high polybrominated diphenyl ether levels in california house cats: house dust a primary source?

HIGH POLYBROMINATED DIPHENYL ETHER LEVELS IN CALIFORNIA HOUSE CATS:HOUSE DUST A PRIMARY SOURCE?

WEIHONG GUO,*y JUNE-SOO PARK,y YUNZHU WANG,y STEVE GARDNER,z CHRISTINA BAEK,y MYRTO PETREAS,yand KIM HOOPERy

yEnvironmental Chemistry Laboratory, California Department of Toxic Substances Control, California Environmental Protection Agency,Berkeley, California, USA

zAlbany Animal Hospital, Albany, California, USA

(Submitted 31 May 2011; Returned for Revision 23 July 2011; Accepted 8 October 2011)

Abstract—Polybrominated diphenyl ethers (PBDEs) are brominated flame retardants that act as endocrine disruptors, affecting thyroidhormone homeostasis. As a follow-up to a recent study showing high PBDE levels in household cats and linking PBDE levels with cathyperthyroidism, we measured PBDEs, polychlorinated biphenyls (PCBs), and organochlorinated pesticides (OCPs) in serum samplesfrom 26 California household cats (16 hyperthyroid, 10 controls) using liquid–liquid extraction and high-resolution gas chromatography/high-resolution mass spectrometry. In the present pilot study, we found that PBDE levels in California house cats were extremely high(SPBDEs median¼ 2,904 ng/g lipid; range, 631–22,537 ng/g lipid). This is approximately 50 times higher than levels in Californiaresidents (SPBDEs geomean¼ 62� 8.9 ng/g lipid, National Health and Nutrition Examination Survey), who have among the highesthuman levels in the world. Polybrominated diphenyl ethers congener patterns (BDE-99 major congener, BDE-209 significant) differedmarkedly from patterns found in California residents (BDE-47 major) or wildlife but resembled patterns found in house dust.Polychlorinated biphenyls and OCPs in cats were highly correlated, consistent with a shared dietary source or pathway of exposure, butdid not correlate with PBDEs. This suggests a different source or pathway of exposure for PBDEs, which was most likely house dust. Theauthors found no evidence that linked levels of PBDEs, PCBs, or OCPs with hyperthyroidism. This may be because of the small samplesize, competing or confounding risk factors, or complicated causal mechanisms. Environ. Toxicol. Chem. 2012;31:301–306.# 2011 SETAC

Keywords—House cat Hyperthyroidism Polybrominated diphenyl ethers Polychlorinated biphenyls House dust

INTRODUCTION

Polybrominated diphenyl ethers (PBDEs) are brominatedflame retardants that have been widely used since the 1970s inconsumer products containing synthetic textiles, polyurethanefoam, or thermoplastics, as well as in electronic equipment [1].Polybrominated diphenyl ethers were manufactured in threecommercial mixtures: penta-BDE (tetra-hexa-BDEs), octa-BDE (hepta-nona-BDEs), and deca-BDE (largely BDE-209).Because of their widespread use, persistence, and tendency tobioaccumulate in the food web, the lower brominated PBDEshave increased dramatically over the last 20 years in indoor (air,dust) and outdoor environments and in wildlife and humans[1–5]. Increases are especially evident in California residentsand wildlife [6–8], perhaps because of California’s uniqueflammability standards [9].

In the mid-2000s, penta-BDE and octa-BDE commercialmixtures were voluntarily withdrawn or banned in Europeancountries and 11U.S. states, including California [8,10,11]. Aphase-out of the commercial deca-BDE is planned [12], in partbecause of the recent findings that BDE-209 breaks down intothe more toxic lower brominated PBDEs [13,14]. Large reser-voirs of PBDEs remain, however, in consumer products eitherstill in use or entombed in landfills, and we may anticipate

continued release of PBDEs into the environment for decades tocome.

Polybrominated diphenyl ethers are found in house andoffice dusts [15,16], and much of the PBDE exposure for adults(80%) and toddlers (89%) is said to come from incidentalingestion of house dust [11,17]. Toddlers and household catsshare activity areas (floors, rugs) in the indoor environment andingestion exposure activities (hand-to-mouth for toddlers,grooming for cats). As such, house dust also may be a signifi-cant source of PBDE exposure for cats, and house cats mighthave relevance as indoor PBDE exposure models for children.

Cat hyperthyroidism, first reported as a new disease in 1979,is now a major health problem among middle-aged and olderhousehold cats and is a leading cause of death for cats world-wide [18,19]. Hyperthyroidism is a multisystem disorder char-acterized by an increase in thyroid hormones (T3 and T4)produced by an enlarged thyroid gland. Causes of the diseasein house cats are unknown, although indoor exposures and diet(canned food intake) are suspected risk factors [20–23].

Polybrominated diphenyl ethers are endocrine disruptors,affecting thyroid homeostasis (as do some polychlorinatedbiphenyls [PCBs] and organochlorinated pesticides [OCPs])because of their structural similarities to thyroxine [24,25].In vivo studies in rats have shown that PBDE exposures eitherdecrease thyroxine levels [26,27] or significantly increasethyroid-stimulating hormones, possibly causing hyperthyroid-ism at very high levels [28]. A recent study reported 20 to100 times higher levels of PBDEs in cats than in humans andsuggested that PBDE exposures may be linked to cat hyper-thyroidism [29]. If cat hyperthyroidism is truly increasing,and if some or part of the increase is due to environmental

Environmental Toxicology and Chemistry, Vol. 31, No. 2, pp. 301–306, 2012# 2011 SETAC

Printed in the USADOI: 10.1002/etc.1700

All Supplemental Data may be found in the online version of this article.The views expressed herein are those of the authors and do not neces-

sarily reflect those of the Department of Toxic Substances Control, Cali-fornia Environmental Protection Agency.

* To whom correspondence may be addressed([email protected]).

Published online 21 November 2011 in Wiley Online Library(wileyonlinelibrary.com).

301

exposures, identifying these causes is important because catsand people share the indoor home environment. Toddlers andyoung children are especially at risk for higher indoor chemicalexposures (e.g., PBDE body burdens in children are 5 to 10-foldhigher than their parents), which may bring hormonal disruptionand neurodevelopmental consequences [11,30–33].

We compared levels and patterns of these analytes in house-hold cats with those found in California residents, wildlife, andhouse dust. Using these data, we suggest possible sources ofPBDE exposures in household cats. In addition, we explored theroles of PBDEs and other potential endocrine disruptors in cathyperthyroidism.

MATERIALS AND METHODS

Study subjects

The 26 cats (16 hyperthyroid and 10 nonhyperthyroid, 3–20years of age) were recruited by five veterinary clinics from 2008to 2010 from 21 households in the San Francisco Bay region ofCalifornia. Blood samples from 10 nonhyperthyroid cats werecollected during routine physical examinations or during treat-ment for nonthyroid problems (e.g., dental disease, wounds,obesity, kidney disease, diabetes, ulcers, and other conditions).Hyperthyroid diagnoses were made by veterinarians based onphysical appearance and T4 values. Blood samples from hyper-thyroid cats were collected within one year of diagnosis. The 26cats in the present study were divided into the following threegroups based on age and thyroid status: younger, nonhyperthy-roid group (non-HT, mean age¼ 6 years, n¼ 4); older, non-hyperthyroid group (non-HT, mean age¼ 14 years, n¼ 6); andolder, hyperthyroid group (HT, mean age¼ 14 years, n¼ 16)(Table 1).

Standards and materials

Nine 13C-labeled PBDEs (13C-BDE-28, 47, 99, 153, 154,183, 197, 207, and 209) (Wellington Laboratories) and 1613C-labeled PCBs and pesticides (13C-PCB-118, 138, 153,170, 180, 194, 101, 105, 156, 13C 2,40-DDT, 13C-4,40-DDE,13C-4,40-DDT, 13C-hexachlorobenzene, 13C-oxychlordane,13C-trans-nonachlor, and 13C-b-BHC) (Cambridge IsotopeLaboratories) were used as internal standards. As a recoverystandard, 13C-PCB-209 (Cambridge Isotope Laboratories) wasused. Native PBDE standards were purchased from WellingtonLaboratories, and native PCBs and OCPs were purchased fromAccuStandard (Supplemental Data, Table S1).

Solvents (hexane, dichloromethane, acetone, isooctane,methyl tert-butyl ether, isopropanol) and other chemicals(hydrochloric acid, sodium hydroxide, sodium sulfate, andpotassium chloride) were of the highest quality available andpurchased from Burdick and Jackson, J.T. Baker, and FisherScientific. Florisil gel, 60 to 100mesh, was from MallinckrodtChemicals.

Sample preparation

Serum collection. Veterinarians collected whole blood sam-ples in red-top Vacutainers (Becton Dickinson) with no interiorcoating, nonsilicone stopper lubrication, and no additives.Blood samples were clotted at room temperature and centri-fuged (1,000 g for 15min). Serum supernatants were transferredto a second set of red-top Vacutainers and centrifuged (1,000 gfor 10min) again. Serum supernatants were transferred tosolvent-rinsed amber glass vials (Wheaton) and stored at�208C until analysis.

Serum extraction. Procedures for serum extraction andcleanup were adapted from earlier methods [34,35]. In brief,after spiking with internal standards, 1ml serum was treatedwith 6M hydrochloric acid (1ml) and 70% isopropanol (6ml)to denature proteins. Analytes of interest were extracted with1:1 v/v mixture of hexane and methyl t-butyl ether (6ml, and re-extracted with 3ml), and the combined extract was washed with1% potassium chloride solution (4ml). Phenolics were sepa-rated from neutrals by adding 0.5M potassium hydroxide in50% ethyl alcohol (2ml) and hexane (4ml, and re-extractedwith 3ml), and phenolics were archived for future analysis. Thecombined neutral fractions were concentrated under nitrogenwith a Turbo Vap LV Evaporator (Caliper LifeSciences),cleaned on a deactivated Florisil column (60–100mesh), andeluted with hexane (60ml), followed by 1:1 v/v hexane/dichloromethane (60ml). Eluates were concentrated and theanalytes stored in amber vials containing 80ml isooctane and20ml recovery standard.

Instrumentation and quantitation

Analyses were performed by gas chromatography/high-res-olution mass spectrometry (DFS, Thermo-Finnigan) using iso-tope dilution. For OCPs and PCBs, 2ml extract was injected intothe programmable temperature vaporizing splitless injectionsystem and separated on an HT8-PCB column (60m� 0.25mminner diameter, 0.25mmfilm thickness; SGE International) withhelium carrier gas and programmed as 1208C to 1808C at208C/min, to 2608C at 28C/min, to 3008C at 58C/min, and held5min. For PBDEs, 2ml extract was injected and separated on aDB-5 MS column (15m� 0.25mm inner diameter, 0.10mmfilm thickness; J&W Scientific) with helium carrier gas andprogrammed at 1758C for 2min, to 2808C at 58C/min, to 3108Cat 78C/min, and held for 5min. The high-resolution massspectrometry was operated in electron impact ionization modeusing multiple ion detection, source temperature of 2608C,ionization energy 42V, electron current typically 0.5 to0.6mA, and mass resolution of 10,000 with perfluorokeroseneas a mass reference.

The concentrations were expressed as lipid weight (ng/g),normalized from wet weight (ng/ml) using total lipid values(Supplemental Data, Table S2). Total lipid was calculated fromcholesterol and triglyceride levels using Phillip’s formula [36],which has been validated for humans but not cats. Calculatedserum lipid levels in cats and humans, however, are similarusing the Phillip’s formula, and we are comfortable makingcomparisons of chemical levels in cats and humans in thepresent study.

Quality assurance/quality control

All glassware was solvent-rinsed (acetone and 95%n-hexane) and baked (5008C for 3 h).

Samples were analyzed using standard laboratory QA/QCprotocol. Each batch of 10 samples was accompanied by alaboratory method blank control (10� diluted bovine serum;HyClone), a matrix spike control (permatrix-spiked bovineserum), and a standard reference material (human serum,SRM 1589a, NIST).

The method detection limit was defined as 3 times thestandard deviation of the concentration in the blank. The meanrecoveries of internal standards were 108% for PBDEs and119% for pesticides and PCBs. Matrix spike recoveries frombovine serum for all measured BDE congeners ranged from71% for BDE-209 to 126% for BDE-153. The mean recovery ofthe standard reference material was 114%.

302 Environ. Toxicol. Chem. 31, 2012 W. Guo et al.

Table 1. Concentrations of major PBDEs, OCPs, and PCBs in cat serum (ng/g lipid)

Group size

All catsNonhyperthyroidyounger cats

Nonhyperthyroidolder cats

Hyperthyroidolder cats Method

detectionlimit26 4 6 16

Age (years)Mean� SE 12.8� 0.7 6.3� 1.4 14.2� 1.4 13.9� 0.4Median (min–max) 13.0 (3.0–20.0) 6.5 (3.0–9.0) 13.5 (11.0–20.0) 14.0 (9.0–18.0)

PBDEsBDE–047Mean�SE 830� 214 297� 101 1,406� 750 727� 157 11.7Median (min–max) 567 (49.3–4941) 221 (1,54–594) 567 (162–4,941) 604 (49.3–3360)

BDE-099Mean�SE 1,884� 521 405� 124 3,733� 2,043 1,561� 231 3.6Median (min–max) 1,351 (176–13554) 322 (220–757) 2,239 (207–13,554) 1,513 (176–4,483)

BDE–100Mean�SE 93.5� 34.7 39.7� 12.8 190� 129 70.8� 23.6 0.9Median (min–max) 33.4 (7.8–826) 37.8 (13.7–69.6) 54.3 (18.6–826) 31.8 (7.8–487)

BDE–153Mean�SE 293� 69.4 43.6� 6.2 562� 253 255� 36.6 0.9Median (min–max) 233 (21.2–1695) 41.2 (31.9–60.1) 442 (21.2–1,695) 260 (29.6–548)

BDE–154Mean�SE 155� 41.0 28.7� 6.7 311� 158 127� 18.2 1.2Median (min–max) 123 (13.1–1046) 24.3 (18.4–48.0) 203 (13.1–1,046) 135 (14.8–301)

BDE–183Mean�SE 20.1� 3.3 4.4� 0.9 31.9� 10.7 19.6� 2.3 1.2Median (min–max) 17.5 (3.0–74.4) 3.7 (3.0–7.1) 33.2 (4.5–74.4) 17.8 (3.6–43.3)

BDE–197Mean�SE 29.5� 7.4 33.8� 26.5 19.9� 9.2 32.0� 8.0 1.2Median (min–max) 16.3 (4.5–153) 8.8 (4.5–113) 11.0 (5.0–64.1) 19.1 (5.6–153)

BDE–207Mean�SE 122� 56.1 380� 337 39.6� 12.3 88.9� 30.7 1.5Median (min–max) 41.0 (13.2–1,391) 50.4 (27.0–1,391) 25.3 (13.2–90.7) 41.0 (15.5–627)

BDE–209Mean�SE 961� 547 3,864� 3,471 284� 61.9 488� 160 50.9Median (min–max) 280 (23.2–14,276) 432 (316–14,276) 279 (90.6–495) 220 (23.2–3,373)

SPBDEsMean�SE 4,505� 1,006 5,373� 3,966 6,709� 3,319 3,461� 485Median (min–max) 2,903 (631–22,537) 1,697 (8,50–17,247) 3,742 (874–22,537) 3,142 (631–9,491)

OCPst–nonachlorMean�SE 318� 240 15.8� 9.9 131� 60.3 463� 312 0.9Median (min–max) 58.1 (0.0–6,315) 6.4 (5.1–45.3) 81.6 (0.0–381) 68.2 (9.4–6,315)

OxychlordaneMean�SE 111� 80.2 3.9� 3.9 44.3� 24.9 163� 104 0.6Median (min–max) 16.5 (0.0–2108) 0.0 (0.0–15.6) 22.9 (0.0–159) 25.5 (0.0–2108)

4,40–DDEMean�SE 530� 94.8 138� 21.9 546� 184 622� 104 5.6Median (min–max) 288 (83.1–1,746) 140 (83.1–191) 472 (106–1,143) 368 (160–1,746)

4, 40–DDTMean�SE 57.7� 16.5 25.75� 11.7 34.8� 29.4 74.3� 19.2 0.6Median (min–max) 28.4 (0.0–365) 23.4 (0.0–56.2) 0.0 (0.0–180) 57.3 (0.0–365)

PCBsPCB–74Mean�SE 4.1� 0.6 1.9� 0.8 4.1� 0.8 4.7� 0.6 0.6Median (min–max) 3.4 (0.0–11.5) 1.9 (0.0–3.7) 3.3 (2.5–6.6) 4.2 (0.0–11.5)

PCB–99Mean�SE 17.2� 2.2 4.3� 1.4 17.4� 3.5 20.4� 2.2 1.4Median (min–max) 14.6 (0.0–43.7) 5.5 (0.0–6.2) 17.4 (7.7–27.2) 17.6 (5.8–43.7)




PCB–153Mean�SE 49.4� 8.3 11.2� 3.8 55.9� 18.5 56.5� 8.6 1.5Median (min–max) 35.5 (0.0–158) 14.1 (0.0–16.5) 47.9 (8.0–124) 45.7 (7.9–158)


High PBDE levels in California house cats Environ. Toxicol. Chem. 31, 2012 303

Data analysis

Because of their skewed distributions, all measurement datawere log-transformed and normality checked using plots and theShapiro-Wilk test. Basic statistical analyses were performed inSTATA, Version 11.0 (StataCorp) to assess correlations amongthe three groups of chemicals measured, correlations betweenthe sum of chemical levels and cat’s age, as well as thedifferences in chemical levels between cat groups (t test).We set the level of significance as a< 0.05.

RESULTS AND DISCUSSION

PBDEs much higher than OCPs, PCBs

The PBDE levels in California household cats were a mean(�SE) and median (min to max) SPBDEs concentration of4,505 ng/g (�1,006 ng/g) and 2,904 ng/g (631–22,537 ng/g),respectively (Table 1), 20-fold higher than PCBs (median¼170 ng/g) and 10-fold higher than dichlorodiphenyldichloro-ethylene (4,40-DDE) (median¼ 288 ng/g), the most dominantOCP. Thus, PBDE levels in cats exceeded the legacy PCB andOCP contaminants.

The PBDE levels in humans and wildlife are higher inCalifornia than elsewhere, and California house cats hadapproximately twofold higher SPBDEs than east coast cats[29]. This may be because California house dust has higherPBDE levels [4] than east coast house dust [3], which, in turn,may be because products sold in California have higher levels of

PBDEs to meet California’s flammability standard TechnicalBulletin 117 [9].

The sum of PBDEs was 40 to 50 times higher in cats than inCalifornia residents sampled in 2003 to 2004 (geomean¼57.2 ng/g lipid) (National Health and Nutrition ExaminationSurvey) [8] and California pregnant women in 2009 (median¼78.3 ng/g lipid) [37]. Levels in cats may be higher because catbehavior, such as sofa nesting and grooming, may lead tohigher house dust exposures. In addition, cats have impairedglucuronidation [38], which may slow PBDE detoxification andincrease bioaccumulation. In contrast, PCB and OCP levels inhouse cats and humans [37,39] were similar.

PBDE congener patterns similar in cats, house dust

Although PCB congener patterns were similar in Californiahouse cats, humans, and urban wildlife (PCB-153 predominat-ing) (Fig. 1), PBDE congener patterns were markedly differ-ent (Fig. 2), with BDE-209 as a significant congener. Themajor PBDE congeners in humans are BDE-47>BDE-99>BDE-100>BDE-154>BDE-153 [8,37,39]. In contrast, thedominant congener in cats was BDE-99, followed by BDE-47>BDE-209>BDE-153>BDE-154>BDE-207, and BDE-100. The PBDE congener pattern for California cats was similarto that for East Coast cats [29]. It was also similar to patternsfound in house dust, where BDE-99 and BDE-209 were majorcongeners [3,4]. The proportion of BDE-209 is higher in housedust than in cat serum, possibly because of different rates of

Table 1. (Continued )

Group size

All catsNonhyperthyroidyounger cats

Nonhyperthyroidolder cats

Hyperthyroidolder cats Method

detectionlimit26 4 6 16


SPCBsMean�SE 203� 29.4 46.3� 11.7 203� 44.6 242� 31.8Median (min–max) 170 (15.1–566) 50.2 (15.1–69.6) 189 (74.6–336) 211 (58.0–566)

Total lipids (mg/dL)Mean�SE 192� 15.6 200� 25.5 206� 32.8 185� 17.6Median (min–max) 166 (92.0–398) 181 (164–272) 193 (124–326) 158 (92.0–398)

PBDE¼ polybrominated diphenyl ethers; OCP¼ organochlorinated pesticides; PCB¼ polychlorinated biphenyls.

Fig. 1. Similar polychlorinated biphenyl (PCB) congener patterns in California house cats, humans, and urban wildlife, with PCB-153 predominating. Samplingtime, sample preparation, and analysis methods from different studies differed. NHANES¼National Health and Nutrition Examination Survey.


BDE-209 breakdown indoors versus in biological systems(e.g., access to ultraviolet light indoors vs presence of enzymesof metabolic debromination in cats).

House dust: A major PBDE source in cats?

The major exposure sources/pathways for PBDEs in house-hold cats are believed to be ingestion of house dust and canned/dried cat food [29]. Our data suggest that house dust may be adominant source. First, congener patterns of PBDEs in Cal-ifornia cats and house dust were similar and differed markedlyfrom serum PBDE patterns in California residents. Second,whereas OCPs (e.g., 4,40-DDE) and SPCBs were stronglycorrelated (r¼ 0.79) with diet as a common exposure pathway[40], PBDEs did not correlate with either OCPs or PCBs,indicating that PBDEs have a nondietary source (e.g., indoordust). Third, PCBs (p¼ 0.0034) and OCPs (p¼ 0.053) weresignificantly lower in younger cats than in older cats; OCP (e.g.,4,40-DDE) and PCB levels strongly correlated with cat’s age(r4,40-DDE¼ 0.62, r PCBs¼ 0.61). Thus, age was a significantmodifier of PCBs and OCPs, but not PBDEs, again consistentwith nondietary intake. Fourth, PCB and OCP levels weresimilar in the serum of California residents and house cats,but PBDEs were much higher in cats, suggesting house dust as amajor source of PBDEs. In addition, house dust ingestion isestimated to account for up to 80 to 90% of the total daily PBDEexposure in a toddler [17], whose rug-crawling and hand-to-mouth behavior more resembles the walking and grooming of acat than does the behavior of the toddler’s parents. Whenlooking into PBDE congener patterns, Fischer et al. [30] showedthat BDE-209 was a major congener (37%) in an 18-month-oldtoddler and in a five-year-old, but not in their parents (18%),consistent with house dust ingestion as a major exposure source/pathway. High proportions of BDE-209 were also found in eggsfrom California urban, but not rural, peregrine falcons (Fig. 1),consistent with urban raptors ingesting PBDE-209–containingurban dusts through preening and eating urban prey (e.g.,pigeons) [7].

Cat hyperthyroidism and PBDEs, PCBs, OCPs

In the present study, very high levels of PBDEwere detected,with some of the levels approaching doses used in in vivotoxicological studies in rats and mice [26–28]. However, catswith elevated T4 values did not have the highest PBDE levels

measured. This may be because PBDE blood levels, unlike T4values, may not reflect the real changes in the most clinicallyaffected organs (e.g., thyroid gland) in the present study. There-fore, serum PBDE levels might not be the best marker whenexamining a possible causal relationship between contaminantexposures and cat hyperthyroidism. In addition, metabolic ratesare altered in hyperthyroid cats and may subsequently result inincreased depuration of PBDEs, PCB, and OCPs from body fat.Small sample size, other risk factors (e.g., genetic variation inchemical uptake or metabolism, and other contaminants), con-founding factors (e.g., different breed, activities), or a morecomplicated causal mechanisms also may mask an association.

Age was a significant modifier of PCB and OCP levels. Ageis also a significant modifier of hyperthyroidism, a diseasecommonly found in older cats. Thus, we restricted our compar-ison of PBDE, PCB, and OCP levels to HT and non-HT cats ofsimilar ages, such as the two older cat groups with very similarmean ages (14.2 years in non-HT and 13.9 years in HT) (Fig. 1).We were unable to replicate the findings of the earlier study [29]and found no differences in levels of PBDEs, PCBs, or OCPsbetween these two groups. One possible explanation may bethat differences reported in the earlier study were driven by theage difference between the two cat groups (10.4 years in non-HT and 14.2 years in HT).

Future directions

As a follow-up to the present study, we are recruiting moreolder (>10 years) non-HT and HT house cats from the SanFrancisco Bay region.We are collecting house dust samples andcat food from the cat households and are asking families tocomplete a questionnaire detailing the diet and indoor/outdooractivities of their cats. We will measure additional contaminantsin cat serum that may share some toxicological properties withthe PBDEs (e.g., perfluorinated compounds, triclosan, metab-olites of PCBs, and PBDEs).

CONCLUSION

We found high serum PBDE levels in California house cats,far exceeding levels of the PCBs’ and OCPs’ legacy contam-inants. Our data suggest that house dust may be the source ofthese high PBDE levels. We found no evidence for an associ-ation between cat hyperthyroidism and serum levels of PBDEs,PCBs, or OCPs.

Fig. 2. Markedly different polybrominated diphenyl ether (PBDE) congener patterns in house cats with BDE-209 as a significant congener, whereas the majorcongeners in humans were BDE-47>BDE-99>BDE-100>BDE-154>BDE-153. Sampling time, sample preparation, and analysis methods from differentstudies differed.

High PBDE levels in California house cats Environ. Toxicol. Chem. 31, 2012 305

SUPPLEMENTAL DATA

Table S1. Native reference standards of PBDEs, PCBs, andchlorinated pesticides, and labeled internal/recovery standards.(46 KB DOC).

Table S2. Concentrations of PBDEs, OCPs and PCBs in26 cats (ng/g lipid). (266 KB XLS).

Acknowledgement—We thankE.Gordon,BerkeleyHumane Society, for hercollaboration. We thank G. Krowech of the California EnvironmentalProtectionAgency for her valuable comments onmetabolism.We also thankall the familieswhoprovided serumsamples from their pet cats for thepresentstudy.

REFERENCES

1. Shaw SD, Kannan K. 2009. Polybrominated diphenyl ethers in marineecosystems of the American continents: Foresight from currentknowledge. Rev Environ Health 24:157–229.

2. Sjodin A, Wong LY, Jones RS, Park A, Zhang Y, Hodge C, Dipietro E,McClure C, Turner W, Needham LL, Patterson DG Jr. 2008. Serumconcentrations of polybrominated diphenyl ethers (PBDEs) andpolybrominated biphenyl (PBB) in the United States population:2003–2004. Environ Sci Technol 42:1377–1384.

3. StapletonHM,DodderNG,Offenberg JH, SchantzMM,Wise SA. 2005.Polybrominated diphenyl ethers in house dust and clothes dryer lint.Environ Sci Technol 39:925–931.

4. Whitehead T, Odion Z, Visita P, Brown FR, Metayer C, Rappaport SR,Buffler PA, Petreas MX. 2010. A method for the determination ofPBDEs, PCBs, pesticides and PAHs in dust. Organohalogen Compd72:181–184.

5. Yogui GT, Sericano JL. 2009. Polybrominated diphenyl ether flameretardants in the U.S. marine environment: A review. Environ Int35:655–666.

6. Hwang HM, Park EK, Young TM, Hammock BD. 2008. Occurrence ofendocrine-disrupting chemicals in indoor dust. Sci Total Environ404:26–35.

7. Park JS, Holden A, Chu V, KimM, Rhee A, Patel P, Shi Y, Linthicum J,Walton BJ, McKeown K, Jewell NP, Hooper K. 2009. Time-trends andcongener profiles of PBDEs and PCBs in California peregrine falcons(Falco peregrinus). Environ Sci Technol 43:8744–8751.

8. Zota AR, Rudel RA, Morello-Frosch RA, Brody JG. 2008. Elevatedhouse dust and serum concentrations of PBDEs in California:Unintended consequences of furniture flammability standards? EnvironSci Technol 42:8158–8164.

9. Blum A. 2007. The fire retardant dilemma. Science 318:194–195.10. California Environmental Protection Agency. 2006. Polybrominated

diphenyl ethers: Recommendations to reduce exposure in California: Areport of the Cal/EPA PBDEworkgroup. Sacramento, California, USA.

11. Lorber M. 2008. Exposure of Americans to polybrominated diphenylethers. J Expo Sci Environ Epidemiol 18:2–19.

12. U.S. Environmental ProtectionAgency. 2009. Polybrominated diphenylethers (PBDEs) action plan. Washington, DC.

13. Holden A, Park JS, Chu V, Kim M, Choi G, Shi Y, Chin T, Chun C,Linthicum J, Walton BJ, Hooper K. 2009. Unusual hepta- andoctabrominated diphenyl ethers and nonabrominated diphenyl etherprofile in California, USA, peregrine falcons (Falco peregrinus): Moreevidence for brominated diphenyl ether-209 debromination. EnvironToxicol Chem 28:1906–1911.

14. Stapleton HM, Dodder NG. 2008. Photodegradation of decabromodi-phenyl ether in house dust by natural sunlight. Environ Toxicol Chem27:306–312.

15. Allen JG, McClean MD, Stapleton HM, Webster TF. 2008. Criticalfactors in assessing exposure to PBDEs via house dust. Environ Int34:1085–1091.

16. Sjodin A, Papke O, McGahee E, Focant JF, Jones RS, Pless-Mulloli T,Toms LM, Herrmann T, Muller J, Needham LL, Patterson DG Jr. 2008.Concentration of polybrominated diphenyl ethers (PBDEs) in householddust from various countries. Chemosphere 73:S131–136.

17. Wilford BH, Shoeib M, Harner T, Zhu J, Jones KC. 2005. Poly-brominated diphenyl ethers in indoor dust in Ottawa, Canada:implications for sources and exposure. Environ Sci Technol 39:7027–7035.

18. Edinboro CH, Scott-Moncrieff JC, Janovitz E, Thacker HL, GlickmanLT. 2004.Epidemiologic study of relationships between consumption ofcommercial canned food and risk of hyperthyroidism in cats. J Am VetMed Assoc 224:879–886.

19. Peterson ME, Ward CR. 2007. Etiopathologic findings of hyper-thyroidism in cats. Vet Clin North Am Small Anim Pract 37:633–645.

20. Buffington CA. 2002. External and internal influences on disease risk incats. J Am Vet Med Assoc 220:994–1002.

21. Kass PH, PetersonME, Levy J, JamesK, BeckerDV, Cowgill LD. 1999.Evaluation of environmental, nutritional, and host factors in cats withhyperthyroidism. J Vet Intern Med 13:323–329.

22. Olczak J, Jones BR, Pfeiffer DU, Squires RA, Morris RS, Markwell PJ.2005. Multivariate analysis of risk factors for feline hyperthyroidism inNew Zealand. N Z Vet J 53:53–58.

23. Wakeling J, Everard A, Brodbelt D, Elliott J, Syme H. 2009. Riskfactors for feline hyperthyroidism in the UK. J Small Anim Pract 50:406–414.

24. Costa LG, Giordano G, Tagliaferri S, Caglieri A, Mutti A. 2008.Polybrominateddiphenyl ether (PBDE)flameretardants:Environmentalcontamination, human body burden and potential adverse health effects.Acta Biomed 79:172–183.

25. Darnerud PO. 2003. Toxic effects of brominated flame retardants inmanand in wildlife. Environ Int 29:841–853.

26. Darnerud PO, AuneM, Larsson L, Hallgren S. 2007. Plasma PBDE andthyroxine levels in rats exposed to Bromkal or BDE-47. Chemosphere67:S386–392.

27. Richardson VM, Staskal DF, Ross DG, Diliberto JJ, DeVito MJ,BirnbaumLS.2008.Possiblemechanismsof thyroidhormonedisruptionin mice by BDE 47, a major polybrominated diphenyl ether congener.Toxicol Appl Pharmacol 226:244–250.

28. Lee E, Kim TH, Choi JS, Nabanata P, Kim NY, Ahn MY, Jung KK,Kang IH, Kim TS, Kwack SJ, Park KL, Kim SH, Kang TS, Lee J,Lee BM, Kim HS. 2010. Evaluation of liver and thyroid toxicity inSprague-Dawley rats after exposure to polybrominated diphenyl etherBDE-209. J Toxicol Sci 35:535–545.

29. Dye JA, Venier M, Zhu L, Ward CR, Hites RA, Birnbaum LS. 2007.Elevated PBDE levels in pet cats: sentinels for humans? Environ SciTechnol 41:6350–6356.

30. Fischer D, Hooper K, Athanasiadou M, Athanassiadis I, Bergman A.2006.Children showhighest levels of polybrominated diphenyl ethers ina California family of four: A case study. Environ Health Perspect114:1581–1584.

31. Toms LM, SjodinA, Harden F, Hobson P, Jones R, Edenfield E,MuellerJF. 2009. Serum polybrominated diphenyl ether (PBDE) levels arehigher in children (2–5 years of age) than in infants and adults. EnvironHealth Perspect 117:1461–1465.

32. Rose M, Bennett DH, Bergman A, Fangstrom B, Pessah IN, Hertz-Picciotto I. 2010. PBDEs in 2–5-year-old children from California andassociations with diet and indoor environment. Environ Sci Technol44:2648–2653.

33. Lunder S, Hovander L, Athanassiadis I, BergmanA. 2010. Significantlyhigher polybrominated diphenyl ether levels in youngU.S. children thanin their mothers. Environ Sci Technol 44:5256–5262.

34. Park JS, LinderholmL, CharlesMJ, AthanasiadouM, Petrik J, KocanA,Drobna B, Trnovec T, Bergman A, Hertz-Picciotto I. 2007. Polychlori-nated biphenyls and their hydroxylated metabolites (OH-PCBS) inpregnant women from eastern Slovakia. Environ Health Perspect115:20–27.

35. Rogers E, Petreas M, Park JS, Zhao G, Charles MJ. 2004. Evaluation offour capillary columns for the analysis of organochlorine pesticides,polychlorinated biphenyls, and polybrominated diphenyl ethers inhuman serum for epidemiologic studies. JChromatogrBAnalyt TechnolBiomed Life Sci 813:269–285.

36. Phillips DL, Pirkle JL, Burse VW, Bernert JT Jr, Henderson LO,Needham LL. 1989. Chlorinated hydrocarbon levels in human serum:Effects of fasting and feeding. Arch Environ Contam Toxicol 18:495–500.

37. Wang Y, Park JS, GuoW, Zota A, PetreasM. 2010. Analysis of PBDEs,PCBs, organochlorinepesticides, andnewBFRalternatives inCaliforniapregnant women by high resolutionmass spectrometry.OrganohalogenCompd 72:181–184.

38. Court MH, Greenblatt DJ. 1997. Molecular basis for deficientacetaminophen glucuronidation in cats: An interspecies comparisonof enzyme kinetics in liver microsomes. Biochem Pharmacol 53:1041–1047.

39. Center for Disease Control and Prevention. 2009. Fourth NationalReport on Human Exposure to Environmental Chemicals. Atlanta,GA, USA.

40. Deutch B, Pedersen HS, Asmund G, Hansen JC. 2007. Contaminants,diet, plasma fatty acids and smoking in Greenland 1999–2005. Sci TotalEnviron 372:486–496.


high polybrominated diphenyl ether levels in california house cats: house dust a primary source?

Documents