Mechanisms of insect resistance to the main insecticide families of public health interest
1. Introduction
Malaria is still a major burden causing the death of nearly 655,000 people each year, mostly in children under the age of five, and affecting those living in the poorest countries [1]. Currently, the major obstacles to malaria control and elimination are the absence of a protective vaccine, the spread of parasite resistance to anti-malarial drugs and the mosquito resistance to insecticides [2]. Controlling mosquito vectors is fundamental to reduce mosquito-borne diseases by targeting vectorial capacity and hence the transmission. Vector control through the use of chemicals for mosquito bed nets and indoor residual spraying is still the cornerstone of malaria prevention [1]. Unfortunately, the extensive use of insecticides since the 1950s has led to the development of strong resistance worldwide hence representing a major public health problem where insecticidal vector control is implemented. Here, we propose to review the current level, distribution and mechanisms of insecticide résistance in malaria vectors and address their impact on the efficacy of vector control interventions. Strategies to prevent and/or delay the spread of insecticide resistance in natural mosquito populations are also discussed.
2. Definition of resistance
According to the
Resistance has been observed in more than 500 insect species worldwide among which more than 50
lt is commonly accepted that the enhanced metabolism and target site modifications are responsible for high level of insecticide resistance in malaria vectors. To date, malaria vectors have developed resistance to the main chemical classes used in public health (i.e. pyrethroids, DDT, carbamates and organophosphates) (table 1) and the occurrence of cross-resistance
3. History of resistance to public health insecticides
Since the humans used chemicals for crop protection and/or the prevention of vector borne diseases, cases of resistances have been reported [11, 12]. Insecticides used for malaria control have included organochlorine, organophosphorus, carbamate, and pyrethroid insecticides, with the latter now taking increasing market share for both indoor residual spraying and Long Lasting Insecticidal mosquito Nets (LLINs) programmes [13]. Resistance has naturally tended to follow the use and switches of these insecticides [5].
|
Historically, DDT was first introduced for mosquito control and malaria eradication programme in 1946. The first case of DDT resistance was reported in
Similar trend was noted in Central America and the Caribbean. Dieldrin spraying against
Much less information is however available for South East Asian malaria vectors, most probably because resistance monitoring was not carried out in routine before the 80s. In Vietnam, DDT resistance was found in 1989 in
In Africa, resistance was initially found in
After the 80s, DDT has been more or less abandoned worldwide and replaced by organophosphate (OP), pyrethroids and, to lesser extent, carbamates. However, insecticide resistance continued to be a problem, and vector control operations were affected, particularly in India, Africa and Latin America, by extensive use of agricultural pesticides. OP resistance, either in the form of broad-spectrum OP resistance or malathion-specific resistance was found in the major malaria vector species worldwide [12]. Pyrethroids were introduced in late 70s in public health and increasingly used in the 90s; however, cases of resistance were rapidly reported in the main malaria vectors worldwide including
It is obvious that insecticide resistance in malaria vectors is increasing worldwide due to the increasing selection pressure on mosquito populations caused by the presence of urban, domestic and/or agricultural pollutants in the environment [50]. Transversal and longitudinal monitoring surveys are essential to address the spatio-temporal changes in resistance (dynamic) and to design appropriate strategies for a better control of resistant malaria vector populations worldwide.
4. Resistance mechanisms
The various mechanisms that enable insects to resist the action of insecticides can be grouped into four distinct categories including metabolic resistance, target-site resistance, reduce penetration and behavioral avoidance. These mechanisms that are shown in the figure 1 are briefly described in the following sections.
4.1. Metabolic resistance
Metabolic resistance is the most common resistance mechanism that occurs in insects. This mechanism is based on the enzyme systems which all insects possess to help them to detoxify naturally occurring xenobiotics/insecticides. It is commonly accepted that insect detoxification systems derived from the plant-insect evolutionary arm race and several insect detoxification enzymes have been associated to the detoxification of plant toxins and all types of chemicals, including insecticides [51]. Over-expression of enzymes capable of detoxifying insecticides or amino acid substitutions within these enzymes, which alter the affinity of the enzyme for the insecticide, can result in high levels of insecticide resistance (see [52] for review). Increased expression of the genes encoding the major xenobiotic metabolizing enzymes is the most common cause of insecticide resistance in mosquitoes. Over expression of detoxyfing enzymes can occur as the result of gene amplification (e.g. duplication) or due to changes in either trans-acting regulator elements or in the promoter region of the gene [5, 53, 54]. The consequence is a significant increase of enzyme production in resistant insects that enables them to metabolize or degrade insecticides before they are able to exert a toxic effect. Three categories of enzymes, namely esterases, P450s and glutathione-S-transferases are known to confer resistance to insecticides in insect pest such as malaria vectors. These large enzyme families contain multiple enzymes with broad overlapping substrate specificities, and one member of the family might be capable of metabolizing limited number of insecticides. Similarly, the level of resistance conferred can vary from low to very high and may differ from compound to compound. Metabolic resistance mechanisms have been identified in mosquito populations for all major classes of insecticides currently used for vector control, including organochlorine, organophosphates, carbamates, and pyrethroids.
Glutathione S-transferases (GSTs). Glutathione transferases (GSTs) are multifunctional enzymes involved in the detoxification of many endogenous and xenobiotic compounds. Conjugation of Glutathione (GSH) to such organic molecules enhances solubility, thus facilitating their eventual elimination [78]. Elevated GST activity has been implicated in resistance to at least four classes of insecticides in insects. Higher enzyme activity is usually due to an increase in the amount of one or more GST enzymes, either as a result of gene amplification or more commonly through increases in transcriptional rate, rather than qualitative changes in individual enzymes [52]. At least six classes of insect GSTs have been identified in
Despite the great advance obtained recently in the identification of the role of detoxifying enzymes in insecticide resistance, force is to note that the function of >90% of metabolic genes is still unknown. Although only a limited number of resistance mechanisms have been implicated to date, the diversity within enzyme families involved in metabolic resistance is likely to contribute substantially to resistance to many insecticide classes. Further functional genomics and post-genomic technology are needed to reveal the contributions of hitherto unsuspected enzymes in insecticide metabolism and/or sequestration and to identify the causal mutations associated with metabolic resistance in mosquitoes. The contribution that these enzymes make towards various insecticide resistance phenotypes in malaria vectors is yet to be elucidated.
4.2. Target-site resistance
The second most common resistance mechanism encountered in insects is target-site resistance. Insecticides generally act at a specific site within the insect, typically within the nervous system (e.g. OP, carbamate, DDT and pyrethroid insecticides). The site of action can be modified in resistant strains of insects such that the insecticide no longer binds effectively. Reduce sensitivity of the target receptors to insecticide results from non-silent point mutations in the gene encoding the protein. For example, the target site for OP and carbamate insecticides is acetylcholinesterase (AChE) in the nerve cell synapses. Several mutations in the gene encoding for an acetylcholinesterase have been found in insects” [87] which result in reduced sensitivity to inhibition of the enzyme by these insecticides [88, 89]. In malaria vectors, the G119S mutation (i.e. glycine to serine substitution at position 119) responsible for carbamate and OP resistance has been reported in
4.3. Reduced penetration
Modifications in the insect cuticle or digestive tract linings that prevent or slow the absorption or penetration of insecticides can be found is some resistant insects. This resistance mechanism is not specific and can affect a broad range of insecticides. Reduced uptake of insecticide, often referred to as cuticular resistance, is frequently described as a minor resistance mechanism. Certainly for pests where the major route of insecticide delivery is via ingestion, this is likely to be the case. However, for malaria control, where insecticides are typically delivered on bed nets or on wall surfaces, uptake of insecticides is primarily through the appendages. An increase in the thickness of the tarsal cuticle, or a reduction in its permeability to lipophilic insecticides, could have a major impact on the bioavailability of an insecticide
4.4. Behavioural resistance
Insecticide resistance in mosquitoes is not always based on biochemical mechanisms such as metabolic detoxification or target site mutations, but may also be conferred by behavioural changes in response to prolonged exposure to an insecticide. Behavioural resistance does not have the same “importance” as physiological resistance but may be considered to be a contributing factor, leading to the avoidance of lethal doses of an insecticide [106, 107]. For example, the first study on the irritant effect of DDT residual deposits was conducted using
5. Method to detect insecticide resistance
Currently most resistance monitoring is dependent on bioassays, using fixed insecticide concentrations and exposure times, and the data is reported as percentage mortality and/or Knock Down (KD) effect. The World Health Organisation (WHO) has defined diagnostic doses (i.e. twice the dosage that killed 100% susceptible mosquitoes of a given species) for most insecticides used in malaria control and produces susceptibility test kits consisting of exposure chambers and insecticide treated filter papers [113-115]. Although simple to perform, these diagnostic dose assays provide limited information and several alternative methods for detecting resistance are available (Table 2). These alternative assays generally detect specific resistance mechanisms, and should always be performed as an addition, not a substitute, to bioassays, to avoid the risk that unknown resistance mechanisms go undetected. It should be noted that none of the current methods listed in Table 2 are suitable for detecting cuticular and/or behavioural resistance. Regular monitoring for insecticide resistance is essential in order to react proactively to prevent insecticide resistance from compromising control. If the frequency of resistance alleles is going to build up unchecked, resistance may eventually become ‘fixed’ in the populations. Once resistance reaches very high levels, strategies to restore susceptibility are unlikely to be effective.
|
|
|
Bioassays using WHO defined diagnostic doses of insecticide | Standardized, simple to perform, detect resistance regardless of mechanism | Lack sensitivity and provide no information about level and type of resistance (except when using with synergists), to be done on live mosquitoes |
Dose response bioassays | Provides data on level of resistance in population, regardless of mechanism | Require large numbers of alive mosquitoes, and data from different groups not readily comparable |
Biochemical assays to detect activity of enzymes associated with insecticide resistance | Provides information on specific mechanisms responsible for resistance | Requires cold chain. Not available for all resistance mechanisms, sensitivity and specificity issues for some assays (e.g. GST) |
Molecular assays to detect resistant alleles | Very sensitive. Can detect recessive alleles and therefore provide an ‘early warning’ of future resistance. | Requires specialized and costly equipment. Only available for a limited number of resistance mechanisms. |
5.1. Bioassays
Guidelines for test procedures and interpretation of results are available from the WHOPES World Health Organization Pesticide Evaluation Scheme
These diagnostic dose assays are simple to perform and provide standardized data sets that, assuming the guidelines are followed, can be readily compared to identify temporal and/or geographical variations in the resistant status of malaria vector populations. However, it is important to recognize some of the limitations of these susceptibility tests. As only a single concentration of insecticide is used, the results do not provide any information about the level of resistance in a population. For example if 50 % of population A and 20 % of population B were killed after exposure to the diagnostic dose of permethrin, it cannot be concluded that population B is more resistant than population A. The results only indicate that both populations are resistant (according to WHO definitions if there is < 80 % mortality, the population is defined as resistant) and that, subject to tests of significance, there is a higher frequency of resistant individuals in population B than in A. Dose response assays would be needed to compare the levels of resistance in two populations (e.g. by measuring the Resistant Ratios and their 95% confidence intervals). For pyrethroids, median knock down time (MKDT) is also a useful quantifiable variable [117]. Similarly, the results of these tests cannot be used to compare the levels of resistance to two different insecticides. If 50 % mortality was observed after exposure to the diagnostic dose of permethrin (0.75 %) whereas mortality was 70% after exposure to the diagnostic dose of deltamethrin (0.05%), it is not correct to state that the population is more resistant to permethrin than deltamethrin. Again, all that can be stated is that the population is resistant to both insecticides.
Partly due to the limitations of the diagnostic dose assays described above and partly due to the difficulties that are sometimes incurred in obtaining a regular supply of the insecticide impregnated papers from WHO, an alternative bioassay methodology has been developed [118] and is being adopted by some monitoring programmes. This method, known as the CDC bottle bioassay, uses glass bottles coated with a known concentration of insecticide. As these test kits are assembled in the users own laboratory, the concentration of insecticide can be readily adjusted enabling dose response curves to be developed to compare two or more strains. A caveat to this is that the flexibility, and the potential variation in the insecticide grade used in the tests, impairs comparison of results between two separate studies.
Both WHO diagnostic doses and CDC bottle bioassays can be modified to incorporate synergists. Synergists such as piperonyl butoxide, that block the activity of two major detoxification enzyme families, can be used to explore the role of different resistance mechanisms. If resistance is due to increased metabolism, exposure to an appropriate synergist prior to insecticide bioassays should increase the level of mortality observed.
5.2. Biochemical tests
Biochemical tests to detect alterations in activities of enzyme families associated with insecticide resistance have been available for over two decades and are sometimes used in combination with insecticide bioassays [119]. These assays employ model substrates to record the overall activity of glutathione transferases, carboxylesterases or cytochrome P450s in individual insects. Biochemical assays are also available to detect target site resistance to organophosphate and carbamate insecticides caused by insensitive acetylcholinesterase (AChE). The enzymatic reaction produces a colour change that is generally visible to the naked eye and hence these assays do not require access to expensive equipment (spectrophotometer is appropriate). However, it is important that the mosquitoes are kept on ice from the point of collection to the performance of the assay and this can often pose logistical challenges. Furthermore, there are sensitivity and specificity issues that limit the utility of some of these assays. For example, with over 100 different cytochrome P450 enzymes in malaria vectors, an assay that measures the total level or activity of this enzyme family may not have the sensitivity to detect over production of the single or small number of P450 enzymes that are thought to be involved in pyrethroid metabolism. This may explain the lack of significant correlation observed in many studies between cytochrome P450 activity and bioassay mortality results [120, 121]. In addition not all members of the enzyme family will have the same affinity for the model substrates used in these assays (e.g. CDNB (1-chloro 2-4, dinitrobenzene) is the substrate typically used to assess glutathione transferase activity but the Epsilon class of GSTs which are responsible for DDT resistance have relatively low activity with this substrate). In order to incorporate data from resistance monitoring into evidence based decisions on appropriate insecticide based interventions for malaria control, it is clearly essential that the data is both reliable and accessible. Although guidelines for conducting the various assays exist, there is little consensus on the number of sites and frequency with which resistance monitoring should occur [122]. It is clear that resistance is a dynamic trait, and wide fluctuations in resistance levels throughout the malaria transmission season have been reported [116, 123, 124]. Resistance can also be very focal, particularly when vector composition differs between sites [125], hence a minimum number of sampling sites should be established, taking into account patterns of vector distribution and insecticide usage. The WHO/AFRO African Network for Vector Resistance was established in 2000 and amongst its objectives was the important goal of improving the dissemination of resistance data. Accordingly a database was established to store the results of resistance monitoring activities by the African Network for Vector Resistance (ANVR) members but until recently, this database was not readily accessible by outside users. The recent establishment of new data base (see section 6), as an online centralized resource for collating data on insecticide resistance in disease vectors and the integration of this with the ANVR database, will hopefully ensure that both published and unpublished data on resistance in malaria vectors are more readily available to all interested parties.
5.3. Molecular tests
A multitude of molecular assays have been developed to detect
6. Current distribution of insecticide resistance
Insecticide resistance has been reported in the main malaria vectors worldwide. Resistance is however not uniformly distributed among vector species and can greatly differ from one village, province, country, region and continent to another. Unfortunately, the highest levels of insecticide resistance were reported in Africa where malaria burden is still the highest in the world [1]. Resistance to pyrethroids, the gold standard insecticides used for LLIN and IRS will be extensively discussed in the present chapter as it remains a real and ever-present danger to future success of malaria vector control. Note that more information on the distribution of insecticide resistance in malaria vectors can be found in
6.1. Africa
Although the occurrence of insecticide resistance in malaria vectors in Africa is not a “new“ event (see section 2.), the speed at which pyrethroid-resistance recently evolved in field populations is worrying as it may jeopardize the current malaria vector control initiatives carried out in the continent. As shown in figure 2, pyrethroid resistance in
Globally, pyrethroid resistance is high in
In Africa, the L1014F mutation is widespread (figure 2) and predominant in the molecular S form compared to the M form, except in Benin [168], Guinea Equatorial [8] and Niger [132]. Some authors suggested that the
Beyond the spread of
To conclude, the immense challenge in Africa will be not to manage and control
6.2. South-East Asia and India
The South East Asia Region (SEAR) that account for 13% of the total malaria cases worldwide (2nd position after Africa) [1] is not spare of insecticide resistance in the main malaria vector species.
In the Mekong region, cross-country monitoring of insecticide resistance has been conducted through the MALVECASIA network (http://www.itg.be/malvecasia/) to help MCPs in the choice of insecticide to use at regional level. Large differences in insecticide resistance status were observed among species and countries.
Insecticide resistance is known to be widespread in other part of Asia such as India. In this country, resistance has a long history (see section 2) and it represents a big challenge for malaria vector control. Among the
The same trend was noted in Sri Lanka where the main malaria vectors species, i.e.
In the delta region of Bangladesh, the
6.3. Latin America
The countries of the Amazon Basin (Bolivia, Brazil, Colombia, Ecuador, Guyana, Peru, Surinam and Venezuela) carry the greatest burden of malaria in the Americas. The primary vectors of this disease in the Amazon basin are
In Colombia, DDT resistance was reported in the late 80’s in some populations of
In neighboring countries, DDT, permethrin and deltamethrin resistance was found in laboratory colonized populations of
In Mexico, high level of DDT resistance and low levels of resistance to organophosphate, carbamate and pyrethroid insecticides were detected in field populations of
To our knowledge, it is the main “published” information available on the distribution, levels and mechanisms of resistance (i.e. accessible through Medline and pub med) in malaria vectors in Latin America. It is then essential to strengthen the capacity of all Latin America countries that suffering from malaria to make insecticide monitoring in routine to obtain much accurate information on the insecticide resistance situation in the malaria vectors. This will provide stake holders with useful information for the implementation of more effective and sustainable malaria control programmes in the region.
7. Impact of pyrethroid-resistance on programmatic malaria control
Few operational reports exist that measure the impact of pyrethroid resistance on epidemiological outcomes of malaria, owing to body of factors that mislead the attributable component of resistance. Where tentative evidence is provided in most cases, the design of the study has been observational and the effect of confounding factors can never be excluded with confidence, making difficult the interpretation of data.
Most probably, the only clearest evidence of control failure being directly linked to pyrethroid resistance was reported from the borders of Mozambique and South Africa. In 1996, the malaria control programme in KwaZulu Natal switched from using DDT to deltamethrin for indoor spraying. Within four years, notified malaria cases had increased about four fold,
Additional evidence was brought on the island of Bioko on the West African Coast. A malaria control strategy based on IRS with lambdacyhalothrin was launched by the Bioko Island Malaria Control Project (BIMCP) funded by the Government of Equatorial Guinea and a consortium of private donors led by Marathon Oil Corporation. One round of IRS using the pyrethroid deltamethrin (K-Orthrine WP50, Bayer Crop Sciences, Isando, South Africa) failed to curtail an increase in the population density of
Another programmatic study was conducted in the highland provinces of Burundi. Between 2002 and 2005, a well targeted vector control programme (conducted in foot of valleys only) combining IRS with pyrethroids and/or PermaNet 1.0 LLINs was initiated in one of the most affected island provinces, Karuzi [225]. Initially, one round per year of pyrethroid-IRS was carried out in all human dwellings and cattle sheds before the seasonal increase in transmission. LLIN distribution preceded the first IRS round in the same year. The S-form of
In a more recent observational study conducted in Malawi, the impact of pyrethroid resistance on operational malaria control has been assessed with more controversial evidence of resistance impacting pyrethroid-based vector control [161]. In this trial, pyrethroid-LLINs were distributed to communities in 2007 followed by a pilot campaign of IRS with lambdacyhalothrin supported by the President’s Malaria Initiatives between 2008-2010 within districts. A series of sentinel sites were established during these periods to track the effect of the increase in pyrethroid resistance in the local malaria vectors (
Similarly, in the Dielmo Village of Senegal, a longitudinal study of inhabitants was carried out between January, 2007, and December, 2010 [226]. In July, 2008, deltamethrin-LLINs were provided to all villagers and asymptomatic carriage of malaria parasites was assessed from cross-sectional surveys. Overall, the incidence density of malaria attacks decreased from 5.45 per 100 person-months before LLINs distribution in 2007 to 0.41 by August 2010, but increased sharply back to 4.57 between September and December, 2010, i.e, in less than 3 years after the distribution of LLINs. Within the same time frame, the malaria vector became gradually resistant to pyrethroids and the prevalence of the 1014F
Another recent study reports the presence of pyrethroid-resistance in malaria vectors
There have been extensive randomized controlled trials (RCTs) (phase III) in part of Africa aiming at investigating the efficacy of ITNs for malaria prevention [227], but very few have assessed how pyrethroid resistance might affect the effectiveness of such intervention. RCTs entail a set of communities randomly divided into groups, one that receives the novel form of vector control intervention, and comparison arms that often receive the old form of vector control tools or nothing. The key difficulty is that it is impossible to address the question to whether vector control would produce a smaller reduction in malaria if the vector mosquitoes are resistant than it would have done if they were susceptible, using RCT methods. This is simply because resistance is not an easy factor that can be allocated randomly to some communities and not to others. The distribution of resistance is patchy and its severity seems to differ from one location (village) to another. Moreover there may be more resistance or survival trend of mosquitoes in some villages than others because of variations in the quality of vector control operations, or in mosquito behavior [228, 229]. This is important to mention, because many health scientists regard evidence from randomized-controlled studies as the only reliable basis for decision-making in public health.
The first RCT that investigated the impact of pyrethroid-resistance on LLIN efficacy was conducted in the Korhogo area in the north of Côte d’Ivoire. The trial encompassed multiple villages where the 1014F
More recently, another RCT of LLINs and/or IRS was conducted in 28 villages in southern Benin, from 2007 to 2010 [231]. The objective of the study was to examine whether carbamate-IRS applied every 8 months, as practiced by the PMI programme in Benin provided additional benefit over LLINs (ie Permanet 2.0) in term of malaria prevention and management of pyrethroid resistance in malaria vectors. Results showed that combination of LLINs and IRS did not reduce malaria transmission and morbidity compared to LLIN alone in an area of pyrethroid resistance [124]. Significant increase of 1014F
Given the many obstacles for evaluating the epidemiological impact of resistance, other alternative methods to measure operational impact has been to measure proxy entomological outcomes, such as the relative mortality and feeding success of resistant and susceptible vectors in experimental huts [232, 233]. Although such results can be remarkably clear, and definitively linked to resistance, experimental hut methods have their own limitations owing to the controlled hut structures that differ in many ways to normal houses in rural African context.
An early experimental hut trial of ITNs was conducted in the western African country of Benin. In southern Benin (Ladji), pyrethroid resistance has evolved in the M form of
One of the problems associated with many of these studies is that, due to the lack of molecular markers for alternative resistance mechanisms (i.e. metabolic or even cuticular and behavioral), the frequency of
8. Resistance management strategies
As a general statement, the use of insecticides does not create resistance by itself but select small proportion of individuals having a genetic mutation that allow them to resist and survive the effects of the insecticide. If this advantage is maintained by constant use of the same insecticide, the resistant insects will reproduce and the genetic changes that confer resistance will be transferred to offspring so that they become more prevalent within the population (figure 3). This selection process will take longer time to occur if the gene conferring resistance is rare or present at a low prevalence. Resistance should not be confused with “induction” that can occur after sub-lethal (or low dose) exposure to any insecticide and/or xenobiotic and is not passed on to offspring [239].
8.1. Main factors influencing resistance development
The evolution of insecticide resistance is complex and depends on several genetic, biological and operational factors [240-242]. The biological factors relate by the life cycle of the insect (e.g. rate of reproduction, number of generation/offspring, rate of migration and isolation, etc), while the genetic factors include the intrinsic characteristics of the resistant genes (e.g. mono
8.1.1. Biological factors
Insect species that have a short life cycle and high rates of reproduction are likely to develop resistance more rapidly than species that have a lower rate of reproduction, as any resistance genes can rapidly spread throughout the population. Because mosquitoes can produce high number of offspring (i.e. females can lay several hundred eggs during their reproductive life) they are much likely to develop resistance to insecticides than other species.
With mosquitoes, the goal is to eliminate all or the majority of the population, however the greater the selection pressure that is put on a population, the faster susceptibility may be lost. Immigration of individuals possessing susceptible genes from untreated areas can beneficially dilute and compete with the resistance genes in the overall population. An early step in a malaria vector control programme should therefore be to estimate the susceptibility status of vector populations (see section 5 for details) and estimate potential immigration of untreated insects. This can be achieved by using genetic markers to estimate the gene flow (migrants) and genetic structure between populations. For example, an isolated area (e.g. island) where the entire area is treated would have a higher risk of developing resistance as few “susceptible” genotypes would join the treated population. The risk of insecticide resistance developing should be considered when planning a resistance management strategy. Awareness of and coordination with neighboring vector control programmes and agricultural activities should be encouraged, so that the regional and potential “side effect” on the target population is considered.
8.1.2. Genetics factor
Resistance genes can range from dominant through semi-dominant to recessive. If dominant or semi-dominant, only one parent needs to possess the characteristic to be fully or partially expressed in the offspring. If recessive, both parents must possess the trait. Fortunately, most resistance mechanisms (e.g.
Epistasis is the non-additive interaction (synergistic
Populations of insects that have never been exposed to insecticides are usually fully susceptible, and resistance genes within those populations are very rare. This usually occurs through a “fitness cost”, which means that insects sharing the resistance allele lack some other attribute or “quality” such that it gives an advantage to the susceptible insects in an insecticide free environment [250]. For example, resistant insects may have lower mating success, be more susceptible to natural enemies [251], or more prone to mortality during over-wintering [252]. Increased production of metabolic enzymes generally shows lower associated fitness cost than those associated with alterations in the structural genes most probably because the primary function of the enzyme is not disrupted [253]. There is good laboratory and field evidence to suggest that the deficit of insecticide selection pressure, in most cases, selects for susceptible genotypes. For example, the absence of homozygote’s resistant genotypes in
8.1.3. Operational factors
In practice, only operational factors such as the insecticide(s) used, the area of coverage (for example for IRS or LLIN), and the timing, rate, and method of application can be manipulated directly to reduce the selection pressure for resistance. Operational factors influence selection by determining the overall fraction of a population exposed (larvae/adults) to a selecting agent and the degree of contact and pick-up of toxicant by exposed pests at what has been termed the "interface between insects and insecticides” [242]. At both stages, operational and intrinsic factors interact in complex ways to establish the net effect of a control treatment on both genetic composition and total population size. Management of resistance therefore entails resolving these interactions to anticipate with some confidence both the suppressive and selective effects of potential control strategies.
How often an insecticide is used is one of the most important factors that influence resistance development [240]. With each use, an advantage is given to the resistant insects within a population. The rate of increase of resistance on any population will generally be faster in the presence of a lower fitness cost and high reproductive and short life cycles producing several generations per season. The length of time that an insecticide remains effective, also called its persistence, is dependent upon the physical chemistry of the insecticide, the type of formulation, the application rate and the substrate. Products which provide a persistent effect provide continual selection pressure in a similar manner to multiple treatments. For example, a space spray will persist for a very short time and will select only against a single generation of mosquitoes. In contrast, a residual wall application (IRS) or Insecticide Treated nets treatment (especially Long Lasting Nets) will persist for months or years providing a selection pressure against many generations of the same insect. For example, repeated application of DDT for indoor residual spraying has contributed to increase the number of DDT-resistant malaria vector species in various geographical settings [255]. Several studies showed however that the use of insecticides in agriculture play a key role in the selection of resistance in mosquitoes [256, 257]. Indeed, most insecticides used in agriculture are of the same chemical classes and have the same targets and modes of action as those used in public health programme. In practice, VC programmes cannot influence the choice of the pesticide used for crop protection and the only thing that can be done is to appropriately select the most judicious insecticide for mosquito control. However, there is more published evidence that public health insecticides can contribute to select for pyrethroid resistance alleles (see section 7 for details). It is obvious that we can expect enhanced selection pressure on resistance genes through the scaling up of LLIN and/or IRS for malaria elimination.
The speed at which an insecticide effectively kills an insect can also influence the evolution of resistance. All current insecticides approved for ITNs or IRS kill extremely rapidly after contact. While fast-acting conventional insecticides can produce even more effective initial control, they impose enormous selection for resistance by killing young female adults. The consequence is that spectacular initial mosquito control can last as little as a few years, thus providing very poor medium- to long-term disease control [258]. Some authors recently suggest that Late Acting insecticides (e.g. entomofungus) may be a more tactical strategy to manage resistance if female mosquitoes are killed after 2 or more gonotrophic cycles [259]. Indeed, the less the insecticide impact on mosquito fitness, the less the strength of selection, especially if the resistance allele is associated with a strong genetic cost. In theory, it would be possible to create an insecticide that would provide effective malaria control yet never be undermined by the evolution of resistant mosquitoes. However, further studies are required as “proof of principle” i.e. to demonstrate that this strategy can be effective for vector management and malaria prevention in a real setting.
8.2. Resistance management — Strategies and tactics
Historically, the practice of using an insecticide until resistance becomes a limiting factor has rapidly eroded the number of suitable/available insecticides for vector control. Rotations, mosaics, and mixtures have all been proposed as resistance management tools [260, 261] but there are very few “success stories” in public health. Numerous mathematical models have been produced to estimate how these tools could be optimally used [262-264] but these models have rarely been tested under field conditions due to the practical difficulties in estimating changes in resistance gene frequencies (especially for metabolic resistance) in large samples of insects [220]. With the advent of different molecular techniques for resistance-gene frequency estimation, field trials of resistance management strategies have now become more feasible.
8.2.1. Approaches to resistance management
Ideally insecticide resistance management should be undertaken using insecticide based approaches in conjunction with other non-insecticidal vector control methods, i.e. as part of Integrated Vector Management (IVM
Rotational strategies are based on the rotation over time of two or preferably more insecticide classes with different modes of action. This approach assumes that if resistance to each insecticide is rare, then multiple resistances will be extremely rare [266]. Rotation allows any resistance developed to the first insecticide to decline over time when the second insecticide class is introduced. As for other strategy, rotations are particularly effective if the resistance gene has an associated fitness cost. The timeframe for rotation needs to be sufficiently short to prevent significant levels of resistance to develop to any one rotation partner. Rotations have been successful in many applications in agriculture and are considered to be effective in slowing the evolution of resistance (see [240] for details
Spatially separated applications of different compounds against the same insect constitute a “mosaic” approach to resistance management [240]. Fine scale mosaics can be achieved in malaria vector control programmes, for example, by using two insecticides in different dwellings within the same village. The aim of this strategy is to preserve susceptibility by spatial restriction of insecticides [4]. If such a fine scale mosaic is to be used, careful records of which insecticide was used in each house are essential. Larger scale mosaics have been shown to be effective for the management of pyrethroid resistance in
A mixture is defined by the simultaneous use of two or more insecticides of unrelated mode of action. If two insecticides A and B, with independent resistance mechanisms, are applied together in a mixture, and if resistance to A and resistance to B are both rare, then we expect doubly resistant insects to be extremely rare, and almost all insects resistant to A will be killed by B, and vice versa [266]. This system of “redundant killing” means that resistance to the two insecticides will evolve much more slowly than if either had been used on its own [271]. This approach may be not successful if resistance to one of the components used is already present at a detectable level and/or if linkage disequilibrium is present in the targeted population [4]. Unlike rotations, the effectiveness of mixtures is not directly related to the degree of fitness cost. Rather the mixture aims to overpower resistance instead of preserving susceptibility. However, for mixtures to work well in practice both insecticides need to be used at their full application rate in order that the efficacy and persistence of the two insecticides would be broadly similar (same decay rate). Further, theoretical models suggest that mixtures might delay resistance longer than rotations or broad mosaics [271, 272]. However, mixtures of products were rarely adopted in malaria vector control programmes on grounds of cost, logistics, and safety issue and because of the limited number of recommended compounds available for both IRS and LLIN. It is not yet clear however how much the addition of a second active ingredient will add to the total cost of manufacturing since the cost of additional insecticide can greatly vary according to the strategy, ie. cost for LLINs would be much lower than that for IRS. For LLIN, previous laboratory and field trials showed interesting prospects for reducing mosquito survival and biting rates with the use of insecticide mixtures applied on mosquito nets against
In this context, combinations expose the vector population to two vector control tools, such that a mosquito that survives contact with one (e.g. LLIN) is exposed to the other one (e.g. IRS), or vice versa. In practice, exposure to two insecticides is not guaranteed but there is some evidence to indicate that this is likely [277]. The effectiveness of combinations in IRM does not depend on the ability to reduce the level of resistance, but on the ability to kill the vector despite the existence of resistance, through the use of another insecticide or intervention, which compensates for resistance [231]. As for other strategy, the combination should not contain insecticides with same mode of action (e.g. avoid pyrethroids for both IRS and LLINs), as this would increase selection pressure rather than reducing it. As combinations require doubling of interventions, cost would be significantly higher than rotations and mosaics. This might nevertheless be warranted in some circumstances, for example where malaria transmission is very high and/or where targeted IRS can help overcome identified resistance to pyrethroids in areas with high LLIN coverage. In practice, combinations would be more easily implemented in countries having sufficient human and financial resources allocated to public health programmes. So far, a small number of observational studies [278-280] and mathematical modeling exercises [263, 264] suggest that VC combination has an added benefit for reduction of the risk of infection because the people not protected by one of the interventions are protected by the other. A recent cluster randomized controlled trial carried out in Benin showed however that neither clinical malaria in children younger than 6 years nor transmission intensity differ between LLIN and carbamate-IRS or Carbamate Treated Plastic Sheeting and the reference group (LLIN alone) and the insecticide combinations did not slow down the evolution of the
9. Conclusions
Insecticide resistance develops in an insect population when individuals carrying genes that allow them to survive exposure to the insecticide pass these genes on. Thus, any activities that control the individuals with the resistance trait will delay the spread of the resistance genes in the population. IRM should then be seen in the context of IVM and should therefore also include activities such as habitat management, community education, and/or larval source management (e.g. biological control). In order to successfully develop and implement any resistance management strategies based on rotations, mosaics, mixtures or combinations, knowledge of the mode of action, chemical properties, and residual life of the available insecticide products is essential. Although insecticides with novel modes of action have recently been introduced in public health (neonicotinoids, pyroles, oxadiazin, etc) few of them appear to have the optimum biological and/or physical properties required for residual wall spray and/or mosquito net. Unfortunately, the exorbitant costs associated with developing and registering new insecticides (see [281] for details) mean that products appear in the more profitable agricultural markets before consideration is given to their public health potential. We have then no other option than to make an appropriate and judicious use of the current insecticides if we want to avoid any disillusion with pyrethroids as we faced before with DDT or dieldrin. The philosopher George Santayana said
References
- 1.
World Health Organization: WHO malaria report : 2011. In: WHO Global Malaria Programme. Edited by Data WLC-i-P. Geneva: WHO; 2011: 259. - 2.
Yassine H, Osta MA: Anopheles gambiae innate immunity.Cell Microbiol , 12(1):1-9. - 3.
Davidson G: Insecticide resistance in Anopheles sundaicus .Nature 1957, 180(4598):1333-1335. - 4.
World Health Organization: Global Plan for Insecticide Resistance Management in Malaria Vectors (GPIRM). In: WHO/HTM/GMP/20125. Edited by Organization WH. Geneva, Switzerland: World Health Organization; 2012: 130. - 5.
Hemingway J, Ranson H: Insecticide resistance in insect vectors of human disease. Annu Rev Entomol 2000, 45:371-391. - 6.
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(2):91-98. - 7.
Ridl FC, Bass C, Torrez M, Govender D, Ramdeen V, Yellot L, Edu AE, Schwabe C, Mohloai P, Maharaj R et al : A pre-intervention study of malaria vector abundance in Rio Muni, Equatorial Guinea: their role in malaria transmission and the incidence of insecticide resistance alleles.Malar J 2008, 7:194. - 8.
Sharp BL, Ridl FC, Govender D, Kuklinski J, Kleinschmidt I: Malaria vector control by indoor residual insecticide spraying on the tropical island of Bioko, Equatorial Guinea. Malar J 2007, 6:52. - 9.
Mitchell SN, Stevenson BJ, Muller P, Wilding CS, Egyir-Yawson A, Field SG, Hemingway J, Paine MJ, Ranson H, Donnelly MJ: Identification and validation of a gene causing cross-resistance between insecticide classes in Anopheles gambiae from Ghana.Proc Natl Acad Sci U S A 2012, 109(16):6147-6152. - 10.
Stevenson BJ, Bibby J, Pignatelli P, Muangnoicharoen S, O'Neill PM, Lian LY, Muller P, Nikou D, Steven A, Hemingway J et al : Cytochrome P450 6M2 from the malaria vectorAnopheles gambiae metabolizes pyrethroids: Sequential metabolism of deltamethrin revealed.Insect Biochem Mol Biol 2011, 41(7):492-502. - 11.
Brown AWA: Insecticide Resistance Mosquitoes: A Pragmatic Rewiew. J Am Mosq Control Assoc 1986, 2(2):123-140. - 12.
Metcalf RL: Insect resistance to insecticides. Pesticide Science 1989, 26(4):333-358. - 13.
WHO: Global Insecticide Use for Vector-Borne Disease Control- 4th edition. In Edited by World Health Organization Geneva: World Health Organization 2009, WHO/HTM/NTD/WHOPES/GCDPP/2009.6. - 14.
Lapied B, Pennetier C, Apaire-Marchais V, Licznar P, Corbel V: Innovative applications for insect viruses: towards insecticide sensitization. Trends Biotechnol 2009, 27(4):190-198. - 15.
Livadas GA, Georgopoulos G: Development of resistance to DDT by Anopheles sacharovi in Greece.Bull World Health Organ 1953, 8(4):497-511. - 16.
Brown AWA, Haworth J, Zahar AR: Malaria eradication and control from a global standpoint. Journal of Medical Entomology 1976, 13(1):1-25. - 17.
Patel TB, Ramachandra Rao T, Halgeri AV, Deobhankar RB: A preliminary note on a probable case of dieldrin kesistance in Anopheles culicifacies in Thana District, Bombay State.Indian J Malariol 1958, 12:367-370. - 18.
Brown AW, Pal R: Insecticide resistance in arthropods. Public Health Pap 1971, 38(0):1-491. - 19.
Brown AW, Haworth J, Zahar AR: Malaria eradication and control from a global standpoint. J Med Entomol 1976, 13(1):1-25. - 20.
Rajagopal R: Malathion resistance in Anopheles culicifacies in Gujarat.Indian J Med Res 1977, 66(1):27-28. - 21.
Rawlings P, Herath PR, Kelly S: Anopheles culicifacies (Diptera: Culicidae): DDT resistance in Sri Lanka prior to and after cessation of DDT spraying.J Med Entomol 1985, 22(4):361-365. - 22.
Penilla RP, Rodriguez AD, Hemingway J, Torres JL, Arredondo Jimenez JI, Rodriguez MH: Resistance management strategies in malaria vector mosquito control. Baseline data for a large-scale field trial against Anopheles albimanus in Mexico.Medical and Veterinary Entomology 1998, 12(3):217-233. - 23.
Van Bortel W, Trung HD, Thuan le K, Sochantha T, Socheat D, Sumrandee C, Baimai V, Keokenchanh K, Samlane P, Roelants P et al : The insecticide resistance status of malaria vectors in the Mekong region.Malar J 2008, 7:102. - 24.
Trung HD, Van Bortel W, Sochantha T, Keokenchanh K, Quang NT, Cong LD, Coosemans M: Malaria transmission and major malaria vectors in different geographical areas of Southeast Asia. Trop Med Int Health 2004, 9(2):230-237. - 25.
Chareonviriyaphap T, Aum-aung B, Ratanatham S: Current insecticide resistance patterns in mosquito vectors in Thailand. Southeast Asian J Trop Med Public Health 1999, 30(1):184-194. - 26.
Hamon J, Subra R, Sales S, Coz J: [Presence in the southwestern part of Upper Volta of a population of Anopheles gambiae "A" resistant to DDT].Med Trop (Mars) 1968, 28(4):521-528. - 27.
Carnevale P, Robert V: Anopheles : Biologie, transmission duPlasmodium et lutte antivectorielle. Bondy: IRD; 2009. - 28.
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(1):53-59. - 29.
Armstrong JA, Ramsdale CD, Ramakrishna V: Insecticide resistance in Anopheles gambiae Giles in Western Sokoto, Northern Nigeria.Ann Trop Med Parasitol 1958, 52(3):247-256. - 30.
Hamon J, Garrett-Jones C: [Resistance to insecticides in the major malaria vectors and its operational importance]. Bull World Health Organ 1963, 28(1):1-24. - 31.
Wondji CS, Dabire RK, Tukur Z, Irving H, Djouaka R, Morgan JC: Identification and distribution of a GABA receptor mutation conferring dieldrin resistance in the malaria vector Anopheles funestus in Africa.Insect Biochem Mol Biol 2011, 41(7):484-491. - 32.
Mouchet J: Mini-Review : Agriculture and Vector Resistance. Insect Sci Applic 1988, 9(3):291-302. - 33.
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(2):114-119. - 34.
Brogdon WG, McAllister JC, Corwin AM, Cordon Rosales C: Oxidase-based DDT-pyrethroid cross-resistance in Guatemalan Anopheles albimanus .Pesticide Biochemistry and Physiology 1999, 64(2):101-111. - 35.
Fonseca-Gonzalez I, Quinones ML, McAllister J, Brogdon WG: Mixed-function oxidases and esterases associated with cross-resistance between DDT and lambda-cyhalothrin in Anopheles darlingi Root 1926 populations from Colombia.Mem Inst Oswaldo Cruz 2009, 104(1):18-26. - 36.
Raghavendra K, Verma V, Srivastava HC, Gunasekaran K, Sreehari U, Dash AP: Persistence of DDT, malathion & deltamethrin resistance in Anopheles culicifacies after their sequential withdrawal from indoor residual spraying in Surat district, India.Indian J Med Res 2010, 132:260-264. - 37.
Tiwari S, Ghosh SK, Ojha VP, Dash AP, Raghavendra K: Reduced susceptibility to selected synthetic pyrethroids in urban malaria vector Anopheles stephensi : a case study in Mangalore city, South India.Malar J 2010, 9:179. - 38.
Elissa N, Mouchet J, Riviere F, Meunier JY, Yao K: Resistance of Anopheles gambiae s.s. to pyrethroids in Cote d'Ivoire.Ann Soc Belg Med Trop 1993, 73(4):291-294. - 39.
Hargreaves K, Koekemoer LL, Brooke BD, Hunt RH, Mthembu J, Coetzee M: Anopheles funestus resistant to pyrethroid insecticides in South Africa.Medical and Veterinary Entomology 2000, 14(2):181-189. - 40.
Chareonviriyaphap T, Rongnoparut P, Juntarumporn P: Selection for pyrethroid resistance in a colony of Anopheles minimus species A, a malaria vector in Thailand.J Vector Ecol 2002, 27(2):222-229. - 41.
Ayad H, Georghiou GP: Resistance to organophosphates and carbamates in Anopheles albimanus based on reduced sensitivity of acetylcholinesterase.Journal of Economic Entomology 1975, 68(3):295-297. - 42.
Hemingway J: Genetics of organophosphate and carbamate resistance in Anopheles atroparvus (Diptera: Culicidae).J Econ Entomol 1982, 75(6):1055-1058. - 43.
Elissa N, Mouchet J, Riviere F, Meunier JY, Yao K: [Susceptibility of Anopheles gambiae to insecticides in the Ivory Coast].Sante 1994, 4(2):95-99. - 44.
N'Guessan R, Darriet F, Guillet P, Carnevale P, Traore-Lamizana M, Corbel V, Koffi AA, Chandre F: Resistance to carbosulfan in Anopheles gambiae from Ivory Coast, based on reduced sensitivity of acetylcholinesterase.Med Vet Entomol 2003, 17(1):19-25. - 45.
Dabire KR, Diabate A, Namontougou M, Djogbenou L, Kengne P, Simard F, Bass C, Baldet T: Distribution of insensitive acetylcholinesterase (ace-1R) in Anopheles gambiae s.l. populations from Burkina Faso (West Africa).Trop Med Int Health 2009, 14(4):396-403. - 46.
Djogbenou L, Dabire R, Diabate A, Kengne P, Akogbeto M, Hougard JM, Chandre F: Identification and geographic distribution of the ACE-1R mutation in the malaria vector Anopheles gambiae in south-western Burkina Faso, West Africa.Am J Trop Med Hyg 2008, 78(2):298-302. - 47.
Djogbenou L, Pasteur N, Akogbeto M, Weill M, Chandre F: Insecticide resistance in the Anopheles gambiae complex in Benin: a nationwide survey.Med Vet Entomol 2011, 25(3):256-267. - 48.
Oduola AO, Idowu ET, Oyebola MK, Adeogun AO, Olojede JB, Otubanjo OA, Awolola TS: Evidence of carbamate resistance in urban populations of Anopheles gambiae s.s. mosquitoes resistant to DDT and deltamethrin insecticides in Lagos, South-Western Nigeria.Parasit Vectors 2012, 5:116. - 49.
USAID: The President’s Malaria Initiative: fourth annual report. In. Washigton: U.S. Agency for International Development; 2010. - 50.
Nkya TE, Akhouayri I, Kisinza W, David JP: Impact of environment on mosquito response to pyrethroid insecticides: Facts, evidences and prospects. Insect Biochem Mol Biol 2012. - 51.
Despres L, David JP, Gallet C: The evolutionary ecology of insect resistance to plant chemicals. Trends Ecol Evol 2007, 22(6):298-307. - 52.
Hemingway J, Hawkes NJ, McCarroll L, Ranson H: The molecular basis of insecticide resistance in mosquitoes. Insect Biochem Mol Biol 2004, 34(7):653-665. - 53.
Guillemaud T, Makate N, Raymond M, Hirst B, Callaghan A: Esterase gene amplification in Culex pipiens .Insect Molecular Biology 1997, 6(4):319-327. - 54.
Hawkes NJ, Hemingway J: Analysis of the promoters for the beta-esterase genes associated with insecticide resistance in the mosquito Culex quinquefasciatus .Biochim Biophys Acta 2002, 1574(1):51-62. - 55.
Vaughan A, Hawkes N, Hemingway J: Co-amplification explains linkage disequilibrium of two mosquito esterase genes in insecticide-resistant Culex quinquefasciatus .Biochem J 1997, 325 ( Pt 2):359-365. - 56.
Herath PR, Miles SJ, Davidson G: Fenitrothion (OMS 43) resistance in the taxon Anopheles culicifacies Giles.J Trop Med Hyg 1981, 84(2):87-88. - 57.
Hemingway J: The genetics of malathion resistance in Anopheles stephensi from Pakistan.Trans R Soc Trop Med Hyg 1983, 77(1):106-108. - 58.
Vontas J, Blass C, Koutsos AC, David JP, Kafatos FC, Louis C, Hemingway J, Christophides GK, Ranson H: Gene expression in insecticide resistant and susceptible Anopheles gambiae strains constitutively or after insecticide exposure.Insect Mol Biol 2005, 14(5):509-521. - 59.
Somwang P, Yanola J, Suwan W, Walton C, Lumjuan N, Prapanthadara LA, Somboon P: Enzymes-based resistant mechanism in pyrethroid resistant and susceptible Aedes aegypti strains from northern Thailand.Parasitol Res 2011, 109(3):531-537. - 60.
Feyereisen R, Lawrence IG, Kostas I, Sarjeet SG: Insect Cytochrome P450. In: Comprehensive Molecular Insect Science. Amsterdam: Elsevier; 2005: 1-77. - 61.
Holt RA, Subramanian GM, Halpern A, Sutton GG, Charlab R, Nusskern DR, Wincker P, Clark AG, Ribeiro JM, Wides R et al : The genome sequence of the malaria mosquitoAnopheles gambiae .Science 2002, 298(5591):129-149. - 62.
Ranson H, Nikou D, Hutchinson M, Wang X, Roth CW, Hemingway J, Collins FH: Molecular analysis of multiple cytochrome P450 genes from the malaria vector, Anopheles gambiae .Insect Mol Biol 2002, 11(5):409-418. - 63.
Nikou D, Ranson H, Hemingway J: An adult-specific CYP6 P450 gene is overexpressed in a pyrethroid-resistant strain of the malaria vector, Anopheles gambiae .Gene 2003, 318:91-102. - 64.
David JP, Strode C, Vontas J, Nikou D, Vaughan A, Pignatelli PM, Louis C, Hemingway J, Ranson H: The Anopheles gambiae detoxification chip: a highly specific microarray to study metabolic-based insecticide resistance in malaria vectors.Proc Natl Acad Sci U S A 2005, 102(11):4080-4084. - 65.
Irving H, Riveron JM, Ibrahim SS, Lobo NF, Wondji CS: Positional cloning of rp2 QTL associates the P450 genes CYP6Z1, CYP6Z3 and CYP6M7 with pyrethroid resistance in the malaria vector Anopheles funestus .Heredity (Edinb) 2012, 109(6):383-392. - 66.
Chiu TL, Wen Z, Rupasinghe SG, Schuler MA: Comparative molecular modeling of Anopheles gambiae CYP6Z1, a mosquito P450 capable of metabolizing DDT.Proc Natl Acad Sci U S A 2008, 105(26):8855-8860. - 67.
McLaughlin LA, Niazi U, Bibby J, David JP, Vontas J, Hemingway J, Ranson H, Sutcliffe MJ, Paine MJ: Characterization of inhibitors and substrates of Anopheles gambiae CYP6Z2.Insect Mol Biol 2008, 17(2):125-135. - 68.
Muller P, Chouaibou M, Pignatelli P, Etang J, Walker ED, Donnelly MJ, Simard F, Ranson H: 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 2008, 17(4):1145-1155. - 69.
Djouaka RF, Bakare AA, Coulibaly ON, Akogbeto MC, Ranson H, Hemingway J, Strode C: Expression of the cytochrome P450s, CYP6P3 and CYP6M2 are significantly elevated in multiple pyrethroid resistant populations of Anopheles gambiae s.s. from Southern Benin and Nigeria.BMC Genomics 2008, 9:538. - 70.
Muller P, Donnelly MJ, Ranson H: Transcription profiling of a recently colonised pyrethroid resistant Anopheles gambiae strain from Ghana.BMC Genomics 2007, 8:36. - 71.
Muller P, Warr E, Stevenson BJ, Pignatelli PM, Morgan JC, Steven A, Yawson AE, Mitchell SN, Ranson H, Hemingway J et al : Field-caught permethrin-resistantAnopheles gambiae overexpress CYP6P3, a P450 that metabolises pyrethroids.PLoS Genet 2008, 4(11):e1000286. - 72.
Wondji CS, Irving H, Morgan J, Lobo NF, Collins FH, Hunt RH, Coetzee M, Hemingway J, Ranson H: Two duplicated P450 genes are associated with pyrethroid resistance in Anopheles funestus , a major malaria vector.Genome Res 2009, 19(3):452-459. - 73.
Wondji CS, Morgan J, Coetzee M, Hunt RH, Steen K, Black WCt, Hemingway J, Ranson H: Mapping a quantitative trait locus (QTL) conferring pyrethroid resistance in the African malaria vector Anopheles funestus .BMC Genomics 2007, 8:34. - 74.
Riveron JM, Irving H, Ndula M, Barnes KG, Ibrahim SS, Paine MJ, Wondji CS: Directionally selected cytochrome P450 alleles are driving the spread of pyrethroid resistance in the major malaria vector Anopheles funestus .Proc Natl Acad Sci U S A 2012, 110(1):252-257. - 75.
Rongnoparut P, Boonsuepsakul S, Chareonviriyaphap T, Thanomsing N: Cloning of cytochrome P450, CYP6P5, and CYP6AA2 from Anopheles minimus resistant to deltamethrin.J Vector Ecol 2003, 28(2):150-158. - 76.
Duangkaew P, Kaewpa D, Rongnoparut P: Protective efficacy of Anopheles minimus CYP6P7 and CYP6AA3 against cytotoxicity of pyrethroid insecticides inSpodoptera frugiperda (Sf9) insect cells.Trop Biomed 2011, 28(2):293-301. - 77.
Duangkaew P, Pethuan S, Kaewpa D, Boonsuepsakul S, Sarapusit S, Rongnoparut P: Characterization of mosquito CYP6P7 and CYP6AA3: differences in substrate preference and kinetic properties. Arch Insect Biochem Physiol 2011, 76(4):236-248. - 78.
Ranson H, Cornel AJ, Fournier D, Vaughan A, Collins FH, Hemingway J: Cloning and Localization of a Glutathione S-transferase Class I Gene from Anopheles gambiae .J Biol Chem 1997, 272(9):5464-5967. - 79.
Ranson H, Hemingway J: Mosquito glutathione transferases. Methods Enzymol 2005, 401:226-241. - 80.
Fournier D, Bride JM, Poirie M, Berge JB, Plapp FW, Jr.: Insect glutathione S-transferases. Biochemical characteristics of the major forms from houseflies susceptible and resistant to insecticides. Journal of Biological Chemistry 1992, 267(3):1840-1845. - 81.
Ranson H, Rossiter L, Ortelli F, Jensen B, Wang XL, Roth CW, Collins FH, Hemingway J: Identification of a novel class of insect glutathione S-transferases involved in resistance to DDT in the malaria vector Anopheles gambiae .Biochemical Journal 2001, 359 Part 2:295-304. - 82.
Gunasekaran K, Muthukumaravel S, Sahu SS, Vijayakumar T, Jambulingam P: Glutathione S transferase activity in Indian vectors of malaria: A defense mechanism against DDT. J Med Entomol 2011, 48(3):561-569. - 83.
Prapanthadara LA, Ketterman AJ: Qualitative and quantitative changes in glutathione S-transferases in the mosquito Anopheles gambiae confer DDT-resistance.Biochem Soc Trans 1993, 21 ( Pt 3)(3):304S. - 84.
Ranson H, Jensen B, Wang X, Prapanthadara L, Hemingway J, Collins FH: Genetic mapping of two loci affecting DDT resistance in the malaria vector Anopheles gambiae .Insect Mol Biol 2000, 9(5):499-507. - 85.
Vontas JG, Small GJ, Hemingway J: Glutathione S-transferases as antioxidant defence agents confer pyrethroid resistance in Nilaparvata lugens .Biochem J 2001, 357(Pt 1):65-72. - 86.
Kostaropoulos I, Papadopoulos AI, Metaxakis A, Boukouvala E, Papadopoulou-Mourkidou E: Glutathione S-transferase in the defence against pyrethroids in insects. Insect Biochem Mol Biol 2001, 31(4-5):313-319. - 87.
Fournier D: Mutations of acetylcholinesterase which confer insecticide resistance in insect populations. Chem Biol Interact 2005. - 88.
Weill M, Lutfalla G, Mogensen K, Chandre F, Berthomieu A, Berticat C, Pasteur N, Philips A, Fort P, Raymond M: Comparative genomics: Insecticide resistance in mosquito vectors. Nature 2003, 423(6936):136-137. - 89.
Alout H, Labbe P, Berthomieu A, Pasteur N, Weill M: Multiple duplications of the rare ace-1 mutation F290V in Culex pipiens natural populations.Insect Biochem Mol Biol 2009. - 90.
Weill M, Malcolm C, Chandre F, Mogensen K, Berthomieu A, Marquine M, Raymond M: The unique mutation in ace-1 giving high insecticide resistance is easily detectable in mosquito vectors. Insect Mol Biol 2004, 13(1):1-7. - 91.
Djogbenou L, Chandre F, Berthomieu A, Dabire R, Koffi A, Alout H, Weill M: Evidence of introgression of the ace-1(R) mutation and of the ace-1 duplication in West African Anopheles gambiae s. s.PLoS ONE 2008, 3(5):e2172. - 92.
Ffrench-Constant RH: The molecular and population genetics of cyclodiene insecticide resistance. Insect Biochem Mol Biol 1994, 24(4):335-345. - 93.
Andreasen MH, Ffrench-Constant RH: In situ hybridization to the Rdl locus on polytene chromosome 3L of Anopheles stephensi .Med Vet Entomol 2002, 16(4):452-455. - 94.
Du W, Awolola TS, Howell P, Koekemoer LL, Brooke BD, Benedict MQ, Coetzee M, Zheng L: Independent mutations in the Rdl locus confer dieldrin resistance to Anopheles gambiae andAn. arabiensis .Insect Mol Biol 2005, 14(2):179-183. - 95.
Davies TG, Field LM, Usherwood PN, Williamson MS: DDT, pyrethrins, pyrethroids and insect sodium channels. IUBMB Life 2007, 59(3):151-162. - 96.
Donnelly MJ, Corbel V, Weetman D, Wilding CS, Williamson MS, Black WCt: Does kdr genotype predict insecticide-resistance phenotype in mosquitoes?Trends Parasitol 2009, 25(5):213-219. - 97.
Martinez Torres D, Chandre F, Williamson MS, Darriet F, Berge JB, Devonshire AL, Guillet P, Pasteur N, Pauron D: Molecular characterization of pyrethroid knockdown resistance ( kdr ) in the major malaria vectorAnopheles gambiae s.s.Insect Molecular Biology 1998, 7(2):179-184. - 98.
Ranson H, Jensen B, Vulule JM, Wang X, Hemingway J, Collins FH: Identification of a point mutation in the voltage-gated sodium channel gene of Kenyan Anopheles gambiae associated with resistance to DDT and pyrethroids.Insect Molecular Biology 2000, 9(5):491-497. - 99.
O'Reilly AO, Khambay BP, Williamson MS, Field LM, Wallace BA, Davies TG: Modelling insecticide-binding sites in the voltage-gated sodium channel. Biochem J 2006, 396(2):255-263. - 100.
Jones CM, Liyanapathirana M, Agossa FR, Weetman D, Ranson H, Donnelly MJ, Wilding CS: Footprints of positive selection associated with a mutation (N1575Y) in the voltage-gated sodium channel of Anopheles gambiae .Proc Natl Acad Sci U S A 2012, 109(17):6614-6619. - 101.
Plapp FW, Jr.: The genetic basis of insecticide resistance in the house fly: evidence that a single locus plays a major role in metabolic resistance to insecticides. Pesticide Biochemistry and Physiology 1984, 22(2):194-201. - 102.
Georghiou GP, Ariaratnam V, Pasternak ME, Lin CS: Organophosphorus multiresistance in Culex pipiens quinquefasciatus in California.Journal of Economic Entomology 1975, 68(4):461-467. - 103.
Vontas J, David JP, Nikou D, Hemingway J, Christophides GK, Louis C, Ranson H: Transcriptional analysis of insecticide resistance in Anopheles stephensi using cross-species microarray hybridization.Insect Mol Biol 2007, 16(3):315-324. - 104.
Awolola TS, Oduola OA, Strode C, Koekemoer LL, Brooke B, Ranson H: Evidence of multiple pyrethroid resistance mechanisms in the malaria vector Anopheles gambiae sensu stricto from Nigeria.Trans R Soc Trop Med Hyg 2009, 103(11):1139-1145. - 105.
Wood O, Hanrahan S, Coetzee M, Koekemoer L, Brooke B: Cuticle thickening associated with pyrethroid resistance in the major malaria vector Anopheles funestus .Parasit Vectors 2010, 3:67. - 106.
Roberts DR, Chareonviriyaphap T, Harlan HH, Hshieh P: Methods of testing and analyzing excito-repellency responses of malaria vectors to insecticides. J Am Mosq Control Assoc 1997, 13(1):13-17. - 107.
Chandre F, Darriet F, Duchon S, Finot L, Manguin S, Carnevale P, Guillet P: Modifications of pyrethroid effects associated with kdr mutation inAnopheles gambiae .Medical and Veterinary Entomology 2000, 14(1):81-88. - 108.
Gahan JB, Lindquist AW: DDT residual sprays applied in buildings to control Anopheles quadrimaculatus .Journal of Economic Entomology 1945, 38 (2):223-230. - 109.
Chareonviriyaphap T, Roberts DR, Andre RG, Harlan HJ, Manguin S, Bangs MJ: Pesticide avoidance behavior in Anopheles albimanus , a malaria vector in the Americas.J Am Mosq Control Assoc 1997, 13(2):171-183. - 110.
Garros C, Marchand RP, Quang NT, Hai NS, Manguin S: First record of Anopheles minimus C and significant decrease ofAn. minimus A in central Vietnam.J Am Mosq Control Assoc 2005, 21(2):139-143. - 111.
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. - 112.
Moiroux N, Gomez MB, Pennetier C, Elanga E, Djenontin A, Chandre F, Djegbe I, Guis H, Corbel V: Changes in Anopheles funestus Biting Behavior Following Universal Coverage of Long-Lasting Insecticidal Nets in Benin.J Infect Dis 2012, 206(10):1622-1629. - 113.
WHO: Guidelines for testing mosquito adulticides intended for Indoor Residual Spraying (IRS) and Insecticide Treated Nets (ITNs). 2006, WHO/CDS/NTD/WHOPES/GCDDP/2006.3. - 114.
WHO: Report of the WHO Informal Consultation Tests procedures for insecticide resistance monitoring in malaria vectors, bio-efficacy and persistence of insecticides on treated surfaces. In. Geneva: World Health Organization: Parasitic Diseases and Vector Control (PVC)/Communicable Disease Control, Prevention and Eradication (CPE); 1998: 43. - 115.
Williams J, Pinto J: Training Manual on Malaria Entomology; For Entomology and Vector Control Technicians (Basic Level) In. Edited by USAID. Washington, D.C.; 2012: 78. - 116.
Ranson H, Abdallah H, Badolo A, Guelbeogo WM, Kerah-Hinzoumbe C, Yangalbe-Kalnone E, Sagnon N, Simard F, Coetzee M: Insecticide resistance in Anopheles gambiae : data from the first year of a multi-country study highlight the extent of the problem.Malar J 2009, 8(1):299. - 117.
Skovmand O, Bonnet J, Pigeon O, Corbel V: Median knock-down time as a new method for evaluating insecticide-treated textiles for mosquito control. Malar J 2008, 7:114. - 118.
Brogdon WG, McAllister JC: Simplification of adult mosquito bioassays through use of time-mortality determinations in glass bottles. J Am Mosq Control Assoc 1998, 14(2):159-164. - 119.
World Health Organization: Techniques to detect insecticide resistance mechanisms (field and laboratory manual). In. Edited by WHO/CDS/CPC/MAL/98.6 WHO. Geneva: World Health Organization; 1998. - 120.
Munhenga G, Masendu HT, Brooke BD, Hunt RH, Koekemoer LK: Pyrethroid resistance in the major malaria vector Anopheles arabiensis from Gwave, a malaria-endemic area in Zimbabwe.Malar J 2008, 7:247. - 121.
Okoye PN, Brooke BD, Koekemoer LL, Hunt RH, Coetzee M: Characterisation of DDT, pyrethroid and carbamate resistance in Anopheles funestus from Obuasi, Ghana.Trans R Soc Trop Med Hyg 2008, 102(6):591-598. - 122.
Kelly-Hope L, Ranson H, Hemingway J: Lessons from the past: managing insecticide resistance in malaria control and eradication programmes. Lancet Infect Dis 2008. - 123.
Chouaibou M, Etang J, Brevault T, Nwane P, Hinzoumbe CK, Mimpfoundi R, Simard F: Dynamics of insecticide resistance in the malaria vector Anopheles gambiae s.l. from an area of extensive cotton cultivation in Northern Cameroon.Trop Med Int Health 2008, 13(4):476-486. - 124.
Djegbe I, Boussari O, Sidick A, Martin T, Ranson H, Chandre F, Akogbeto M, Corbel V: Dynamics of insecticide resistance in malaria vectors in Benin: first evidence of the presence of L1014S kdr mutation inAnopheles gambiae from West Africa.Malaria Journal 2011, 10(1):261. - 125.
Dabire KR, Diabate A, Pare-Toe L, Rouamba J, Ouari A, Fontenille D, Baldet T: Year to year and seasonal variations in vector bionomics and malaria transmission in a humid savannah village in west Burkina Faso. J Vector Ecol 2008, 33(1):70-75. - 126.
Bass C, Nikou D, Donnelly MJ, Williamson MS, Ranson H, Ball A, Vontas J, Field LM: Detection of knockdown resistance ( kdr ) mutations inAnopheles gambiae : a comparison of two new high-throughput assays with existing methods.Malar J 2007, 6:111. - 127.
Corbel V, N'Guessan R, Brengues C, Chandre F, Djogbenou L, Martin T, Akogbeto M, Hougard JM, Rowland M: Multiple insecticide resistance mechanisms in Anopheles gambiae andCulex quinquefasciatus from Benin, West Africa.Acta Trop 2007, 101(3):207-216. - 128.
Diabate A: The Role of Agricultural Uses of Insecticides in Resistance to Pyrethroids in Anopheles gambiae S.L. in Burkina Faso.Am J Trop Med Hyg 2002, 67(6):617-622. - 129.
Carnevale P, Toto JC, Guibert P, Keita M, Manguin S: Entomological survey and report of a knockdown resistance mutation in the malaria vector Anopheles gambiae from the Republic of Guinea.Trans R Soc Trop Med Hyg , 104(7):484-489. - 130.
Yawson AE, McCall PJ, Wilson MD, Donnelly MJ: Species abundance and insecticide resistance of Anopheles gambiae in selected areas of Ghana and Burkina Faso.Med Vet Entomol 2004, 18(4):372-377. - 131.
C. Fanello VP, A. della Torre, F. Santolamazza, G. Dolo, M. Coulibaly, A. Alloueche, C. F. Curtis, Y. T. Touré and M. Coluzzi: The pyrethroid knock-down resistance gene in the Anopheles gambiae complex in Mali and further indication of incipient speciation withinAn. gambiae s.s.Insect Molecular Biology 2003, 12(3):241-245. - 132.
Czeher C, Labbo R, Arzika I, Duchemin J-B: Evidence of increasing Leu-Phe knockdown resistance mutation in Anopheles gambiae from Niger following a nationwide long-lasting insecticide-treated nets implementation.Malaria Journal 2008, 7(1):189. - 133.
Awolola TS, Brooke BD, Hunt RH, Coetze M: Resistance of the malaria vector Anopheles gambiae s.s. to pyrethroid insecticides, in south-western Nigeria.Annals of Tropical Medicine and Parasitology 2002, 96(8):849-852. - 134.
Koffi AA, Alou LP, Adja MA, Kone M, Chandre F, N'Guessan R: Update on resistance status of Anopheles gambiae s.s. to conventional insecticides at a previous WHOPES field site, "Yaokoffikro", 6 years after the political crisis in Cote d'Ivoire.Parasit Vectors 2012, 5:68. - 135.
Dabire KR, Diabate A, Agostinho F, Alves F, Manga L, Faye O, Baldet T: Distribution of the members of Anopheles gambiae and pyrethroid knock-down resistance gene (kdr ) in Guinea-Bissau, West Africa.Bull Soc Pathol Exot 2008, 101(2):119-123. - 136.
Etang J, Fondjo E, Chandre F, Morlais I, Brengues C, Nwane P, Chouaibou M, Ndjemai H, Simard F: First report of knockdown mutations in the malaria vector Anopheles gambiae from Cameroon.Am J Trop Med Hyg 2006, 74(5):795-797. - 137.
Ndjemai HN, Patchoke S, Atangana J, Etang J, Simard F, Bilong CF, Reimer L, Cornel A, Lanzaro GC, Fondjo E: The distribution of insecticide resistance in Anopheles gambiae s.l. populations from Cameroon: an update.Trans R Soc Trop Med Hyg 2009. - 138.
Nwane P, Etang J, Chouaibou M, Toto JC, Kerah-Hinzoumbe C, Mimpfoundi R, Awono-Ambene HP, Simard F: Trends in DDT and pyrethroid resistance in Anopheles gambiae s.s. populations from urban and agro-industrial settings in southern Cameroon.BMC Infect Dis 2009, 9:163. - 139.
Kerah-Hinzoumbe C, Peka M, Nwane P, Donan-Gouni I, Etang J, Same-Ekobo A, Simard F: Insecticide resistance in Anopheles gambiae from south-western Chad, Central Africa.Malar J 2008, 7:192. - 140.
Janeira F, Vicente JL, Kanganje Y, Moreno M, Do Rosario VE, Cravo P, Pinto J: A primer-introduced restriction analysis-polymerase chain reaction method to detect knockdown resistance mutations in Anopheles gambiae .J Med Entomol 2008, 45(2):237-241. - 141.
Mourou JR, Coffinet T, Jarjaval F, Pradines B, Amalvict R, Rogier C, Kombila M, Pages F: Malaria transmission and insecticide resistance of Anopheles gambiae in Libreville and Port-Gentil, Gabon.Malar J 2010, 9:321. - 142.
Himeidan YE, Chen H, Chandre F, Donnelly MJ, Yan G: Short report: permethrin and DDT resistance in the malaria vector Anopheles arabiensis from eastern Sudan.Am J Trop Med Hyg 2007, 77(6):1066-1068. - 143.
Abdalla H, Matambo TS, Koekemoer LL, Mnzava AP, Hunt RH, Coetzee M: Insecticide susceptibility and vector status of natural populations of Anopheles arabiensis from Sudan.Transactions of the Royal Society of Tropical Medicine and Hygiene 2008, 102(3):263-271. - 144.
Costantini C, Ayala D, Guelbeogo WM, Pombi M, Some CY, Bassole IH, Ose K, Fotsing JM, Sagnon N, Fontenille D et al : Living at the edge: biogeographic patterns of habitat segregation conform to speciation by niche expansion inAnopheles gambiae .BMC Ecol 2009, 9(1):16. - 145.
Kulkarni MA, Malima R, Mosha FW, Msangi S, Mrema E, Kabula B, Lawrence B, Kinung'hi S, Swilla J, Kisinza W 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.Trop Med Int Health 2007, 12(9):1061-1073. - 146.
Kabula B, Tungu P, Matowo J, Kitau J, Mweya C, Emidi B, Masue D, Sindato C, Malima R, Minja J et al : Susceptibility status of malaria vectors to insecticides commonly used for malaria control in Tanzania.Trop Med Int Health 2012, 17(6):742-750. - 147.
Coleman M, Casimiro S, Hemingway J, Sharp B: Operational impact of DDT reintroduction for malaria control on Anopheles arabiensis in Mozambique.J Med Entomol 2008, 45(5):885-890. - 148.
Ratovonjato J, Le Goff G, Rajaonarivelo E, Rakotondraibe EM, Robert V: [Recent observations on the sensitivity to pyrethroids and DDT of Anopheles arabiensis andAnopheles funestus in the central Highlands of Madagascar; preliminary results on the absence of thekdr mutation inAn. arabiensis ].Arch Inst Pasteur Madagascar 2003, 69(1-2):63-69. - 149.
Ramphul U, Boase T, Bass C, Okedi LM, Donnelly MJ, Muller P: Insecticide resistance and its association with target-site mutations in natural populations of Anopheles gambiae from eastern Uganda.Trans R Soc Trop Med Hyg 2009. - 150.
Verhaeghen K, Bortel WV, Roelants P, Okello PE, Talisuna A, Coosemans M: Spatio-temporal patterns in kdr frequency in permethrin and DDT resistantAnopheles gambiae s.s. from Uganda.Am J Trop Med Hyg 2010, 82(4):566-573. - 151.
Abate A, Hadis M: Susceptibility of Anopheles gambiae s.l. to DDT, malathion, permethrin and deltamethrin in Ethiopia.Trop Med Int Health 2011, 16(4):486-491. - 152.
Ochomo E, Bayoh MN, Brogdon WG, Gimnig JE, Ouma C, Vulule JM, Walker ED: Pyrethroid resistance in Anopheles gambiae s.s. andAnopheles arabiensis in western Kenya: phenotypic, metabolic and target site characterizations of three populations.Med Vet Entomol 2012. - 153.
Mathias DK, Ochomo E, Atieli F, Ombok M, Bayoh MN, Olang G, Muhia D, Kamau L, Vulule JM, Hamel MJ et al : Spatial and temporal variation in thekdr allele L1014S inAnopheles gambiae s.s. and phenotypic variability in susceptibility to insecticides in Western Kenya.Malar J 2011, 10:10. - 154.
Chanda E, Hemingway J, Kleinschmidt I, Rehman AM, Ramdeen V, Phiri FN, Coetzer S, Mthembu D, Shinondo CJ, Chizema-Kawesha E et al : Insecticide resistance and the future of malaria control in Zambia.PLoS ONE 2011, 6(9):e24336. - 155.
Mouatcho JC, Munhenga G, Hargreaves K, Brooke BD, Coetzee M, Koekemoer LL: Pyrethroid resistance in a major African malaria vector Anopheles arabiensis from Mamfene, northern KwaZulu-Natal, South Africa.South African Journal of Science 2009, 105(3-4):127-131. - 156.
Mouatcho JC, Hargreaves K, Koekemoer LL, Brooke BD, Oliver SV, Hunt RH, Coetzee M: Indoor collections of the Anopheles funestus group (Diptera: Culicidae) in sprayed houses in northern KwaZulu-Natal, South Africa.Malar J 2007, 6:30. - 157.
Brooke BD, Kloke G, Hunt RH, Koekemoer LL, Temu EA, Taylor ME, Small G, Hemingway J, Coetzee M: Bioassay and biochemical analyses of insecticide resistance in southern African Anopheles funestus (Diptera: Culicidae).Bulletin of Entomological Research 2001, 91(4):265-272. - 158.
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(6):e11010. - 159.
Kloke RG, Nhamahanga E, Hunt RH, Coetzee M: Vectorial status and insecticide resistance of Anopheles funestus from a sugar estate in southern Mozambique.Parasit Vectors 2011, 4:16. - 160.
Hunt R, Edwardes M, Coetzee M: Pyrethroid resistance in southern African Anopheles funestus extends to Likoma Island in Lake Malawi.Parasit Vectors 2010, 3:122. - 161.
Wondji CS, Coleman M, Kleinschmidt I, Mzilahowa T, Irving H, Ndula M, Rehman A, Morgan J, Barnes KG, Hemingway J: Impact of pyrethroid resistance on operational malaria control in Malawi. Proc Natl Acad Sci U S A 2012, 109(47):19063-19070. - 162.
Anto F, Asoala V, Anyorigiya T, Oduro A, Adjuik M, Owusu-Agyei S, Dery D, Bimi L, Hodgson A: Insecticide resistance profiles for malaria vectors in the Kassena-Nankana district of Ghana. Malaria Journal 2009, 8(1):81. - 163.
Djouaka R, Irving H, Tukur Z, Wondji CS: Exploring mechanisms of multiple insecticide resistance in a population of the malaria vector Anopheles funestus in Benin.PLoS ONE 2011, 6(11):e27760. - 164.
Dabire KR, Baldet T, Diabate A, Dia I, Costantini C, Cohuet A, Guiguemde TR, Fontenille D: Anopheles funestus (Diptera: Culicidae) in a humid savannah area of western Burkina Faso: bionomics, insecticide resistance status, and role in malaria transmission.J Med Entomol 2007, 44(6):990-997. - 165.
Faraj C, Adlaoui E, Brengues C, Fontenille D, Lyagoubi M: [Resistance of Anopheles labranchiae to DDT in Morocco: identification of the mechanisms and choice of replacement insecticide].Eastern Mediterranean health journal = La revue de sante de la Mediterranee orientale = al-Majallah al-sihhiyah li-sharq al-mutawassit 2008, 14(4):776-783. - 166.
Mostafa AA, Allam KA: Studies on the present status of insecticides resistance on mosquitoes using the diagnostic dosages in El-Fayium Governorate, a spot area of malaria in Egypt. J Egypt Soc Parasitol 2001, 31(1):177-186. - 167.
Balkew M, Elhassan I, Ibrahim M, GebreMichael T, Engers H: Very high DDT-resistant population of Anopheles pharoensis Theobald (Diptera: Culicidae) from Gorgora, northern Ethiopia.Parasite 2006, 13(4):327-239. - 168.
Yadouleton AW, Padonou G, Asidi A, Moiroux N, Bio-Banganna S, Corbel V, N'Guessan R, Gbenou D, Yacoubou I, Gazard K et al : Insecticide resistance status inAnopheles gambiae in southern Benin.Malar J 2010, 9:83. - 169.
Pinto J, Lynd A, Vicente JL, Santolamazza F, Randle NP, Gentile G, Moreno M, Simard F, Charlwood JD, do Rosario VE et al : Multiple Origins of Knockdown Resistance Mutations in the Afrotropical Mosquito VectorAnopheles gambiae .PLoS ONE 2007, 2(11):e1243. - 170.
della Torre A, Fanello C, Akogbeto M, Dossou-yovo J, Favia G, Petrarca V, Coluzzi M: Molecular evidence of incipient speciation within Anopheles gambiae s.s. in West Africa.Insect Mol Biol 2001, 10(1):9-18. - 171.
Weill M, Chandre F, Brengues C, Manguin S, Akogbeto M, Pasteur N, Guillet P, Raymond M: The kdr mutation occurs in the Mopti form ofAnopheles gambiae s.s. through introgression.Insect Molecular Biology 2000, 9(5):451-455. - 172.
Reimer LJ, Tripet F, Slotman M, Spielman A, Fondjo E, Lanzaro GC: An unusual distribution of the kdr gene among populations ofAnopheles gambiae on the island of Bioko, Equatorial Guinea.Insect Mol Biol 2005, 14(6):683-688. - 173.
Protopopoff N, Verhaeghen K, Van Bortel W, Roelants P, Marcotty T, Baza D, D'Alessandro U, Coosemans M: A significant increase in kdr inAnopheles gambiae is associated with an intensive vector control intervention in Burundi highlands.Trop Med Int Health 2008, 13(12):1479-1487. - 174.
Pinto J, Lynd A, Elissa N, Donnelly MJ, Costa C, Gentile G, Caccone A, do Rosario VE: Co-occurrence of East and West African kdr mutations suggests high levels of resistance to pyrethroid insecticides inAnopheles gambiae from Libreville, Gabon.Med Vet Entomol 2006, 20(1):27-32. - 175.
Moreno M, Vicente JL, Cano J, Berzosa PJ, de Lucio A, Nzambo S, Bobuakasi L, Buatiche JN, Ondo M, Micha F et al : Knockdown resistance mutations (kdr ) and insecticide susceptibility to DDT and pyrethroids inAnopheles gambiae from Equatorial Guinea.Trop Med Int Health 2008, 13(3):430-433. - 176.
Verhaeghen K, Van Bortel W, Roelants P, Backeljau T, Coosemans M: Detection of the East and West African kdr mutation inAnopheles gambiae andAnopheles arabiensis from Uganda using a new assay based on FRET/Melt Curve analysis.Malaria Journal 2006, 5(1):16. - 177.
Koekemoer LL, Spillings BL, Christian RN, Lo TC, Kaiser ML, Norton RA, Oliver SV, Choi KS, Brooke BD, Hunt RH et al : Multiple insecticide resistance inAnopheles gambiae (Diptera: Culicidae) from Pointe Noire, Republic of the Congo.Vector Borne Zoonotic Dis 2011, 11(8):1193-1200. - 178.
Reimer L, Fondjo E, Patchoke S, Diallo B, Lee Y, Ng A, Ndjemai HM, Atangana J, Traore SF, Lanzaro G et al : Relationship betweenkdr mutation and resistance to pyrethroid and DDT insecticides in natural populations ofAnopheles gambiae .J Med Entomol 2008, 45(2):260-266. - 179.
Badolo A, Traore A, Jones CM, Sanou A, Flood L, Guelbeogo WM, Ranson H, Sagnon N: Three years of insecticide resistance monitoring in Anopheles gambiae in Burkina Faso: resistance on the rise?Malar J 2012, 11:232. - 180.
Santolamazza F, Calzetta M, Etang J, Barrese E, Dia I, Caccone A, Donnelly MJ, Petrarca V, Simard F, Pinto J et al : Distribution of knock-down resistance mutations inAnopheles gambiae molecular forms in west and west-central Africa.Malar J 2008, 7(1):74. - 181.
Ridl F, Bass C, Torrez M, Govender D, Ramdeen V, Yellot L, Edu A, Schwabe C, Mohloai P, Maharaj R et al : A pre-intervention study of malaria vector abundance in Rio Muni, Equatorial Guinea: Their role in malaria transmission and the incidence of insecticide resistance alleles.Malaria Journal 2008, 7(1):194. - 182.
Reimer L, Fondjo E, Patchok, Salomon, Diallo B, Lee Y, Ng A, Ndjemai HM, Atangana J, Traore SF et al : Relationship Betweenkdr Mutation and Resistance to Pyrethroid and DDT Insecticides in Natural Populations ofAnopheles gambiae .Journal of Medical Entomology 2008, 45:260-266. - 183.
Matambo TS, Abdalla H, Brooke BD, Koekemoer LL, Mnzava A, Hunt RH, Coetzee M: Insecticide resistance in the malarial mosquito Anopheles arabiensis and association with thekdr mutation.Medical and Veterinary Entomology 2007, 21(1):97-102. - 184.
Kulkarni M, Rowland M, Alifrangis M, Mosha F, Matowo J, Malima R, Peter J, Kweka E, Lyimo I, Magesa S et al : Occurrence of the leucine-to-phenylalanine knockdown resistance (kdr ) mutation inAnopheles arabiensis populations in Tanzania, detected by a simplified high-throughput SSOP-ELISA method.Malaria Journal 2006, 5(1):56. - 185.
Chen H, Githeko AK, Githure JI, Mutunga J, Zhou G, Yan G: Monooxygenase Levels and Knockdown Resistance ( kdr ) Allele Frequencies inAnopheles gambiae andAnopheles arabiensis in Kenya.Journal of Medical Entomology 2008, 45:242-250. - 186.
Etang J, Manga L, Toto JC, Guillet P, Fondjo E, Chandre F: Spectrum of metabolic-based resistance to DDT and pyrethroids in Anopheles gambiae s.l. populations from Cameroon.J Vector Ecol 2007, 32(1):123-133. - 187.
Hargreaves K, Hunt RH, Brooke BD, Mthembu J, Weeto MM, Awolola TS, Coetzee M: Anopheles arabiensis andAn. quadriannulatus resistance to DDT in South Africa.Med Vet Entomol 2003, 17(4):417-422. - 188.
Amenya DA, Naguran R, Lo TC, Ranson H, Spillings BL, Wood OR, Brooke BD, Coetzee M, Koekemoer LL: Over expression of a cytochrome P450 (CYP6P9) in a major African malaria vector, Anopheles funestus , resistant to pyrethroids.Insect Mol Biol 2008, 17(1):19-25. - 189.
Somboon P, Prapanthadara LA, Suwonkerd W: Insecticide susceptibility tests of Anopheles minimus s.l.,Aedes aegypti ,Aedes albopictus , andCulex quinquefasciatus in northern Thailand.Southeast Asian J Trop Med Public Health 2003, 34(1):87-93. - 190.
Verhaeghen K, Van Bortel W, Trung HD, Sochantha T, Coosemans M: Absence of knockdown resistance suggests metabolic resistance in the main malaria vectors of the Mekong region. Malar J 2009, 8:84. - 191.
Chareonviriyaphap T, Rongnoparut P, Chantarumporn P, Bangs MJ: Biochemical detection of pyrethroid resistance mechanisms in Anopheles minimus in Thailand.J Vector Ecol 2003, 28(1):108-116. - 192.
Rodpradit P, Boonsuepsakul S, Chareonviriyaphap T, Bangs MJ, Rongnoparut P: Cytochrome P450 genes: molecular cloning and overexpression in a pyrethroid-resistant strain of Anopheles minimus mosquito.J Am Mosq Control Assoc 2005, 21(1):71-79. - 193.
Verhaeghen K, Van Bortel W, Trung HD, Sochantha T, Keokenchanh K, Coosemans M: Knockdown resistance in Anopheles vagus ,An. sinensis ,An. paraliae andAn. peditaeniatus populations of the Mekong region.Parasit Vectors 2011, 3(1):59. - 194.
Kang S, Jung J, Lee S, Hwang H, Kim W: The polymorphism and the geographical distribution of the knockdown resistance ( kdr ) ofAnopheles sinensis in the Republic of Korea.Malar J 2012, 11:151. - 195.
Tan WL, Wang ZM, Li CX, Chu HL, Xu Y, Dong YD, Wang ZC, Chen DY, Liu H, Liu DP et al : First report on co-occurrence knockdown resistance mutations and susceptibility to beta-cypermethrin inAnopheles sinensis from Jiangsu Province, China.PLoS ONE 2012, 7(1):e29242. - 196.
Syafruddin D, Hidayati AP, Asih PB, Hawley WA, Sukowati S, Lobo NF: Detection of 1014F kdr mutation in four major Anopheline malaria vectors in Indonesia.Malar J 2010, 9:315. - 197.
Singh OP, Dykes CL, Das MK, Pradhan S, Bhatt RM, Agrawal OP, Adak T: Presence of two alternative kdr -like mutations, L1014F and L1014S, and a novel mutation, V1010L, in the voltage gated Na+ channel ofAnopheles culicifacies from Orissa, India.Malar J 2010, 9:146. - 198.
Mishra AK, Chand SK, Barik TK, Dua VK, Raghavendra K: Insecticide resistance status in Anopheles culicifacies in Madhya Pradesh, central India.J Vector Borne Dis 2012, 49(1):39-41. - 199.
Sharma SN, Shukla RP, Raghavendra K: Susceptibility status of An. fluviatilis andAn. culicifacies to DDT, deltamethrin and lambdacyhalothrin in District Nainital, Uttar Pradesh.Indian J Malariol 1999, 36(3-4):90-93. - 200.
Singh OP, Dykes CL, Lather M, Agrawal OP, Adak T: Knockdown resistance ( kdr )-like mutations in the voltage-gated sodium channel of a malaria vectorAnopheles stephensi and PCR assays for their detection.Malar J 2011, 10:59. - 201.
Tikar SN, Mendki MJ, Sharma AK, Sukumaran D, Veer V, Prakash S, Parashar BD: Resistance status of the malaria vector mosquitoes, Anopheles stephensi andAnopheles subpictus towards adulticides and larvicides in arid and semi-arid areas of India.J Insect Sci 2011, 11:85. - 202.
Baruah K, Lal S: A report on the susceptibility status of Anopheles minimus (Theobald) against DDT and deltamethrin in three districts of Assam.J Vector Borne Dis 2004, 41(1-2):42-44. - 203.
Karunaratne SH, Hemingway J: Malathion resistance and prevalence of the malathion carboxylesterase mechanism in populations of mosquito vectors of disease in Sri Lanka. Bull World Health Organ 2001, 79(11):1060-1064. - 204.
Kelly-Hope LA, Yapabandara AM, Wickramasinghe MB, Perera MD, Karunaratne SH, Fernando WP, Abeyasinghe RR, Siyambalagoda RR, Herath PR, Galappaththy GN et al : Spatiotemporal distribution of insecticide resistance inAnopheles culicifacies andAnopheles subpictus in Sri Lanka.Trans R Soc Trop Med Hyg 2005, 99(10):751-761. - 205.
Perera MD, Hemingway J, Karunaratne SP: Multiple insecticide resistance mechanisms involving metabolic changes and insensitive target sites selected in anopheline vectors of malaria in Sri Lanka. Malar J 2008, 7:168. - 206.
Surendran SN, Jude PJ, Weerarathne TC, Parakrama Karunaratne SH, Ramasamy R: Variations in susceptibility to common insecticides and resistance mechanisms among morphologically identified sibling species of the malaria vector Anopheles subpictus in Sri Lanka.Parasit Vectors 2012, 5:34. - 207.
Mittal PK, Wijeyaratne P, Pandey S: Status of Insecticide Resistance of Malaria, Kala-azar and Japanese Encephalitis Vectors in Bangladesh, Bhutan, India and Nepal (BBIN). In. Edited by Project EH. Washington 2004. - 208.
Rowland M: Location of the gene for malathion resistance in Anopheles stephensi (Diptera: Culicidae) from Pakistan.J Med Entomol 1985, 22(4):373-380. - 209.
Abai MR, Mehravaran A, Vatandoost H, Oshaghi MA, Javadian E, Mashayekhi M, Mosleminia A, Piyazak N, Edallat H, Mohtarami F et al : Comparative performance of imagicides onAnopheles stephensi , main malaria vector in a malarious area, southern Iran.J Vector Borne Dis 2008, 45(4):307-312. - 210.
Lak SH, vatandoost H, Entezarmahdi MR, Ashraf H, Abai MR, Nazari M: Monitoring of Insecticide Resistance in Anopheles sacharovi (Favre, 1903) in Borderline of Iran, Armenia, Naxcivan and Turkey, 2001.Iranian J Publ Health 2002, 31(3-4):96-99. - 211.
Vatandoost H, Mashayekhi M, Abaie MR, Aflatoonian MR, Hanafi-Bojd AA, Sharifi I: Monitoring of insecticides resistance in main malaria vectors in a malarious area of Kahnooj district, Kerman province, southeastern Iran. J Vector Borne Dis 2005, 42(3):100-108. - 212.
Malcolm CA: Current status of pyrethroid resistance in anophelines. Parasitol Today 1988, 4(7):S13-15. - 213.
Quinones ML, Suarez MF: Irritability to DDT of natural populations of the primary malaria vectors in Colombia. J Am Mosq Control Assoc 1989, 5(1):56-59. - 214.
Suarez MF, Quinones ML, Palacios JD, Carrillo A: First record of DDT resistance in Anopheles darlingi .J Am Mosq Control Assoc 1990, 6(1):72-74. - 215.
Fonseca-Gonzalez I: Estatus de la resistencia a insecticidas de los vectores primarios de malaria y dengue en Antioquia, Chocó, Norte de Santander y Putumayo, Colombia. Universidad de Antioquia, Colombia; 2008. - 216.
Fonseca-Gonzalez I, Cardenas R, Quinones ML, McAllister J, Brogdon WG: Pyrethroid and organophosphates resistance in Anopheles (N.) nuneztovari Gabaldon populations from malaria endemic areas in Colombia.Parasitol Res 2009, 105(5):1399-1409. - 217.
Chareonviriyaphap T, Golenda CF, Roberts DR, Andre RG: Identification of Elevated Esterase Activity in a Pyrethroid-Resistant Population of Anopheles albimanus Wiedemann.ScienceAsia 1999, 25 153-156. - 218.
Brogdon WG, McAllister JC, Corwin AM, Cordon Rosales C: Independent selection of multiple mechanisms for pyrethroid resistance in Guatemalan Anopheles albimanus (Diptera: Culicidae).Journal of Economic Entomology 1999, 92(2):298-302. - 219.
Zamora Perea E, Balta Leon R, Palomino Salcedo M, Brogdon WG, Devine GJ: Adaptation and evaluation of the bottle assay for monitoring insecticide resistance in disease vector mosquitoes in the Peruvian Amazon. Malar J 2009, 8:208. - 220.
Hemingway J, Penilla RP, Rodriguez AD, James BM, Edge W, Rogers H, Rodriguez MH: Resistance management strategies in malaria vector mosquito control. A large-scale field trial in Southern Mexico. Pesticide Science 1997, 51(3):375-382. - 221.
Dzul FA, Patricia Penilla R, Rodriguez AD: [Susceptibility and insecticide resistance mechanisms in Anopheles albimanus from the southern Yucatan Peninsula, Mexico].Salud Publica Mex 2007, 49(4):302-311. - 222.
South Africa Department of Health: Malaria Updates. In. Pretoria, S.A: S.A.D.H.; 2003. - 223.
Maharaj R, Mthembu DJ, Sharp BL: Impact of DDT re-introduction on malaria transmission in KwaZulu-Natal. S Afr Med J 2005, 95(11):871-874. - 224.
Roberts DR, Manguin S, Mouchet J: DDT house spraying and re-emerging malaria. Lancet 2000, 356(9226):330-332. - 225.
Protopopoff N, Van Bortel W, Marcotty T, Van Herp M, Maes P, Baza D, D'Alessandro U, Coosemans M: Spatial targeted vector control in the highlands of Burundi and its impact on malaria transmission. Malar J 2007, 6:158. - 226.
Trape J-F, Tall A, Diagne N, Ndiath O, Ly AB, Faye J, Dieye-Ba F, Roucher C, Bouganali C, Badiane A et al : Malaria morbidity and pyrethroid resistance after the introduction of insecticide-treated bednets and artemisinin-based combination therapies: a longitudinal study.The Lancet Infectious Diseases 2011. - 227.
Lengeler C: Insecticide-treated bed nets and curtains for preventing malaria. Cochrane Database of Systematic reviews 2009(2):1-58. - 228.
Kitau J, Oxborough RM, Tungu PK, Matowo J, Malima RC, Magesa SM, Bruce J, Mosha FW, Rowland MW: Species shifts in the Anopheles gambiae complex: do LLINs successfully controlAnopheles arabiensis ?PLoS ONE 2012, 7(3):e31481. - 229.
Bradley J, Matias A, Schwabe C, Vargas D, Monti F, Nseng G, Kleinschmidt I: Increased risks of malaria due to limited residual life of insecticide and outdoor biting versus protection by combined use of nets and indoor residual spraying on Bioko Island, Equatorial Guinea. Malar J 2012, 11:242. - 230.
Henry MC, Assi SB, Rogier C, Dossou-Yovo J, Chandre F, Guillet P, Carnevale P: Protective efficacy of lambda-cyhalothrin treated nets in Anopheles gambiae pyrethroid resistance areas of Cote d'Ivoire.Am J Trop Med Hyg 2005, 73(5):859-864. - 231.
Corbel V, Akogbeto M, Damien GB, Djenontin A, Chandre F, Rogier C, Moiroux N, Chabi J, Banganna B, Padonou GG et al : Combination of malaria vector control interventions in pyrethroid resistance area in Benin: a cluster randomised controlled trial.Lancet Infect Dis 2012, 12(8):617-626. - 232.
Darriet F, N' Guessan R, Koffi AA, Konan L, Doannio JMC, Chandre F, Carnevale P: Impact of the resistance to pyrethroids on the efficacy of impregnated bednets used as a means of prevention against malaria: results of the evaluation carried out with deltamethrin SC in experimental huts. Bulletin de la Société de Pathologie Exotique 2000, 93(2):131-134. - 233.
Corbel V, Chandre F, Brengues C, Akogbeto M, Lardeux F, Hougard JM, Guillet P: Dosage-dependent effects of permethrin-treated nets on the behaviour of Anopheles gambiae and the selection of pyrethroid resistance.Malar J 2004, 3(1):22. - 234.
N'Guessan R, Corbel V, Akogbeto 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(2):199-206. - 235.
N'Guessan R, Asidi A, Boko P, Odjo A, Akogbeto M, Pigeon O, Rowland M: An experimental hut evaluation of PermaNet(R) 3.0, a deltamethrin-piperonyl butoxide combination net, against pyrethroid-resistant Anopheles gambiae andCulex quinquefasciatus mosquitoes in southern Benin.Trans R Soc Trop Med Hyg 2010, 104(12):758-765. - 236.
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(7):1101-1106. - 237.
Osse R, Gnanguenon V, Sezonlin M, Aikpon R, Padonou G, Yadouleton A, Akogbeto M: Relationship between the presence of kdr and Ace-1 mutations and the infection withPlasmodium falciparum inAnopheles gambiae s.s. in Benin.Journal of Parassitology & Vector Biology 2012, 4(3):31-39. - 238.
Moiroux N, Boussari O, Djenontin A, Damien G, Cottrell G, Henry MC, Guis H, Corbel V: Dry season determinants of malaria disease and net use in Benin, West Africa. PLoS ONE 2012, 7(1):e30558. - 239.
Poupardin R, Reynaud S, Strode C, Ranson H, Vontas J, David JP: Cross-induction of detoxification genes by environmental xenobiotics and insecticides in the mosquito Aedes aegypti : impact on larval tolerance to chemical insecticides.Insect Biochem Mol Biol 2008, 38(5):540-551. - 240.
IRAC: Prevention and Management of Insecticide Resistance in Vectors of Public Health Importance In: Resistance Management for Sustainable Agriculture and Improved Public Health : Second Edition 2010 Insecticide Resistance Action Commitee; 2010: 72pp. - 241.
Georghiou GP, Taylor CE: Genetic and biological influences in the evolution of insecticide resistance. Journal of Economic Entomology 1977, 70(3):319-323. - 242.
Denholm I, Rowland MW: Tactics for managing pesticide resistance in arthropods: theory and practice. Annu Rev Entomol 1992, 37:91-112. - 243.
Djogbenou L, Weill M, Hougard JM, Raymond M, Akogbeto M, Chandre F: Characterization of insensitive acetylcholinesterase (ace-1R) in Anopheles gambiae (Diptera: Culicidae): resistance levels and dominance.J Med Entomol 2007, 44(5):805-810. - 244.
Berticat C, Bonnet J, Duchon S, Agnew P, Weill M, Corbel V: Costs and benefits of multiple resistance to insecticides for Culex quinquefasciatus mosquitoes.BMC Evol Biol 2008, 8:104. - 245.
Moore JH, Williams SM: Traversing the conceptual divide between biological and statistical epistasis: systems biology and a more modern synthesis. Bioessays 2005, 27(6):637-646. - 246.
Shono T, Zhang L, Scott JG: Indoxacarb resistance in the house fly, Musca domestica .Pesticide Biochemistry and Physiology 2004, 80(2):106-112. - 247.
Shono T, Kasai S, Kamiya E, Kono Y, Scott JG: Genetics and mechanisms of permethrin resistance in the YPER strain of house fly. Pesticide Biochemistry and Physiology 2002, 73(1):27-36. - 248.
Scott JG, Shono T, Georghiou GP: Genetic analysis of permethrin resistance in the house fly, Musca domestica L.Experientia 1984, 40(12):1416-1418. - 249.
Hardstone MC, Leichter CA, Scott JG: Multiplicative interaction between the two major mechanisms of permethrin resistance, kdr and cytochrome P450-monooxygenase detoxification, in mosquitoes.J Evol Biol 2009, 22(2):416-423. - 250.
Berticat C, Boquien G, Raymond M, Chevillon C: Insecticide resistance genes induce a mating competition cost in Culex pipiens mosquitoes.Genet Res 2002, 79(1):41-47. - 251.
Agnew P, Berticat C, Bedhomme S, Sidobre C, Michalakis Y: Parasitism increases and decreases the costs of insecticide resistance in mosquitoes. Evolution Int J Org Evolution 2004, 58(3):579-586. - 252.
Foster SP, Harrington R, Devonshire AL, Denholm I, Devine GJ, Kenward MG: Comparative survival of insecticide-susceptible and resistant peach-potato aphids, Myzus persicae (Sulzer) (Hemiptera: Aphididae), in low temperature field trials.Bull Ent Res 1996, 86:17-27. - 253.
Shi MA, Lougarre A, Alies C, Fremaux I, Tang ZH, Stojan J, Fournier D: Acetylcholinesterase alterations reveal the fitness cost of mutations conferring insecticide resistance. BMC Evol Biol 2004, 4:5. - 254.
Djogbenou L, Noel V, Agnew P: Costs of insensitive acetylcholinesterase insecticide resistance for the malaria vector Anopheles gambiae homozygous for the G119S mutation.Malar J 2010, 9(1):12. - 255.
Brogdon WG, McAllister JC: Insecticide resistance and vector control. Emerg Infect Dis 1998, 4(4):605-613. - 256.
Diabate A, Baldet T, Chandre F, Akoobeto M, Guiguemde TR, Darriet F, Brengues C, Guillet P, Hemingway J, Small GJ et al : The role of agricultural use of insecticides in resistance to pyrethroids inAnopheles gambiae s.l. in Burkina Faso.Am J Trop Med Hyg 2002, 67(6):617-622. - 257.
Yadouleton A, Martin T, Padonou G, Chandre F, Asidi A, Djogbenou L, Dabire R, Aikpon R, Boko M, Glitho I et al : Cotton pest management practices and the selection of pyrethroid resistance inAnopheles gambiae population in northern Benin.Parasit Vectors 2011, 4:60. - 258.
Harrison G: Mosquitoes, malaria and man: A history of hostilities since 1880.; 1978. - 259.
Read AF, Lynch PA, Thomas MB: How to make evolution-proof insecticides for malaria control. PLoS Biol 2009, 7(4):e1000058. - 260.
Roush RT, Hoy CW, Ferro DN, Tingey WM: Insecticide resistance in the Colorado potato beetle (Coleoptera: Chrysomelidae): influence of crop rotation and insecticide use. Journal of Economic Entomology 1990, 83(2):315-319. - 261.
Georghiou GP: Insecticide resistance and prospects for its management. Residue Reviews 1980, 76:131-145. - 262.
Tabashnik BE: Managing resistance with multiple pesticide tactics: theory, evidence, and recommendations. J Econ Entomol 1989, 82(5):1263-1269. - 263.
Chitnis N, Schapira A, Smith T, Steketee R: Comparing the effectiveness of malaria vector-control interventions through a mathematical model. Am J Trop Med Hyg 2010, 83(2):230-240. - 264.
Yakob L, Dunning R, Yan G: Indoor residual spray and insecticide-treated bednets for malaria control: theoretical synergisms and antagonisms. J R Soc Interface 2011, 8(59):799-806. - 265.
World Health Organization: Global strategic framework for integrated vector management. Geneva; 2004. - 266.
Curtis CF: Theoretical models of the use of insecticide mixtures for management of resistance. Bull Ent Res 1985, 75: 259-265. - 267.
Hougard JM, Poudiougo P, Guillet P, Back C, Akpoboua LK, Quillevere D: Criteria for the selection of larvicides by the Onchocerciasis Control Programme in west Africa. Ann Trop Med Parasitol 1993, 87(5):435-442. - 268.
WHO: Pesticides and their application for the control of vectors and pests of public health importance; Sixth edition. In. Edited by WHO/CDS/NTD/WHOPES/GCDPP/2006.1 WHO, Geneva; 2006: 1-125. - 269.
Corbel V, Chabi J, Dabire RK, Etang J, Nwane P, Pigeon O, Akogbeto M, Hougard JM: Field efficacy of a new mosaic long-lasting mosquito net (PermaNet 3.0) against pyrethroid-resistant malaria vectors: a multi centre study in Western and Central Africa. Malar J 2010, 9:113. - 270.
Killeen GF, Okumu FO, N'Guessan R, Coosemans M, Adeogun A, Awolola S, Etang J, Dabire RK, Corbel V: The importance of considering community-level effects when selecting insecticidal malaria vector products. Parasit Vectors 2011, 4:160. - 271.
Mani GS: Evolution of resistance in the presence of two insecticides. Genetics 1985, 109(4):761-783. - 272.
Roush RT: Designing resistance management programs: how can you choose? Pesticide Science 1989, 26(4):423-441. - 273.
Hougard JM, Corbel V, N'Guessan R, Darriet F, Chandre F, Akogbeto M, Baldet T, Guillet P, Carnevale P, Traore-Lamizana M: Efficacy of mosquito nets treated with insecticide mixtures or mosaics against insecticide resistant Anopheles gambiae andCulex quinquefasciatus (Diptera: Culicidae) in Cote d'Ivoire.Bull Entomol Res 2003, 93(6):491-498. - 274.
Asidi AN, N'Guessan R, Koffi AA, Curtis CF, Hougard JM, Chandre F, Corbel V, Darriet F, Zaim M, Rowland MW: Experimental hut evaluation of bednets treated with an organophosphate (chlorpyrifos-methyl) or a pyrethroid (lambdacyhalothrin) alone and in combination against insecticide-resistant Anopheles gambiae andCulex quinquefasciatus mosquitoes.Malar J 2005, 4(1):25. - 275.
Ohashi K, Nakada K, Ishiwatari T, Miyaguchi J, Shono Y, Lucas JR, Mito N: Efficacy of pyriproxyfen-treated nets in sterilizing and shortening the longevity of Anopheles gambiae (Diptera: Culicidae).J Med Entomol 2012, 49(5):1052-1058. - 276.
Mosqueira B, Duchon S, Chandre F, Hougard JM, Carnevale P, Mas-Coma S: Efficacy of an insecticide paint against insecticide-susceptible and resistant mosquitoes - part 1: laboratory evaluation. Malar J 2010, 9:340. - 277.
Ngufor C, N'Guessan R, Boko P, Odjo A, Vigninou E, Asidi A, Akogbeto M, Rowland M: Combining indoor residual spraying with chlorfenapyr and long-lasting insecticidal bed nets for improved control of pyrethroid-resistant Anopheles gambiae : an experimental hut trial in Benin.Malar J 2011, 10:343. - 278.
Kleinschmidt I, Schwabe C, Shiva M, Segura JL, Sima V, Mabunda SJ, Coleman M: Combining indoor residual spraying and insecticide-treated net interventions. Am J Trop Med Hyg 2009, 81(3):519-524. - 279.
Okumu FO, Moore SJ: Combining indoor residual spraying and insecticide-treated nets for malaria control in Africa: a review of possible outcomes and an outline of suggestions for the future. Malar J 2011, 10:208. - 280.
Brosseau L, Drame PM, Besnard P, Toto JC, Foumane V, Le Mire J, Mouchet F, Remoue F, Allan R, Fortes F et al : Human antibody response toAnopheles saliva for comparing the efficacy of three malaria vector control methods in Balombo, Angola.PLoS ONE 2012, 7(9):e44189. - 281.
Bill_&_Melinda_Gates_Fondation, Boston_Consulting_Group: Market Assessment for Public Health Pesticide Products. In.; 2007.
Notes
- Cross resistance: occurs when a resistance mechanism, which allows insects to resist one insecticide, also confers resistance to another insecticide. Cross resistance can occur between insecticides from different chemical classes.
- Multiple resistance: occurs when insects develop resistance to several compounds by expressing multiple resistance mechanisms. The different resistance mechanisms can combine to provide resistance to multiple classes of products.
- World Health Organization Pesticide Evaluation Scheme
- Integrated Vector Management can be defined as “a rational decision making process for the optimal use of resources for vector control”. IRM is therefore an integral part of IVM, as only through the active management of insecticide resistance can the available resources be optimally and sustainably used.