10. Tene Fossog B, Kopya E, Ndo C, Menze-Djantio B, Costantini C, Njiokou F, et al. Water quality and Anopheles gambiae larval tolerance to pyrethroids in the Cities of Douala and Yaoundé (Cameroon). J Trop Med. 2012;2012:1–10.
89.
go back to reference van den Berg H, Zaim M, Yadav RS, Soares A, Ameneshewa B, Mnzava A, et al. Global trends in the use of insecticides to control vector-borne diseases. Environ Health Perspect. 2012;120:577–82.PubMedPubMedCentral van den Berg H, Zaim M, Yadav RS, Soares A, Ameneshewa B, Mnzava A, et al. Global trends in the use of insecticides to control vector-borne diseases. Environ Health Perspect. 2012;120:577–82.PubMedPubMedCentral
90.
go back to reference Stuck L, Lutambi A, Chacky F, Schaettle P, Kramer K, Mandike R, et al. Can school-based distribution be used to maintain coverage of long-lasting insecticide-treated bed nets: evidence from a large scale programme in southern Tanzania? Health Policy Plan. 2017;32:980–9.PubMed Stuck L, Lutambi A, Chacky F, Schaettle P, Kramer K, Mandike R, et al. Can school-based distribution be used to maintain coverage of long-lasting insecticide-treated bed nets: evidence from a large scale programme in southern Tanzania? Health Policy Plan. 2017;32:980–9.PubMed
92.
go back to reference Hanson K, Marchant T, Nathan R, Mponda H, Jones C, Bruce J, et al. Household ownership and use of insecticide-treated nets among target groups after implementation of a national voucher programme in the United Republic of Tanzania: plausibility study using three annual cross sectional household surveys. BMJ. 2009;339:b2434.PubMedPubMedCentral Hanson K, Marchant T, Nathan R, Mponda H, Jones C, Bruce J, et al. Household ownership and use of insecticide-treated nets among target groups after implementation of a national voucher programme in the United Republic of Tanzania: plausibility study using three annual cross sectional household surveys. BMJ. 2009;339:b2434.PubMedPubMedCentral
93.
go back to reference WHOPES. Review of spinosad 0.5% GR & 12% SC lambda-cyhalothrin 10% CS K-O TAB 1-2-3 Interceptor. Geneva: World Health Organization; 2007. WHOPES. Review of spinosad 0.5% GR & 12% SC lambda-cyhalothrin 10% CS K-O TAB 1-2-3 Interceptor. Geneva: World Health Organization; 2007.
94.
go back to reference WHO. Review of olyset nets and bifenthrin 10%WP. Geneva: World Health Organization; 2001. WHO. Review of olyset nets and bifenthrin 10%WP. Geneva: World Health Organization; 2001.
Metadata
Title
Dynamics and monitoring of insecticide resistance in malaria vectors across mainland Tanzania from 1997 to 2017: a systematic review
Authors
Deokary Joseph Matiya
Anitha B. Philbert
Winifrida Kidima
Johnson J. Matowo
Publication date
01-12-2019
Publisher
BioMed Central
Keyword
Malaria
Published in
Malaria Journal / Issue 1/2019
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-019-2738-6

Other articles of this Issue 1/2019

Malaria Journal 1/2019 Go to the issue