J Arthropod-Borne Dis, September 2019, 13(3): 259–267 S Sayono: Effect of D-Allethrin … 259 http://jad.tums.ac.ir Published Online: September 30, 2019 Original Article Effect of D-Allethrin Aerosol and Coil to the Mortality of Mosquitoes *Sayono Sayono, Puji Lestari Mudawamah, Wulandari Meikawati, Didik Sumanto Department of Epidemiology and Tropical Diseases, School of Public Health, Universitas Muhammadiyah Semarang, Semarang, Indonesia (Received 20 Mar 2018; accepted 16 Jun 2019) Abstract Background: Commercial insecticides were widely used by communities to control the mosquito population in their houses. D-allethrin is one of insecticide ingredients widely distributed in two different concentrations namely 0.15% of aerosol and 0.3% of coil formulations. We aimed to understand the mortality of indoor mosquitoes after being exposed to d-allethrin 0.15% (aerosol) and 0.3% (coil) formulations. Methods: This quasi-experiment study applied the posttest-only comparison group design. The aerosol and coil d-al- lethrin were used to expose the wild mosquitoes in twelve dormitory bedrooms of SMKN Jawa Tengah, a vocational high school belonging to Central Java Provincial Government, on March 2017. The compounds were exposed for 60 min to each bedroom with four-week interval for both of formulations. The knockdown mosquitoes were collected into a plastic cup and delivered to the laboratory for 24h holding, morphologically species identification and mortality re- cording. History of insecticide use in the dormitory was recorded by an interview with one student in each bedroom. Data were statistically analyzed with independent sample t-test and Mann-Whitney. Results: As many as 57 knockdown mosquitoes belonging to three species were obtained namely Culex fuscocephala, Cx. quinquefasciatus and Aedes aegypti with mortality rate of 50.88% after 24h holding. Knockdown and mortality of mosquitoes were significantly different based on d-allethrin formulations. D-allethrin concentrations were not effective for controlling Culex mosquitoes but effective for Ae. aegypti. Conclusion: Further efficacy of d-allethrin 0.15% aerosol to eradicate Ae. aegypti is necessary to be conducted in sup- porting the Dengue vector control. Keywords: D-Alletrin; Insecticide; Culex fuscocephala; Culex quinquefasciatus; Aedes aegypti Introduction Mosquitoes play an important role as vec- tor of several kinds of diseases. The different species of mosquito could transmit different dis- ease agents, although some species can trans- mit a number of pathogens (1, 2). Aedes mos- quitoes have been known as vector of dengue, Chikungunya and Zika viruses (3) as well as Filarial parasites in certain condition (4). Culex mosquitoes can transmit Japanese encephalitis virus and filarial worms, while Anopheles trans- mits malaria and filarial worms. Armigeres spp. and Mansonia spp. also transmit filarial worms (1, 2). Some mosquito species are found in resi- dential environments with different abundance. Eight mosquito species were reported from six habitats in Thailand with the order of relative abundance were Cx. quinquefasciatus, Cx. vish- nui, Cx. gelidus, Ae. aegypti, Mansonia spp., Anopheles spp., and Cx. bitaeniorhynchus, re- spectively (5). Nine mosquito species were found in urban settlement, in Nigeria namely Cx. quin- quefasciatus, Cx. annulioris, Anopheles gambi- ae, An. funestus, An. rhodesiensis, An. arabiensis and Ae. aegypti. Three mosquito species showed the highest relative abundance i.e., Cx. quin- quefasciatus (50.24%), Anopheles spp. (26.5%), and Ae. aegypti (0.2%) (6). In Mojokerto, East Java Province, Indonesia, five mosquito species were found in settlements namely Ae. aegypti, Ae. albopictus, Ae. laniger, Cx. bitaeniorhynchus and Cx. quinquefasciatus (7). Aedes aegypti is the dominant species in urban settlements (7) and the Dengue endemic areas (8), while Cx. *Corresponding author: Dr Sayono Sayono, E-mail: say.epid@gmail.com http://jad.tums.ac.ir/ J Arthropod-Borne Dis, September 2019, 13(3): 259–267 S Sayono: Effect of D-Allethrin … 260 http://jad.tums.ac.ir Published Online: September 30, 2019 quinquefasciatus is the dominant species in ru- ral area (7). Urban people in the Dengue endemic areas often used insecticide to repel and against mos- quito exposure with several formulations such as repellent, aerosol, mosquito coil and electric mat. The most common of insecticide com- pounds are d-allethrin, prallethrin, transfluthrin, and diethyl toluamide (DEET) (9, 10). Commer- cial insecticides usually applied by communi- ty with ignored the written instruction (11). This unstandardized practice can cause a neg- ative impact such as mortality of non-target organisms, environmental pollution, and the emergence of insect vectors resistance (12). The resistance of mosquito vectors to py- rethroid insecticide class has been reported from several countries. Aedes aegypti is resistant to several pyrethroid compounds in Vietnam (13), Martinique (14), and Indonesia (15, 16). Anoph- eles barbirostris was resistant to some insecti- cide compounds namely lambda-cyhalothrin 0.05% and etofenprox 0.5% and tolerant to bendiocarb 0.1% (17). The resistance of Cx. quinquefasciatus to pyrethroid was reported from Japan and China that indicated by a ge- netic mutation (18). This species was reported resistant to permethrin, deltamethrin, and ben- diocarb in Benin, Nigeria (19). Permethrin re- sistant of Cx. quinquefasciatus also reported from Central Java, Indonesia (20), and Man- sonia is tolerant to pyrethroid insecticide (21). Cx. pipiens is reported resistant to four of in- secticide classes namely pyrethroid, organochlo- rine, carbamate, and organophosphate in Iran (22). Household insecticides circulating in Indo- nesia mostly contain pyrethroid compounds in either single or combination formulations, in- cluding d-allethrin. These insecticides are of- ten used in the dense population settlement with uncontrolled doses. Susceptibility of mosqui- toes to the compounds is necessary evaluated. We aimed to understand the susceptibility of mosquitoes to d-allethrin 0.15% aerosol and 0.3 % coil compounds in an urban settlement. Materials and Methods Study site This quasi-experimental study was conduct- ed in twelve of sixteen bedrooms at the dormi- tory of SMKN (Vocational High School) Jawa Tengah on March 2017. Each of the 4x6 square meter bedrooms contains six beds and represents the densely populated settlement. The two of d-allethrin formulations were applied at the twelve of bedrooms sequentially. Application of d-allethrin aerosol and coil insecticide The d-allethrin aerosol insecticide was ap- plied in the morning when the bedrooms are empty. Clothes and snacks were moved out from bedrooms. All of ventilation, windows, door, and holes in the rooms were closed. Tempera- ture and humidity of each room were meas- ured by hygrometer and recorded. Each bed- room was divided into two sections and six quadrant direction for spraying of aerosol in- secticide (Fig. 1). Six sprayings were done in each bedroom for five seconds according to the directions based on the previous study (23) with modifications. All of the bedrooms were closed for 60min after the aerosol insecticide was sprayed. The volume of sprayed liquid is equal- ized by measuring the weight of the insecti- cide bottle before and after it is sprayed. The d-allethrin mosquito coil formulation was obtained from the market and applied four weeks following application of the aerosol for- mulation based on the previous study with mod- ifications (24). A mosquito coil was burned on the tip and placed for 60min in the center of each bedroom. Application of those different insecticide formulations was done in the equal condition of bedrooms. Laboratory works The knockdown mosquitoes from each bed- room were collected in the plastic cups and labeled by name of the bedroom and delivered to Epidemiology Laboratory, Faculty of Pub- lic Health of Universitas Muhammadiyah Se- http://jad.tums.ac.ir/ J Arthropod-Borne Dis, September 2019, 13(3): 259–267 S Sayono: Effect of D-Allethrin … 261 http://jad.tums.ac.ir Published Online: September 30, 2019 marang for twenty-four-hour holding. Each cup was placed in different mosquito cage. Tem- perature and humidity of the recovery room were maintained at the 27±2 Celsius degree and 80± 10%. The ten percent of sugar solution was placed in each mosquito cage for feeding the live mosquitoes. Mortality of mosquito was calcu- lated based on species. Mosquito identification used the arthropod identification key of Wal- ter Reed Biosystematics Unit (25). Data analysis The relative abundance, exposure frequency and dominance rate of mosquitoes were calcu- lated based on the formulas below (26): Dominance rate= relative abundance x frequency The different of knockdown and mortality of mosquitoes were analyzed based on d-alle- thrin formulation. History of insecticide use in the dormitory was showed in a frequency table. Ethical approval Protocol of this study was approved by Eth- ics Committee of Faculty of Medicine of Uni- versitas Diponegoro Semarang. Informed con- sent and research permission were obtained from dormitory management. Results Knockdown and mortality of mosquitoes As many as 57 knockdown mosquitoes were obtained from this study, and mortality of mos- quito was 50.88%. Majority of the knockdown (94.44%), dead (96.43%) and alive (92.31%) mosquito were obtained from the d-allethrin aerosol exposed-group, and contrast conditions were found in the mosquito coil exposed-group. A number of the knockdown, dead and alive mosquitoes were significantly different based on the d-allethrin formulations (Table 1). Morphological identification Results of morphological identification of mosquito were found three species. Two spe- cies belong to Culex genus and one species belongs to Aedes genus, namely Cx. fuscoceph- ala, Cx. quinquefasciatus and Ae. aegypti. Men- tion order of the three mosquito species also represents the order of relative abundance, ex- posure frequency and dominance rate (Tables 2, 3). History of Commercial Insecticide Use Results of interview with respondent of each bedroom showed that majority of dormitory in- habitants used insecticide to expel the mosqui- toes almost every day, mainly the repellent. The d-allethrin compound was also used among in- habitants (Table 4). Fogging or residual spray- ing was not used in this dormitory. Table 1. Knockdown, dead and alive mosquitoes based on the insecticide (d-allethrin-0.15% compound) formulations Insecticide formulation Mosquito conditions Knockdown Dead Alive Aerosol Number 57 29 28 Minimum 1 1 0 Maximum 13 7 6 Mean 4.50 2.33 2.17 Standard deviation 3.26 1.92 1.75 Mosquito coil Number 3 1 2 Minimum 0 0 0 Maximum 2 1 2 http://jad.tums.ac.ir/ J Arthropod-Borne Dis, September 2019, 13(3): 259–267 S Sayono: Effect of D-Allethrin … 262 http://jad.tums.ac.ir Published Online: September 30, 2019 Mean 0.25 0.08 0.17 Standard deviation 0.62 0.29 0.58 P-value 0.01 0.02 0.01 The higher number of mosquitoes was obtained from the aerosol formulation rather than mosquito coil indi- cating the faster effect of this formulation Table 2. Abundance, frequency, and dominance rate of mosquito species Spices Number of mosquitoes Relative abundance (%) Frequency Dominance rate Culex fuscochepala 41 71.93 0.45 32.96 Culex quinqueasciatus 15 26.31 0.29 7.67 Aedes aegypti 1 1.75 0.4 0.07 Three mosquitoes species were found in the dormitory with the high abundance of the Culex genera Table 3. Knockdown, dead, alive and mortality of mosquitoes based on the species and d-allethrin formulations Species Insecticide formulation Knockdown Dead alive Mortality (%) Culex fuscochepala Aerosol 41 20 21 48.78 Mosquito coil 0 0 0 0.00 Culex quinquefasciatus Aerosol 12 7 5 58.33 Mosquito coil 3 1 2 33.33 Aedes aegypti Aerosol 1 1 0 100.00 Mosquito coil 0 0 0 0.00 Total 57 29 28 50.88 Mortality of mosquitoes after exposed with d-allethrin 0.15% and 0.30% insecticide compounds were very low. This condition indicated that Culex mosquitoes were resistant to these concentrations Table 4. Information about insecticide use among students at the boarding school Variables f % Commercial insecticide use 1. Yes 10 83,3 2. No 2 16,7 Insecticide formulation 1. Aerosol 1 10,0 2. Electric mat 3 30,0 3. Repellent (lotion) 6 60,0 Insecticide compounds 1. Diethyltoluamid 12.5% 4 40,0 2. Diethyltoluamid 13% 1 10,0 3. Diethyltoluamid 15% 1 10,0 4. D-aletrin 0.15% and Praletrin 0.2% 2 20,0 5. Praletrin 13.16g/l 2 20,0 Frequency of insecticide use in a week 1. 1–3 times 4 40,0 2. 4–5 times 2 20,0 3. 6–7 times 4 40,0 Majority of inhabitants at the dormitory use insecticide, mainly in repellent formulation with DEET compound, although the daily use is under 50% of students. Forty percent of inhabitants used pyrethroid compounds Table 1. Continued … http://jad.tums.ac.ir/ J Arthropod-Borne Dis, September 2019, 13(3): 259–267 S Sayono: Effect of D-Allethrin … 263 http://jad.tums.ac.ir Published Online: September 30, 2019 Fig. 1. Direction of insecticide spraying. The bedroom was divided into six spraying directions that indicated by the rows Discussion This result showed that d-allethrin aerosol formulation can eradicate and kill more mos- quitoes rather than the coil formulation, although this compound indicated effective result for Ae- des mosquitoes only. This finding required fur- ther investigation to obtain sufficient evidence of Ae. aegypti susceptibility to d-allethrin. Using the aerosol formulation allowed that the drop- lets of insecticide will effectively contact with the mosquito’s body, and inhale via respiratory system of mosquitoes (27). The mortality rate of mosquitoes in this study indicated the low efficacy of d-allethrin 0.15% to the mosquito population in the dormitory rooms. This result matched with the facts that majority of dormitory residents use commercial insecti- cide for preventing mosquito attack with high frequency, mainly repellant, electric mat, and aerosol formulation. Those insecticide formula- tions also contain the d-allethrin 0.15% com- pound (Table 4). High frequency of household insecticide use will correlate with insecticide re- sistance among Culex mosquitoes (28). Re- sistance of mosquitoes to d-allethrin compounds is similar to the previous report from Malaysia and Indonesia that the mosquito coil containing d-allethrin 0.2% compound resulted in the low mortality rate (24, 29, 30), but different from the reports of aerosol insecticide application con- taining d-allethrin and d-trans allethrin from Thailand that showed mortality rate of mosqui- toes were 96% (31) and 90% (32), respective- ly. Although distinctly different with the find- ings in Thailand, results of this study correspond to similar finding in Central Java Province that Cx. quinquefasciatus mosquitoes in endemic are- as of Lymphatic filariasis have been resistant to the pyrethroid compound, in particular, per- methrin 0.75% (20). In Iran Cx. pipiens Linn. was resistant to some pyrethroid compounds and other insecticide classes (22). Permethrin and d-allethrin derived from the same class of insecticide, pyrethroid. This insecticide class has target site the voltage-gated sodium channel gene (33). The different types of pyrethroid com- pounds will have a similar effect to disrupt the voltage-gated sodium channel gene (34) and cause the genetic mutation of codon 1014 of the gene that indicated by substitution of amino ac- id leucine to phenylalanine or serine (35). Although the dormitory is located in the Dengue endemic of urban residential, there is only a few the Aedes mosquito found. This phe- nomenon is caused that the dormitory is sur- rounded by a two-meter high wall fence, and there was no puddle of clean water as a place for microhabitat of this species. This wall can prevent the entrance of mosquito into the dor- mitory areas. The female Ae. aegypti use the opened clean water of the domestic containers in laying their eggs rather than natural water con- tainers such as leaf midrib, tree hole or bamboo stems (36). Culex is the dominant mosquito genus in this settlement. This result is in accordance with the findings in Thailand (5) and Nigeria (6), but dif- ferent from the findings in Mojokerto, Indone- sia where the results of larval surveys in various breeding places in the urban settlement obtained the dominant mosquitoes are Ae. aegypti (7). Ae- des aegypti was the dominant mosquito species in the Dengue endemic areas (8). In this case, the dormitory is located in an urban environment with dense building and surrounded the sewers with stagnant water. This condition provides a http://jad.tums.ac.ir/ J Arthropod-Borne Dis, September 2019, 13(3): 259–267 S Sayono: Effect of D-Allethrin … 264 http://jad.tums.ac.ir Published Online: September 30, 2019 good habitat for breeding site of Culex mos- quitoes. Theoretically, the favorite habitat of this species is stagnant of water surface such as hoof- prints, rain pools, irrigation channels, discard- ed tubes, ditch, sewer, and ponds (37, 38). Other studies on the abundance of mosqui- toes in the educational environment were report- ed from Thailand (39), Sabah, Malaysia (40), Makassar, Indonesia (41) that the dominant mos- quito is the genus Culex, similar to the dormito- ry of this study although Cx. quniquefasciatus is not dominant species (42, 43). The further in- vestigation is needed to analyze the wild mosqui- to susceptibility to d-allethrin compound by us- ing the laboratory strain of mosquito as the con- trol group, and the causation between environ- mental profiles, kinds of breeding site and insec- ticide use to the abundance and dominance of mosquito species, and the occurrence of diseases. Conclusion There were three mosquito species found in the bedrooms of SMKN Jawa Tengah belong- ing to two genera namely Culex and Aedes. Ex- posure of d-allethrin 0.15% in space spray for- mulation caused higher knockdown and dead mosquito rather than d-allethrin 0.3% in mos- quito coil formulation. Overall, the mortality rate of mosquito reached 50.88% which indicat- ed a resistant status to this insecticide compound, except Ae. aegypti. Further investigation is need- ed to determine Ae. aegypti abundance at the dormitory and resistant status of Culex mosqui- to to another insecticide compounds. Acknowledgements We would like to thank for SMKN Jawa Tengah (Vocational High School of Central Ja- va Government) given the research permission. All authors declare that there is no conflict of interest. References 1. Sarwar M (2015) Insect-Borne Disease Trans- mitted by Some Important Vectors of Class Insecta Hurtling Public Health. Int J Bioinform Biomed Enggin. 1(3): 311– 317. 2. Singh N, Shukla S, Gupta V, Tandia N, Singh P (2015) Mosquito borne zoonotics dis- ease. Livest Sci. 6: 65–72. 3. 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