J. Cosmet. Sci., 70, 197–207 (July/August 2019) 197 Infl uence of Sex Ratio and Density on the Comparative Repellency of IR3535® Against Caged Aedes, Anopheles, and Culex Mosquitoes S ILVANA KITADAI NAKAYAMA, RÜEDIGER GRAF, ANJA-MARTINA BOHLMANN, JUTTA ZURLAGE, HOWARD EPSTEIN, MÁRCIA R.T. DE CAMARGO RANZANI, and FRANK PFLÜECKER, Merc k S.A., 064565-130 São Paulo, Brazil (S.K .N.), Department of Chemical Engineering and Biotechnology, University of Applied Sciences Darmstadt, 64239, Darmstadt, Germany (R.G .), Merck KGaA, Performance Materials, 64293 Darmstadt, Germany (A.- M.B., J.Z., F.P.,), EMD Performance Materials Corp., Philadelphia, PA (H .E.), Bioagri Institute, 13515-000 São Paulo, Brazil (M.R. T.de.C.) Accepte d for publication June 18, 2019. Synopsis Studie s on topical repellent effi cacy conducted with caged mosquitoes in the laboratory are important to both the development and regulation of insect repellents. Guidelines for laboratory studies stipulate specifi c densities, sex ratios, and biting rates, whereas those for fi eld studies are governmentally required before a promising repellent can be registered for human use. These protocols stipulate minimum biting rates alone. Relatively little is known, however, about the infl uence of mosquito density and sex ratio on their biting propensity, either in the fi eld or laboratory. Using Environmental Protection Agency guidelines for cage testing, we studied the infl uence of mosquito density and sex ratio in laboratory repellency tests of the biopesticide Ethyl butylacetylaminopropionate (IR3535™) (20%) against three mosquito species (Aedes aegypti, Anopheles aquasalis, and Culex quinquefasciatus). DEET [3-(N-acetyl-N-butyl) aminopropionic acid ethyl ester] (20%) in a laboratory prepared formulation was used as a comparison article. Studies were conducted by trained investigators at the BioAgri Laboratories in Brazil. We found that higher mosquito density generally decreased protection time, but that the infl uence of sex ratio was more complex. The presence of male mosquitoes increased protection times against Aedes and Anopheles perhaps because mate-seeking males interfered with female feeding. Interestingly, by contrast, protection times decreased against Culex in the presence of males. Such considerations may potentially assist in improving the match between cage and fi eld testing under a broader range of conditions that permit more accurate labeling of repellents for safe and effective use by consumers. INTRODU C TION Mosquit o repellents are important for personal protection against nuisance biting and mosquito-transmitted pathogens, including those that cause malaria, dengue fever, and Addre ss all correspondence to Howard Epstein at howard.epstein@emdgroup.com.
JOURNAL OF COSMETIC SCIENCE 198 West Nile fever (1). The protection a repellent affords is infl uenced by numerous factors, including attributes of the insects, hosts, environmental conditions, repellent formula- tion, and dosing, and the interactions of these factors are reviewed by Barnard (2) and Carroll (3). Many of these factors have been studied with laboratory strains of caged female mosquitoes however, no general consensus has been reached regarding the opti- mal mosquito biting rate and density for cage-based repellency tests (2). Indeed, contem- porary cage-testing guidelines issued by regulatory arms of federal and international public health agencies differ substantially when reviewing the U.S. Environmental Pro- tection Agency (EPA) (4), the European Union (5), and the World Health Organization (6) guidelines. In a co mplementary approach, the performance of repellent formulations that prove promis- ing in the laboratory is often verifi ed under expected conditions of use in nature with wild mosquito populations. In that circumstance, some of the factors that infl uence effi cacy are not controlled, permitting natural variation. Uncontrolled variables include environmental conditions and mosquito species demography. Furthermore, fi eld tests frequently include more human subjects than are feasible in laboratory tests, better representing the range of people to be protected. Review of submitted data from fi eld tests is required as part of required vetting for permission to market labeled repellents by the U.S. EPA and E.U. Biocides Division, and likewise recommended by the World Health Organization (6). Factors that may infl uence repellent performance in nature, including population density, sex ratio, and age structure, can readily be measured in the laboratory. Biological factors that have been shown by cage studies to infl uence the effi cacy of topical mosquito repel- lents include larval diet, carbohydrate availability to adult mosquitoes, age and reproduc- tive history of adult female mosquitoes, partial blood engorgement, and inherent qualities of repellent-treated test subjects (7–9). Biting patterns can also vary with the size of the cage and density (7,8,10). Sex ratio infl uences have not been quantifi ed, although exclud- ing males from laboratory tests to control interference with females is conventional. Given that males are naturally present in wild populations, a more systematic approach to laboratory studies of sex ratio and repellency is needed. Although laboratory tests allow controlled conditions to aid identifi cation of new repellents for fi eld evaluation (2), sex ratio and its interplay with population density are understudied factors for which labora- tory testing remains warranted. Cage-based laboratory testing of mosquito repellents is the standard approach for screen- ing actives and formulations before and during product development, because it is more convenient, is lower in cost than fi eld testing and repeatable in the laboratory setting. These studies are also suitable for comparing performance among marketed repellent products for consumer education. Cage testing allows environmental variables to be con- trolled and manipulated on the other hand, such testing does not match typical condi- tions of repellent use by consumers. Given the reciprocal liabilities of laboratory and fi eld studies, an additional study of factors infl uencing laboratory performance offers potential to improve the design and interpretation of insect repellent development studies and sug- gests factors that may be important to the design of fi eld studies and laboratory cage studies. Currently, the best approach to fi eld and laboratory testing is to conduct testing with as many individuals as possible. In this study, we examine the effects of sex ratio and density on repellent performance against three genera of mosquitoes under caged conditions. This study provides data for
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