Printer Friendly

Laboratory and semi-field evaluations of two (transfluthrin) spatial repellent devices against Aedes aegypti (L.) (Diptera: Culicidae).

Aedes aegypti (L.), also known as the "yellow fever mosquito," is an important vector of viral diseases such as yellow fever, dengue, Chikungunya, and, most recently, Zika virus. (1,2) Despite current vector control efforts, the incidence and geographical expansion of these pathogens continue to increase at an alarming rate. For example, the incidence of dengue has increased 30 fold over the last 50 years. (3) The World Health Organization (WHO) estimates 50-100 million cases occur annually in over 100 endemic countries, putting almost half of the world's population at risk. More than 70% of the population at risk for dengue worldwide live in member states of the WHO southeast Asia and western Pacific region. (3) As a result, the Department of Defense (DoD) personnel and family members stationed in these regions are at risk.

Vector control remains the primary defense against vector-borne diseases. Standard preventive deterrence against vector-borne diseases incorporates integrated pest management (IPM) with personal protective measures (PPMs). The IPM approach to pest control integrates cultural, biological, physical, and chemical methods which minimize health and environmental risk. Often in situations when the threat of vector-borne disease transmission is high, direct suppression of vectors using pesticides is favored over nonchemical control methods. However, the repeated failure of conventional insecticides to control vector species in some areas continues to put Soldiers at risk. Furthermore, the failure to control vector populations may result in additional chemical applications that potentially contribute to other vector control problems such as pesticide resistance, unintended exposure to nontarget organisms, and environmental pollution.

The PPM standards mandated by the military include use of a topical repellent, N, N-diethyl-3-methylbenzamide (DEET) or 1-piperidinecarboxylic acid 2(2-hydroxyethyl)-1-methylpro-pylester) (Picaridin), proper wear of a permethrin-treated uniform, and the use of a bed net. (4) Additionally, malaria prophylaxis is prescribed when service members are deployed in endemic areas. However, compliance with PPM standards remains a problem among service members. (5-7) Sanders et al (8) reported that responders in a 2004 study of personnel returning from Iraq and Afghanistan indicated that a majority (51%) did not use DEET, even though most knew that it was readily available. A report on the use of PPM among confirmed malaria cases in 2012 revealed that compliance with 4 preventive measures (use of DEET, proper uniform wear, adherence to prophylaxis, and postdeployment antirelapse therapy) was 0%. (9) Even when compliance with PPM is high, service members are still exposed to vectors during physical training or while off duty. Additional control methods are needed to augment the DoD's current vector control strategy.

SPATIAL REPELLENTS

Recently, area (spatial) repellents have received interest as a novel system for vector control. Spatial repellents work by releasing chemicals into the air to reduce mosquito entry into treated spaces and to inhibit blood-feeding behavior. An additional benefit of this type of behavioral modification is a delayed or diminished development in the emergence of insecticide resistance. (10) Several types of commercial spatial repellent products have been reported in the literature: impregnated plastic or paper strips, (11) coils, (12-14) candles, (15-17) fan emanators, (18-21) heat-generating devices, (20-22) and microdispensers. (23)

Impregnated Plastic

Plastic or other substrates impregnated with fluorinated pyrethroids (metofluthrin and transfluthrin) can passively deliver spatial repellents without external energy input. Yayo et al (11) investigated the effect of Rambo Insecticide Paper (0.45% transfluthrin) on indoor resting densities and biting rates of 2 important malaria vectors (Anopheles funestus Giles and An. gambiae s.l.) at a peri-urban field site in Nigeria. A significant reduction in both indoor resting density (91%) and biting rate (86%) was reported. Passive emanators may be preferred by the DoD, as these devices would be most likely to meet logistical and safety requirements.

Mosquito Coils

Mosquito coils are the most commonly used household insecticidal product in the world. (12) Avicor et al (13) conducted a laboratory evaluation of 3 commercial coil products for protection efficacy against An. gambiae Giles in southern Ghana. All 3 coils (FISH M (0.005% metofluthrin)) 86%, Shieldtox (0.15% d-trans allethrin) 74%, and Tesco Value (0.3% allethrin) 72% showed high knockdown efficacy. Hill et al (12) demonstrated the effectiveness of using the Transfluthrin mosquito coil (Raid, SC Johnson, Racine, WI) in households to reduce malaria transmission. The Transfluthrin mosquito coil provided 77% protection against Plasmodium falciparum Welch. Msangi et al (14) assessed feeding inhibition and repellency of 3 pyrethroid brands (Kiboko, Total, and Risasi) of mosquito coils in experimental huts in northern Tanzania. Induced exophily was high for Culex quinquefasciatus Say (95%), but was low in An. gambiae (61%) for all products tested. Feeding inhibition was significantly reduced for both species: Cx. quinquefasciatus (97%) and An. gambiae (88%).

Fan Emanators

Fan emanators that vaporize metofluthrin are marketed as promising tools with long-lasting spatial protection against mosquitoes. Various studies have evaluated the efficacy of the Off! Clip-On device (SC Johnson). Xue et al (18) evaluated this device in the field in northeastern Florida, which proved to be 70% and 79% effective at repelling Aedes albopictus Skuse and Ae. taeniorhynchus (Wiedemann) from human test subjects. In a semifield study in Israel, the device reduced biting on the arms of volunteers against Ae. albopictus by 96% and Cx. pipiens L. by 95%. (19) Lloyd et al (20) reported a 64% reduction in Ae. albopictus collected from Biogents Sentinel (BGS) traps located near the repellent device. The Off! Clip-On device has also been reported to have limited to no effect on certain species. In a semi-field study conducted by Dame et al, (21) the device failed to reduce the populations of An. quadrimaculatus Say and Psorophora columbiae (Dyar and Knab) collected in surrogate traps. Reduction rates for this study ranged from 8% to 16%.

Heat Generating Devices

The ThermaCell (Thermacell Repellents, Bedford, MA) spatial repellent device (active ingredient allethrin), is one of the most popular heat generating devices on the market. Collier et al (22) conducted a study in Louisiana using several spatial repellent devices (Dragon fly/Mosquito Cognito, ThermaCell, SC Johnson OFF! Mosquito Lantern) and systems to determine their effect on backyard mosquito population levels, in which the ThermaCell device was the most effective device in reducing mosquito populations (Cx. salinarius Coquillett, Cx. quinquefasciatus, and Ae. vexans (Meigen)). In a field study conducted in Jacksonville Florida, (20) the number of Ae. albopictus repelled by the ThermaCell was significantly higher than the other spatial repellents evaluated (Lentek Bite Shield and Bug Button Mosquito Eliminator).

The objectives for this study were (1) to evaluate the efficacy of two commercially available transfluthrin spatial repellents for inhibiting Ae. aegypti (L.) host-seeking behaviors (anemotaxis, landing, and blood feeding) under laboratory conditions, and (2) determine if these products were effective in reducing the number of host-seeking Ae. aegypti from entering a baited military-style tent in a controlled semi-field environment.

MATERIALS AND METHODS

Mosquitoes

Aedes aegypti eggs (Liverpool and Orlando strain) were obtained from the US Department of Agriculture (USDA) Agricultural Research Service (ARS) Center for Medical, Agricultural, and Veterinary Entomology, Gainesville, Florida. They were reared in an insectary using a 12:12 hour (light/dark) photoperiod at 26[degrees]C and 35% to 50% relative humidity (RH). Larvae were fed ground tropical fish flakes (Tetra Werke, Melle, Germany). Adults were held in screened, 3.79 liter plastic buckets, and fed with a cotton pad moistened with 10% aqueous sucrose solution. Adult female mosquitoes were 5 to 10 days old and incubated in plastic buckets along with a water-moistened pad without sugar for 24 hours before they were used in bioassays.

Spatial Repellent Devices Evaluated

Two transfluthrin-based spatial repellent (SC Johnson Company) products: Raid Dual Action Insect Repellent and Home Freshener, and Raid Shield were evaluated in this study (Figure 1).

In 2012, SC Johnson, Cornell University's Center for Sustainable Global Enterprise, and the Bill and Melinda Gates Foundation created the WOW, which is a business concept that creates access to pest control products that can help prevent malaria in at-risk populations at the "base of the pyramid," as well as home-cleaning and personal care products valued by rural consumers. The Raid Dual Action Insect Repellent and Home Freshener is one of 6 products developed from the WOW program in Ghana. The product consists of a spray bottle (0.40% transfluthrin) and a colorful plastic poster decorated with a well-known Ghanaian adinkra symbol.

Raid Shield is a product developed for research purposes (not commercially available) by the SC Johnson Company. It is a clear plastic strip that is impregnated with transfluthrin (1%). Once the plastic strip is exposed to air, transfluthrin is slowly released into the immediate area.

Laboratory Evaluations (Wind Tunnel)

Laboratory evaluations were conducted in a 3.0 m x 61 cm x 60 cm wind tunnel (Figure 2A) at the USDA-ARS Invasive Insect Biocontrol and Behavior Laboratory in Beltsville, Maryland. With a few minor deviations, the wind tunnel was set up in accordance with Klun et al. (24) Air temperature in the chamber was controlled by a window air conditioner and baseboard electric heaters and maintained at 25[degrees]C [+ or -] 4[degrees]C in the tunnel. The RH inside the chamber was maintained at 25% to 35% using a misting humidifier. The upwind end of the tunnel was connected to the air conditioning chamber by a cowling that housed a 61 cm diameter fan driven by a rheostat-controlled Dayton Electric Model 2Z846A motor that pushed conditioned air through an air filter into the tunnel. Air flow within the tunnel was monitored using an air flow gauge, while temperature and relative humidity was recorded using a HOBO data logger (Onset Computer Corp, Bourne, MA).

The wind tunnel was fitted with a 6-well mosquito feeding reservoir (Figure 2B) that was positioned at the upwind end of the tunnel parallel to tunnel airflow. The reservoir was placed on a stand made of 0.5 cm thick Plexiglas with a 33.8 cm x 15.4 cm base and a 29.8 cm x 7.0 cm (length x width) upper shelf with 1.2 cm high edges at each end of the shelf to secure the reservoir on the shelf. Positioned on the shelf, the top surface of the reservoir was 18 cm above the tunnel floor, at the center of the tunnel, and 47 cm away from the upwind tunnel screen. In order to maintain a constant temperature (38[degrees]C) for the blood contained in the reservoir, it was modified and connected to a water bath circulator (Lauda E100, Wobser GMBH and Co, Konigshofell, Germany). A breath-delivery tube (2.5 m x 22 mm inner diameter; Tri-Anim, Sylmar, CA) ran from outside of the upwind end of the tunnel to breath exhaust position inside the tunnel 20 cm above the tunnel floor, at the tunnel center, and 20 cm from the upwind end of the tunnel.

Prior to each test, the upper surface of the feeding reservoir was coated with a thin layer of high-vacuum silicone grease (Dow Corning Corp, Midland, MI), and the wells were filled (approximately 6 ml capacity) with human blood from the Walter Reed Army Institute of Research (WRAIR), Silver Spring, MD, to which Adenosine triphosphate (ATP) was added on the day of testing to obtain a concentration of [10.sup.-3] mmol/L ATP. The filled cells were covered with an Edicol collagen membrane (G Street Fabrics, Rockville, MD). During treatment evaluations, the treatment device was suspended from the wind tunnel ceiling facing downwind and positioned 38 cm in front of the feeding reservoir.

Trials for each spatial repellent device were replicated 5 times. Each trial consisted of one control test followed by 5 consecutive treatment tests. The purpose of the control evaluation was to establish a baseline for mosquito activity under normal conditions (untreated) and to confirm the absence of pesticide contamination in the wind tunnel. A test began by placing a mosquito release canister containing 20 female Ae. aegypti (Liverpool-strain) inside the wind tunnel. Subsequently, human breath was expired from the breath-delivery tube for 5 seconds and the mosquitoes were released and allowed to freely fly inside the wind tunnel for 10 minutes. During this time period an observer recorded the frequency of probing and landing occurring on the mosquito feeding reservoir. Upon completion of the 10-minute period, the mosquitos were visually examined for evidence of knockdown from chemical exposure and feeding status (blood-fed or unfed). Mosquitoes were removed from the chamber using a vacuum aspirator.

Semi-field Evaluations (Enclosures)

Semi-field evaluations were conducted using 2 outdoor enclosures (Figure 3A), located at the Navy Entomology Center of Excellence in Jacksonville, Florida. Each enclosure consisted of a metal frame that measured 6.1 m wide x 10.7 m long x 3.4 m high. The enclosure was completely covered with mosquito screen and had a concrete base. Several potted plants were placed in the interior of each enclosure to mimic the natural outdoor habitat. A single military style tent (3-person) was placed at the far end of the enclosure, opposite the entrance. Each tent housed a BGS 2.0 trap baited with dry ice and BGS proprietary lure. Temperature, relative humidity, and wind speed were measured throughout the evaluation using a HOBO data logger.

Enclosure experiments were conducted simultaneously in the 2 enclosures. Prior to each trial, one of the enclosures was randomly selected as the treatment and the other as the control. Inside the treatment enclosure, the spatial repellent device was placed on the outside of the tent near the upper door opening (Figure 3B). Trials were conducted in the morning (8 AM to 11 am) which corresponded with the peak host-seeking period of Ae. aegypti. Two hundred female Ae. aegypti (Orlandostrain) were simultaneously released into each enclosure and allowed to move freely for one hour. At the end of the trial, the mosquitoes inside the tents were collected from the BGS traps and vacuumed out using an aspirator.

Statistical Analysis

Laboratory (Wind Tunnel) Study

Statistical 2-way hypothesis tests were conducted at the 95% confidence level ([alpha]=0.05) to assess differences in landing, probe, blood-fed, and knock down counts among the 2 products (Raid Dual Action and Raid Shield) and treatments (Control and treatment).

Semi-field Study

Statistical 3-way and 2-way hypothesis tests were conducted at the 95% confidence level ([alpha]=0.05) to assess differences in mosquito counts (inside tent and BGS traps) between the 2 products (Raid Dual Action and Raid Shield), between the treatment and control, and between the 2 enclosures. Preliminary goodness-of-fit testing using the Kolmogorov-Smirnov test for normality (25) and the Bartlett test for homoscedacity (homogeneity of variances) (26,27) indicated that the data were non-normal and non-homoscedastic. Thus, the nonparametric Kruskal-Wallis test (28) was used instead of the parametric ANOVA test for the statistical analysis. Post hoc Tukey multiple-comparison, (29) Newman-Keuls, Duncan multiple-range, (30,31) and Scheffe multiple-contrast (32) tests were evaluated based on an optimization analysis, and the optimal model was used to identify the specific pair-wise combinations that are significantly different from each other and contribute to the overall variance source. Interaction effects of air temperature and humidity on mosquito counts were evaluated by regression analysis. All statistical analysis was performed using Intel Visual Fortran Compiler XE 2013 (Intel Corporation, Santa Clara, CA).

Results

Laboratory (Wind Tunnel)

Both products were effective in reducing host-seeking activity of Ae. aegypti in the wind tunnel. Figure 4A shows the treatment effect of both products on the mean landing counts of the mosquitoes. The mean baseline (control) landing counts for the Raid Dual Action and Raid Shield were reduced by 95% (P <.006) and 74% (P <.006) respectively. Mean probing counts for the Raid Dual Action were reduced by 95% (P <.02), while the probing counts for the Raid Shield were decreased by 69% (P <.02) (Figure 4B). Baseline blood-feeding success was significantly reduced (P <.002) for both treatments: Raid Dual Action (100%) and Raid Shield (96%) (Figure 4C). Figures 5 and 6 show the time analysis (50 minutes) for the mean counts of landing, probing, and blood feeding for each treatment. Maximum reduction rates occurred during the first 30 minutes. After 30 minutes, reduction rates dropped below 50%. Blood-feeding reduction rates remained above 85% for the duration of the 50 minute test. Overall, knock-down effects for both products were minimal. Average knock-down was 1.08 mosquitoes, with a maximum count of 4 (20%).

Semi-field (Enclosure)

Weather conditions at NECE, Naval Air Station, Jacksonville, Florida were hot and humid. Temperature and relative humidity recorded inside the semi-field enclosures averaged 25.5[degrees]C (max=29[degrees]C and min=21[degrees]C) and 86.8% (max=97% and min=66%). The prevailing wind direction was from the northeast with average daily wind speeds less than one kph. Regression analysis showed negative correlation of rep-averaged mosquito counts with temperature (C[degrees]) and humidity (%) (r=-0.4637, df=16, P=.3406). Collections of mosquitoes from treatment (with a spatial repellent device) tents were significantly lower than the control (without a spatial repellent device) tents (P <.0001; Figure 7). The Raid Shield reduced mosquito entry into tents by 88%, while the Dual Action only decreased entry by 66%.

COMMENT

Various definitions and characterizations of spatial repellents have been reported in the literature. Dethier (33) defined spatial repellents as any stimulus constituting a vapor physical state which elicits an avoidance reaction. Gouck et al (34) expanded the definition to include any compound or agent that can produce repellency at a distance. Nolen et al (35) defined spatial repellents as "an inhibiting compound, dispensed into the atmosphere of three dimensional space which inhibits the ability of mosquitoes to locate and track a target such as a human or livestock." Results from our investigation indicated that both of the SC Johnson spatial repellent products functioned as spatial repellents. The active ingredient used in both products was the synthetic pyrethroid transfluthrin. Unlike many of the other common pyrethroid chemicals, transfluthrin has a high vapor pressure which enables the chemical to passively vaporize at ambient temperature. Other pyrethroids such as permethrin require an external energy source for volatilization. In order to be a practical tool for Soldiers, a spatial repellent device must be effective, nontoxic, simple to construct and operate, and it should not require frequent maintenance. The 2 products used in this study are lightweight, inexpensive, contained low amounts of pesticide, and are easy to set up. From a logistics standpoint, these devices are available in high quantity and can be easily integrated into military logistic transportation platforms. For example, more than a hundred of these devices could be carried in a Soldier's rucksack and the load effect would be minimal. The operation of these devices only consisted of placing it at the desired location and exposing the treated surface to the air (spray the product on the poster (Dual Action) or open the folded plastic (Raid Shield)). Compliance with mandated topical repellent use remains an issue in the military. Unlike topical repellents, these devices do not require reapplication by the user. Furthermore, the protection from the device benefits more than one person at a time.

Our laboratory (wind tunnel) evaluations of the SC John son spatial repellent products showed significant reductions in host-seeking behaviors (landing, probing and blood-feeding) of Ae. aegypti. However, reduction rates significantly decreased after 30 minutes. Previous studies using transfluthrin showed high efficacy with longer periods of effectiveness. Ogoma et al (36) evaluated transfluthrin treated fabric (hessian cloth) against laboratory reared An. arabiensis Patton. A single hessian strip (4.0 m x 0.3 m) treated with 10 ml of transfluthrin reduced the mosquito attack rate on human volunteers by 99% and consistently conferred greater than 90% protective efficacy for a period of 6 months. Andres et al (37) evaluated transfluthrin dispensed from modified mosquito landing boxes against An. arabiensis in a semi-field system. The protective transfluthrin bubble provided 68.9% protection to human volunteers, and continued to show knockdown effects up to 3 weeks in postlaboratory testing. Govella et al (38) tested transfluthrin treated strips in the field against An. gambiae. The strips conferred 99% protection and remained effective for over 3 months. One major limitation of our study was control of the amount of active ingredient used. Material Safety Data Sheets for both products showed that the amount of transfluthrin was less than 60 mg (less than 2% concentration). In comparison with previous studies, these amounts were relatively low. Additionally, it is important to note that the 2 products are marketed for indoor use.

Knockdown is the incapacitation of arthropods as a result of contact with a sublethal dose of pesticide. In this study, knockdown effects from transfluthrin exposure were low for both products. However, the relative knockdown of mosquitoes was consistently higher for the Dual Action device. This is particularly interesting due to the fact that the Dual Action device contained less transfluthrin. In the wind tunnel, mosquitoes often made direct contact with the Dual Action device. This was not observed with the Raid Shield device. The Dual Action product was designed with a multipurpose function of repelling insects and serving as a home freshener.

Our semi-field experiment demonstrated a tactical utility for spatial repellents. The BGS traps are commonly used by mosquito vector control districts to conduct surveillance and have been proven to be highly effective for collecting Ae. aegypti and Ae. albopictus. In this study, BGS traps baited with C[O.sub.2] were placed in military style tents and served as surrogates for humanbait collectors. Mosquito entry into military style tents was moderately reduced when using the spatial repellent devices. As expected due to environmental conditions, there was a significant variation in the amount of reduction. However, mosquito levels in treated tents remained well below that of control tents. This result suggests that the transfluthrin spatial repellents used in this study may have functioned as attraction inhibitors. A more likely explanation is that this behavior involved excito-repellency. For example, the mosquitoes could have detected and followed the C[O.sub.2] source inside the tent, but due to increased transfluthrin exposure, some of them quickly egressed from the tent to seek fresh air. Other studies suggest that placement of the device inside certain structures enhances the spatial repellent effect. Kawada et al (39) evaluated metofluthrin-impregnated plastic strips against Ae. aegypti in houses located in My Tho City, Vietnam. Multiple regression analysis of environmental factors indicated that both an increase in average room temperature and a decrease in area of openings in rooms that were treated with metofluthrin-impregnated strips positively affected its spatial repellency. Transfluthrin exposure could have also negatively affected other key mosquito behaviors such as blood-feeding and ovipositon. Unfortunately, the experimental design for the semi-field experiment did not include evaluations of these behaviors. Therefore, the effect of the transfluthrin on the mosquitoes that entered the experimental tents remains unknown.

This study suggests that spatial repellents have great potential for enhancing existing vector control and PPM efforts. However, sole reliance on this technology is not practical. Although spatial repellents have shown high efficacy rates in the field reaching levels of 99% protection, changing environmental conditions (wind, precipitation, temperature, and humidity) may present a major challenge for sustaining high efficacy rates. Traditional military approaches to mosquito control are based on the use of insecticides for area-wide abatement and PPM (topical repellents, treated uniforms, and bed nets). However, there is much concern among entomologists that these approaches may be severely restricted in the future due to insecticide resistance. Over the past few decades, there has been an overreliance on the use of pyrethroid insecticides for mosquito control. Global malaria eradication programs depend almost exclusively on pyrethroid-based indoor residual spraying and long-lasting insecticidal nets (LLINs). Although this strategy has been viewed as having an important role in the recent reductions in global malaria mortality, major malaria vectors have developed resistance to this class of insecticides and the resistance alleles are very common in mosquito populations throughout the world. One way to overcome resistance is to rotate different classes of insecticides into a control program. Unfortunately, the acquisition of other classes of insecticides is often difficult and their cost is significantly higher than pyrethroids. Spatial repellents such as transfluthrin are readily available and are relatively inexpensive. A potential means of slowing the evolution of pyrethroid resistance may be the integration of spatial repellents into the program strategy. (40) For example, the incorporation of a spatial repellent with LLINs would result in a 3-tier line of defense: (1) the spatial repellent, (2) contact pyrethroid, and (3) physical barrier (net). The spatial repellent would provide protection outside of the LLIN and contribute to reducing selection for resistance. Additional studies that explore the effects of integrating spatial repellents into DoD field vector control activities are warranted.

ACKNOWLEDGEMENTS

We thank SC Johnson and Company for their cooperation and assistance in providing the 2 products, Raid Dual Action Insect Repellent and Home Freshener and Raid Shield, used in the study.

We thank Anna Katrina Briley and Jason Fajardo for providing mosquitoes as well as for their assistance with the semi-field trials at NECE. We also thank Dr Muhammad Farooq for collecting the weather data at the Navy Entomology Center of Excellence.

Financial support for this project was provided by the Defense Health Program 6.7.

REFERENCES

(1.) Webb CE, Doggett SL. Exotic mosquito threats require strategic surveillance and response planning. Public Health Res Pract. 2016; 26(5). doi: 10.17061/ phrp2651656.

(2.) Castellanos J. Zika, evidencia de la derrota en la batalla contra Aedes aegypti. Biomedica. 2016; 36(1):5-9.

(3.) World Health Organization. Dengue and severe dengue fact sheet [internet]. July 2016. Available at: http://www.who.int/mediacentre/factsheets/fs117/ en/. Accessed March 8, 2017.

(4.) Technical Guide 36, Personal Protective Tech niques Against Insects and Other Arthropods of Military Importance. Washington, DC: US Armed Forces Pest Management Board. 2015. Available at: http://www.acq.osd.mil/eie/afpmb/docs/tech guides/tg36.pdf. Accessed March 8, 2017.

(5.) Dunn L, Mcguire J, Rockswold P. Outbreak report: malaria in a U.S. Marine Reserve unit deployed to Benin. MSMR. 2010; 17(1):8-9.

(6.) Wanja E. Observed noncompliance with implementation of vector-borne disease preventive measures among deployed forces. US Army Med Dep J. April-June 2010:56-64.

(7.) Brisson M, Brission P. Compliance with anti-malarial chemoprophylaxis in a combat zone. Am J Trop MedHyg. 2012; 86(4):587-590.

(8.) Sanders J, Putnam S, Frankart C, et al. Impact of illness and non-combat injury during Operations Iraqi Freedom and Enduring Freedom (Afghanistan). Am J Trop Med Hyg. 2005; 73(4):713-719.

(9.) Shaha D, Pacha L, Garges E, Scoville S, Mancuso J. Confirmed malaria cases among active duty components U.S. Army personnel, January-September 2012. MSMR. 2013; 20(1):6-9.

(10.) Achee N, Sardelis M, Dusfour I, Chauhan K, Grieco P. Characterization of spatial repellent, contact irritant, and toxic chemical actions of standard vector control compounds. J Am Mosq Control Assoc. 2009; 25(2): 156-167.

(11.) Yayo A, Ado A, Habib A, et al. Effectiveness of transfluthrin-impregnated insecticide (paper rambo) and mechanical screening against culicine and anopheline mosquito vectors in Kumbotso, Kano, Nigeria. Mol Entomol. 2016; 7(4):1-8.

(12.) Hill N, Zhou H, Wang P, Guo X, Carneiro L, Moore S. A household randomized, controlled trial of the efficacy of 0.03% transfluthrin coils alone and in combination with long-lasting insecticidal nets on the incidence of Plasmodium falciparum and Plasmodium vivax malaria in Western Yunnan Province, China. Malaria J. 2014; 13:208.

(13.) Avicor S, Wajidi M, Jaal Z. Laboratory evaluation of three commercial coil products for protection efficacy against Anopheles gambiae from southern Ghana: a preliminary study. Trop Biomed. 2015; 32(2):386-389.

(14.) Msangi S, Mwang'onde B, Mahande A, Kweka E. Field evaluation of the bio-efficacy of three pyrethroid based coils against wild populations of anthropophilic mosquitoes in northern Tanzania. J Glob Infect Dis. 2010; 2(2):116-120.

(15.) Muller G, Junnila A, Butler J, Kravchenko V, Revay E, Weiss, R, Schlein Y. Efficacy of botanical repellents geraniol, linalool, and citronella against mosquitoes. J Vector Ecol. 2009; 34(1):2-8.

(16.) Muller G, Junnila A, Kravchenko V, Revay E, Butler J, Orlova O, Weiss R, Schlein Y. Ability of essential oil candles to repel biting insects in high and low biting pressure environments. J Am Mosq Control Assoc. 2008; 24(1):154-160.

(17.) Lindsay LR, Surgeoner GA, Heal JD, Gallivan GJ. Evaluation of the efficacy of 3% citronella candles and 5% citronella incense for protection against field populations of Aedes mosquitoes. J Am Mosq Control Assoc. 1996; 12(2 Pt 1):293-294.

(18.) Xue R, Qualls W, Smith M, Gaines M, Weaver J, Debboun M. Field evaluation of the Off! Clip-on Mosquito Repellent (metofluthrin) against Aedes albopictus and Aedes taeniorhynchus (Diptera: Culicidae) in northeastern Florida. J Med Entomol. 2012; 49(3):652-655.

(19.) Revay E, Junnila A, Xue R, Kline D, Bernier U, Kravchenko V, Qualls W, Ghattas N, Muller G. Evaluations of commercial products for personal protection against mosquitoes. Acta Trop. 2013; 125(2):226-230.

(20.) Lloyd AM, Farooq M, Diclaro JW, Kline DL, Estep AS. Field evaluation of commercial off-the-shelf spatial repellents against the Asian tiger mosquito, Aedes Albopictus (Skuse), and the potential for use during deployment. US Army Med Dep J. AprilJune 2013:80-86.

(21.) Dame D, Meisch M, Lewis C, Kline D, Clark G. Field evaluation of four spatial repellents devices against Arkansas rice-land mosquitoes. J Am Mosq Control Assoc. 2014; 30(1):31-36.

(22.) Collier B, Perich M, Boquin G, Harrington S, Francis M. 2006. Field evaluation of mosquito control devices in southern Louisiana. J Am Mosq Control Assoc. 2006; 22(3):444-450.

(23.) Bernier U, Clark G, Gurman P, Elman N. The use of microdispensers with spatial repellents for personal protection against mosquito biting. J Med Entomol. 2015; 53(2):470-472.

(24.) Klun J, Kramer M, Debboun M. Four simple stimuli that induce host-seeking and blood-feeding behaviors in two mosquito species, with a clue to DEET's mode of action. J Vector Ecol. 2013; 38(1):143-153.

(25.) Smirnov N. On the estimation of discrepancy between empirical curves of distribution for two independent samples. Bull Moscow Univ Intern Ser (Math). 1939; 2:3-16.

(26.) Bartlett M. Some examples of statistical methods of research in agriculture and applied biology. J R Stat Soc. 1937; 4(suppl 2):137-170.

(27.) Bartlett M. Properties of sufficiency and statistical tests. Proc R Stat Soc A. 1937; 160(901):268-282.

(28.) Kruskal W, Wallis W. Use of ranks in one-criterion analysis of variance. J Am Statist Assoc. 1952; 47:583-621.

(29.) Tukey J. One degree of freedom for non-additivity. Biometrics. 1949; 5:232-242.

(30.) Newman D. The distribution of range in samples from a normal population, expressed in terms of an independent estimate of standard deviation. Biometrika. 1939; 31:20-30.

(31.) Duncan D. Multiple range and multiple F tests. Biometrics. 1955; 11:1-42.

(32.) Scheffe H. A method of judging all contrast in the analysis of variance. Biometrika. 1953; 40:87-104.

(33.) Dethier V, Brown L, Smith C. The designation of chemicals in terms of the responses they elicit from insects. JEcon Entomol. 1960; 53:134-136.

(34.) Gouck H, McGovern TP, Beroza M. Chemicals tested as space repellents against yellow-fever mosquitoes. I. Esters. J Econ Entomol. 1967; 60(6):1587-1590.

(35.) Nolen JA, Bedoukian RH, Maloney RE, Kline DL, inventors; Biosensory Inc, Bedoukian Research Inc, assignees. Method, apparatus and compositions for inhibiting the human scent tracking ability of mosquitoes in environmentally defined three dimensional spaces. US patent 6 362 235. March 26, 2002.

(36.) Ogoma SB, Ngonyani H, Simfukwe ET, Mseka A, Moore J, Killeen GF. Spatial repellency of transfluthrin-treated hessian strips against laboratoryreared Anopheles arabiensis mosquitoes in a semifield tunnel cage. Parasit Vectors. 2012; 5:54.

(37.) Andres M, Lorenz L, Mbeleya E, Moore S. Modified mosquito landing boxes dispensing transfluthrin provide effective protection against Anopheles arabiensis mosquitoes under simulated outdoor conditions in a semi-field system. Malar J. 2015; 14:255.

(38.) Govella N, Ogoma S, Paliga J, Chaki P, Killeen G. 2015. Impregnating hessian strips with the volatile pyrethroid transfluthrin prevents outdoor exposure to vectors of malaria and lymphatic filariasis in urban Dar es Salaam, Tanzania. Parasit Vectors. 8:322.

(39.) Kawada H, Iwasaki T, Tien T, Mai N, Shono Y, Katayama Y, Takagi M. 2006 Field evaluation of spatial repellency of metofluthrin-impregnated latticework plastic strips against Aedes aegypti (L.) and analysis of environmental factors affecting its efficacy in My Tho City, Tien Giang, Vietnam. Am J Trop Med Hyg. 75:1153-1157.

(40.) Ogoma S, Lorenz L, Ngonyani H, et al. An experimental hut study to quantify the effect of DDT and airborne pyrethroids on entomological parameters of malaria transmission. Malar J. 2014; 13:131.

MAJ Lee P. McPhatter, MS, USA

Paula D. Mischler, PhD

Meiling Z. Webb, PhD

Kamal Chauhan, PhD

CPT Erica J. Lindroth, MS, USA

Alec G. Richardson, PhD

Mustapha Debboun, PhD, BCE

AUTHORS

MAJ McPhatter is with the Entomology Branch, Walter Reed Army Institute of Research, Silver Spring, Maryland.

Dr Mischler is with the Entomology Branch, Walter Reed Army Institute of Research, Silver Spring, Maryland.

Dr Webb is with the Invasive Insect Biocontrol & Behavior Laboratory, US Department of Agriculture-Agricultural Research Service, Beltsville, Maryland.

Dr Chauhan is with the Invasive Insect Biocontrol & Behavior Laboratory, US Department of Agriculture-Agricultural Research Service, Beltsville, Maryland.

CPT Lindroth is with the Navy Entomology Center of Excellence, Jacksonville, Florida.

Dr Richardson is with the Navy Entomology Center of Excellence, Jacksonville, Florida.

Dr Debboun is the Director of the Mosquito & Vector Control Division, Harris County Public Health, Houston, Texas.

Caption: Figure 1. The SC Johnson spatial repellents tested in this study: (A) Raid Dual Action Insect Repellent and Home Freshener; (B) Raid Shield.

Caption: Figure 2. (A) Wind tunnel at the Invasive Insect Biocontrol & Behavior Laboratory, USDA-ARS, Beltsville, MD. (B) Mosquito feeding reservoir.

Caption: Figure 3. (A) A semi-field enclosure used in this study. (B) A commercial tent used in this study.

Caption: Figure 4. Treatment effects of both products on host-seeking activity: (A) Mean ([+ or -]SE) mosquito landing counts; (B) Mean ([+ or -]SE) number of mosquito probes; (C) Mean ([+ or -]SE) number of blood-fed mosquitoes. Note: Bars tagged with the same letter are not significantly different.

Caption: Figure 5. Time-series analysis of the Raid Dual Action effects on Ae. aegypti host-seeking activity: (A) Mean mosquito landing counts; (B) Mean number of mosquito probes; (C) Mean number of blood-fed mosquitoes.

Caption: Figure 6. Time-series analysis of the Raid Shield effects on Ae. aegypti host-seeking activity: (A) Mean mosquito landing counts; (B) Mean number of mosquito probes; (C) Mean number of blood-fed mosquitoes.

Caption: Figure 7. Mean ([+ or -] SE) mosquito capture rate per tent for control and treatments. Note: Bars tagged with the same letter are not significantly different.
COPYRIGHT 2017 U.S. Army Medical Department Center & School
No portion of this article can be reproduced without the express written permission from the copyright holder.
Copyright 2017 Gale, Cengage Learning. All rights reserved.

Article Details
Printer friendly Cite/link Email Feedback
Author:McPhatter, Lee P.; Mischler, Paula D.; Webb, Meiling Z.; Chauhan, Kamal; Lindroth, Erica J.; Richard
Publication:U.S. Army Medical Department Journal
Article Type:Report
Date:Jan 1, 2017
Words:5775
Previous Article:The role of birds in Arboviral disease surveillance in Harris County and the City of Houston, Texas.
Next Article:Georgia's collaborative approach to expanding mosquito surveillance in response to Zika virus: a case study.
Topics:

Terms of use | Privacy policy | Copyright © 2021 Farlex, Inc. | Feedback | For webmasters |