Background
In the United States alone, 82 million households used insecticides in 2012 and $2.65 billion were spent in the “home and garden sector”, representing 50% of all expenditures on insecticides [
1]. One of the most prominent pests targeted with insecticides is the German cockroach (
Blattella germanica). There are many reasons for eliminating indoor cockroach infestations, but primary among them is the central role that cockroaches play as etiological agents in allergic disease and asthma [
2]. Allergens produced by German cockroaches can trigger allergies and asthma in sensitized individuals, and the National Cooperative Inner-City Asthma Study found that asthma morbidity was highest in children that experienced both a positive skin-test response and high exposure to cockroach allergens [
3]. The National Survey of Lead and Allergens in Housing, a nationwide survey conducted by the U.S. National Institute of Environmental Health Sciences (NIEHS) and the U.S. Department for Housing and Urban Development (HUD), found detectable levels of the cockroach allergen Bla g 1 in 63% of homes [
4], with higher concentrations in high-rise apartments, urban settings, older homes, and low-income households [
4,
5]. Moreover, because cockroaches move freely between waste and food, they can acquire, carry, and disseminate pathogenic bacteria, helminths, fungi, protozoa, and viruses in their digestive system [
6]. Thus, the persistence of cockroaches in homes poses significant health risks to humans.
Indoor cockroach infestations are often targeted with residual liquid or aerosol sprays that contain broad-spectrum insecticides, most commonly pyrethroids [
7]. However, high levels of resistance to pyrethroids and their repellency to cockroaches severely compromise the efficacy of most residual sprays [
7]. Moreover, these products can deposit considerable insecticide residues throughout the home [
8]. Environmental data collected by the U.S. Environmental Protection Agency (EPA) and HUD on a stratified, nationally representative sample of 1131 residences found extensive pesticide residues in homes [
9]. Despite the continual use of residual sprays, insecticides formulated as baits offer more effective and safer alternatives in cockroach interventions [
10,
11].
Because professional pest control interventions can be prohibitively expensive, consumer-based pesticide products are commonly used in do-it-yourself (DIY) pest control, especially in low-income homes. Total-release foggers (TRFs) are often deployed as spatial insecticides, designed to fill a room with fine particles of aerosolized insecticide. They are considered by consumers to be highly effective against all pests (as the common name “bug bomb” implies). TRFs generally contain toxicity category III (based on acute toxicity) active ingredients (pyrethrins and pyrethroids), various synergists meant to inhibit microsomal detoxification by insects, and aerosol propellants that are often flammable. These products are responsible for substantial acute and chronic health effects, explosions and fires, and persistent environmental contamination indoors. These effects were first characterized by a 2008 US Centers for Disease Control and Prevention (CDC) report that summarized 466 fogger exposures in eight States over a five-year period, documenting respiratory, gastrointestinal, neurological, ocular, dermatologic, and cardiovascular adverse symptoms [
12]. A similar summary from Texas, USA documented 2855 fogger exposures over an 8-year period [
13]. Despite these reports, the magnitude of health, economic, and environmental damage is poorly documented, and likely underestimated. Indeed, a follow-up report from the New York City Department of Health and Mental Hygiene, USA [
14] stated that the 2008 CDC report understated reported exposures. This follow-up report also showed that health effects are much more likely to occur from exposures to TRFs than from other pesticide formulations, and moderate or major health effects were more than twice as likely to occur from TRF exposures as from all pesticides, and seven times as likely as from rodenticides. While many of the fogger-associated illnesses and injuries result from inadvertent exposures during their deployment (leaving the premises too late, re-entering too soon, discharging too many foggers, failing to notify others), studies suggest that TRFs deposit large amounts of insecticides in areas easily accessible to humans, especially small children [
8,
15]. The residual pyrethroids on household surfaces can exacerbate a number of chronic health conditions [
16], although the health effects from chronic exposure are still under debate.
TRF products appear to contribute significantly to the disproportional pesticide exposure already documented for those living in affordable housing [
17,
18]. The report from New York City’s Department of Health and Mental Hygiene [
14] contends that “the health risks associated with the use of foggers are not justified given their likely poor efficacy”. Recently, Jones and Bryant [
19] showed that over-the-counter TRFs were indeed ineffective at controlling bed bug infestations. Surprisingly however, there are no reports on the relative efficacy of modern TRF products against their primary target, the German cockroach. Therefore, we designed a study to assess the efficacy and exposure risks of TRFs in cockroach-infested homes.
Methods
Ethics statement
The North Carolina State University Institutional Review Board (IRB) approved this study (#1459). Before participation, adult participants (> 21 yrs. old) provided written informed consent. Demographic data on participants were not gathered in this study, as we were interested in a cockroach intervention and the environmental outcomes in cockroach-infested residences, independent of the demography of the residents.
Recruitment of participants
Apartments in five low-income communities within the city of Raleigh NC, U.S.A., were visited and residents were queried regarding cockroach infestations. Apartments were in multi-unit low-rise buildings, duplexes, and row homes. Residents were first informed of the purpose of the study, provided informed consent, then asked if (a) they had seen any live cockroaches, and (b) if they were interested in participating in the study. If the resident reported seeing cockroaches and agreed to participate, the home was visually inspected for the presence of cockroaches. If the home was expected to qualify based on sufficient numbers of live German cockroaches or evidence of cockroaches, the home was recruited into the study. Official enrollment followed standard cockroach population quantification, implemented through trapping (see “Intervention effectiveness – Assessment of relative cockroach population size” below).
Interventions
Four different TRF products were used, representing several insecticide active ingredients and manufacturers: Hot Shot No-Mess Fogger2 with Odor Neutralizer (Hot Shot 2; 85 g, 0.333% tetramethrin, 0.834% permethrin, 1.667% piperonyl butoxide; Spectrum Group-United Industries, St. Louis, MO, U.S.A.), Hot Shot No-Mess Fogger3 with Odor Neutralizer (Hot Shot 3; 170 g, 0.200% tetramethrin, 0.860% cypermethrin, 0.500% piperonyl butoxide; Spectrum Group-United Industries), Raid Max Concentrated Deep Reach Fogger (Raid Deep; 60 g, 1.716% cypermethrin; SC Johnson, Racine, WI, U.S.A.), and Raid Fumigator (10 g, 12.600% permethrin; SC Johnson). Five replicate homes were treated with each TRF product, one home in each of five apartment complexes (20 TRF-treated homes).
Each TRF was discharged in the kitchen following the product label instructions and EPA precautions (
https://www.epa.gov/safepestcontrol/safety-precautions-total-release-foggers; last accessed April 15, 2017). Briefly, all residents vacated the apartments for 4–6 h, windows and doors were closed, air conditioning and gas stove pilot lights were turned off, cabinet doors were opened and contents as well as immovable kitchen appliances were covered with newspapers, and aquaria were moved out of the kitchen. Four to six hours later, the apartment was ventilated, newspapers discarded, dishes rinsed, and residents allowed to re-enter.
Running in parallel, 10 additional apartments were treated with only gel baits. Five homes, one in each apartment complex, were treated with a consumer bait, Combat Gel Bait (0.010% fipronil; Combat Insect Control Systems-The Dial Corporation, Scottsdale, AZ, U.S.A.), and another set of five homes, one in each apartment complex, received a professional bait, Maxforce Gel Bait (0.010% fipronil; Bayer Environmental Science, Robinson Township, PA, U.S.A.). Bait was dispensed as needed at each of three visits (baseline, two weeks, one month). At the conclusion of the study, all TRF-treated apartments were provided thorough gel bait interventions.
Intervention effectiveness – Assessment of relative cockroach population size
At baseline, and subsequently two and four weeks after treatment, six glue-board sticky-traps (Victor Roach Pheromone Trap, Woodstream Corporation, Lititz, PA, U.S.A.) were placed in kitchen locations where cockroaches commonly aggregate. The traps were collected the following day and enumerated in the lab. Changes in each cockroach population (apartment) were assessed relative to the baseline trap catch. Homes were enrolled in the study if at least 50 cockroaches were trapped at baseline.
TRF efficacy – Caged sentinel cockroaches
After enrollment, cockroaches were collected from the kitchen using a modified Eureka Mighty-Mite 7.0-A vacuum cleaner (Eureka Company, Charlotte, NC, U.S.A.). Live cockroaches were collected into a mesh-lined plastic tube attached to the distal end of the vacuum’s extension tube. Apartment-collected male cockroaches were used as caged sentinels for determining product efficacy in the same apartment where they were collected. Prior to discharging the TRF, 40 laboratory raised, insecticide-susceptible adult male cockroaches and 40 home-specific apartment-collected males were placed into the home as sentinels. Twenty cockroaches from both the laboratory population and the apartment-specific population were placed in two uncovered cages on the floor 1.0 m away from the TRF (referred to as “floor”), and the other 20 cockroaches from each population were placed in two uncovered cages in an upper cabinet (lowest shelf, referred to as “upper cabinet”). The inside walls of the cages were coated with petroleum jelly to prevent cockroaches from escaping. Four to six hours after the TRF was discharged, and it was safe to re-enter the apartment, the sentinel cockroaches were collected, returned to the laboratory, transferred to a clean cage, and assessed for mortality 24 h later.
Pesticide residue analysis
Kitchens were sampled for insecticide residues at three time points during the study: before TRF use (baseline), immediately (4–6 h) after TRF discharge, and one month later. Areas sampled included the floor at both 0.5 m and 1.0 m from the site of the TRF, the nearest countertop to the TRF (~ 0.9 m high), the inside (base) of an upper level cabinet (~ 1.4 m), and the nearest wall to the TRF at a height of 0.9 m (representing the height of a child). The same areas of the kitchen, but not the same spots, were sampled at each subsequent visit. Samples were collected by wiping an area of 100 cm2 with a cotton swab wetted with isopropyl alcohol for 1 min. Each swab sample was placed into a 20 ml glass vial, immediately returned to the laboratory and stored at − 30 °C until extraction.
Swab samples were analyzed for the specific active ingredients used in the TRF products, which included permethrin (sum of cis- and trans- isomers), cypermethrin (sum of all isomers), tetramethrin (sum of all isomers), and PBO (pyrethroid synergist). Additionally, swab samples were analyzed for fipronil residues (active ingredient from baits used). Each sample was fortified with 500 ng of the surrogate recovery standard (SRS) 13C6-trans-permethrin (Cambridge Isotope Laboratories Inc., Tewksbury, MA, U.S.A.). Samples were extracted and sonicated twice with ethyl acetate. Solvent volume was then reduced, and samples were cleaned using a 3 ml prefabricated solid phase extraction (SPE) column containing 500 mg of silica gel (Supelclean LC-Si SPE Tube, Sigma Aldrich, St. Louis, MO, U.S.A.). The SPE column was conditioned with 5 ml of hexane, the sample was loaded onto the column and eluted with 5 ml of 50% ether in hexane. Each eluted sample was spiked with 500 ng of the internal standard (IS) 4,4′-dibromobiphenyl (DBBP, AccuStandard Inc., New Haven, CT, U.S.A.), evaporated to near dryness under nitrogen, resuspended in 1 ml of hexane, and stored at − 30 °C until analysis.
Samples were analyzed using an Agilent Technologies 6890 GC coupled to an Agilent 5975 mass spectrometer (GC-MS). The GC was equipped with a 30 m × 0.25 mm × 0.25 μm (5%-phenyl)-methylpolysiloxane Agilent J&W HP-5 ms column preceded by a 3 m deactivated guard column. The temperature program was: 100 °C for 1 min, then 5 °C/min to 225 °C, then 2 °C/min to 256 °C, then 10 °C/min to 320 °C where it was held for 10 min. Mass spectrometry conditions were: transfer line at 280 °C, ionization source at 230 °C, and quadrupole at 150 °C. One quantification ion was used for each pesticide (Table
1). Ten calibration curve solutions ranging from 0.1 μg/ml to 100 μg/ml for all TRF insecticides (Sigma-Aldrich) were used to generate calibration curves via log-transformed linear regression. Extracted samples were corrected for both the SRS and IS and quantified using the calibration curve. Each calibration curve solution was run a minimum of three times, interspersed evenly among field-collected samples. If any compound exceeded the upper point in the calibration curve by more than 15%, the sample was diluted and re-analyzed. Method detection limits (MDLs) were determined using the guidelines from 40 CFR Part 136, Appendix B.
Table 1
Retention times, quantification ions, and qualification ions for insecticide residue analyses by GC-MS.
Fipronil | 23.00 | 367 | 213 |
Piperonyl butoxide | 28.90 | 176 | 149 |
Tetramethrin | 29.95–30.30 | 164 | 123 |
Permethrin (cis- and trans-) | 35.35–35.80 | 183 | 163 |
Cypermethrin | 38.50–39.40 | 163 | 181 |
Data analyses
Two-way repeated measures ANOVA was used to compare changes in cockroach population levels over time (baseline, two weeks, four weeks) among different treatments (TRFs and baits). Due to interactive effects, repeated measures ANOVA was used to evaluate changes in cockroach population within each treatment, with means at different times compared using the Tukey-Kramer multiple comparison test.
Three-way ANOVA was used to compare sentinel cockroach percent mortality (arcsine square root transformed) among TRF products, population (laboratory-raised or apartment-collected), and location (floor or upper cabinet).
The effects of each TRF treatment on insecticide residues were evaluated using repeated measures ANOVA (within each treatment) on log-transformed values. Treatments were defined by the insecticide(s) in each TRF product and swab locations quantified over time, with means at 4–6 h and one month after the TRF intervention compared to the baseline mean using Dunnett’s test. Prior to log-transformation, all values had the respective insecticide MDL added to them. Comparisons were also made among swab locations for each TRF treatment 4–6 h after discharge using ANOVA. Insecticide residues were evaluated only for the Combat gel bait group, and not the Maxforce bait group, at baseline and one month. Additionally, three apartments were removed from the study for either failing to complete the study or not following the approved protocol. Also, some samples have missing values due to problems with sample collection or sample analysis (reflected by sample size).
All statistical analyses were performed using SAS 9.4 (SAS Institute, Cary, NC, U.S.A.).
Acknowledgements
We thank residents of several affordable housing communities in Raleigh, North Carolina, U.S.A., who participated in this study; this study would not have been possible without their support and partnership. We also acknowledge Michelle McCombs (RTI International, NC, U.S.A.) for guidance in the initial steps of GC-MS analysis and Woodstream Corporation for donating sticky traps.