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Assessing transferable residues from intermittent exposure to flea control collars containing the organophosphate insecticide chlorpyrifos

Abstract

Children can be exposed to pesticides from numerous residential sources such as carpet, house dust, toys and clothing from treated homes, and flea control remedies on pets. In the present studies, 48 pet dogs (24 in each of two studies) of different breeds and weights were treated with over-the-counter flea collars containing chlorpyrifos (CP), an organophosphorus insecticide. Transferable insecticide residues were quantified on cotton gloves used to rub the dogs for 5 min and on cotton tee shirts worn by a child (Study 2 only). First morning urine samples were also obtained from adults and children in both studies for metabolite (3,5,6-trichloro-2-pyridinol) quantification. Blood samples were obtained from treated dogs in Study 1 and plasma cholinesterase (ChE) activity was monitored. Transferable residues on gloves for all compounds were highest near the neck of the dogs and were lowest in areas most distant from the neck. Rubbing samples (over the collar) at two weeks post-collar application contained 447±57 μg CP/glove while samples from the fur of the back contained 8±2 μg CP/glove. In Study 2, cotton tee shirts worn by children at 15 days post-collar application for 4 h showed CP levels of 134±66 ng/g shirt. There were significant differences between adults and children in the levels of urinary metabolites with children generally having higher urinary levels of metabolites than adults (grand mean±SE; 11.6±1.1 and 7.9±0.74 ng/mg creatinine for children and adults, respectively, compared to 9.4±0.8 and 6.9±0.5 ng/mg creatinine before collar placement). Therefore, there was little evidence that the use of this flea collar contributed to enhanced CP exposure of either children or adults.

Introduction

Pesticides have been used extensively in and around the home, and it has been estimated that as many as 80% of US households apply pesticides at least once each year (NRC, 1993; Hore et al., 2005). The exposure of children to pesticides has received increased attention since the publication of the National Research Council's Pesticides in the Diet of Infants and Children (1993). The increased awareness generated by this report led to the passage of the Food Quality Protection Act of 1996, which calls for a “reasonable certainty of no harm” for sensitive populations (e.g., infants, children and the elderly) when pesticide residue standards are being set by the US Environmental Protection Agency.

Research has shown that children can be exposed to pesticides from numerous sources such as carpet, clothing, house dust and toys in treated houses (Fenske et al., 1990; Castorina et al., 2003; Colt et al., 2003; Rohrer et al., 2003; Hore et al., 2005). Pesticide exposures have also been documented from children who played outside in treated lawns and/or gardens (Woody, 1984; Morgan et al., 2001). However, pesticide exposure from parasite control product residues on pet animals has been largely overlooked.

The organophosphorus insecticide chlorpyrifos (CP) (O,O-diethyl-O-[3,5,6-trichloro-2-pyridyl]-phosphorothioate) is a broad-spectrum, chlorinated insecticide that was first registered in 1965. In the 1990s, it was the most widely used insecticide with about 11 million pounds used annually in non-agricultural settings (residential, commercial and veterinary/medical) (USEPA, 1999) for the control of termites, ants, roaches and arachnid pests in and around the home. It was also used in commercial, over-the-counter collars for flea and tick control on family pets. Although it is no longer used in over-the-counter flea control products after some of its uses were recently eliminated, two other organophosphates, tetrachlorvinphos and DDVP (dichlorvos), are still used in flea control products (collars and shampoos). Therefore, the quantification of potential exposures resulting from these flea control products is necessary for pesticide cumulative risk assessments. The studies reported here were initiated before this use of CP was eliminated. Our laboratories also have on-going tests with other currently available flea control products, including tetrachlorvinphos.

At present, there is very little information available related to children's pesticide exposure from treated pets. Homeowners utilize a variety of flea and tick collars, topical pesticide applications, as well as shampoos, dips and treatment of yards with powders, sprays and granular forms of insecticides for flea control. Potential exposure has been reported from pets tracking residues into a home after diazinon application to a lawn (Morgan et al., 2001). Our laboratories have also reported transferable residues of CP and phosmet from the fur of pets following an insecticide dip (Boone et al., 2001, 2006).

Over 31% of households in the U.S. own dogs as pets with a mean of 1.69 dogs per household (52.9 million dogs total). Additionally, 59% of these pet-owning households have at least one child residing in the household (American Veterinary Medical Association, 1997). Therefore, the potential for pesticide exposure from pets is significant. The goal of the present study was to determine the amount of CP that could be transferred to humans from pet dogs that were treated with a CP-containing flea collar that was commercially available over-the-counter. Transferable residues were quantified in cotton gloves used to rub dogs for 5 min periods after collar application, as well as in cotton tee shirts worn by children (who played with the dogs) at selected times post-collar application. First morning urine samples were collected from one adult and one child in each participating household for the purpose of quantifying the amount of 3,5,6-trichloro-2-pyridinol (TCPy; the primary CP urinary metabolite) as an index of exposure to CP. The dissipation of transferable residues, as well as potential correlations with length and type of exposure (direct or indirect), were evaluated.

Methods

Study Design

These experiments were designed to determine the levels of residues transferred to white cotton gloves from rubbing the back of a dog at three locations: near the base of the tail, at the neck with the collar removed, and at the neck with the collar in place. The potential contact with and absorption of the insecticide was estimated by CP residues in tee shirts worn by children for average 4-h periods at selected times after pesticide application, as well as TCPy levels in a first morning urine sample the morning following wearing the tee shirt. Urinary TCPy was also monitored from an adult in the household on the same sampling days.

Two study designs were employed with 24 families participating in each study. Participating families were volunteers who routinely used flea control products on their pet dogs. Study 1 was a longer-term study conducted over 168 days because the collar used was recommended by the manufacturer for 6-month use. Petting samples, plasma cholinesterase in the dogs, and urinary metabolites in children and adults were monitored. On the basis of results from this study, which indicated that residues remained relatively constant throughout this period, Study 2 was performed over 21 days, in which petting samples, residue samples of CP in tee shirts worn by the children, and urinary metabolites in children and adults were monitored.

Chemicals

The flea collars used (Zodiac—PowerBrand, 8% CP; manufactured by Wellmark, Bensenville, IL, USA) were donated by the manufacturer.

All solvents used were Optima grade (suitable for gas chromatography) and were obtained from Fisher Scientific. The CP standard was greater than 99% pure and was obtained from Chem Service (West Chester, PA, USA). The TCPy assay kit was obtained from Strategic Diagnostics (Newark, DE, USA). The creatinine kit and all chemicals for the cholinesterase assays were purchased from Sigma Chemical Company (St Louis, MO, USA).

Animals

The care and use of dogs were in accordance with the Guide for the Care and Use of Laboratory Animals (1996) in a clinical facility in the College of Veterinary Medicine at Mississippi State University. This facility is accredited by the Association for Assessment and Accreditation of Laboratory Animal Care (AAALAC). The dogs used during both studies were monitored by the project veterinarian (J.W.T.). All procedures used were previously approved by the Mississippi State University Animal Care and Use Committee.

Dogs of a variety of breeds were selected from pet owners who were staff or students at the College of Veterinary Medicine, Mississippi State University. Each dog had no known organophosphate compound exposure 1 month before the initiation of the research project, weighed at least 10 pounds, and was at least 4 months of age. Both male and female dogs were used in the studies; however, pregnant or nursing females were not included. During the studies, participants agreed not to use any other products containing organophosphate insecticides on their pets, as well as in or around their households.

Human Test Subjects

Human test subjects were residents in the same households as the dogs. Each participating household had a child (either gender) in the age range of 3–12 years who regularly played with the dog, a participating adult of either gender, and routinely used flea control products on their dogs. The age, gender, height and weight of both child and adult test subjects were recorded, as well as an estimate of the amount of time and degree of contact the child and adult had with the dog on the day of the tee shirt samples (which was the day preceding the urine sample). A description of the protocol was provided to the participants, and an informed consent form was obtained from the adults. The children were informed verbally of the procedures and oral or written assent was obtained from them and their parents. The sampling protocols described below and approval forms were approved by the Institutional Review Board for Research on Human Subjects at Mississippi State University.

Rubbing Protocol

The dogs were rubbed in a marked 10 × 25 cm area with clean, white cotton gloves for a continuous 5 min period as described previously (Boone et al., 2001). The gloves had been previously laundered and pre-extracted with methylene chloride to help reduce the amount of interfering, loose cotton fiber content. Rubbing was with firm pressure in both directions. Three samples were taken in the following order to avoid cross contamination: (1) near the base of the tail; (2) at the neck with the collar removed; and (3) at the neck with the collar back in place (i.e. rubbing over the collar). These three samples were designed to assess, respectively: (1) migration of the insecticide from the collar to distant areas of the body; (2) transfer of insecticide from the collar to the fur adjacent to the collar; and (3) transfer of insecticide from the collar itself. Two studies were conducted with different sampling times. During Study 1, rubbing samples were obtained before placement of the collar (day 0), at 4 h, and 1, 3, 7, 14, 28, 56, 84, 112, 140 and 168 days following collar placement. During Study 2, rubbing samples were obtained before collar placement (day 0), and then at 14 and 20 days following collar placement.

Tee Shirt Protocol

During Study 2, each child subject was supplied with a new, clean (laundered but not solvent-extracted), short-sleeved, white cotton tee shirt to wear on the day before the treatment (day 0) and on 1, 4, 8, 15 and 20 days post-collar placement. Each tee shirt was worn during the afternoon and evening of the sampling day for an average 4 h period, and each child was instructed not to alter his/her normal behavior with respect to the dog. At the end of the day, the tee shirt was placed into a solvent-washed glass bottle for subsequent extraction. A 100-cm2 section from the front chest area of each shirt was cut out and used for extraction, as this region is the most likely region of the shirt to contain residues from the child's interaction with the dog.

Urine Sampling Protocol

During Study 1, urine samples were obtained from one child and one adult in each household before application of the collar and on 3, 7, 28, 84 and 168 days after the collar was applied. For Study 2, urine samples were collected from the child wearing the tee shirt and from one adult in the same household before collar application and on days 16–21 post-collar placement. In both studies, first morning urine samples were collected, with the instructions to participants to collect the entire void (Kissel et al., 2005). Following collection, the samples were brought to our laboratories, acidified with concentrated hydrochloric acid to free any conjugated TCPy, and frozen until analysis (Shackelford et al., 1999).

Determination of CP on Gloves and Tee Shirts

The gloves and tee shirts used to collect residue samples were 100% cotton. The gloves used in both studies were stored, extracted and analyzed as described earlier (Boone et al., 2001). CP residues in tee shirts were determined using the same procedures described for the gloves, with the exception of the methylene chloride pre-extraction step.

Determination of TCPy in Urine

The concentration of TCPy was determined in urine samples using a RaPID Assay Trichloropyridinol Test Kit (#A00208; Strategic Diagnostics, Newark, DE, USA), an enzyme linked immunosorbent assay (ELISA) for the determination of TCPy and related compounds (Shackelford et al., 1999). Neither CP nor trichlopyr, parent compounds yielding TCPy as a metabolite, exhibited any cross-reactivity in the assay. Urinary TCPy levels were adjusted for urinary creatinine concentration for both adults and children (ages 3–12 years of age) (Barr et al., 2005). Creatinine content of urine was determined by colorimetric determination at 500 nm using a creatinine kit (Sigma Diagnostics, St Louis, MO, USA; Creatinine Kit no. 555).

Plasma Cholinesterase Assay

During Study 1, blood samples were taken from each dog at the same time as rubbing samples. Blood samples were centrifuged after collection to obtain plasma, which was stored at 4°C overnight, and cholinesterase (ChE) activity was determined within 24 h after collection as described previously (Boone et al., 2001). Cholinesterase (ChE) determinations were done using the following combinations of inhibitors and substrates to investigate plasma enzymes: butyrylcholinesterase (BChE) using butyrylthiocholine (BTCh) iodide as a substrate and tetraisopropyl pyrophosphoramide (iso-OMPA) as an inhibitor, and acetylcholinesterase (AChE) using acetylthiocholine (ATCh) iodide as a substrate and eserine sulfate as an inhibitor. All assays were a modification of the procedure described in Chambers and Chambers (1989), which is based on the spectrophotometric method of Ellman et al. (1961). Protein concentration was determined by the method of Lowry et al. (1951) for standardization.

Statistical Analysis

ANOVA calculations were performed with the GLM procedure of the SAS® System for Windows, Version 8.2, using the 0.05 level of significance. When significant differences between treatment groups were found, means were separated using the least significant difference test. The clinical importance of the differences was assessed using confidence intervals (Braitman, 1991). Each data set (gloves, tee shirts and adjusted urine) was analyzed separately for each collar or age group using one-way analysis of variance for a randomized complete block design (household is the blocking factor).

Evaluation of the data for possible correlations among transferable residues of chlorpyrifos, time tee shirts were worn, time adults and children spent with the dogs and urinary TCPy concentrations was performed using Spearman's correlation coefficient. The calculation was performed using the CORR procedure of the SAS System for Windows, Version 9.1 (SAS Institute Inc., Cary NC, USA). The level of significance was 0.05.

Results

In both studies, significant increases in transferable residues of chlorpyrifos to cotton gloves were observed compared with pretreatment samples. Transferable residues from the cotton gloves were greatest in samples obtained on and adjacent to the collar and were lowest in areas more distant from the collar. Figure 1 and Table 1 show the mean transferable residues obtained at each sampling time for the long-term (Study 1) and short-term (Study 2) studies, respectively. These residues are categorized based on sites of collection (e.g. collar, neck, and back). The residues observed in Study 2 were generally higher than those of Study 1.

Figure 1
figure1

Mean transferable chlorpyrifos residues from 24 treated dogs to cotton gloves±SE (Study 1).

Table 1 Mean transferable chlorpyrifos residues from 24 treated dogs to cotton gloves±SE, 24 replications (Study 2).

Figure 2 shows the average amounts of transferable residues obtained from the analysis of cotton tee shirts worn by children at selected times after collar placement (Study 2 only). No significant differences were observed from one treatment day to another with respect to the amount of chlorpyrifos on the front center of the tee shirts, but all residues were greater than pretreatment values. The average residue for all sampling times was 153±55 ng/g shirt.

Figure 2
figure2

Mean chlorpyrifos residues on cotton tee shirts worn by children at selected times post application in the second study. Horizontal bar shows the mean and SE of the pretreatment values.

Throughout both studies, children generally had significantly greater urinary concentrations of TCPy than adults. However, no significant differences in TCPy concentrations were observed among the adults or among the children compared with their respective pretreatment samples in either of the two studies except on post-treatment days 28 and 84 in Study 1, where TCPy concentrations in children's urine were significantly greater than pretreatment samples. In Study 2 where daily samples were taken over a 5-day period (days 16–20), the overall mean values for urinary TCPy were 7.9±0.7 and 11.6±1.1 ng/mg creatinine in adults and children, respectively. Figures 3 and 4 show the average TCPy concentrations in urine for the children and adults in both studies. The range of adult urinary TCPy values was 1.9–39.4 and 0.2–36.6 ng/mg creatinine in Study 1 and Study 2, respectively (Figure 5). For children, concentrations were in a range from 2.3 to 47.0 and 0.01 to 63.7 ng/mg creatinine in Study 1 and Study 2, respectively (Figure 6). Ninety-six percent of the values in both studies were between 0.2 and 19.6 ng/mg creatinine for adults and between 0.01 and 38.7 ng/mg creatinine for children with only 4% of the values occurring above these ranges (Figures 5 and 6).

Figure 3
figure3

Mean 3,5,6-trichloro-2-pyridinol urinary concentrations by day expressed in ng/mg creatinine — Study 1.

Figure 4
figure4

Mean 3,5,6-trichloro-2-pyridinol urinary concentrations by day expressed in ng/mg creatinine — Study 2.

Figure 5
figure5

Range of urinary 3,5,6-trichloro-2-pyridinol concentrations in adults.

Figure 6
figure6

Range of urinary 3,5,6-trichloro-2-pyridinol concentrations in children.

During Study 1, significant increases in plasma ChE inhibition in the dogs were observed 3 days after collar application, and maximum inhibition (69%) was observed at 112 days post-collar application (Figure 7). Although both AChE and BChE were measured, only BChE data are reported here because its activity was generally 10-fold higher than AChE activity throughout the study, and because it demonstrated a higher level of inhibition than AChE. BChE inhibition appeared to plateau at about 63%.

Figure 7
figure7

Percent inhibition of butyrylcholinesterase±SE from the plasma of dogs wearing flea control collars containing chlorpyrifos.

At the 0.05 level of significance, there were no significant correlations present among transferable chlorpyrifos tee shirt residues, time tee shirts were worn, time spent with the dogs and urinary TCPy concentrations. However, there were positive trends in the data for some families when comparing the amount of time children spent in direct (petting, grooming, feeding) and indirect (in the same room with but not touching the dog) contact with treated dogs and the amount CP on tee shirts. Positive trends were also observed between the amount of time children spent in direct contact with treated dogs and urinary TCPy concentrations.

Discussion

Different breeds of dogs, different families and different samplers were used in these studies to include the variability present in dog physiology, dog and human activity, petting pressure when sampling, and different dog skin and fur conditions. It is assumed that this variability is similar to that which would be encountered in the overall population of actual pet owners using over-the-counter flea control collars. The two studies were conducted by two different groups of workers and used 48 different dogs (24 in each of the two studies). These differences in samplers, etc., are believed to be responsible for the higher residues observed in Study 2 compared to Study 1.

During Study 1, transferable CP residues were lowest (168±27 μg/glove) at the 4-h over-the collar sampling time and reached a maximum of 391±75 μg/glove at 14-days post-collar application. From 14-days post-collar application until the end of the study, there was a 20% decline in detectable CP residues obtained over the collars compared with the peak level. This same trend was also observed with the samples obtained from the fur around the necks without the collars in place. Mean CP residues obtained from the backs of the dogs remained fairly constant throughout the study, reflecting the slow release of insecticide from the collar matrix. The slow rise in CP concentration from the backs of treated animals reflects the lag time required for release and distribution of the insecticide. Because the residues were relatively constant after 14 days in Study 1, transferable residues were obtained only on days 14 and 20 post-collar application during Study 2. The results indicate maximum CP residues are available for transfer at 2 weeks post-collar application and that transferable residues of a similar or slightly lower level can be detected as much as 168 days post-collar application of this particular collar. As expected, transferable residues are greater in and around the treated area and decrease in areas more distant from the treated area because of the time required for distribution of CP. The lack of correlation between glove residues and urinary TCPy was disappointing, but not inconsistent with the lack of correlation between residues on passive dosimeters and biomonitoring of urinary metabolites in many occupational exposure studies (Honeycutt et al., 2000; Geer et al., 2004; Fenske and Day, 2005).

During Study 2, children wore cotton tee shirts on days 15 to 19 post-collar application for the purpose of further evaluating transferable residues and to determine whether this might be a suitable surrogate for urinary metabolite levels. The children were asked not to alter their activities with respect to their dogs during the sampling period so that detected residues would be representative of what might be expected upon casual and normal contact with treated dogs. All of the observed CP residues on the 100-cm2 sample from the chest of the shirts were significantly greater than pretreatment residues, but there were no significant differences observed from one treatment day to another. This, like the petting protocol, also demonstrates the presence of transferable CP residues at 2 weeks post-collar application.

Published studies have reported the half-life of CP metabolites in urine to be between 15 and 41 h (Nolan et al., 1984; Meuling et al., 2005; Barr and Angerer, 2006). Thus, the collection of a 24-h urine sample is preferred for urinary metabolite quantification because it will provide a better estimate of the previous day's exposure. However, first-morning voids are more practical to obtain than 24-h samples and have been used in many biological monitoring studies to evaluate the concentration of environmental chemicals in human urine (Barr and Angerer, 2006). Kissel et al. (2005) demonstrated that first-morning voids are the best predictors of weighted-average daily metabolite concentrations in the absence of a 24-h sample. However, with spot samples such as first-morning voids, there is variability in the volume of urine and the concentrations of endogenous and exogenous chemicals from void to void that must be considered.

In the present studies, urinary creatinine concentration, a widely used method for adjusting for sample dilution, was determined for each sample and was used to standardize the amount of TCPy in urine samples. The urinary creatinine concentrations of both adults and children were of similar magnitude to those reported in the NHANES III (Barr et al., 2005). During Study 1, maximum average amounts of TCPy in children's urine were observed on post-treatment days 28 (16.1 ng/mg creatinine) and 84 (17.4 ng/mg creatinine), both of which were significantly greater than the pretreatment values. These numbers represent an approximate 37% increase over pretreatment levels. From day 84 to the conclusion of the study at 168 days post-collar application, TCPy concentrations declined by 20% and were near pretreatment levels (Figure 3). During Study 2, urinary TCPy levels varied only slightly for both adults and children during the 5-day sampling period, with children still having significantly higher urinary TCPy concentrations than adults (Figure 4), but there were no significant differences between post-treatment and pretreatment values except on day 18. Therefore, there appears to be relatively little exposure from this flea control collar.

BChE activity in dog plasma was greater than AChE activity, was more sensitive to inhibition, and would thus serve as the most effective biomarker of insecticide action and persistence after exposure to CP flea and tick control applications in dogs. ChE (i.e. BChE) inhibition was significant by three days post-collar application (27%). By post-collar application day 56 (63% Inhibition), no other significant increases in total ChE inhibition were observed. Although the dogs were not the focus of Study 1, there is some concern that dogs with this level of inhibition might be vulnerable to exposures from additional anticholinesterases, as significant ChE inhibition was observed soon after treatment and was maintained throughout the duration of the study. However, dogs were under the careful observation by the veterinarian of the project (J.W.T.) and no cholinergic signs were observed.

The data generated here are useful in determining the amounts of pesticides to which children could be exposed from pets treated with an over-the-counter CP flea collar formulation. While there appeared to be little, if any, additional exposure to CP as a result of use of these collars on pets, it is presently unknown how representative these data will be for other flea control formulations presently available. Consequently, caution should be observed when applying these types of insecticides and all label directions should be followed. More information is needed regarding the behavior of children with their pets, the lengths of fur, fur composition and contact with untreated surfaces by treated dogs in order to adequately address pesticide exposure and the resulting risks.

While there are no perfect measurement techniques for determining the amount of pesticide exposure resulting from contact with treated pets, we feel the cotton glove and tee shirt models utilized here are tools that may be used as a surrogate for potential pesticide exposure. Previous reproducibility tests performed in our laboratory have shown that the decrease in CP residues on gloves with time is a result of decline by degradation or wear and is not the result of removal by the sampling procedures (Boone et al., 2001, 2006). These data show that the use of cotton gloves and tee shirts for monitoring transferable residues yields reproducible results and that they do not remove appreciable amounts of the insecticide available for exposure.

While we anticipated there would be substantial correlation among time spent with the dog, tee shirt residues, and urinary TCPy, there were no such statistically significant correlations. We recognize the collection of 24 h urine samples for metabolite quantification and videotaping the families to obtain exposure data would have been ideal and would have provided more accurate data to help determine the presence or absence of correlations. However, neither of these techniques were feasible in the present studies. Furthermore, the metabolism of CP is complex and involves a variety of cytochrome P450s and esterases, whose levels are expected to vary among individuals. Thus, variability in urinary metabolite levels together with a lack of correlation with activity patterns is not surprising.

In summary, the results of these studies show that maximal exposure to this particular CP flea collar from direct contact with hands occurred within 2 weeks of collar application and was potentially greatest in the areas on/near the collar. Transferable residues to both cotton gloves and tee shirts were significantly greater than pretreatment concentrations, indicating that significant transfer of CP residues can and does occur. However, there was not a corresponding rise in urinary TCPy concentrations, which means that very little, if any, CP is being absorbed by adults and children. It should be noted, however, that all urine pretreatment samples (both adults and children) contained appreciable amounts of TCPy, which is indicative of the widespread use of CP. In conclusion, there is little evidence that use of this flea collar resulted in enhanced CP exposure to either children or adults.

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Acknowledgements

This research was supported by grants from the US Environmental Protection Agency's Science to Achieve Results (STAR) program (Grant Numbers R825170 and R828017). Although the research described in the article has been funded wholly or in part by the US Environmental Protection Agency's STAR program, it has not been subjected to any EPA review and therefore does not necessarily reflect the views of the Agency, and no official endorsement should be inferred. We thank Ms. Susan Waldrop, Ms. Nicole Holifield, Ms. Melissa Joyce, and Mr. Collin Zumwalt for assistance with cholinesterase assays and chemical analyses, and Dr. Carolyn Boyle for statistical advice. This research was also supported by the Mississippi Agriculture and Forestry Experiment Station (MAFES) and the College of Veterinary Medicine, Mississippi State University. This article is MAFES publication number J-11059 and the Center of Environmental Health Sciences publication number 111.

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Correspondence to Janice E Chambers.

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Chambers, J., Boone, J., Davis, M. et al. Assessing transferable residues from intermittent exposure to flea control collars containing the organophosphate insecticide chlorpyrifos. J Expo Sci Environ Epidemiol 17, 656–666 (2007). https://doi.org/10.1038/sj.jes.7500570

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Keywords

  • chlorpyrifos
  • organophosphate insecticide
  • flea control
  • transferable residue
  • dog fur
  • human exposure

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