To date, An. funestus has been shown resistant to major insecticides used in public health across Africa (Dia et al., 2013, Brown, 1986, Ranson et al., 2011, Coetzee and Koekemoer, 2013, Wondji et al., 2009, Wondji et al., 2012) (See Table 1.3 and Figure 1.14). However, pattern of resistance to insecticides differ across regions of Africa and this may have impact on insecticide resistance management strategies, because variation in the resistance pattern makes extrapolation from one locality to another, one region to another,or one country to another not feasible.
1.7.2.1 Southern Africa:
First report of pyrethroid resistance in An. funestus was in South Africa. After ~40 years of annual spray with DDT and eradication of An. funestus from South Africa, a switch to pyrethroid deltamethrin in Kwazulu/Natal (KZN) Province of South Africa in 1996 resulted in six-fold increase in malaria incidence by 1999 (Hargreaves et al., 2000). The surge in malaria incidence in KZN was due to a highly endophilic An. funestus, established to be resistant to pyrethroid insecticides. Thereafter, in
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2001 Brooke (Brooke et al., 2001) reported high Type II pyrethroids and propoxur resistance in An. funestus from southern Mozambique, and in 2006 An. funestus highly resistant to Type II pyrethroids deltamethrin and ʎ-cyahalothrin were described from southern Mozambique (Casimiro et al., 2006). The population from Mozambique were also resistant to permethrin and marginally resistant to bendiocarb and propoxur, but fully susceptible to malathion and DDT.
Since then rapidly growing resistance to pyrethroids insecticides (Coetzee et al., 2013) as well as multiple resistant populations of An. funestus have been continuously reported in southern Africa. For example, Cuamba and colleagues in 2010 reported highly pyrethroid resistant populations of An. funestus from Chokwe, Mozambique (Cuamba et al., 2010), a region from which pyrethroid susceptibility have been described by Casimiro (Casimiro et al., 2006). In Malawi, high and multiple resistance to pyrethroids permethrin and deltamethrin as well as carbamates bendiocarb and propoxur were reported in 2010 (Hunt et al., 2010) in An. funestus population that are in turn fully susceptible to malathion, fenitrothion, pirimiphos methyl, dieldrin and DDT. A contrasting pattern of resistance was observed in Zambian populations of An. funestus (Chanda et al., 2011) that were found to be pyrethroid and DDT-resistant but susceptible to malathion consistent with other southern African populations. The Zambian population were also susceptible to bendiocarb in contrast to the Malawian and Mozambican populations described above.
The increase in pyrethroid resistance in An. funestus became finally selected: “pyrethroid resistance has been selected in Malawi over the last 3 years in the two major malaria vectors An. gambiae and An. funestus, with a higher frequency of resistance in the latter” (Wondji et al., 2012). Wondji and colleagues found that An. funestus from the Chikwawa, Malawi are resistant to the carbamate, bendiocarb and three pyrethroids (permethrin, deltamethrin and λ-cyhalothrin) and susceptible to DDT and pirimiphos methyl. This pattern of pyrethroid resistance for permethrin and deltamethrin was further confirmed in An. funestus population from Malawi and Mozambique, with Mozambican population exhibiting higher resistance with no mortality recorded after 1h, 30 minutes exposure to discriminating dose of pyrethroids (Riveron et al., 2013).
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Table 1.3 Mechanism of resistance in An. funestus to main insecticide used in public health
Country
Insecticides
Resistance Mechanism
Reference
South Africa Pyrethroids, Type II N.D. (Hargreaves et al., 2000) Mozambique Pyrethroids, Type I and II, propoxur Mixed function oxidases (Brooke et al., 2001) Mozambique Pyrethroids, Type I and II, bendiocarb, propoxur Mixed function oxidases (Casimiro et al., 2006) Mozambique Pyrethroids, Type I and II P450 monoxygenases: CYP6P9a, CYP6P9b (Cuamba et al., 2010) Malawi Pyrethroids, Type I and II, bendiocarb, propoxur N.D. (Hunt et al., 2010) Zambia Pyrethroids, Type I and II, DDT N.D. (Chanda et al., 2011) Malawi Pyrethroids, Type I and II, bendiocarb P450 monoxygenases: CYP6P9a, CYP6P9b (Wondji et al., 2012) Uganda Pyrethroids, Type I and II, DDT P450 monoxygenases: CYP6P9a, CYP6P9b (Morgan et al., 2010) Kenya Pyrethroids, Type I and II, DDT Mixed function oxidases (McCann et al., 2014), (Kawada et al., 2011) Uganda Pyrethroids, Type I and II, DDT P450 monoxygenases: CYP6P9a, CYP6P9b (Mulamba et al., 2014b)
Ghana Pyrethroids, Type I, DDT Mixed function oxidases (Okoye et al., 2008) Ghana Bendiocarb, DDT N.D. (Hunt et al., 2011) Burkina Faso Dieldrin Rdl mutation (Dabire et al., 2007), (Wondji
et al., 2011) Benin Pyrethroids, Type I and II, DDT, bendiocarb CYP6P9b, CYP6Z1; GSTs: GSTδ1_5, GSTe2P450 monoxygenases: CYP6P9a, (Djouaka et al., 2011) Benin Pyrethroids, Type I, DDT GSTe2 (Riveron et al., 2014b)
N.D. Resistance mechanism not determined.
Figure 1.14: Insecticide resistance in An. funestus in Africa. Symbols indicate the presence of resistance in a country, and their position is not representative of actual geographical sites. Abbreviation: DDT, dichlorodiphenyltrichloroethane; DR Congo, Democratic Republic of the Congo. Adapted from (Coetzee and Koekemoer, 2013).
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These and other studies not cited established that southern African An. funestus (from Malawi, Mozambique and Zambia) are resistant to pyrethroids and the resistance had been steeply increasing. While Malawian and Mozambican populations were resistant to carbamates bendiocarb and propoxur but susceptible to DDT, in contrast, Zambian population were resistant to DDT but susceptible to bendiocarb (Coetzee and Koekemoer, 2013). And all populations from these three countries were fully sensitive to organophosphate malathion and organochlorine dieldrin.
1.7.2.2 East Africa
Prior to 2010 there was no in-depth report on the resistance status of An. funestus to major insecticides used in public health in Uganda. In 2010, pyrethroid resistance was described in An. funestus from Uganda (Morgan et al., 2010). The population from Tororo was highly resistant to pyrethroids, marginally resistant to DDT, but fully susceptible to carbamate bendiocarb and organophosphates malathion and organochlorine dieldrin. Pyrethroids (permethrin and deltamethrin) and DDT resistance was reported as well in some populations of An. funestus from Masindi, north- western Uganda (Mulamba et al., 2014a) confirming the observations of Morgan and colleagues. This pattern of resistance was confirmed as increasing across Uganda and in Kisumu, western Kenya. Widespread resistance to Type I and Type II pyrethroids and DDT was recently confirmed by Mulamba and colleagues (Mulamba et al., 2014b) in An. funestus from several localities across Uganda, as well as populations from Kisumu, Kenya. However, as observed in the previous studies full susceptibility to bendiocarb, malathion and dieldrin was reported in these Ugandan and Kenyan populations.
After long term implementation of insecticide treated bed nets in western Kenya, An. funestus
re-emerged as a major malarial vector in 2008 (McCann et al., 2014) with high infection rate and resistance to permethrin and deltamethrin, with mortalities lower than obtained with An. gambiae
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1.7.2.3 West and Central Africa
Reliable literature on resistance status of An. funestus from West and Central Africa is only published from studies carried out in Benin, Ghana, Burkina Faso and Cameroon (Coetzee and Koekemoer, 2013).
In Ghana, in 2006 An. funestus and An. gambiae were described as the major vector species in Obuasi gold mine (Coetzee et al., 2006) with the An. funestus from the study resistant to DDT and bendiocarb but susceptible to pyrethroids and malathion. A follow up study in this locality (Okoye et al., 2008) confirmed DDT resistance and discovered in addition resistance to permethrin. Further studies documented pyrethroid resistance in other regions of Ghana including Kassena-Nankana district (Anto et al., 2009) and four other localities were resistance to bendiocarb and DDT was discovered (Hunt et al., 2011). However, the populations tested from all localities by Hunt and colleagues were 100% susceptible to deltamethrin and malathion.
In contrast, in Burkina Faso study carried out in three sites confirmed that An. funestus
populations were resistant to dieldrin but susceptible to pyrethroids and DDT (Dabire et al., 2007). Few years later another study published a result in agreement with the previous observation. In An. funestus populations from Burkina Faso and Cameroon, Wondji and colleagues (Wondji et al., 2011) reported high dieldrin resistance while Southern (Malawi and Mozambique) and East African (Ugandan) populations were fully susceptible to this insecticide. However, within the last few decades few researches have been conducted in Burkina Faso, Cameroon and other neighbouring West African countries to establish resistance status of An. funestus populations toward pyrethroids and other insecticides used in public health.
In 2011 multiple resistant populations of An. funestus were reported in Pahou, southern Benin, West Africa (Djouaka et al., 2011). In contrast with the findings in most southern African populations (susceptibility to DDT and high resistance to Type I and Type II pyrethroids), the
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population from Benin were highly resistant to DDT with no mortality in females at all after one hour exposure. The population were also resistant to permethrin and deltamethrin (moderate), as well as bendiocarb. In line with the observations from Burkina Faso and Cameroon, the population from Benin exhibited moderate resistance to dieldrin as well. Full susceptibility to malathion was observed in line with the observation all across Africa. Further study in population of An. funestus from Kpome, Benin Republic and Gounougou, Cameroon confirmed that the populations from Kpome were highly resistant to DDT (just like in Pahou), and revealed moderate resistance to the organochlorine in the population from Gounougou, Cameroon (Riveron et al., 2014b).
In essence, across Africa, insecticide resistance in An. funestus show contrasting pattern and is increasing (Nkya et al., 2013), possibly due to selection pressure from agricultural practices and escalated usage of insecticides used in public health related vector controls.