Occurrence of benzophenone-3 in indoor air from Albany, New York, USA, and its implications for inhalation exposure

Science of the Total Environment 537 (2015) 304–308

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Occurrence of benzophenone-3 in indoor air from Albany, New York, USA, and its implications for inhalation exposure Yanjian Wan a,b, Jingchuan Xue a, Kurunthachalam Kannan a,c,⁎ a Wadsworth Center, New York State Department of Health, and Department of Environmental Health Sciences, School of Public Health, State University of New York at Albany, Empire State Plaza, P.O. Box 509, Albany, NY 12201-0509, United States b Center for Disease Control and Prevention of Yangtze River Administration and Navigational Affairs, General Hospital of the Yangtze River Shipping, Wuhan 430019, China c Biochemistry Department, Faculty of Science and Experimental Biochemistry Unit, King Fahd Medical Research Center, King Abdulaziz University, Jeddah 21589, Saudi Arabia

H I G H L I G H T S

G R A P H I C A L

A B S T R A C T

• Benzophenones were determined in 81 indoor air samples. • Benzophenone-3 ranged from 0.19 to 72.0 ng/m3 with the highest levels in cars. • Inhalation exposure dose to benzophenone-3 ranged from 0.42 to 1.50 ng/kg-bw/d. • The contribution of inhalation to total benzophenone-3 intake was b5%.

a r t i c l e

i n f o

Article history: Received 25 June 2015 Received in revised form 30 July 2015 Accepted 5 August 2015 Available online xxxx Editor: Adrian Covaci Keywords: Benzophenone-3 Indoor air Human exposure UV filter Cosmetics

a b s t r a c t Benzophenone-3 (BP-3) is a widespread environmental contaminant and an estrogenic compound. Very little is known with regard to the occurrence in indoor air and the inhalation exposure of humans to BP-3. In this study, 81 indoor air samples were collected from various locations in Albany, New York, USA, in 2014 and analyzed for BP-3 by high performance liquid chromatography-tandem mass spectrometry (HPLC-MS/MS). BP-3 was found in all indoor air samples and the overall concentrations in bulk air (vapor plus particulate phases) were in the range of 0.19–72.0 ng/m3 (geometric mean: 2.67 ng/m3). The highest concentrations (geometric mean: 10.7 ng/m3) were found in cars, followed by barber shops (6.57) ˃ public places (5.75) N homes (3.27) ˃ offices (1.96) ˃ garages (1.04) ˃ laboratories (0.47). The estimated geometric mean daily intake (EDI) of BP-3 for infants, toddlers, children, teenagers, and adults through indoor air inhalation from homes was 1.83, 1.74, 1.18, 0.69, and 0.51 ng/kg-bw/day, respectively. Although high concentrations of BP-3 were measured in some microenvironments, the estimated contribution of indoor air to total BP-3 intake was b 5% of the total BP-3 intake in humans. This is the first survey on the occurrence of BP-3 in indoor air. © 2015 Elsevier B.V. All rights reserved.

⁎ Corresponding author at: Wadsworth Center, Empire State Plaza, P.O. Box 509, Albany, NY 12201-0509, United States. E-mail address: [email protected] (K. Kannan).

http://dx.doi.org/10.1016/j.scitotenv.2015.08.020 0048-9697/© 2015 Elsevier B.V. All rights reserved.

Y. Wan et al. / Science of the Total Environment 537 (2015) 304–308

1. Introduction

2. Materials and methods

Benzophenone-3 (2-hydroxy-4-methoxybenzophenone; BP-3) occurs naturally in some plants (IARC, 2012). BP-3 and its derivatives (e.g., BP-1, BP-8) are also commercially manufactured for use as a sunscreen in skin lotions, perfumes, and cosmetics to prevent UV-light from damaging scents and colors in such products (Liao and Kannan, 2014; Kim and Choi, 2014). BP derivatives are also used as UV-light stabilizers in plastic surface coatings and in polymers (Suzuki et al., 2005). Additionally, BP derivatives are used as UV-curing agents in sunglasses, and laundry and household cleaning products (IARC, 2012). Due to the extensive use, BP-3 is a widespread environmental contaminant and has been detected in the environment (Kim and Choi, 2014) and biological samples including human urine (Xue et al., 2015; Gao et al., 2015), serum (Hines et al., 2015; Tarazona et al., 2013), breast milk (Rodriguez-Gomez et al., 2015; Ye et al., 2008), amniotic fluid (Philippat et al., 2013), adipose fat (Wang et al., 2015) and placental tissue (Vela-Soria et al., 2011). Occurrence of BP-3 in 98% of urine samples collected from the United States population suggested that human exposure to this compound is widespread (Calafat et al., 2008). BP-3 has been reported to elicit estrogenic and anti-androgenic activities (Schlumpf et al., 2001; Schreurs et al., 2005; Suzuki et al., 2005) in laboratory studies. Hormonal balance and reproductive performances were affected by exposure to BP-3 in laboratory animals (Ozaez et al., 2014). Exposure to BP-3 derivatives in women has been associated with higher odds of developing endometriosis (Kunisue et al., 2012). A recent epidemiological study reported that elevated exposure of men to BP-type UV filters diminished couples' fecundity, resulting in a longer time to achieve pregnancy in women (Buck-Louis et al., 2014). Assessing the sources of human exposure to BP-3 is a subject of considerable interest, if we have to devise solutions to mitigate exposures. Thus far, BP-3 has been reported to occur in personal care products (Liao and Kannan, 2014), sediments and sewage sludge (Zhang et al., 2011), surface water (Poiger et al., 2004; Tsui et al., 2014), drinking water (Diaz-Cruz et al., 2012), foodstuffs (Balmer et al., 2005; Fent et al., 2010), and indoor dust (Wang et al., 2013). However, little is known on human exposure to BP-3 through inhalation of indoor air. Indoor air is a significant source of human exposure to contaminants such as polybrominated diphenyl ethers, perfluoroalkyl sulfonamides, siloxanes, and phthalates (Shoeib et al., 2004; Tran and Kannan, 2015a; Tran and Kannan, 2015b; Ma et al., 2014). Because of the widespread use of BP-3 in household as well as personal care products, this compound is expected to occur in indoor air, and inhalation can be an important route of human exposure. In this study, we conducted a survey of BP-3 in 81 indoor air samples collected in Albany, New York, USA (7 cars, 5 hair salons, 13 homes [day and night], 13 offices, 12 laboratories, 13 public places and 5 automobile [4 repairing, 1 parking] garages). BP-3 exposures via indoor air inhalation for various age groups (infants, toddlers, children, teenagers, and adults) were calculated on the basis of the measured concentrations. This is the first study to report the occurrence of BP-3 in indoor air.

2.1. Chemicals

305

BP-3 (98%), 2,4-dihydroxybenzophenone (BP-1 or UV-0, CAS# 131-56-6, 99%), 2,2′-dihydroxy-4-methoxybenzophenone (BP-8 or UV-24, CAS# 131-53-3, 98%), 2,2′,4,4′-tetrahydroxybenzophenone (BP-2, CAS# 131-55-5, 97%), and 4-hydroxybenzophenone (CAS# 1137-42-4, 98%) were purchased from Sigma-Aldrich (St. Louis, MO, USA). Isotopically-labeled BP-3 ( 13C 6 -BP-3, 99%, CLM-8525) was purchased from Cambridge Isotope Laboratories (Andover, MA, USA). Methanol and ethyl acetate were purchased from J. T. Baker (Phillipsburg, NJ, USA).

2.2. Sample collection and preparation Pre-cleaned polyurethane foam (PUF) plugs (ORBO-1000 PUF dimensions: 2.2 cm O.D × 7.6 cm length) were purchased from Supelco (Bellefonte, PA, USA). To test the background levels of BP-3, new PUF plugs (purchased from the vendor) were extracted with ethyl acetate and analyzed by liquid chromatography-tandem mass spectrometry (LC-MS/MS). It was found that each pair of newly purchased PUF plugs contained 3.59 ± 1.68 ng BP-3 (n = 5). Therefore, all PUF plugs required additional clean-up prior to use. PUF plugs were cleaned up by shaking with 100 mL of ethyl acetate for 30 min, twice. The cleaned PUFs were stored in a glass bottle, and kept in an oven at 100 °C until use. The quartz fiber filters (Whatman, grade QM-A, pore size: 2.2 μm with a particle retention rating at 98% efficiency in liquid, 32 mm diameter) were cleaned, and weighed before and after the collection of air samples as described earlier (Tran and Kannan, 2015b). Two PUF plugs and the quartz fiber filter were assembled in a glass tube as described earlier (Tran and Kannan, 2015b). All glassware used in sampling and analysis was rinsed with ethyl acetate and methanol and kept at 450 °C immediately prior to use. Indoor air samples were collected for 3 to 24 h by a low-volume air sampler (LP-20; A.P. Buck Inc., Orlando, FL, USA) at a flow rate of 5 L/min. Air samples (both PUFs and quartz fiber filters) were kept in glass bottles for no longer than 2 days prior to analysis. The samples were collected from September to December 2014 at several locations in Albany, New York, USA. The sampling locations were grouped into 7 categories: homes, offices, laboratories, cars, barber shops, automobile garages, and public places (e.g., shopping malls). Prior to analysis, samples (both PUFs and filters) were spiked with 10 ng of 13C6-BP-3 as an internal standard. PUF plugs were extracted by shaking in an orbital shaker (Eberbach Corp., Ann Arbor, MI, USA) with 100 mL ethyl acetate for 30 min, twice. The particulate samples were extracted with ethyl acetate by shaking for three times, 5 min every time. The extracts were concentrated in a rotary evaporator at 40 °C to approximately 5 mL, transferred to a 12-mL glass tube and concentrated by a gentle stream of nitrogen to exactly 1 mL, and then transferred into a glass vial.

Table 1 Concentrations of BP-3 in the particulate phase (μg/g), vapor phase (ng/m3) and bulk air (ng/m3) of indoor air samples collected from various locations in Albany, New York, USA in 2014. Locations

Barber shops Cars Homes Labs Offices Public places Garages Total

n

5 7 26 12 13 13 5 81

⁎ GM = geometric mean.

Vapor phase (ng/m3)

Particulate phase (μg/g)

Bulk air (ng/m3)

⁎GM

Median

Range

GM

Median

Range

GM

Median

Range

29.4 66.4 32.5 21.4 61.9 50.7 8.81 35.5

14.6 43.9 31.2 21.7 70.7 48.8 8.15 32.0

8.64–189 17.9–477 4.69–205 5.69–218 13.1–171 21.5–147 3.58–23.2 3.58–477

3.96 5.28 1.53 0.05 0.51 1.50 0.56 0.85

3.42 13.3 1.64 0.08 0.59 1.18 0.58 0.93

1.90–13.7 0.20–70.0 0.07–18.0 bLOQ–0.20 0.04–9.18 0.39–12.2 0.30–0.88 bLOQ–70.0

6.57 10.7 3.27 0.47 1.96 5.75 1.04 2.67

5.39 18.3 2.92 0.42 2.09 4.71 0.85 2.91

2.95–19.4 1.57–72.0 1.15–24.7 0.19–4.06 0.43–11.9 2.57–13.9 0.59–2.74 0.19–72.0

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Y. Wan et al. / Science of the Total Environment 537 (2015) 304–308 13 C6-BP-3 spiked into each samples ranged from 83% to 106%. Quantification was performed by the isotope-dilution method.

2.5. Calculation of daily exposure doses Based on the concentrations of BP-3 measured in indoor air samples, estimated daily intake (EDI; ng/kg bw/day) of BP-3 through indoor air inhalation was calculated as shown in Eq. (1) (USEPA, 2011): EDIinh ¼ C  AIR  IEF=BW

ð1Þ

where C is the concentration of BP-3 in indoor air samples (ng/m3), AIR is the air inhalation rate (m3/day), IEF is the indoor exposure fraction (the fraction of time spent indoors) and BW is the body weight (kg). We assumed an absorption efficiency of 100% for BP-3 from indoor air to systemic blood circulation although there exists uncertainty in absorption factors. Details of the parameters and data used in EDIinh calculation are shown in Table S1 and Table S2 (Supporting Information). 2.6. Statistical analysis Fig. 1. Concentrations (GM, ng/m3) of BP-3 in vapor phase and bulk air of indoor air samples (n = 81) collected from various locations in Albany, New York, USA.

2.3. Instrumental analysis Identification and quantification of target analytes were accomplished with a Shimadzu Prominence Modular HPLC system (Shimadzu Corporation, Kyoto, Japan), interfaced with an Applied Biosystems API 3200 electrospray triple quadrupole mass spectrometer (ESI-MS/MS; Applied Biosystems, Foster City, CA, USA). Ten microliters of the extract were injected onto a Betasil C18 column (2.1 mm × 100 mm, 5 μm; Thermo Electron Corporation, Waltham, MA, USA), which was connected to a Javelin guard column (Betasil C18, 20 × 2.1 mm; Thermo Electron Corporation). Further details of the HPLC and MS/MS parameters have been described earlier (Liao and Kannan, 2014).

2.4. Quality assurance and quality control The calibration curve was linear over a concentration range of 0.2 ng/mL to 100 ng/mL. Limit of quantitation (LOQ) for BP-3 was 0.2 ng/mL. Procedural blanks and matrix spike samples were included in each batch of 20 samples analyzed. BP-3 was found in procedural blanks without PUFs (0.23 ± 0.02 ng) or quartz filter (b LOQ, approximately 0.10 ng). The concentrations found in procedural blanks containing two PUFs (0.46 ± 0.16 ng) and one quartz filter (b LOQ, 0.1 ng) were subtracted from measured sample values. A mid-point calibration standard and methanol blank were injected after every 10 samples to monitor for drift in instrumental response and carry-over from previous injections. The relative recoveries of

Statistical analysis was performed with SPSS ver. 18. Geometric mean (GM), median, and concentration ranges were used to describe the results. Concentrations below the LOQ were substituted with a value equal to LOQ divided by the square root of 2 for the calculation of GM. Measured concentration values were not normally distributed and, therefore, were log-transformed for the analysis of variance (ANOVA) or t-test. Differences among groups were compared by oneway ANOVA with the Tukey test. All statistical tests were considered significant if the two-tailed p-value was b 0.05. 3. Results and discussion 3.1. Concentrations of BP-3 in particulate phase BP-3 was found in all indoor air samples, but other derivatives (BP-2, 4-hydroxybenzophenone and other possible metabolites of BP-3, BP-1, BP-8) (Wang et al., 2013) were not found in any of the samples. The concentrations of BP-3 in the particulate phase (Table 1) were calculated based on the weight of airborne particles collected in the glass fiber filter (ranged from 0.05 mg to 0.78 mg). The concentrations of BP-3 in the particulate phase ranged from 3.58 to 477 μg/g (GM: 35.5 μg/g, median: 32.0 μg/g). The highest concentrations of BP-3 were found in cars (GM: 66.4 μg/ g, median: 43.9 μg/g), which can be explained by use of specific products such as air fresheners. Personal care products such as perfumes and skin lotions are important sources of BP-3 in the indoor environment (Liao and Kannan, 2014; Kim and Choi, 2014), which might explain the high concentrations found in some air samples collected in cars and barber shops. Because airborne particles are a source of indoor dust after deposition, concentrations of BP-3 measured in airborne particles were

Table 2 Estimated daily intake (EDIinh, ng/day) to BP-3 through inhalation of indoor air, based on geometric mean, median and 95th percentile concentrations. Locations

Barber shops Cars Homes Labs Offices Public places Garages Total

EDIinh (ng/day), geometric mean

EDIinh (ng/day), median

EDIinh (ng/day), 95th percentile

Infants

Toddlers

Children

Teenagers

Adults

Infants

Toddlers

Children

Teenagers

Adults

Infants

Toddlers

Children

Teenagers

Adults

28.7 46.8 14.3 2.05 8.57 25.1 4.54 11.7

44.0 71.6 21.9 3.15 13.1 38.5 6.96 17.9

65.2 106 32.4 4.66 19.4 57.0 10.3 26.5

90.3 147 44.9 6.46 26.9 79.0 14.3 36.7

82.5 134 41.1 5.90 24.6 72.2 13.1 33.5

23.6 80.0 12.8 1.84 9.13 20.6 3.71 12.7

36.1 123 19.6 2.81 14.0 31.5 5.69 19.5

53.5 181 29.0 4.17 20.7 46.7 8.4 28.9

74.1 252 40.1 5.77 28.7 64.7 11.7 40.0

67.7 230 36.7 5.28 26.3 59.2 10.7 36.5

55.1 142 18.6 3.54 15.5 33.9 8.61 15.3

84.4 218 28.5 5.42 23.8 52.0 13.2 23.5

125 322 42.2 8.02 35.2 77.0 19.5 34.8

173 447 58.4 11.1 48.8 107 27.1 48.3

158 408 53.4 10.2 44.6 97.5 24.8 44.1

Y. Wan et al. / Science of the Total Environment 537 (2015) 304–308

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Table 3 Estimated daily intakes (EDIinh ng/kg bw/day) of BP-3 through inhalation of indoor air at different locations for various age groups. Locations

GM (ng/kg bw/day)

Barber shops Cars Homes Labs Offices Public places Garages Total

95th percentile (ng/kg bw/day)

Infants

Toddlers

Children

Teenagers

Adults

Infants

Toddlers

Children

Teenagers

Adults

3.68 5.99 1.83 0.26 1.10 3.22 0.58 1.50

3.49 5.69 1.74 0.25 1.04 3.06 0.55 1.42

2.38 3.87 1.18 0.17 0.71 2.08 0.38 0.97

1.39 2.26 0.69 0.10 0.41 1.22 0.22 0.56

1.03 1.68 0.51 0.07 0.31 0.90 0.16 0.42

7.06 18.2 2.38 0.45 1.99 4.35 1.10 1.97

6.70 17.3 2.26 0.43 1.89 4.12 1.05 1.87

4.56 11.8 1.54 0.29 1.29 2.81 0.71 1.27

2.66 6.87 0.90 0.17 0.75 1.64 0.42 0.74

1.98 5.10 0.67 0.13 0.56 1.22 0.31 0.55

compared with those reported in indoor dust. The median concentrations of BP-3 in airborne particles from homes (31.2 μg/g) in this study were 51 times higher than the concentration of BP-3 and its metabolites reported in indoor dust (612 ng/g) from homes in Albany, New York (Wang et al., 2013). The differences in the concentrations measured in airborne particles (b100 μm) and settled dust (up to 2 mm) may be related to the differences in particle sizes between these two matrices.

3.2. Concentrations of BP-3 in vapor phase and bulk air Similar to that found in particulate phase, none of the BP-3 derivatives was found in vapor phase. The concentrations of BP-3 found in vapor phase (GM: 0.85 ng/m3, median: 0.93 ng/m3, range: bLOQ-70.0 ng/m3) and bulk air (particulate plus vapor phases; GM: 2.67 ng/m3, median: 2.91 ng/m3, range: 0.19–72.0 ng/m3) are shown in Table 1. The concentrations of BP-3 determined in particulate phase, vapor phase and bulk air collected during day and night times in homes were not significantly different (Table S3). Statistical differences in the concentrations of BP-3 in bulk indoor air from various locations are presented in Table S4. The concentrations of BP-3 in vapor phase in barber shops (i.e., hair salons) were higher than in particulate phase, whereas BP-3 concentrations in laboratories, offices, and public places were much lower in vapor phase than those in particulate phase (Fig. 1). This difference may be related the presence of aerosols containing high concentrations of BP-3 released from cosmetics and hair care products used in barber shops. BP-3 concentrations as high as 6800 ng/g were found in hair care products from the United States (Liao and Kannan, 2014). It should be noted that several environmental factors including temperature, relative humidity, and amount and type of particulate matter can affect partitioning of BP-3 in air (Tran and Kannan, 2015a). The overall median ratio for concentrations of BP-3 between vapor phase and bulk air was 0.4, suggesting preferential partitioning of BP-3 to particulate phase. The log-Kow value of BP-3 was 4.0, which suggests its tendency to adsorb to suspended particles (Kim and Choi, 2014). Furthermore, BP-3 has a vapor pressure of 5.26 × 10−6, which suggests that it is relatively less volatile (Kim and Choi, 2014).

Table 4 Estimated daily intakes (EDI) of BP-3 calculated through indoor air inhalation in comparison with other pathways of exposure. Location

Age group

EDI (ng/day)

Route/medium

Reference

USA

Children Adults Adults

GM, 187 GM, 294 GM, 305

Wang et al., 2013 Liao and Kannan, 2014

Children Adults Children Adults

GM, 1.60 GM, 0.25 GM, 0.97 GM, 0.42

Urine Urine Personal care product/dermal Indoor dust/ingestion Indoor air/inhalation

This study

Wang et al., 2013

3.3. Human exposure to BP-3 via inhalation Factors such as age, time spent in indoor microenvironments (i.e., home, office/laboratory, and car), and the inhalation rate, can influence exposure doses (USEPA, 2011) (Table S2). The inhalation exposure to BP-3 was calculated based on the measured concentrations in the bulk air. For the estimation of daily intake (EDI) of BP-3 through inhalation, we categorized the population into five age groups: infants (b1 year), toddlers (1–3 years), children (4–11 years), teenagers (12–21 years), and adults (≥21 years) according to the U.S. Environmental Protection Agency's Exposure Factors Handbook (USEPA, 2011). The calculated exposure dose of BP-3 through inhalation from various microenvironments for adults (GM: 33.5 ng/day, median: 36.5 ng/day) is shown in Table 2. The exposure dose for adults from cars was the highest (GM: 134 ng/day, median: 230 ng/day), followed by barber shops, public places, homes, offices, garages, and laboratories, which were (GM for adults) 82.5, 72.2, 41.1, 24.6, 13.1 and 5.90 ng/day, respectively (Table 2). However, further studies are needed to evaluate BP-3 levels in bulk indoor air with only inhalable particulates and vapor phase. By taking body weight into consideration, the exposure doses from indoor air calculated for infants, toddlers and children were 2–3 times higher (GM: 1.83, 1.74, and 1.18 ng/kg bw/day, respectively) than those of teenagers and adults (GM: 0.69 and 0.51 ng/kg bw/day, Table 3). Significant difference (p b 0.01) was observed in the geometric means of EDIs (ng/kg-bw/day) between infants/toddlers and adults (Table S5). The inhalation exposure doses of BP-3 calculated in this study were similar to the values reported based on the ingestion of indoor dust (Table 4) (Wang et al., 2013), at 1.60 and 0.25 ng/kg bw/day for children and adults in the USA, respectively. It has been reported that the dermal exposure dose (based on dermal permeation factors of 0.001–1) to BP-3 from personal care products in the United States was 305 ng/kg bw/day (Liao and Kannan, 2014). BP-3 exposure doses from indoor air calculated (based on assumption that inhalation absorption rate was 100%) in this study (0.97 and 0.42 ng/kg bw/day for children and adults, respectively, Table 4) were two orders of magnitude lower than the exposure doses calculated from personal care products (Liao and Kannan, 2014) and based on the urinary concentrations of BP-3 and its metabolites (187 and 294 ng/kg bw/day for children and adults, respectively) (Wang et al., 2013). Thus, inhalation is a minor source of exposure to BP-3 by humans. In summary, the highest concentrations of BP-3 in indoor air samples were found in cars (geometric mean: 10.7 ng/m3), followed by barber shops (6.57) N public places (5.75) N homes (3.27) N offices (1.96) N garages (1.04) N laboratories (0.47). Although high concentrations of BP-3 were measured in some indoor air samples, the contribution of dust and indoor air to total BP-3 intake is minor (b5% of the total BP-3 intake). To our knowledge, this is the first study to describe the widespread occurrence of BP-3 in indoor air. The sources of high levels of BP-3 in certain indoor microenvironments need further investigation.

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