First report of field evolved resistance to agrochemicals in dengue mosquito, Aedes albopictus (Diptera: Culicidae), from Pakistan

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Background Agrochemicals have been widely used in Pakistan for several years. This exposes mosquito populations, particularly those present around agricultural settings, to an intense selection pressure for insecticide resistance. The aim of the
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  RESEARCH Open Access First report of field evolved resistance toagrochemicals in dengue mosquito,  Aedesalbopictus  (Diptera: Culicidae), from Pakistan Hafiz Azhar Ali Khan 1* , Waseem Akram 2* , Khurram Shehzad 3 and Essam A Shaalan 4 Abstract Background:  Agrochemicals have been widely used in Pakistan for several years. This exposes mosquitopopulations, particularly those present around agricultural settings, to an intense selection pressure for insecticideresistance. The aim of the present study was to investigate the toxicity of representative agrochemicals againstvarious populations of   Aedes albopictus  (Skuse) collected from three different regions from 2008-2010. Results:  For organophosphates and pyrethroids, the resistance ratios compared with susceptible Lab-PK were inthe range of 157-266 fold for chlorpyrifos, 24-52 fold for profenofos, 41-71 fold for triazofos, and 15-26 fold forcypermethrin, 15-53 fold for deltamethrin and 21-58 fold for lambdacyhalothrin. The resistance ratios forcarbamates and new insecticides were in the range of 13-22 fold for methomyl, 24-30 fold for thiodicarb, and 41-101 fold for indoxacarb, 14-27 fold for emamectin benzoate and 23-50 fold for spinosad. Pair wise comparisons of the log LC 50s  of insecticides revealed correlation among several insecticides, suggesting a possible cross resistancemechanism. Moreover, resistance remained stable across 3 years, suggesting field selection for general fitness hadalso taken place for various populations of   Ae. albopictus . Conclusion:  Moderate to high level of resistance to agrochemicals in Pakistani field populations of   Ae. albopictus  isreported here first time. The geographic extent of resistance is unknown but, if widespread, may lead to problemsin future vector control. Background Dengue fever and dengue hemorrhagic fever (DF/DHF)are vector borne diseases of public health concerns intropical and subtropical parts of the world [1], affectingmillions of people annually  [2]. The incidence of DFand DHF has increased cyclically in Pakistan since thefirst recognized outbreak in 1994 with  Ae. albopictus (Skuse) as the core mosquito vector in this respect [3].Currently, controlling this vector with insecticidal habi-tat spraying remains an important option to minimizethe incidence of dengue fever [4], resulting in resur-gence and development of insecticidal resistance.Insecticide resistance has become a limiting factor inthe use of these compounds in chemical control of many insect pests. The exploration of more efficienttoxic chemicals and other control tactics are necessary with the increasing world population and preservationof species diversity [5]. Frequent use of chemicals, suchas pesticides, coupled with monoculture crops on alarge scale, has generated pesticide resistance in insectpests, resurgence and difficulties in pest management[6]. By 2007, intensive use of pesticides had resulted inat least 553 arthropod species resistant to one or moreclasses of insecticides (organochlorines, organopho-sphates, carbamates and pyrethroids) [7]. Of these, 60percent are agricultural pests and the remaining 40 per-cent are pests of medical importance [8]. Resistance inmedical pests or disease vectors is a serious threat tothe control of vector-borne diseases, owing to the factof insecticide-based strategies such as insecticide treatednets, indoor residual spraying, insecticide treatment of  * Correspondence: azhar_naturalist@yahoo.com; areeba14@yahoo.com 1 Department of Entomology, University College of Agriculture, BahauddinZakariya University, Multan, Pakistan 2 Department of Agri-Entomology, University of Agriculture, Faisalabad,PakistanFull list of author information is available at the end of the article Khan  et al  .  Parasites & Vectors  2011,  4 :146http://www.parasitesandvectors.com/content/4/1/146 © 2011 Khan et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative CommonsAttribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction inany medium, provided the srcinal work is properly cited.  breeding habitats and also because of agricultural prac-tices [9].Various disease vectors are present in agro-ecozonesand are therefore likely to be exposed to chemicals usedto control agricultural pests. Despite the lack of concreteevidence, the massive use of agrochemicals has beenconsidered as a key factor contributing to the emer-gence of vector resistance to insecticides [10]. Insecti-cide resistance in disease vectors due to the selectionpressure from agrochemicals has been reported fromdifferent parts of the world [9,11-15], however, no such reports have so far been reported from Pakistan.Crop losses caused by insect pest in Pakistan are upto56%, and 20-40% of these losses are in cotton,  Gossypiumhirsutum  L. [16]. As a result, agrochemicals with broadtoxicity to target pests and non target organisms are beingwidely used in cotton insect pest management. The over-use of chemicals can lead to the phenomenon of insecti-cide resistance both in target and non target organisms. Inthe current study, we were interested to establish whether  Ae. albopictus , present in cotton cultivated fields, haddeveloped resistance to agrochemicals (organophosphates,carbamates, pyrethroids and newer compounds). Thesechemicals are commonly used for the control of cottoninsect pests in Punjab province, Pakistan [17]. We werealso interested in investigating whether resistance to differ-ent insecticides was increasing or remained the same from2008-2010. The present paper reports the first knownoccurrence of high level resistance to agrochemicals in  Ae.albopictus . The data from such studies are expected tohelp in future management strategies so that the develop-ment of resistance is delayed to a maximum in  Ae. albo- pictus  under field conditions of Pakistan. Materials and methods Mosquitoes We collected natural populations of   Ae. albopictus  fromupper Punjab, Pakistan (Lahore, Sargodha and Faisala-bad districts) from 2008-2010. The growers usually undertake more insecticides on cotton than any othercrop [17]. We therefore collected  Ae. albopictus  popula-tions from cotton fields as there were higher chances of evolution of resistance on cotton than other crops. Thecollection sites within the districts were kept constantacross three years. Moreover, a group of   Ae. Albopictus collected in a date from a determinate place was consid-ered as a population. The samples of larvae and pupaefrom each district were colonized under laboratory con-ditions at 27 ± 1°C and 65 - 70% RH. Larvae were fedon fish food (TetraMin ® ). Adults were kept in plasticcages (30 × 40 × 40) where males were provided cottonwicks soaked with 20% sucrose solution and femaleswere fed on blood of white rats thrice a week [4].Fourth instar larvae of the F1 progeny were reared forbioassays. However, some bioassays were performed onthe F2 generation due to insufficient numbers of F1 pro-geny. The laboratory susceptible strain of   Ae. albopictus was collected in 2005 from mountainous areas of Isla-mabad with zero or very low chemical use and it wasdesignated as Lab-PK. This population was reared in thelaboratory for >40 generations without exposure toinsecticides. The Lab-PK population showed lowestLC 50  values for all the tested insecticides, and hence wasused as a reference strain to calculate resistance ratios. Insecticides Commercial formulations of different insecticides usedfor bioassays consisted of chlorpyrifos (Lorsban 40 EC,Dow Agro Sciences, United Kingdom), profenofos (Cur-acron 50 EC, Syngenta Crop Protection, Switzerland),triazofos (Hostathion 40 EC, Bayer Crop Science), cyper-methrin (Arrivo 10 EC, FMC, Philadelphia; PA), delta-methrin (Decis Super 10.5 EC, Bayer Crop Science,Multan, Pakistan), lambdacyhalothrin (Karate EC Syn-genta Crop Protection Switzerland ), methomyl (LannateLV 239 g [AI]/liter, DuPont, Pakistan), thiodicarb (Lar- vin SC 375 g [AI]/liter, Bayer Crop Science, Multan,Pakistan), indoxacarb (Steward 15SC, DuPont, Pakistan),spinosad (Tracer 24SC, Dow Agro Sciences, UK) andemamectin benzoate (Proclaim 1.9 EC, Syngenta, UK) Bioassays Bioassays were performed as described previously  [18]using acetone solution of insecticides. One milliliter of appropriate insecticide solution was dispensed with apipette above the water surface in each glass beakercontaining 99 ml of distilled water. Each insecticide wastested within a range of seven to eight concentrations todetermine LC 50  value, including controls, and each con-centration was replicated at least four times. Ten 4 th instar larvae were placed in the glass beaker in eachreplication and the total number of larvae tested perconcentration was 40. The bioassays were kept at a tem-perature of 27 ± 1°C, 65% RH and a photoperiod of 14L:10D hours. Mortality was recorded after 24 hours [18],except for spinosad, which was assayed after 48 hoursdue to the slower acting nature of this insecticide. Lar- vae were considered dead if they could not be inducedto move when probed with a probe. Stability of resistance A decline or increase in resistance to the tested insecti-cides in field populations from 1 year to the next wasmeasured by calculating R values i.e., respond permonth. The R values were estimated as below: R = [log(final LC 50 ) − log(initial LC 50 )]/ n , Khan  et al  .  Parasites & Vectors  2011,  4 :146http://www.parasitesandvectors.com/content/4/1/146Page 2 of 11  Where  ‘ n ’    is the number of months (6 months) afterwhich a second population was collected from the samefield. Decline or increase in resistance is presented in -and/or + values of   R  [16]. Data analysis Mortality data, where necessary, were corrected by Abbott ’ s formula [19]. Data were analyzed using probitanalysis based on Finney (1971) [20] to determine theLC 50  values and their 95% fiducial limits (FLs) usingMINITAB 15 statistical software [21]. Due to the inher-ent variability of bioassays, pair wise comparisons of LC 50  values were made, and if 95% FLs of two treat-ments did not overlap at 1% level of significance, they were considered significant [22]. Resistance ratios (RRs)were calculated by dividing the LC 50  values of fieldpopulations with LC 50  of susceptible Lab-PK. To deter-mine cross resistance among the tested insecticides, pairwise correlation coefficients ( r  ) of log LC 50  values of thefield populations were also calculated. The slopes of regression lines were compared using  t  -test in Statistix8.1 [23].To determine insecticide resistance, the level of insec-ticide resistance was scaled by using resistance ratios(RRs) in terms of widely accepted values as follows: sus-ceptibility (RR = 1), low resistance (RR = 2-10), moder-ate resistance (RR = 11-30), high resistance (RR = 31-100) and a very high resistance (RR > 100) [24]. Results Toxicity of insecticides to susceptible population The results obtained from the bioassays with the Lab-PK population (Table 1, 2) revealed that chlorpyrifoswas significantly more toxic (non overlapping of 95%FL; P < 0.01) than the insecticides tested viz., profeno-fos, triazofos, cypermethrin, deltamethrin, lambdacyhalo-thrin, methomyl, thiodicarb, indoxacarb, emamectinbenzoate and spinosad. Emamectin benzoate was theleast effective compound than the other insecticidestested. The slopes of regression lines of all the insecti-cides were similar (P > 0.05). Toxicity of insecticides to field population The toxicity of all eleven insecticides against field popu-lation was significantly lower than Lab-PK (95% FL didnot overlap, Table 1, 2). Organophosphates The levels of resistance to chlorpyrifos in samples fromall the three districts of Punjab were generally very high,with resistance ratios 157-266 fold. All the field popula-tions tested with chlorpyrifos in 3 consecutive yearsshowed very high levels of resistance (RR > 100). Thehighest level of resistance (266 fold) was observed inMarch 2009 from Faisalabad, whereas the lowest (157fold) was from Lahore in March 2009 (Table 1). Theslopes of regression lines of all the populations were sig-nificantly shallower than Lab-PK population (P < 0.05).Among 15 populations tested for profenofos, fivepopulations had moderate levels of resistance (24-26fold) than the Lab-PK population, and the remaining 10populations had high levels of resistance (34-52 fold).The highest level of resistance was found in populationfrom Faisalabad in March 2010, whereas the lowest levelwas found in population from Sargodha in September2008 (Table 1). The slopes of regression lines of all thepopulations were significantly shallower than the Lab-PK population (P < 0.05).All the 15 populations tested for triazofos had highlevels of resistance (41-71 fold). The highest level of resistance was seen in populations from Sargodha inSeptember 2009, whereas the lowest level was observedin populations from Lahore in September 2009 (Table1). Pyrethroids Moderate levels of resistance was found in all the popu-lations tested against cypermethrin (15-26 fold, Table 1)compared with the lab-PK population. The lowest levelof resistance was observed in populations from Sargodhain March 2010. The slopes of regression lines of all thepopulations were significantly shallower than Lab-PKpopulation (P < 0.05).Moderate to high levels of resistance were observed inpopulations tested for deltamethrin (15- to 53 fold,Table 1). One population from Lahore and four popula-tions from Sargodha had moderate levels of resistance(15-25 fold) while the remaining populations werehighly resistant (31-53 fold). Of 15 populations testedagainst lambdacyhalothrin, only three populations fromSargodha had moderate levels of resistance with resis-tance ratios ranging from 21-30 fold compared withLab-PK population (Table 1). The slopes of regressionlines of all the field populations were similar (P > 0.05). Carbamates Methomyl was significantly less toxic to field popula-tions (P < 0.01) compared to Lab-PK. All the field popu-lations tested for methomyl had moderate levels of resistance (13-22 fold) compared with Lab-PK (Table 2).The lowest level was observed in populations from Sar-godha in September 2009. The slopes of regression linesof all the field populations were similar (P > 0.05) butshallower than the Lab-PK (P < 0.05).Out of 15 populations tested for thiodicarb, threepopulations from Lahore, two from Faisalabad and threefrom Sargodha were moderately resistant with resistanceratios ranging from 24-30 fold compared with Lab-PK Khan  et al  .  Parasites & Vectors  2011,  4 :146http://www.parasitesandvectors.com/content/4/1/146Page 3 of 11  Table 1 Toxicity of organophosphates and pyrethroids against field populations of   Ae. albopictus Insecticide Location Time LC 50  (95% FL) (µg mL -1 ) Slope ± SE  c 2 df P RR* DR** n***Chlorpyrifos  Lab-PK 0.009 (0.002-0.013) 2.25 ± 0.31 0.69 5 0.98 1 _ 280Lahore Mar. 2009 1.92 (1.27-4.95) 1.04 ± 0.25 5.73 6 0.46 156.6 _ 320Sep. 2009 2.61 (1.35-13.21) 0.59 ± 0.26 5.84 6 0.44 247.8 0.222 320Mar. 2010 2.88 (1.27-15.44) 0.56 ± 0.25 3.95 6 0.68 242.2 0.030 320Sep. 2010 3.36 (1.33-8.55) 0.67 ± 0.26 2.65 6 0.85 240 0.041 320Faisalabad Sep. 2008 2.08 (1.26-7.31) 0.66 ± 0.30 3.34 6 0.77 224.4 _ 320Mar. 2009 2.40 (1.39-18.57) 0.59 ± 0.27 5.51 6 0.48 266 0.010 320Sep. 2009 1.71 (1.19-3.48) 0.93 ± 0.27 5.76 6 0.45 190 -0.014 320Mar. 2010 2.00 (1.32-5.15) 0.84 ± 0.28 6.11 6 0.41 222 -0.003 320Sep. 2010 2.12 (1.37-6.32) 0.81 ± 0.29 6.21 6 0.40 235.6 0.001 320Sargodha Sep. 2008 1.74 (1.15-4.29) 0.77 ± 0.25 6.51 6 0.37 193 _ 320Mar. 2009 1.89 (1.25-4.77) 0.81 ± 0.27 9.40 6 0.15 210 0.006 320Sep. 2009 1.57 (1.15-2.76) 1.09 ± 0.27 11.3 6 0.08 174 -0.007 320Mar. 2010 1.48 (1.16-2.23) 1.57 ± 0.35 9.45 6 0.15 164 -0.012 320Sep. 2010 1.69 (1.24-3.00) 1.22 ± 0.32 10.3 6 0.11 187.8 -0.002 320 Profenofos  Lab-PK 0.02 (0.015-0.04) 2.41 ± 0.27 2.44 6 0.88 1 _ 320Lahore Sep. 2008 0.56 (0.43-0.77) 1.25 ± 0.22 9.34 6 0.16 28 _ 320Mar. 2009 0.70 (0.53-1.04) 1.09 ± 0.31 5.24 5 0.39 35 0.016 280Sep. 2009 0.73 (0.55-1.07) 1.10 ± 0.40 7.49 6 0.28 36.5 0.019 320Mar. 2010 0.79 (0.59-1.23) 1.05 ± 0.23 5.90 6 0.43 39.5 0.025 320Sep. 2010 0.82 (0.52-2.26) 0.62 ± 0.23 0.53 5 0.99 41 0.028 280Faisalabad Sep. 2008 0.80 (0.62-1.15) 1.17 ± 0.33 11.6 6 0.07 40 _ 320Mar. 2009 0.82 (0.64-1.18) 1.19 ± 0.24 3.90 6 0.69 41 0.001 320Sep. 2009 0.98 (0.75-1.48) 1.11 ± 0.40 7.38 6 0.29 49 0.015 320Mar. 2010 1.03 (0.77-1.62) 1.03 ± 0.37 8.62 6 0.17 51.5 0.018 320Sep. 2010 0.71 (0.56-0.96) 1.31 ± 0.23 9.78 6 0.13 35.5 -0.009 320Sargodha Sep. 2008 0.49 (0.35-0.72) 0.97 ± 0.20 1.95 5 0.86 24 _ 280Mar. 2009 0.54 (0.42-0.73) 1.44 ± 0.23 9.09 6 0.17 27 0.007 320Sep. 2009 0.68 (0.52-0.94) 1.23 ± 0.32 6.44 6 0.38 34 0.024 320Mar. 2010 0.52 (0.35-0.84) 0.91 ± 0.25 2.08 5 0.84 26 0.004 280Sep. 2010 0.55 (0.39-0.74) 1.23 ± 0.25 8.09 6 0.17 27.5 0.008 320 Triazofos  Lab-PK 0.036 (0.02-0.06) 2.39 ± 1.29 8.06 6 0.23 1 _ 320Lahore Sep. 2008 1.80 (1.18-4.71) 0.75 ± 0.20 8.18 6 0.22 50 _ 320Mar. 2009 1.94 (1.28-4.99) 0.82 ± 0.19 11.8 6 0.07 53.9 0.005 320Sep. 2009 1.49 (1.11-2.44) 1.16 ± 0.27 7.82 6 0.25 41.4 -0.014 320Mar. 2010 1.62 (1.22-2.70) 1.36 ± 0.33 8.20 6 0.23 45 -0.008 320Sep. 2010 1.80 (1.28-3.50) 1.12 ± 0.31 7.57 6 0.27 50 0 320Faisalabad Sep. 2008 2.26 (1.31-12.26) 0.58 ± 0.16 5.89 5 0.32 62.8 _ 280Mar. 2009 2.00 (1.29-6.08) 0.79 ± 0.29 10.0 5 0.08 55.6 -0.009 280Sep. 2009 2.26 (1.38-11.23) 0.70 ± 0.29 6.29 5 0.28 62.8 0 280Mar. 2010 2.26 (1.42-8.69) 0.81 ± 0.32 4.33 5 0.50 62.8 0 280Sargodha Sep. 2008 2.57 (0.55-4.51) 0.64 ± 0.29 4.73 6 0.58 71.4 _ 320Mar. 2009 1.96 (0.88-3.01) 0.81 ± 0.27 8.49 6 0.21 54.5 -0.019 320Sep. 2009 1.72 (0.99-2.50) 1.04 ± 0.29 11.3 6 0.08 47.8 -0.029 320Mar. 2010 1.74 (0.92-2.61) 0.86 ± 0.40 5.63 6 0.47 48.3 -0.028 320Sep. 2010 2.18 (0.89-3.47) 0.87 ± 0.31 3.01 6 0.81 60.6 -0.012 320 Cypermethrin  Lab-PK 0.04 (0.02-0.09) 2.41 ± 0.45 5.96 6 0.43 1 _ 320Lahore Sep. 2008 0.86 (0.66-1.29) 1.11 ± 0.23 8.62 6 0.20 21.5 _ 320Mar. 2009 0.71 (0.57-0.95) 1.40 ± 0.35 11.6 6 0.72 17.8 -0.014 320Sep. 2009 0.63 (0.52-0.85) 1.46 ± 0.22 10.4 6 0.11 15.8 -0.023 320Mar. 2010 0.89 (0.69-1.30) 1.16 ± 0.24 11.3 6 0.08 22.3 0.003 320 Khan  et al  .  Parasites & Vectors  2011,  4 :146http://www.parasitesandvectors.com/content/4/1/146Page 4 of 11  (Table 2). The remaining 7 populations were highly resistant to this chemical (31-37 fold). New insecticides Among the 15 populations tested with indoxacarb, only one population from Faisalabad in September 2010showed very high resistance (101 fold) while the remain-ing populations were highly resistant with resistanceratios ranging from 41-89 fold compared with Lab-PK(Table 2). The lowest level of resistance was found inpopulations from Lahore in September 2008. All thepopulations tested for emamectin benzoate were Table 1 Toxicity of organophosphates and pyrethroids against field populations of   Ae. albopictus  (Continued) Sep. 2010 0.83 (0.64-1.15) 1.24 ± 0.42 6.43 6 0.38 20.8 -0.003 320Faisalabad Sep. 2008 1.02 (0.78-1.54) 1.11 ± 0.37 9.79 6 0.13 25.5 _ 320Mar. 2009 0.78 (0.55-1.00) 1.19 ± 0.43 6.56 6 0.36 19.5 -0.019 320Sep. 2009 0.94 (0.54-1.34) 0.82 ± 0.22 4.21 6 0.65 23.5 -0.006 320Mar. 2010 0.94 (0.60-1.27) 1.00 ± 0.30 6.29 6 0.39 23.5 -0.006 320Sep. 2010 0.87 (0.53-1.21) 0.87 ± 0.23 4.03 5 0.55 21.8 -0.012 280Sargodha Sep. 2008 0.68 (0.52-0.83) 1.49 ± 0.41 9.15 6 0.17 17 _ 320Mar. 2009 0.58 (0.46-0.70) 1.55 ± 0.24 11.9 6 0.06 14.5 -0.012 320Sep. 2009 0.69 (0.50-0.87) 1.26 ± 0.44 7.49 6 0.28 17.3 0.001 320Mar. 2010 0.70 (0.55-0.86) 1.57 ± 0.52 8.37 6 0.21 17.5 0.002 320Sep. 2010 0.66 (0.49-0.83) 1.35 ± 0.37 10.5 6 0.11 16.5 -0.002 320 Deltamethrin  Lab-PK 0.028 (0.02-0.04) 2.29 ± 0.24 3.39 6 0.76 1 _ 320Lahore Sep. 2008 1.06 (0.74-1.34) 1.18 ± 0.18 4.08 6 0.67 37.9 _ 320Mar. 2009 1.22 (0.76-1.68) 0.98 ± 0.25 4.34 6 0.63 43.6 0.010 320Sep. 2009 0.92 (0.61-1.23) 1.02 ± 0.23 4.49 6 0.61 32.9 -0.010 320Mar. 2010 0.41 (0.262-5.61) 0.82 ± 0.13 0.55 4 0.97 14.6 -0.069 240Sep. 2010 1.15 (0.57-1.74) 0.72 ± 0.16 2.25 5 0.81 41.1 0.006 280Faisalabad Sep. 2008 1.48 (0.82-2.14) 0.88 ± 0.21 4.12 6 0.66 52.8 _ 320Mar. 2009 1.35 (0.77-1.92) 0.92 ± 0.36 1.57 5 0.91 48.2 -0.007 280Sep. 2009 1.16 (0.72-1.60) 0.95 ± 0.21 3.78 6 0.71 41.4 -0.018 320Mar. 2010 1.27 (0.70-1.83) 0.82 ± 0.40 3.81 6 0.70 45.4 -0.011 320Sep. 2010 1.31 (0.77-1.71) 1.04 ± 0.38 8.61 6 0.17 46.8 -0.009 320Sargodha Sep. 2008 0.70 (0.51-0.88) 1.33 ± 0.52 6.10 6 0.41 25 _ 320Mar. 2009 0.88 (0.63-1.13) 1.21 ± 0.28 5.52 6 0.48 31.4 0.017 320Sep. 2009 0.63 (0.49-0.77) 1.66 ± 0.34 11.9 6 0.06 22.5 -0.008 320Mar. 2010 0.68 (0.44-0.99) 0.99 ± 0.42 5.65 6 0.46 24.3 -0.002 320Sep. 2010 0.68 (0.51-0.83) 1.44 ± 0.36 9.20 6 0.16 24.3 -0.002 320 Lambdacyh-alothrin  Lab-PK 0.02 (0.014-0.033) 2.32 ± 0.51 3.56 6 0.74 1 _ 320Lahore Sep. 2008 0.91 (0.59-1.22) 1.00 ± 0.16 9.41 5 0.09 45.5 _ 280Mar. 2009 1.16 (0.72-1.60) 0.97 ± 0.24 8.61 5 0.13 58 0.018 280Sep. 2009 0.91 (0.61-1.20) 1.10 ± 0.26 9.22 5 0.10 45.5 0 280Mar. 2010 0.90 (0.56-1.23) 0.92 ± 0.28 8.24 5 0.14 45 -0.001 280Sep. 2010 1.15 (0.63-1.66) 0.81 ± 0.18 6.58 5 0.25 57.5 0.017 280Faisalabad Sep. 2008 0.84 (0.57-1.11) 1.05 ± 0.20 9.28 6 0.16 42 _ 320Mar. 2009 0.65 (0.44-0.87) 1.10 ± 0.31 9.71 6 0.14 33 -0.018 320Sep. 2009 0.83 (0.61-1.05) 1.28 ± 0.44 12.0 6 0.06 41.5 -0.001 320Mar. 2010 0.81 (0.59-1.03) 1.27 ± 0.36 8.85 6 0.18 40.5 -0.003 320Sep. 2010 0.78 (0.52-1.04) 1.03 ± 0.26 8.41 6 0.21 39 -0.005 320Sargodha Sep. 2008 0.42 (0.30-0.54) 1.42 ± 0.61 10.7 6 0.09 21 _ 320Mar. 2009 0.59 (0.46-0.72) 1.62 ± 0.46 10.1 6 0.12 29.5 0.025 320Sep. 2009 0.64 (0.49-0.80) 1.56 ± 0.44 10.4 6 0.11 32 0.030 320Mar. 2010 0.55 (0.43-0.68) 1.56 ± 0.48 8.10 6 0.23 27.5 0.020 320Sep. 2010 0.65 (0.45-0.86) 1.09 ± 0.26 7.05 6 0.32 32.5 0.032 320 *Resistance ratio = LC 50  field population/LC 50  of susceptible strain**Rate of increase or decrease in resistance, *** Number of larvae tested in a bioassay Khan  et al  .  Parasites & Vectors  2011,  4 :146http://www.parasitesandvectors.com/content/4/1/146Page 5 of 11
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