Efficacy of 13 Commercial Household Aerosol Insecticides Against Aedes aegypti (Diptera: Culicidae) From Morelos, Mexico

Efficacy of 13 Commercial Household Aerosol Insecticides Against Aedes aegypti (Diptera:... Abstract In Mexico, Aedes aegypti (L.) (Diptera: Culicidae) is the primary vector of Dengue, Zika, and Chikungunya viruses. Control programs include community participation using personal protection such as household aerosol insecticides. In both, urban or rural areas, the use of aerosol insecticides is a common practice to avoiding mosquito biting. Thus, information on the efficacy of commercial products must be available. This study reports the efficacy of 13 household aerosol insecticides against Ae. aegypti from an endemic dengue area in Mexico. To test each insecticide, six netting cages, containing 10 non-blood fed female mosquitoes each one, were placed in different locations inside a bedroom. Readings at 30 min and 24 h after exposure were recorded. No products showed 100% mortality after 30 min of exposure. Only three products killed the 100% of the individuals 24 h after exposure. Results showed a high mortality variance among insecticides. Location in the room also impacts the insecticide efficacy. Mosquitoes located inside cabinets or with behind an obstacle (preventing an accurate insecticide exposure) showed lower mortalities. Products and spraying methods could and should be improved. Aedes aegypti, aerosol, community participation, household insecticide, Mexico Aedes aegypti and Aedes albopictus (L.) (Diptera: Culicidae) mosquitoes are the most important vectors of arthropod-borne virus (Dengue, Chikungunya and Zika viruses) (Mayer et al. 2017). In Mexico, recent outbreaks of emerging diseases, such as Chikungunya and Zika fever (Rivera-Ávila 2014, Guerbois et al. 2016), and the elevated number of dengue cases, made mosquito control a primary priority. Currently, the most common and affordable strategy to control mosquito-borne diseases transmission relies on actions against population densities and mosquito bites. Control programs include governmental planned strategies and community participation (Gubler and Clark 1996). Community participation comprises the use of insecticide-treated nets, coils, repellents (natural or synthetic), and household aerosol insecticides. In Mexico, the use of aerosol insecticides is a common practice (Loroño-Pino et al. 2014). In this type of dispensing system, the active ingredient is suspended as a fog or mist. Since particles are released through a small hole, the ingredients tend to float (Sarwar 2015). Their low cost and perceptible rapid killing action made aerosols widely used to kill domestic insects. These products are usually applied in greenhouses, office buildings, churches and schools (Garcia-Rejon et al. 2008). Previous studies showed the positive impact of the use of insecticidal aerosol cans (Osaka et al. 1999, Khadri et al. 2009). However, to our current knowledge, in Mexico there are no studies regarding the effectiveness of commercial aerosol insecticide in habitable rooms. Rooms in homes, offices, or schools are the principal environments for transmission (Garcia-Rejon et al. 2008). Therefore, it is important to know which products can be relied on to provide active protection in these areas. Insecticides are still the most effective control strategy. However, selection for traits that allow mosquitoes to survive the insecticide exposure has led to the evolution of resistance (Saavedra-Rodriguez et al. 2007, Saavedra-Rodriguez et al. 2015, García et al. 2009, Siller et al. 2011, Aponte et al. 2013, Flores et al. 2013). Therefore, information on the efficacy of commercial insecticides in endemic populations for vector-borne diseases would be useful. This information also may help to support integrated methods of mosquito management. This study reports the knockdown effect (after 30 min of exposure) and 24 h mortality of 13 products against Ae. aegypti from an endemic Dengue area in Mexico. Materials and Methods Mosquito Strain To obtain the mosquitoes, egg samples were collected using ovitraps in the municipality of Jojutla (18°36′53″N, 99°10′49″W) at Morelos State, Mexico. Clutches of eggs were used to get the laboratory colony for testing. The first generation of mosquitoes reared was used in the assay. Two- to five-d-old non-fed females were used in the assay. Egg hatching, maintenance of the larval and adult populations were conducted at the Centro Regional de Control de Vectores ‘Panchimalco.’ The conditions are generally 27 ± 2°C, 80 ± 10% relative humidity and 12:12 (L:D) h photoperiod. Evaluation of Spraying Six netting cages, containing 10 non–blood-fed female mosquitoes each one, were placed in different locations inside a bedroom (Fig. 1). Cage 1 was placed on the center of the room (above a bed or center table), cage 2 was placed inside any closed storage cabinet (e.g., wardrobe, dresser, drawer), cage 3 was placed >50 cm under bed, bedside cabinet or table (i.e., with obstacle), cage 4 was placed 50–70 cm above the floor (over a table or dresser or desk) behind T.V. or mirrors (i.e., with obstacle), cage 5 was placed 50–70 cm above the floor without any obstacle, and cage 6 was placed 170 cm above the floor near a wall without obstacle. The control cages were placed in the same locations in a different room. Each insecticide test was assessed through two replicates (in different bedrooms). Bedrooms of houses, hotels, or dormitories were used for the assays. Bedrooms were selected only if the six locations were available. Surface area of the rooms was 15.5 (±8.6) m2 with a mean temperature of 28.2 (±2.5)°C and 27.2 (±3.9)% humidity. Doors and windows were closed and fans were turned off. When present, room air conditioner was turned off several hours before exposure. Fig. 1. View largeDownload slide Cage location inside the room. (a) Mosquito cage net, (b) Center of the room 50–70 cm above the floor, (c) inside storage cabinets, (d) with obstacle >50 cm above the floor, e) with obstacle at 50–70 cm above the floor, (f) without obstacle at 50–70 cm above the floor, and (g) without obstacle <170 cm above the floor near a wall. Fig. 1. View largeDownload slide Cage location inside the room. (a) Mosquito cage net, (b) Center of the room 50–70 cm above the floor, (c) inside storage cabinets, (d) with obstacle >50 cm above the floor, e) with obstacle at 50–70 cm above the floor, (f) without obstacle at 50–70 cm above the floor, and (g) without obstacle <170 cm above the floor near a wall. Thirteen commercial insecticides, with national distribution, were purchased for testing (Table 1). The aerosol was sprayed from the center of the room (with the door closed) with the nozzle valve held 45° upward and moved through 360°. The product was applied in accordance with manufacturer’s written instructions. Immediately after application, the person who performed the spraying left the room and closed the door. The number of mosquitoes knocked down was recorded at 30 min post spraying over. We used this time point since it has been shown that insecticide residues can be found at higher concentrations during the first 30 min post spraying (Ramesh and Vijayalakshmi 2001). After an hour of exposure, mosquitoes were transferred to clean holding cups and maintained on ad libitum sucrose solution at the Centro Regional de Control de Vectores ‘Panchimalco.’ Mortality was recorded at 24 h post exposure. Table 1. Names, active ingredients, and doses of 13 commercial aerosol insecticides used in this study Insecticide brand  Active ingredients/dose  Product discharge (g/kg/room)  Baygon Casa y Jardin  Prallethrin = 0.0160 g/kg, phenothrin= 0.020 g/kg  16.05  Baygon Total  Cyfluthrin = 0.0029 g/kg, imiprothrin = 0.0099 g/kg  Not available  H24 Casa y Jardin  Tetramethrin = 0.0478 g/kg, cifenothrin = 0.016 g/kg  16.0  H24 Citronox  Tetramethrin = 0.025 g/kg, cifenothrin = 0.0085 g/kg  Not available  H24 Mata Moscos y Mosquitos  Tetramethrin = 0.042 g/kg, cifenothrin = 0.014 g/kg  14.35  Oko Azul  Tetramethrin = 0.0488 g/kg, cifenothrin = 0.0293 g/kg  19.55  Oko Casa y Jardin  Tetramethrin = 0.0258 g/kg, phenothrin = 0.0258 g/kg  8.15  Oko Green Multiusos  Tetramethrin = 0.0527 g/kg, cifenothrin = 0.0316 g/kg  21.1  Oko Morado  Allethrin = 0.0477 g/kg  14.35  Ortho Home Defense  Tetramethrin = 0.02 g/kg, phenothrin = 0.02 g/kg  10.0  Raid Accion Total  Imiprothrin = 0.0081 g/kg, cypermethrin = 0.0261 g/kg, prallethrin = 0.0078 g/kg  26.13  Raid Casa y Jardin  Prallethrin= 0.0313 g/kg, phenothrin= 0.0391 g/kg  31.3  Raid Mata Moscos y Mosquitos  Phenothrin= 0.002694 g/kg, prallethrin= 0.011225 g/kg, tetramethrin = 0.024695 g/kg  22.45  Insecticide brand  Active ingredients/dose  Product discharge (g/kg/room)  Baygon Casa y Jardin  Prallethrin = 0.0160 g/kg, phenothrin= 0.020 g/kg  16.05  Baygon Total  Cyfluthrin = 0.0029 g/kg, imiprothrin = 0.0099 g/kg  Not available  H24 Casa y Jardin  Tetramethrin = 0.0478 g/kg, cifenothrin = 0.016 g/kg  16.0  H24 Citronox  Tetramethrin = 0.025 g/kg, cifenothrin = 0.0085 g/kg  Not available  H24 Mata Moscos y Mosquitos  Tetramethrin = 0.042 g/kg, cifenothrin = 0.014 g/kg  14.35  Oko Azul  Tetramethrin = 0.0488 g/kg, cifenothrin = 0.0293 g/kg  19.55  Oko Casa y Jardin  Tetramethrin = 0.0258 g/kg, phenothrin = 0.0258 g/kg  8.15  Oko Green Multiusos  Tetramethrin = 0.0527 g/kg, cifenothrin = 0.0316 g/kg  21.1  Oko Morado  Allethrin = 0.0477 g/kg  14.35  Ortho Home Defense  Tetramethrin = 0.02 g/kg, phenothrin = 0.02 g/kg  10.0  Raid Accion Total  Imiprothrin = 0.0081 g/kg, cypermethrin = 0.0261 g/kg, prallethrin = 0.0078 g/kg  26.13  Raid Casa y Jardin  Prallethrin= 0.0313 g/kg, phenothrin= 0.0391 g/kg  31.3  Raid Mata Moscos y Mosquitos  Phenothrin= 0.002694 g/kg, prallethrin= 0.011225 g/kg, tetramethrin = 0.024695 g/kg  22.45  View Large Statistical Analysis Percentages of lethality were calculated as the number of knocked down (30 min of exposure) or dead (24 h mortality) mosquitoes/total mosquitoes × 100 (WHO 2009). To accommodate responses with non-normal distributions and investigated the effects of insecticide, cage location and their interaction, on the knockdown and mortality percentages, a generalized linear model (Likelihood Type 3 analysis) was used. Analyses were undertaken using the Fit Model-GLM module of JMP 6.0 (SAS Institute Inc.). The control cages values were used as the baseline for comparison. We were not able to perform analysis using the active ingredient as a grouping variable because doses were dissimilar, even among products with the same formulation. Results The knockdown and mortality percentages are shown in Supp Table 2 (online only). At 30 minutes of exposure, differences in the percentages of knocked down mosquitoes among insecticides were observed (Aerosol effect: Likelihood ratio χ2 = 242.98, d.f. = 13, P <0.0001) (e.g., Baygon total, H24 Casa and Jardin and H24 Mata Moscas y Mosquitos; see Fig. 2a and c–f; Supp Tables 1 and 2 [online only]). Location was also important, the analysis showed differences among the cages inside the room (Location effect: Likelihood ratio χ2 = 271.32, d.f. = 6, P <0.0001). Knocked down effect in locations such as inside cabinets and with obstacle was reduced (Fig. 2c–f; Supp Tables 1 and 3 [online only]). Our analysis also revealed strong effects of insecticide-by-location interaction on knockdown percentages (Aerosol × Location effect: Likelihood ratio χ2 = 179.09, d.f. = 78, P <0.0001). The interaction shown that, despite some insecticides induced an increased knockdown effect than others, there were some locations where its effectiveness was not always as higher than expected (Fig. 2; Supp Table 1 [online only]). Fig. 2. View largeDownload slide Thirty minutes mean (±SD) knockdown and 24-h mean (±SE) mortality of Ae. aegypti mosquitoes form Jojutla, Morelos exposed to 13 aerosol insecticides. Percentage of mortality in: (a) center of the room, (b) inside storage cabinets, (c) with obstacle >50 cm above the floor, (d) with obstacle at 50–70 cm above the floor, (e) without obstacle at 50–70 cm above the floor, and (f) without obstacle <170 cm above the floor near a wall. Fig. 2. View largeDownload slide Thirty minutes mean (±SD) knockdown and 24-h mean (±SE) mortality of Ae. aegypti mosquitoes form Jojutla, Morelos exposed to 13 aerosol insecticides. Percentage of mortality in: (a) center of the room, (b) inside storage cabinets, (c) with obstacle >50 cm above the floor, (d) with obstacle at 50–70 cm above the floor, (e) without obstacle at 50–70 cm above the floor, and (f) without obstacle <170 cm above the floor near a wall. At 24 h after exposure, the overall mortality increased (Fig. 2, Supp Tables 1 and 2 [online only]). For the different locations throughout the room, H24 Casa and Jardin, H24 Mata Moscas y Mosquitos, and Oko Green Multiusos were the only insecticides that induced a 100% mortality. Meanwhile, Oko Azul was the product with the worst performance (Fig. 2; Supp Table 2 [online only]). Mosquitos exposed to Raid Casa y Jardin, Oko Azul, and to some degree to H24 Citronox and Raid Mata Moscos y Mosquitos, recovered from the knockdown (Fig. 2; Supp Table 1 [online only]). Differences among insecticides were still detected (Aerosol effect: Likelihood ratio χ2 = 341.22, d.f. = 13, P <0.0001). Likewise, differences among cage location were observed (Location effect: Likelihood ratio χ2 = 412.17, d.f. = 6, P <0.0001). The inside cabinet location was the location with lower mortality, whereas the center of the room showed the higher mortality. Interestingly, cages located <170 cm above the floor also did not show the higher mortalities (Fig. 2b; Supp Table 3 [online only]) and mortality rates in the location with obstacle increased. The interaction shown that, despite some insecticides had an increased mortality effects than others, there were some locations where its effectiveness was not always as higher than expected (Aerosol × Location effect: Likelihood ratio χ2 =0186.49, d.f. = 78, P = 0.0066) (Fig. 2; Supp Table 1 [online only]). Control groups mortality, at both times, was 0. Discussion The use of household aerosol insecticides allowed us to establish insecticide susceptibility status of Ae. aegypti in Morelos, Mexico. Our results at 30 min after exposure exhibited the null existence of a 100% killing action commercial household aerosol insecticide. A rapid killing action not only could avoid the bite of an infected mosquito but also will prevent resistance. At 24 h post-exposure, H24 Casa y Jardin, H24 Mata Moscas y Mosquitos, and OKO Green Multiusos showed a 100% mortality in all the evaluated locations. Considerable variation in mortality among and within products was observed (from 100 to 30% mortality). Despite the slow killing action, these household insecticides could be another tool to reduce mosquito incidence inside homes, offices, or schools. The low percentages observed do not necessarily indicate resistance, but a lower insecticide efficacy. Only for the products showing mosquitoes recovery after spraying, a degree of resistance could be argued. Not only metabolic or genetic resistance could be related to the variable killing efficacy but also the behavioral responses of the mosquito to insecticides (Chareonviriyaphap et al. 2013). Unfortunately, with our methodology, we were unable to quantify behavioral avoidance responses. Nevertheless, in Ae. aegypti, insecticide contact irritancy and repellency have an important role in female behavioral avoidance (Kongmee et al. 2004, Mongkalangoon et al. 2009). Mosquito escape responses may interfere with other behaviors such as feeding and oviposition selection. Therefore, studies monitoring the behavioral response could give more information about the actual efficacy of insecticides. Spray characteristics could also influence insecticide efficacy. Droplet diameter, velocity separation/agglomeration and collision, number of holes or nozzle diameter, might be different among products leading to differences in their killing efficacy (Ikeda et al. 2006). Previous studies showed that in hidden places, mortality increased at 2 h post spraying (Khadri et al. 2009). It is possible that the number of droplets required to kill the mosquitoes inside cabinets or places with obstacles was insufficient. We recommend opening cabinets and drawers while spraying and a direct spray at semi-exposed places. If not included, we encourage manufactures to clearly label these recommendations. The differences between active ingredients might result in different mortalities. Since doses were dissimilar even among products with the same formulation, it was impossible to evaluate the different formulation mixtures. However, our results showed that tetramethrin and cifenothrin products (H24 Casa and Jardin, H24 Mata Moscas y Mosquitos and Oko Green Multiusos, Table 1; Supp Table 1 [online only]) had the highest knockdown and mortality percentages. But important to mention, the less efficient product (Oko Azul) also contains tetramethrin and cifenothirn (with even higher doses than the efficient products). Other products with higher mortality (<90 %; Supp Table 1 [online only]) differ in their active ingredients (Table 1), as a consequence, a generalization about a formulation cannot be done. Most of these commercial insecticides are not species specific, and their formulation is intended to kill a broad of arthropod species. However, most of them promise an efficient killing action, but it did not happen. The “Jojutla” strain used in this study has been tested for natural and synthetic repellents, showing that the products did not provide satisfactory levels of personal protection against mosquito bites (Kuri-Morales et al. 2017). The strain also presents resistance to bifenthrin, δ-phenothrin, α-cypermethrin, and possible resistance to deltamethrin and permethrin (based on WHO criteria) (Kuri-Morales, unpublished data), as happens with other Mexican mosquito populations ( Saavedra-Rodriguez et al. 2007, Saavedra-Rodriguez et al. 2015; Garcia et al. 2009; Aponte 2013). Thus, since all the active ingredients used in this study were pyrethroids, it is not surprising to find partial susceptibility to aerosols against this strain. It is possible that the products with the higher efficacy found in our study have a combination of accurate spraying characteristics (e.g., droplet diameter, velocity, and nozzle diameter) and appropriate dose and formulations. The overall impact of commercial insecticides on vector-borne diseases epidemics remains unknown. The use of these aerosol insecticides could contribute to control dengue transmission and enhance efficient community protection and participation. For example, reduction in dengue hemorrhagic fever cases in areas where insecticides were given to the patient′s family to spray their home was observed (Osaka et al. 1999). Community spends a considerable amount of money to kill mosquitoes (Loroño-Pino et al. 2014). Therefore, it is necessary to guide the selection of an appropriate and effective household insecticide. Assessments presented here are evidence that products and spraying methods could and should be improved. Supplementary Material Supplementary data are available at Journal of Medical Entomology online. Acknowledgments We thank A. Contreras-Mendez, A. Martinez-Gaona, C. Ramirez-Huicochea, and L. Rosas-Trinidad of the Centro Regional de Control de Vectores Panchimalco, Jojutla for logistical support. This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors. The use of trade names is for the purposes of providing scientific information only, and does not constitute endorsement by the authors’ institutional affiliations. We thank two anonymous reviewers for their helpful suggestions and comments. References Cited Aponte, A. H., Penilla P. R., Dzul-Manzanilla F., Che-Mendoza A., Lopez A. D., and Solis F.. 2013. The pyrethroid resistance status and mechanisms in Aedes aegypti from the Guerrero state, Mexico. Pestic. Biochem. Physiol . 107: 226– 234. Google Scholar CrossRef Search ADS   Chareonviriyaphap, T., Bangs M. 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Mosquito coils, vaporizer mats, liquid vaporizers, ambient emanators and aerosols. Geneva. WHO/HTM/NTD/WHOPES/2009.3. © The Author(s) 2017. Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Journal of Medical Entomology Oxford University Press

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Abstract

Abstract In Mexico, Aedes aegypti (L.) (Diptera: Culicidae) is the primary vector of Dengue, Zika, and Chikungunya viruses. Control programs include community participation using personal protection such as household aerosol insecticides. In both, urban or rural areas, the use of aerosol insecticides is a common practice to avoiding mosquito biting. Thus, information on the efficacy of commercial products must be available. This study reports the efficacy of 13 household aerosol insecticides against Ae. aegypti from an endemic dengue area in Mexico. To test each insecticide, six netting cages, containing 10 non-blood fed female mosquitoes each one, were placed in different locations inside a bedroom. Readings at 30 min and 24 h after exposure were recorded. No products showed 100% mortality after 30 min of exposure. Only three products killed the 100% of the individuals 24 h after exposure. Results showed a high mortality variance among insecticides. Location in the room also impacts the insecticide efficacy. Mosquitoes located inside cabinets or with behind an obstacle (preventing an accurate insecticide exposure) showed lower mortalities. Products and spraying methods could and should be improved. Aedes aegypti, aerosol, community participation, household insecticide, Mexico Aedes aegypti and Aedes albopictus (L.) (Diptera: Culicidae) mosquitoes are the most important vectors of arthropod-borne virus (Dengue, Chikungunya and Zika viruses) (Mayer et al. 2017). In Mexico, recent outbreaks of emerging diseases, such as Chikungunya and Zika fever (Rivera-Ávila 2014, Guerbois et al. 2016), and the elevated number of dengue cases, made mosquito control a primary priority. Currently, the most common and affordable strategy to control mosquito-borne diseases transmission relies on actions against population densities and mosquito bites. Control programs include governmental planned strategies and community participation (Gubler and Clark 1996). Community participation comprises the use of insecticide-treated nets, coils, repellents (natural or synthetic), and household aerosol insecticides. In Mexico, the use of aerosol insecticides is a common practice (Loroño-Pino et al. 2014). In this type of dispensing system, the active ingredient is suspended as a fog or mist. Since particles are released through a small hole, the ingredients tend to float (Sarwar 2015). Their low cost and perceptible rapid killing action made aerosols widely used to kill domestic insects. These products are usually applied in greenhouses, office buildings, churches and schools (Garcia-Rejon et al. 2008). Previous studies showed the positive impact of the use of insecticidal aerosol cans (Osaka et al. 1999, Khadri et al. 2009). However, to our current knowledge, in Mexico there are no studies regarding the effectiveness of commercial aerosol insecticide in habitable rooms. Rooms in homes, offices, or schools are the principal environments for transmission (Garcia-Rejon et al. 2008). Therefore, it is important to know which products can be relied on to provide active protection in these areas. Insecticides are still the most effective control strategy. However, selection for traits that allow mosquitoes to survive the insecticide exposure has led to the evolution of resistance (Saavedra-Rodriguez et al. 2007, Saavedra-Rodriguez et al. 2015, García et al. 2009, Siller et al. 2011, Aponte et al. 2013, Flores et al. 2013). Therefore, information on the efficacy of commercial insecticides in endemic populations for vector-borne diseases would be useful. This information also may help to support integrated methods of mosquito management. This study reports the knockdown effect (after 30 min of exposure) and 24 h mortality of 13 products against Ae. aegypti from an endemic Dengue area in Mexico. Materials and Methods Mosquito Strain To obtain the mosquitoes, egg samples were collected using ovitraps in the municipality of Jojutla (18°36′53″N, 99°10′49″W) at Morelos State, Mexico. Clutches of eggs were used to get the laboratory colony for testing. The first generation of mosquitoes reared was used in the assay. Two- to five-d-old non-fed females were used in the assay. Egg hatching, maintenance of the larval and adult populations were conducted at the Centro Regional de Control de Vectores ‘Panchimalco.’ The conditions are generally 27 ± 2°C, 80 ± 10% relative humidity and 12:12 (L:D) h photoperiod. Evaluation of Spraying Six netting cages, containing 10 non–blood-fed female mosquitoes each one, were placed in different locations inside a bedroom (Fig. 1). Cage 1 was placed on the center of the room (above a bed or center table), cage 2 was placed inside any closed storage cabinet (e.g., wardrobe, dresser, drawer), cage 3 was placed >50 cm under bed, bedside cabinet or table (i.e., with obstacle), cage 4 was placed 50–70 cm above the floor (over a table or dresser or desk) behind T.V. or mirrors (i.e., with obstacle), cage 5 was placed 50–70 cm above the floor without any obstacle, and cage 6 was placed 170 cm above the floor near a wall without obstacle. The control cages were placed in the same locations in a different room. Each insecticide test was assessed through two replicates (in different bedrooms). Bedrooms of houses, hotels, or dormitories were used for the assays. Bedrooms were selected only if the six locations were available. Surface area of the rooms was 15.5 (±8.6) m2 with a mean temperature of 28.2 (±2.5)°C and 27.2 (±3.9)% humidity. Doors and windows were closed and fans were turned off. When present, room air conditioner was turned off several hours before exposure. Fig. 1. View largeDownload slide Cage location inside the room. (a) Mosquito cage net, (b) Center of the room 50–70 cm above the floor, (c) inside storage cabinets, (d) with obstacle >50 cm above the floor, e) with obstacle at 50–70 cm above the floor, (f) without obstacle at 50–70 cm above the floor, and (g) without obstacle <170 cm above the floor near a wall. Fig. 1. View largeDownload slide Cage location inside the room. (a) Mosquito cage net, (b) Center of the room 50–70 cm above the floor, (c) inside storage cabinets, (d) with obstacle >50 cm above the floor, e) with obstacle at 50–70 cm above the floor, (f) without obstacle at 50–70 cm above the floor, and (g) without obstacle <170 cm above the floor near a wall. Thirteen commercial insecticides, with national distribution, were purchased for testing (Table 1). The aerosol was sprayed from the center of the room (with the door closed) with the nozzle valve held 45° upward and moved through 360°. The product was applied in accordance with manufacturer’s written instructions. Immediately after application, the person who performed the spraying left the room and closed the door. The number of mosquitoes knocked down was recorded at 30 min post spraying over. We used this time point since it has been shown that insecticide residues can be found at higher concentrations during the first 30 min post spraying (Ramesh and Vijayalakshmi 2001). After an hour of exposure, mosquitoes were transferred to clean holding cups and maintained on ad libitum sucrose solution at the Centro Regional de Control de Vectores ‘Panchimalco.’ Mortality was recorded at 24 h post exposure. Table 1. Names, active ingredients, and doses of 13 commercial aerosol insecticides used in this study Insecticide brand  Active ingredients/dose  Product discharge (g/kg/room)  Baygon Casa y Jardin  Prallethrin = 0.0160 g/kg, phenothrin= 0.020 g/kg  16.05  Baygon Total  Cyfluthrin = 0.0029 g/kg, imiprothrin = 0.0099 g/kg  Not available  H24 Casa y Jardin  Tetramethrin = 0.0478 g/kg, cifenothrin = 0.016 g/kg  16.0  H24 Citronox  Tetramethrin = 0.025 g/kg, cifenothrin = 0.0085 g/kg  Not available  H24 Mata Moscos y Mosquitos  Tetramethrin = 0.042 g/kg, cifenothrin = 0.014 g/kg  14.35  Oko Azul  Tetramethrin = 0.0488 g/kg, cifenothrin = 0.0293 g/kg  19.55  Oko Casa y Jardin  Tetramethrin = 0.0258 g/kg, phenothrin = 0.0258 g/kg  8.15  Oko Green Multiusos  Tetramethrin = 0.0527 g/kg, cifenothrin = 0.0316 g/kg  21.1  Oko Morado  Allethrin = 0.0477 g/kg  14.35  Ortho Home Defense  Tetramethrin = 0.02 g/kg, phenothrin = 0.02 g/kg  10.0  Raid Accion Total  Imiprothrin = 0.0081 g/kg, cypermethrin = 0.0261 g/kg, prallethrin = 0.0078 g/kg  26.13  Raid Casa y Jardin  Prallethrin= 0.0313 g/kg, phenothrin= 0.0391 g/kg  31.3  Raid Mata Moscos y Mosquitos  Phenothrin= 0.002694 g/kg, prallethrin= 0.011225 g/kg, tetramethrin = 0.024695 g/kg  22.45  Insecticide brand  Active ingredients/dose  Product discharge (g/kg/room)  Baygon Casa y Jardin  Prallethrin = 0.0160 g/kg, phenothrin= 0.020 g/kg  16.05  Baygon Total  Cyfluthrin = 0.0029 g/kg, imiprothrin = 0.0099 g/kg  Not available  H24 Casa y Jardin  Tetramethrin = 0.0478 g/kg, cifenothrin = 0.016 g/kg  16.0  H24 Citronox  Tetramethrin = 0.025 g/kg, cifenothrin = 0.0085 g/kg  Not available  H24 Mata Moscos y Mosquitos  Tetramethrin = 0.042 g/kg, cifenothrin = 0.014 g/kg  14.35  Oko Azul  Tetramethrin = 0.0488 g/kg, cifenothrin = 0.0293 g/kg  19.55  Oko Casa y Jardin  Tetramethrin = 0.0258 g/kg, phenothrin = 0.0258 g/kg  8.15  Oko Green Multiusos  Tetramethrin = 0.0527 g/kg, cifenothrin = 0.0316 g/kg  21.1  Oko Morado  Allethrin = 0.0477 g/kg  14.35  Ortho Home Defense  Tetramethrin = 0.02 g/kg, phenothrin = 0.02 g/kg  10.0  Raid Accion Total  Imiprothrin = 0.0081 g/kg, cypermethrin = 0.0261 g/kg, prallethrin = 0.0078 g/kg  26.13  Raid Casa y Jardin  Prallethrin= 0.0313 g/kg, phenothrin= 0.0391 g/kg  31.3  Raid Mata Moscos y Mosquitos  Phenothrin= 0.002694 g/kg, prallethrin= 0.011225 g/kg, tetramethrin = 0.024695 g/kg  22.45  View Large Statistical Analysis Percentages of lethality were calculated as the number of knocked down (30 min of exposure) or dead (24 h mortality) mosquitoes/total mosquitoes × 100 (WHO 2009). To accommodate responses with non-normal distributions and investigated the effects of insecticide, cage location and their interaction, on the knockdown and mortality percentages, a generalized linear model (Likelihood Type 3 analysis) was used. Analyses were undertaken using the Fit Model-GLM module of JMP 6.0 (SAS Institute Inc.). The control cages values were used as the baseline for comparison. We were not able to perform analysis using the active ingredient as a grouping variable because doses were dissimilar, even among products with the same formulation. Results The knockdown and mortality percentages are shown in Supp Table 2 (online only). At 30 minutes of exposure, differences in the percentages of knocked down mosquitoes among insecticides were observed (Aerosol effect: Likelihood ratio χ2 = 242.98, d.f. = 13, P <0.0001) (e.g., Baygon total, H24 Casa and Jardin and H24 Mata Moscas y Mosquitos; see Fig. 2a and c–f; Supp Tables 1 and 2 [online only]). Location was also important, the analysis showed differences among the cages inside the room (Location effect: Likelihood ratio χ2 = 271.32, d.f. = 6, P <0.0001). Knocked down effect in locations such as inside cabinets and with obstacle was reduced (Fig. 2c–f; Supp Tables 1 and 3 [online only]). Our analysis also revealed strong effects of insecticide-by-location interaction on knockdown percentages (Aerosol × Location effect: Likelihood ratio χ2 = 179.09, d.f. = 78, P <0.0001). The interaction shown that, despite some insecticides induced an increased knockdown effect than others, there were some locations where its effectiveness was not always as higher than expected (Fig. 2; Supp Table 1 [online only]). Fig. 2. View largeDownload slide Thirty minutes mean (±SD) knockdown and 24-h mean (±SE) mortality of Ae. aegypti mosquitoes form Jojutla, Morelos exposed to 13 aerosol insecticides. Percentage of mortality in: (a) center of the room, (b) inside storage cabinets, (c) with obstacle >50 cm above the floor, (d) with obstacle at 50–70 cm above the floor, (e) without obstacle at 50–70 cm above the floor, and (f) without obstacle <170 cm above the floor near a wall. Fig. 2. View largeDownload slide Thirty minutes mean (±SD) knockdown and 24-h mean (±SE) mortality of Ae. aegypti mosquitoes form Jojutla, Morelos exposed to 13 aerosol insecticides. Percentage of mortality in: (a) center of the room, (b) inside storage cabinets, (c) with obstacle >50 cm above the floor, (d) with obstacle at 50–70 cm above the floor, (e) without obstacle at 50–70 cm above the floor, and (f) without obstacle <170 cm above the floor near a wall. At 24 h after exposure, the overall mortality increased (Fig. 2, Supp Tables 1 and 2 [online only]). For the different locations throughout the room, H24 Casa and Jardin, H24 Mata Moscas y Mosquitos, and Oko Green Multiusos were the only insecticides that induced a 100% mortality. Meanwhile, Oko Azul was the product with the worst performance (Fig. 2; Supp Table 2 [online only]). Mosquitos exposed to Raid Casa y Jardin, Oko Azul, and to some degree to H24 Citronox and Raid Mata Moscos y Mosquitos, recovered from the knockdown (Fig. 2; Supp Table 1 [online only]). Differences among insecticides were still detected (Aerosol effect: Likelihood ratio χ2 = 341.22, d.f. = 13, P <0.0001). Likewise, differences among cage location were observed (Location effect: Likelihood ratio χ2 = 412.17, d.f. = 6, P <0.0001). The inside cabinet location was the location with lower mortality, whereas the center of the room showed the higher mortality. Interestingly, cages located <170 cm above the floor also did not show the higher mortalities (Fig. 2b; Supp Table 3 [online only]) and mortality rates in the location with obstacle increased. The interaction shown that, despite some insecticides had an increased mortality effects than others, there were some locations where its effectiveness was not always as higher than expected (Aerosol × Location effect: Likelihood ratio χ2 =0186.49, d.f. = 78, P = 0.0066) (Fig. 2; Supp Table 1 [online only]). Control groups mortality, at both times, was 0. Discussion The use of household aerosol insecticides allowed us to establish insecticide susceptibility status of Ae. aegypti in Morelos, Mexico. Our results at 30 min after exposure exhibited the null existence of a 100% killing action commercial household aerosol insecticide. A rapid killing action not only could avoid the bite of an infected mosquito but also will prevent resistance. At 24 h post-exposure, H24 Casa y Jardin, H24 Mata Moscas y Mosquitos, and OKO Green Multiusos showed a 100% mortality in all the evaluated locations. Considerable variation in mortality among and within products was observed (from 100 to 30% mortality). Despite the slow killing action, these household insecticides could be another tool to reduce mosquito incidence inside homes, offices, or schools. The low percentages observed do not necessarily indicate resistance, but a lower insecticide efficacy. Only for the products showing mosquitoes recovery after spraying, a degree of resistance could be argued. Not only metabolic or genetic resistance could be related to the variable killing efficacy but also the behavioral responses of the mosquito to insecticides (Chareonviriyaphap et al. 2013). Unfortunately, with our methodology, we were unable to quantify behavioral avoidance responses. Nevertheless, in Ae. aegypti, insecticide contact irritancy and repellency have an important role in female behavioral avoidance (Kongmee et al. 2004, Mongkalangoon et al. 2009). Mosquito escape responses may interfere with other behaviors such as feeding and oviposition selection. Therefore, studies monitoring the behavioral response could give more information about the actual efficacy of insecticides. Spray characteristics could also influence insecticide efficacy. Droplet diameter, velocity separation/agglomeration and collision, number of holes or nozzle diameter, might be different among products leading to differences in their killing efficacy (Ikeda et al. 2006). Previous studies showed that in hidden places, mortality increased at 2 h post spraying (Khadri et al. 2009). It is possible that the number of droplets required to kill the mosquitoes inside cabinets or places with obstacles was insufficient. We recommend opening cabinets and drawers while spraying and a direct spray at semi-exposed places. If not included, we encourage manufactures to clearly label these recommendations. The differences between active ingredients might result in different mortalities. Since doses were dissimilar even among products with the same formulation, it was impossible to evaluate the different formulation mixtures. However, our results showed that tetramethrin and cifenothrin products (H24 Casa and Jardin, H24 Mata Moscas y Mosquitos and Oko Green Multiusos, Table 1; Supp Table 1 [online only]) had the highest knockdown and mortality percentages. But important to mention, the less efficient product (Oko Azul) also contains tetramethrin and cifenothirn (with even higher doses than the efficient products). Other products with higher mortality (<90 %; Supp Table 1 [online only]) differ in their active ingredients (Table 1), as a consequence, a generalization about a formulation cannot be done. Most of these commercial insecticides are not species specific, and their formulation is intended to kill a broad of arthropod species. However, most of them promise an efficient killing action, but it did not happen. The “Jojutla” strain used in this study has been tested for natural and synthetic repellents, showing that the products did not provide satisfactory levels of personal protection against mosquito bites (Kuri-Morales et al. 2017). The strain also presents resistance to bifenthrin, δ-phenothrin, α-cypermethrin, and possible resistance to deltamethrin and permethrin (based on WHO criteria) (Kuri-Morales, unpublished data), as happens with other Mexican mosquito populations ( Saavedra-Rodriguez et al. 2007, Saavedra-Rodriguez et al. 2015; Garcia et al. 2009; Aponte 2013). Thus, since all the active ingredients used in this study were pyrethroids, it is not surprising to find partial susceptibility to aerosols against this strain. It is possible that the products with the higher efficacy found in our study have a combination of accurate spraying characteristics (e.g., droplet diameter, velocity, and nozzle diameter) and appropriate dose and formulations. The overall impact of commercial insecticides on vector-borne diseases epidemics remains unknown. The use of these aerosol insecticides could contribute to control dengue transmission and enhance efficient community protection and participation. For example, reduction in dengue hemorrhagic fever cases in areas where insecticides were given to the patient′s family to spray their home was observed (Osaka et al. 1999). Community spends a considerable amount of money to kill mosquitoes (Loroño-Pino et al. 2014). Therefore, it is necessary to guide the selection of an appropriate and effective household insecticide. Assessments presented here are evidence that products and spraying methods could and should be improved. Supplementary Material Supplementary data are available at Journal of Medical Entomology online. Acknowledgments We thank A. Contreras-Mendez, A. Martinez-Gaona, C. Ramirez-Huicochea, and L. Rosas-Trinidad of the Centro Regional de Control de Vectores Panchimalco, Jojutla for logistical support. This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors. The use of trade names is for the purposes of providing scientific information only, and does not constitute endorsement by the authors’ institutional affiliations. We thank two anonymous reviewers for their helpful suggestions and comments. References Cited Aponte, A. H., Penilla P. R., Dzul-Manzanilla F., Che-Mendoza A., Lopez A. D., and Solis F.. 2013. The pyrethroid resistance status and mechanisms in Aedes aegypti from the Guerrero state, Mexico. Pestic. Biochem. Physiol . 107: 226– 234. Google Scholar CrossRef Search ADS   Chareonviriyaphap, T., Bangs M. 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Mosquito coils, vaporizer mats, liquid vaporizers, ambient emanators and aerosols. Geneva. WHO/HTM/NTD/WHOPES/2009.3. © The Author(s) 2017. Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.

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Journal of Medical EntomologyOxford University Press

Published: Mar 1, 2018

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