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Journal of Exposure Science and Environmental Epidemiology (2007), 1–8r 2007 Nature Publishing Group All rights reserved 1559-0631/07/$30.00 Pesticide loadings of select organophosphate and pyrethroid pesticides inurban public housing RHONA JULIENa, GARY ADAMKIEWICZa, JONATHAN I. LEVYa, DEBORAH BENNETTa,b,MARCIA NISHIOKAc AND JOHN D. SPENGLERa aHarvard School of Public Health, Harvard University, Boston, Massachusetts, USAbUniversity of California, Davis, California, USAcBattelle Memorial Institute, Columbus, Ohio, USA We investigated the magnitude and distribution of pyrethroid and organophosphate pesticide loadings within public housing dwellings in Boston,Massachusetts and compared the results using various sampling methods. We collected dust matrices from living room and kitchen in 42 apartments andanalyzed for eleven pyrethoids (e.g., permethrin and cyfluthrin) and two organophosphates (chlorpyrifos and diazinon) in house dust using GC/MS.
Agreement between sampling methods were evaluated using Spearman correlations and Kappa statistics. Permethrin and chlorpyrifos were detected inkitchen floor wipes in all homes, followed in frequency of detects by diazinon (98%), cypermethrin (90%) and cyfluthrin (71%). At least six pesticideswere detected in kitchen floor wipes in the majority of the homes (range 3–8). Positive and statistically significant correlations among dust matrices wereobserved between kitchen floor wipes and living room vacuum dust, including for diazinon (r ¼ 0.62) and cyfluthrin (r ¼ 0.69). Detection of severalpesticides including banned or restricted use products in some public housing units, underscore the need for alternative pest management strategies thatembrace the safe and judicious use of pest control products.
Journal of Exposure Science and Environmental Epidemiology advance online publication, 9 May 2007; doi:10.1038/sj.jes.7500576 Keywords: chlorpyrifos, house dust, pesticides, public housing, pyrethoids, urban.
given the fact that pest management may have the objectiveof reducing allergen exposures and related asthma develop- In the US, people spend approximately 90% of their time indoors (Gurunathan et al., 1998) and about 74% of While it is known that non-dietary exposure to pesticides households use pesticides (US EPA, 2002), indicating that occurs mostly in the home (Lewis et al., 1994; Whitmore indoor residential exposures may be a significant exposure et al., 1994; Simcox et al., 1995), significant data gaps exist pathway for many individuals. In urban multiunit dwellings, for residential pesticide exposure in urban households, as pesticide usage is prevalent due to problems with pest most studies have focused primarily on agricultural commu- infestation (Landrigan et al., 1999; Whyatt et al., 2002), nities and their exposures to organophosphates, including especially in older, poorly maintained housing stock (Kitch diazinon and chlorpyrifos (Simcox et al., 1995; Loewenherz et al., 2000). In these homes, pesticide usage is sometimes et al., 1997; Gordon et al., 1999; Fenske et al., 2000, 2002).
excessive (Landrigan et al., 1999) and oftentimes includes the More recently, studies have focused on urban settings and use of prohibited or restricted-use pesticides (Adgate et al., have highlighted the widespread use of pesticides indoors (Quackenboss et al., 2000; Pang et al. 2002; Whyatt et al.
Adverse health effects associated with pesticide exposure from residential use include altered fetal growth from Two classes of pesticides, which have been widely used in prenatal exposure (Berkowitz et al., 2004; Whyatt et al., residential settings, including urban multiunit dwellings, are 2004), childhood cancer (Buckley et al., 2000; Daniels et al., organophosphate and pyrethroid pesticides (Landrigan et al., 2001; Flower et al., 2004) and asthma (Salam et al., 2004).
1999). Based on the potential to cause adverse health effects The association with asthma may be particularly concerning, to occupants, especially children, two organophosphates(chlorpyrifos and diazinon) were withdrawn from the indoorresidential market in 2001 and 2002, respectively (US EPA, 1. Address all correspondence to: Dr. R. Julien, 64 Beaumont Street, 2000a, b). Organophosphates exert their toxic effect by inhibiting the enzymatic degradation of the neurotransmitter Tel.: þ 1 617 918-1782. Fax: þ 1 617 918-0782.
acetylcholine; at extremely high doses, inhibition of acetyl- E-mail: [email protected] 4 December 2006; accepted 4 February 2007 choline esterase results in the continued firing of the neuron and subsequent paralysis or death of the affected organism participants can be found elsewhere (Clougherty et al., With the withdrawal of the organophosphates, pyrethroids are being used increasingly to control pests indoors (Adgate et al., 2000). Synthetic pyrethroids have insecticidal proper- Home visits were scheduled for families who provided written ties similar to the botanical pesticides known as pyrethrins consent for their participation in the IPM program. During (i.e., neurotoxin with rapid paralysis or ‘‘quick knock-down these visits, environmental measurements as well as health effect’’ of target pest). However, pyrethroids are more and quality of life information related to asthma were persistent in the environment than the naturally occurring obtained both before and after IPM interventions. During pyrethrins and are therefore used indoors as well as in the first visit, vacuum dust and floor wipe samples were agricultural applications (Todd et al., 2003). The toxic mode collected to provide baseline information about the pre- of action for pyrethroids is the disruption of the conductance valence and surface loadings of target pesticides. Environ- of neuronal impulses, which results in the generation of mental measurements were recorded between July 2002 and multiple action potentials that leads to tremors and August 2003 from homes in all three developments.
incoordination. These cellular level effects can lead to various Additional information on household characteristics such as ethnicity and pesticide use were collected at the time of In addition to the limited exposure data on pyrethroids, enrollment. Data discussed in this paper will only focus on there is not a single standardized or consistent approach for the measurements taken before the IPM interventions, to analysis or comparison among pesticide exposure studies establish baseline pesticide loadings.
(Quandt et al., 2004), as previous studies have focused on Floor wipes were taken on vinyl floor surfaces in both various matrices including blood, urine, air and/or vacuum living room and kitchen from standardized locations.
dust or floor wipes to quantify exposures (Lioy et al., 2002).
Kitchen floor wipes were taken adjacent to the stove and Therefore, the aim of the current study was to quantify the living room floor wipes were taken adjacent to the sofa. If distribution of common pesticides (e.g., select pyrethroids the latter location was not feasible (e.g., due to clutter), an and diazinon and chlorpyrifos) within the homes of public alternate area adjacent to the linen closet in the hallway was housing residents in Boston and compare pesticide loadings designated. For the floor wipe samples, we used a sampling from various collection media. We used house dust as our protocol that was adapted from the National Human target medium, since our selected pesticides are semi-volatile Exposure Assessment Survey in Arizona (NHEXAS-AZ) (organophosphates) or nonvolatile (pyrethroids), and are (Gordon et al., 1999), which involved wiping a one-square- foot area (0.0929 m2) with a three-inch square (58 cm2; (Berger-preie et al., 1997). Dust samples were collected from Johnson and Johnsont) sterile gauze wetted with 5 ml 99% the kitchen, where pesticides are most frequently applied due isopropanol. Once collected, each wipe sample was placed in to cockroach infestation (Brenner et al., 2003), and from the a labeled 60 ml amber glass jar and placed in a cooler.
living room, where families tend to spend significant time Vacuum dust samples were collected only in the living while indoors. In addition, we examined the agreement room due to anticipated low dust loadings on bare kitchen between floor wipes and vacuum dust sampling methods floors (Nishioka et al., 1999). Living room samples were when classifying pesticide exposure within these homes.
collected from all accessible surfaces including sofas andcarpets since these fabric surfaces are primary reservoirs fordust borne pesticides (Lewis et al., 1994) and can serve as asource of continued exposure to occupants (Fenske et al., 1991; Simcox et al., 1995; Gurunathan et al., 1998;Landrigan et al., 1999). Vacuum dust was obtained using a The current study is a component of the Healthy Public sampling protocol that was adapted from the epidemiologic Housing Initiative (HPHI), a longitudinal intervention study study conducted in Cape Cod, Massachusetts that looked targeting apartments of pediatric asthmatics (between 4 and at the associations between environmental exposures and 17 years of age) living in urban housing. Sixty households breast cancer (Rudel et al., 2001). The sampling apparatus were recruited from three public housing developments in consisted of a 9 A Eureka Mighty-mitet vacuum cleaner, Boston, Massachusetts. Of the households who were adjusted to collect dust in a 19 Â 90 mm cellulose extraction recruited for the intervention study, 43 households partici- thimble which was placed into an extended arm. This arm pated in the Integrated Pest Management (IPM) program, was connected at one end to the vacuum cleaner and capped which was one of the primary environmental interventions at the other end with a crevice tool. The samples were tested. Environmental measurements for the current study collected by slowly moving the crevice tool using back and were obtained from 42 of these households. Additional forth motions over the designated areas for a total sampling information on HPHI and characteristics of the study time of five minutes. Once samples were collected, the Journal of Exposure Science and Environmental Epidemiology (2007), 1–8 cellulose thimbles were removed from the extended arm using grammed to 2801C. Two diagnostic ions were monitored gloves and placed into a labeled zip loct bag and stored in a for identification of each analyte.
cooler. Both vacuum dust and floor wipe samples were laterstored in a freezer at À221C until shipment for analysis.
analyzed with each sample set and were used to assess method performance. For the 78 dust analyses, the QA/QC To determine pesticide concentrations, each sample was samples included eight solvent method blanks, three solvent analyzed for two organophosphates (chlorpyrifos and method spikes (100 ng/analyte), three reference dust samples, diazinon) and eleven pyrethroids [allethrin (cis- and trans- six fortified reference dust samples and five duplicate isomers) coelute, bifenthrin, isomers of cyfluthrin (three analyses. Low-level dust fortification was 50 ng/analyte, chromatographically resolved isomers), cyhalothrin, cyper- except 62.5 ng/isomer for cyfluthrin and cypermethrin, and methrin (three resolved isomers), deltamethrin, esfenvalerate, 250 ng/analyte for esfenvalerate and deltamethrin; high-level permethrin (cis- and trans- isomers), resmethrin, sumithrin and tetramethrin]. Target pesticides were selected because of The average solvent spike recovery was 86%, with a range potential adverse health effects, persistence indoors and/or of 82712 to 93713% for chlorpyrifos and sumithrin, respectively. The average low-level spike recovery was 93%,with a range of 5677 to 120710% for resmethrin andcyhalothrin, respectively. The average high-level spike recovery was 107%, with a range of 84723–132748% sample, up to 0.50 g, was weighed and fortified with 250 ng for diazinon and tetramethrin, respectively. There was a of the compound class-specific surrogate recovery standards consistent interference to allethrin in the method that prevented detection and quantification of this analyte in dust C6-labelled mix of cis/trans-permethrin for pyrethroids.
sample extracts. For the 31 pairs of analytes detected in the The dust was extracted using ultrasonication in 12 ml of 1:1 duplicate samples, the average relative percent difference for hexane:acetone. After centrifugation, 10 ml of the extract was concentration was 25% (0–154%). The SRS recoveries in the removed, concentrated and solvent exchanged into hexane. A dust samples showed very good method performance on a C18 solid phase extraction (SPE) cartridge (1000 mg; sample-by-sample basis: recovery of 93710% for fenchlor- dichloromethane (DCM), 15% diethyl ether in hexane and hexane. The extract was added, the sample was eluted in The QA/QC samples for the 192 wipe samples included 15 reverse order with these solvents and the resulting eluant was field matrix blanks and 15 matrix spikes, with the latter concentrated to a final 1 ml volume. Dibromobiphenyl was fortified with 150 ng/analyte (with scaling as described above added as the internal standard for quantification. A nine- for cyfluthrin, cypermethrin, esfenvalerate, deltamethrin) point calibration curve, spanning the range of 0–750 ng/ml before extraction. Average recovery in the spiked wipes was for analytes and 0–300 ng/ml for SRSs, was analyzed 98%, with a range of 8679 to 112713% for cypermethrin concurrently with each sample set. Linear regression isomers and chlorpyrifos, respectively. The SRS recoveries in analysis was used to establish the calibration curve for each the wipe samples showed good method performance on a analyte. Samples with analytes that exceeded the calibration sample-by-sample basis: recovery of 78715% for fenchlor- curve range by more than 15% were diluted, respiked with internal standard and reanalyzed. After quantification, analyte concentrations were corrected by the recovery of the matched compound class SRS in that sample.
The normality of each pesticide distribution was determinedusing the Shapiro–Wilks test. Where the data were skewed, we used non-parametric tests for analyses. In order to ensure with 100 ng of fenchlorphos and 13C6-trans-permethrin, unbiased estimates of the correlations, samples with con- and extracted using accelerated solvent extraction (ASE) centrations below the limit of detection (LOD) were assigned technology (ASE 200; Dionex Corp) in an 11 ml cell using random values between zero and the LOD according to an DCM at 2000 psi and 1001C through two cycles. The extract was concentrated, solvent exchanged, cleaned up and Because there is no ‘‘gold standard’’ for sampling indoor analyzed as described above for the dust extracts.
concentrations of dust-borne pesticides, we examined the Extracts were analyzed using GC/MS in the multiple ion agreement between two sampling methods conducted in this detection mode (6890 GC interfaced to a 5973 MSD; study, vacuum dust and floor wipe sampling. We first Agilent) using a DB-1701 GC column (30 m; 0.25 mm id; evaluated the relationships within matrices (kitchen vs. living 0.15 mm film thickness) with the GC temperature pro- room floor wipes) and between matrices (living room floor Journal of Exposure Science and Environmental Epidemiology (2007), 1–8 wipes vs. vacuum dust) using Spearman rank correlations.
correlations among specific isomers for each compound. For For floor wipes, we also tested whether concentrations kitchen floor wipes, permethrin and chlorpyrifos were significantly differed between the kitchen and living room, detected in every home. Diazinon and cypermethrin were detected at fairly high frequencies (X90%). Cyfluthrin was We categorized measured concentrations as dichotomous detected in 71% of homes. For living room floor wipes, variables and evaluated the agreement between the vacuum permethrin and chlorpyrifos were also detected at fairly dust method and the kitchen floor wipe method. As there are high frequencies, followed by diazinon, which was detected no well-defined thresholds for health effects for the target in 80% of the homes. For vacuum dust, similarly high pesticides, we considered three alternatives: above/below the detection frequencies were also observed, with cis- and LOD, the 50th percentile and the 75th percentile. Agreement trans-permethrin detected in every home. In addition to was evaluated using the Kappa statistic, which captures the detection frequency, the data in Table 2i indicate that level of agreement between these two alternate measurement most analytes have pesticide loadings that vary across approaches (where 1 ¼ perfect agreement, 0 ¼ no agreement several orders of magnitude. This variation in pesticide above that expected by chance, À1 ¼ perfect disagreement).
distribution is also illustrated in Figure 1, which presents All statistical analyses were performed using SAS Version 9 the cumulative frequency distribution of the five most prevalent analytes in kitchen floor wipes. The distributionof cyfluthrin, which is a restricted-use pesticide in certainformulations such as 25% emulsified concentrate (US EPA,2003), is somewhat broader and more skewed than the distribution for the other pyrethroids. At the upper end ofthe distribution (490th percentile), cyfluthrin loadings were Table 1 provides study demographics and information on over 2 orders of magnitude higher than the loadings at the participants’ choice of pest control methods, including traps (41%), non-volatile formulations (gels (25%)) and volatile One way to examine the degree to which analytes occur formulations (sprays (34%), and smoke bombs (27%)).
simultaneously with one another is to consider the number of Although 84% of the families reported pesticide use within analytes detected in each home. All homes had at least two the past year, 92% indicated an interest in using pest control pesticides present in vacuum dust, and 17 homes (49%) had remedies that did not rely on pesticides.
five or more present. Similarly, in examining kitchen floor Table 2i reports summary statistics for kitchen and living wipes, all homes had at least three pesticides present and 27 room floor wipes and vacuum dust in the baseline pre- homes (64%) had six or more present. For the living room intervention samples. Target analytes with isomers (e.g., floor wipes, 17 homes (56%) had five or more pesticides permethrin, cypermethrin and cyfluthrin) are presented as the sum for each compound based on high Spearman rank We also considered the agreement between sampling sites and between sampling methods (Table 2ii). Spearman rankcorrelations were positive and statistically significant for the Table 1. Selected household characteristics of IPM participants majority of prevalent analytes (diazinon, chlorpyrifos, permethrin and cyfluthrin), ranging from 0.38 to 0.64between living room and kitchen floor wipes, from 0.41 to 0.69 between kitchen floor wipes and living room vacuum dust samples and from 0.44 to 0.61 between living room floor Based on the results for the Wilcoxon rank-sum test (not shown here), with the exception of cypermethrin, there were no statistically significant differences in pesticide loadings between living room and kitchen floor wipes for the prevalent analytes. Thus, given the similarity between these two matrices for the prevalent analytes, only the results from the kitchen floor wipes will be represented To test the agreement between the two forms of measurements (floor wipes and vacuum dust) from the Self-report cockroach infestation as severe perspective of categorization as high/low exposure based on specific exposure thresholds (Table 3), the magnitude of Total percentage will exceed 100% because families used multiple pesticide types at any given time in the home.
Kappa coefficients was considered for the following exposure Journal of Exposure Science and Environmental Epidemiology (2007), 1–8 Table 2i. Summary statistics for pesticide prevalence (% above limit of detection) and pesticide loadings in kitchen and living room floor wipesamples (mg/m2) and vacuum dust (mg/g) Kitchen floor wipes (N ¼ 42)Chlorpyrifos thresholds, LOD, the median percentile and the 75th percentile. Kappa coefficients were positive and strong(significantly 40) for cyfluthrin at all three thresholds The findings of the high prevalence of pesticides, for example, (0.33, 0.47 and 0.30), permethrin (0.59 and 0.51) and permethrin and chlorpyrifos, in these urban housing units diazinon (0.53 and 0.51) at the median and 75th percentile, are consistent with other studies that obtained information respectively, and for chlorpyrifos (0.35), at the median on pesticide prevalence via surveys and questionnaires percentile. We were unable to compute Kappa coefficients for (Landrigan et al., 1999; Adgate et al., 2000; Kinney et al., the two most ubiquitous target pesticides (permethrin and chlorpyrifos) due to 100% detection in at least one medium While sampling occurred after diazinon and chlorpyrifos (Sim and Wright 2005) and in general, the high detection were removed from the residential market, the measured rates for the analytes in question limit the statistical power of concentrations in house dust can most likely be attributed to the persistence of these pesticides indoors. However, the Journal of Exposure Science and Environmental Epidemiology (2007), 1–8 Table 3. Test of equivalence between kitchen floor wipe and vacuum dust methods (N ¼ 34), considering multiple exposed/unexposedthresholds Values represent Kappa statistics and standard errors.
concentrations above the 90th percentile exceeded the median concentrations by several orders of magnitude, which may indicate that a subset of residents is applying the productincorrectly.
Since few studies have measured concentrations of these analytes in house dust in urban settings, there are limited data to make a determination of whether residents in these public Figure 1. Cumulative frequencies of five target pesticides detected in housing developments are disproportionately exposed to pesticides and may be at risk of adverse health effects. Astudy which looked at exposures to several pesticides Table 2ii. Spearman correlations between sampling matrices and including chlorpyrifos, diazinon and cis- and trans-perme- betwen sampling locations for the most prevalent pesticides (LR ¼ thrin in predominantly single-family homes measured geo- metric mean concentrations of approximately 113 ng/g forchlorpyrifos, 25 ng/g for diazinon, 337 ng/g for cis-perme- thrin and 517 ng/g for trans-permethrin (Colt et al., 2004).
These measurements were similar to our median concentra- tions in vacuum dust, although it should be noted that the limit of detection in that particular study was an order of magnitude higher than the limit of detection in our measurements were also observed in the floor dust of a daycare setting with preschoolers, with observed median *Statistically significant at the 0.05 level.
chlorpyrifos concentrations of 135 ng/g (Morgan et al., **Statistically significant at the 0.01 level.
2005). However, these measurements were taken before thephase-out of organophosphates. We are also unaware of presence of cyfluthrin was a cause for concern for several other studies, which measured levels of numerous analytes, reasons. It is the active ingredient found primarily in a especially pyrethroids, in low-income multiunit dwellings, product known as Tempo. Based on information obtained which underscores the importance and uniqueness of our from the Material Safety Data Sheet (MSDS) prepared by findings. And given the known neurological pathways the manufacturer, Bayer (e.g., MSDS #R000023651 and affected by pyrethroids, the levels we have observed in this MSDS #29752), this compound is available in a variety of study suggest that the current substitution of organophos- formulations (e.g., wettable powders and suspension con- phates with these chemicals may incur their own health risks centrate) and in certain formulations is licensed for pest management professionals and/or commercial use only.
In terms of our methodological conclusions, there were Moreover, field staff were informed that Tempo was being some positive and statistically significant correlations between applied by residents in its concentrated form and was not the vacuum dust and floor wipe samples. However, based on mixed with water as required per labeling instructions. This our findings of a modest agreement between these two misuse of Tempo would result in substantially higher matrices for some analytes, we are unable to conclude that exposures than intended and should be investigated in further floor wipe samples can serve as a universal proxy for vacuum detail. In homes where cyfluthrin was detected, the dust samples. In instances where there was a strong Journal of Exposure Science and Environmental Epidemiology (2007), 1–8 agreement between the analytes, for example, permethrin and To the best of our knowledge, this study is the first to diazinon, this may be due in part to the liquid formulation of report on concentrations of 10 pyrethroids and two these pesticides (e.g., smoke bombs and aerosol sprays) used organophosphates in an urban setting, and more specifically, in the home. Applications such as smoke bombs intentionally in a multiunit residential setting. Our results show a wide distribute the pesticide throughout the home. The aerosol range of pesticide levels with certain pyrethroids (permethrin) spray is a more targeted application; however, there is and organophosphates (chlorpyrifos) detected in every home, potential for considerable overspray. Due to relatively high and restricted-use pesticides (cyfluthrin) detected in a vapor pressures as well as movement of dust, many pesticides majority of homes. In addition, the significant correlation migrate from treated areas to non-target surfaces (Guru- between vacuum and floor wipe sampling methods for certain nathan et al., 1998; Lioy et al., 2002; Bennett and Furtaw ubiquitous analytes indicates that kitchen floor wipe samples 2004). The frequency of pesticide use and the close proximity could potentially serve as a less expensive and non-intrusive of rooms in our study homes, which is quite typical in inner- proxy, which can be especially helpful in a challenging city public housing, will undoubtedly facilitate this process.
On the other hand, if Tempo (with cyfluthrin as its active imply that interventions may be warranted in these develop- ingredient) is applied in powdered form in the kitchen, ments, with efficient and practical methods needed to barring any mechanical means of resuspension such as preferentially select homes for possible interventions, given the substantial variability in concentrations across units.
that significant deposition onto non-target surfaces will Equally important are the policy implications of our findings, occur. For cypermethrin, we do not have information on which suggest that efforts should be made to promote and whether the product formulation that was used in these institutionalize viable and safer pest control alternatives in homes came in liquid formulation (emulsifiable concentrates) or dry formulation (e.g., wettable powder and dust granules),making it difficult to determine the precise reason for non-agreement.
There are some potential limitations that influence the interpretation of our findings. In exposure studies where Funding was provided by US Department of Housing and dermal exposure is the potential pathway under considera- Urban Development (grant# MALHH0077-00), W.K.
tion, dislodgeable pesticides (i.e., pesticide residue on a Kellogg Foundation, Boston Foundation and Jessie B.
surface that is removed by the skin) are regarded as the most Cox Charitable Trust Melvin W. First Scholarship and appropriate measurement for human exposure (Fenske et al., Akira Yamaguchi Endowment. Special thanks to the families 1991). Our choice of isopropanol as the wetting agent to who participated in the study, as well as the community collect floor wipe samples likely improved our collection partners for their cooperation and commitment to the success efficiency, but may also result in removal of these residues from both the surface and sub-surface, impairing compar-ability with other exposure measures.
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