Science of the Total Environment 497–498 (2014) 467–474

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Phthalate diesters in Airborne PM2.5 and PM10 in a suburban area of Shanghai: Seasonal distribution and risk assessment Jing Ma a, Liu-lu Chen a, Ying Guo b,c, Qian Wu b,c, Ming Yang a, Ming-hong Wu a, Kurunthachalam Kannan b,c,d,⁎ a

School of Environmental and Chemical Engineering, Shanghai University, Shanghai 200444, China Wadsworth Center, New York State Department of Health, Albany, NY 12201-0509, USA Department of Environmental Health Sciences, School of Public Health, State University of New York at Albany, Albany, NY 12201-0509, USA d Biochemistry Department, Faculty of Science and Experimental Biochemistry Unit, King Fahd Medical Research Center, King Abdulaziz University, Jeddah 21589, Saudi Arabia b c

H I G H L I G H T S • Phthalate diesters are ubiquitous in atmospheric PM2.5 and PM10 • High concentrations of phthalates were found on PM2.5 in summer • Estimated cancer risk from DEHP in PM was below the USEPA's acceptable limit

a r t i c l e

i n f o

Article history: Received 18 April 2014 Received in revised form 4 August 2014 Accepted 4 August 2014 Available online xxxx Editor: Eddy Y. Zeng Keywords: PM2.5 PM10 Phthalate diesters Incremental lifetime cancer risks Air pollution

a b s t r a c t Concentrations of nine phthalate diesters in 24-h airborne PM2.5 and PM10 were determined from October 2011 to August 2012 in a suburban area in Shanghai, China. Dimethyl phthalate (DMP), diethyl phthalate (DEP), di-n-butyl phthalate (DBP), di-iso-butyl phthalate (DIBP), benzyl butyl phthalate (BzBP), and di(2ethylhexyl) phthalate (DEHP) were frequently detected in airborne particulate matter at sum concentrations of these six compounds ranging from 13.3 to 186 ng/m3, with an average value of 59.8 ng/m3 in PM2.5, and from 10.1 to 445 ng/m3, with an average value of 132 ng/m3 in PM10. DEHP, DBP, and DIBP were the major phthalate diesters found in PM samples. DEHP was found predominantly in coarse (size fraction of between PM2.5 and PM10) particles, whereas DMP, DEP, DBP, DIBP, and BzBP were found predominantly in fine (PM2.5) particles. The concentrations of phthalates in PM during warm months (207 ng/m3 for PM10 and 71.9 ng/m3 for PM2.5, on average) were significantly higher than those during cold months (76.9 ng/m3 for PM10 and 50.4 ng/m3 for PM2.5). Significant positive correlations were found between concentrations of total phthalates, DEHP, and BzBP, with the total mass and organic carbon content of PM. Based on the concentrations of DEHP, incremental lifetime cancer risks (ILCR) from inhalation exposure were estimated using a Monte Carlo simulation. Although the 95% probabilities for the ILCR values for the general population were below the U.S. Environmental Protection Agency (EPA) threshold of 10−6, our result is an underestimate of the actual health risk because we only considered the outdoor inhalation exposure to DEHP in this study. © 2014 Elsevier B.V. All rights reserved.

1. Introduction Air pollution remains a major global public health issue (Yang and Holgate, 2013). A key outdoor air pollutant of concern is particulate matter (PM). PM, especially fine particles (PM2.5, particle size below 2.5 μm), due to their small size and abundance, can be inhaled through the nasal pharynx and mouth, reach the lungs, and be deposited in the

⁎ Corresponding author at: Wadsworth Center, New York State Department of Health, Empire State Plaza, PO Box 509, Albany, NY 12201-0509, USA. Tel.: +1 518 474 0015; fax: +1 518 473 2895. E-mail address: [email protected] (K. Kannan).

http://dx.doi.org/10.1016/j.scitotenv.2014.08.012 0048-9697/© 2014 Elsevier B.V. All rights reserved.

alveoli (Kim et al., 1994; Gunasekar and Stanek, 2011). The adverse effects of PM2.5 exposure on human health have been consistently demonstrated in numerous epidemiological studies (Harrison and Yin, 2000; WHO, 2005; Abou Chakra et al., 2007; Akyüz and Cabuk, 2009). Concerned that these particles cause a wide range of health effects, the World Health Organization (WHO) developed guidelines for addressing the risks from PM exposure. Recently, the International Agency for Research on Cancer (IARC) declared that lung cancer caused by air pollution is primarily due to the fine particles present in the air (Straif et al., 2013). The exact mechanisms of injury and the chronic/acute health risks instigated by airborne fine PM have not been fully understood. Further, morphological properties, chemical composition, mineral content, or microbial flora associated with PM have not been adequately

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characterized. Currently, the general consensus is that harmful contaminants, such as heavy metals (lead, cadmium, mercury, and others) (Pandey et al., 2013; Wu et al., 2013; Zhang et al., 2013), and organic compounds (polycyclic aromatic hydrocarbons [PAHs]), chlorinated PAHs, oxygenated PAHs, PCBs, dioxin, and furans) (Gilli et al., 2007; Lundstedt et al., 2007; Ohyama et al., 2007; Skarek et al., 2007; Aristizábal et al., 2011; Ristovski et al., 2012; Ma et al., 2013) absorbed on the surface of PM play a key role in increasing toxicity, leading to inflammation, oxidative stress, and activation of the innate immune system (Yang and Holgate, 2013). To our knowledge, limited earlier studies have determined phthalate diesters in airborne fine particles, especially in Shanghai, China, where air pollution has become a major concern in recent years (Salgueiro-Gonzalez et al., 2013). Phthalate diesters are produced in large volumes for use as plasticizers in PVC plastics, personal care products, food packaging, children's toys, and building materials (Chen et al., 2012). There is a wealth of data on the distribution of phthalates in environmental media, including surface water, air, soil, sediment, indoor dust, and foodstuffs (Fromme et al., 2002; Peijnenburg and Struijs, 2006; Guo and Kannan, 2011; Salapasidou et al., 2011; Yang et al., 2013). A few studies have examined phthalate exposure in humans through dietary intake and dust ingestion (Wensing et al., 2005; Guo and Kannan, 2011; Chen et al., 2012). Studies with regard to carcinogenic risk of phthalates through inhalation exposure, however, are quite limited (Pei et al., 2013). The objectives of this study were to determine concentrations and profiles of nine phthalate diesters in PM10 and PM2.5 in suburban air collected from Shanghai during the summer and winter seasons and to evaluate the factors (PM mass and organic carbon [OC]) that influence the concentrations in PM. Moreover, exposure dose and incremental lifetime cancer risk (ILCR) for the general population in suburban areas of Shanghai were investigated using a Monte Carlo simulation of phthalate concentrations measured in airborne PM.

The method for the analysis of phthalate diesters was similar to that described previously (Guo and Kannan, 2011). Briefly, a portion (4 cm × 7 cm) of each quartz filter sample was extracted in a 12-mL glass tube after being cut into small pieces. Samples were spiked with 50 ng of deuterated (d4) internal standards of all target analytes and allowed to equilibrate for 3 h at room temperature. Samples were extracted three times with 4 mL of n-hexane:acetone (4:1, v:v) by ultrasonication for 30 min, followed by shaking in an orbital shaker for 20 min each time. After centrifugation at 4000 rpm for 5 min, the combined extracts were concentrated under a gentle stream of nitrogen to 1 mL, for gas chromatography coupled with mass spectrometry (GC/MS, 6890 N/5973, Agilent Technologies, Santa Clara, CA, USA) analysis. GC separation was accomplished by a 30-m DB-5 fused silica capillary column (30 m length × 0.25 mm i.d., 0.25 μm film thickness). Aliquots of 1 μL of extract were injected in splitless mode at 280 °C. The column oven temperature was programmed from 80 °C (1 min hold) to 180 °C at 12 °C/min (1 min), was raised to 230 °C at 6 °C/min, then increased to 270 °C at 8 °C/min (2 min), and finally raised to 300 °C at 30 °C/min (12 min). The MS was operated in an electron impact (70 eV) selected ion monitoring (SIM) mode. Ions m/z 163, 279, and 149 were monitored for the identification and quantification of DMP, DNOP, and seven other phthalates, respectively. The fragment ion m/z 177 was monitored for confirmation of DEP, m/z 223 for DIBP and DBP, m/z 223 and 206 for BzBP, 167 for DCHP, m/z 167 and 279 for DEHP, and m/z 279 for DNHP.

2. Materials and Methods

2.3. Quality Assurance and Quality Control

2.1. Sample Collection and Standards

Only glass tubes and glass pipettes were used in extraction, and cleanup steps and all glassware were baked at 450 °C for 6 h prior to use. Phthalate concentrations were determined from calibration curves of native (target) and internal standards, prepared at concentrations ranging from 5 to 2000 ng/mL. For each batch of 10 samples, a solvent blank (n-hexane, n = 7), a laboratory blank (baked clean quartz filter, n = 7), and a field blank (clean filters exposed to the same field conditions as the sample, n = 7) were analyzed to monitor for contamination arising from sampling and analytical procedures. The average recoveries of deuterated internal standards spiked into individual samples were 78 ± 6% for d-DMP, 82 ± 5% for d-DEP, 84 ± 7% for d-DIBP, 85 ± 7% for d-DBP, 86 ± 8% for d-DNHP, 89 ± 9% for d-BzBP, 87 ± 8% for d-DCHP, 87 ± 11% for d-DEHP, and 94 ± 16% for d-DNOP. Trace concentrations of DMP, DEP, DIBP, DBP, BzBP, and DEHP were detected in laboratory and field blanks, with average respective concentrations of 4.2, 11.8, 110, 52, 0.95, and 201 pg/m3; these concentrations were subtracted from sample values. The limit of quantification (LOQ) was calculated from the lowest concentration of the calibration curve and the sample volume collected; the LOQ was 0.05 ng/m3 for all target analytes. Concentrations below the LOQ were assigned a value of zero for statistical analysis. Data analysis was performed using SPSS Version 15.0. Statistical significance was set at p b 0.05.

Atmospheric PM10 and PM2.5 were collected at the rooftop (approximately 20 m above ground level) of a building on the campus of Shanghai University in the Baoshan District, Shanghai (latitude 31°19' N, longitude 121°23' E). The sampling site is 1.5 km from the nearest highway, which has heavy traffic and is surrounded by small cement and chemical industrial plants as well as by residential areas. The sampling site is a typical suburban residential area in China. Samples were collected for 24 h on quartz fiber filters (GM-A, 20.3 cm × 25.4 cm, PALL Pallflex Inc., Ann Arbor, MI, USA), with two high-volume air samplers (GUV-15HBL1, Thermo Andersen, Smyrna, GA, USA) equipped with a cutting head for 2.5 μm and 10 μm particle sizes. The samplers were operated at a constant flow rate of 1.13 m 3 /min. Each sample of 24-h duration was collected every six days, for a period of 10 months (from October 26, 2011, to August 7, 2012). During the days of wet precipitation, air sampling was delayed until the weather became clear. A total of 77 24-h samples were collected during the study period. Prior to sampling, all of the quartz filters were baked at 450 °C for 6 h to remove adsorbed organic contaminants and then wrapped in clean aluminum foil. After the collection of samples, the filters were wrapped in pre-cleaned aluminum foil, sealed in polyethylene bags, and stored at − 29 °C until extraction. The field blanks comprising quartz filters that had been maintained at 40% relative humidity and at 20 °C for over 48 h were weighed before and after sampling, sealed in polyethylene bags, and stored at −29 °C, similar to the process followed with the actual samples. Dimethyl phthalate (DMP), diethyl phthalate (DEP), di-n-butyl phthalate (DBP), di-iso-butyl phthalate (DIBP), benzyl butyl phthalate (BzBP), bis (2-ethylhexyl) phthalate (DEHP), di-n-hexyl phthalate

(DNHP), dicyclohexyl phthalate (DCHP), di-n-octyl phthalate (DNOP), and their corresponding d4 (deuterated) internal standards (except for BzBP) were purchased from AccuStandard, Inc. (New Haven, CT, USA), with a purity of N 99%. 2.2. Chemical and Instrumental Analysis

3. Results and Discussion 3.1. Size association and seasonal distribution of phthalates in PM2.5 and PM10 The concentrations of individual and total phthalate diesters associated with airborne PM2.5 and PM10 are illustrated in Fig. 1 (additional details are presented in Table S1 and Table S2 in the Supplementary

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Fig. 1. Concentrations of (A) PM2.5-bound total phthalates and DEHP (ng/m3), and mass concentrations of PM2.5 (μg/m3), (B) PM10-bound total phthalates and DEHP (ng/m3), and mass concentrations of PM10 (μg/m3), (C) mean concentrations of phthalate compounds (ng/m3) in airborne PM2.5 (n = 39), (D) mean concentrations of phthalate compounds (ng/m3) in airborne PM10 (n = 38) in suburban air in Shanghai, China, during the sampling period of October 2011–August 2012. (For interpretation of the references to colour in this figure, the reader is referred to the web version of this article.)

Data). Six of the nine target phthalate diesters (DMP, DEP, DBP, DIBP, BzBP, and DEHP) were found at detection rates of 56% to 100%, both in PM2.5 and PM10, while DIBP, DBP, and DEHP were found in 100% of the PM samples analyzed. The mean and median concentrations of total phthalate diesters in PM10 were 132 ng/m3 and 95.3 ng/m3, respectively, with a range of 10.1–445 ng/m3. The mean and median concentrations of total six phthalate diesters in PM2.5 were 59.8 ng/m3 and 47.0 ng/m3 , respectively, with a range of 13.3–186 ng/m3 ; these values were significantly lower than the concentrations found in PM10 (p b 0.01, one sample t-test). The concentrations of total and individual phthalates in PM10 and PM2.5 were log-normally distributed (Kolmogorov–Smirnov test, p N 0.05). Among the nine phthalates analyzed, DEHP, DBP, and DIBP were the dominant compounds found in PM. The average concentrations of these three compounds were 125–900 times higher than the concentrations of the next three major phthalate diesters (DMP, DEP, and BzBP). Concentrations of DEHP were 7 and 3 times higher than the concentrations of DIBP in PM10 and PM2.5, respectively, and were 14 and 6 times higher than the concentrations of DBP in PM10 and PM2.5, respectively. On average, 63% of DEHP concentrations were associated with coarse (size distribution between PM2.5 and PM10) particles; other detectable phthalate diesters were found predominantly in (70%) fine (PM2.5) particles. This result suggests preferential sorption of the majority of phthalates on the surface of fine particles, which can be attributed to large specific surface area of fine particles. The profile of concentrations of phthalates in PM, DEHP N DIBP N DBP, is consistent with the data reported previously in organic aerosols (Wang et al., 2006) and in indoor dust samples from China (Guo and Kannan, 2011). The concentrations of phthalates in summer months (on average, 207 ng/m3 in PM10 and 71.9 ng/m3 in PM2.5) were significantly higher than those in winter months (76.9 ng/m3 in PM10 and 50.4 ng/m3 in PM2.5) (Fig. 2). A similar pattern was reported in other cities in China

(Wang et al., 2006). Phthalate diesters are not covalently bound to polymeric matrixes, and they are semi-volatile compounds. Therefore, an increase in ambient temperature can increase their emission rates from plastic products, which would contribute to high levels of phthalates in the air during warmer months (Thuren and Larsson, 1990; Fujii et al., 2003; Clausen et al., 2012). However, it was reported

Fig. 2. Concentrations of phthalate diesters (ng/m3; sum of nine diesters) in PM2.5 during winter months (A, n = 22) and summer months (B, n = 17); in PM10 during winter months (C, n = 22) and summer months (D, n = 16) during 2011–2012 in Shanghai (from this study). Whisker boxes show the range between the 25th and 75th percentiles. Asterisks indicate statically significant (p ≤ 0.01, one-sample t-test) higher concentrations in warmer months than in colder months both for PM2.5 and PM10. (For interpretation of the references to colour in this figure, the reader is referred to the web version of this article.)

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that the concentrations of phthalates decreased significantly with increasing temperature, which was attributed to photochemical reactions with atmospheric free radicals during summer months (Wang et al., 2008). Very few studies have reported the occurrence of phthalates in airborne particles. The sum concentration of DMP, DEP, DIBP, DBP, BzBP, and DEHP in PM2.5 aerosols from Shanghai in 2003 (Wang et al., 2006) was up to 341 ng/m3, and the concentration of DEHP alone was up to 277 ng/m3. The total concentration of six phthalate diesters and DEHP found in our study were significantly lower than those reported earlier in both winter and summer months (p ≤ 0.01), which suggests that phthalate concentrations in PM have decreased in the last decade in Shanghai, possibly due to an improvement in plastic waste disposal technology. Nevertheless, the mean concentration of DEHP in PM10 found in our study was 5–20 times higher than that reported from Thessaloniki, Greece (21.3 ng/m3 on average) (Salapasidou et al., 2011), Amsterdam, the Netherlands (11.9 ng/m3) (Peijnenburg and Struijs, 2006), and Paris, France (5.4 ng/m3) (Teil et al., 2006). The mean concentration of DEHP in PM2.5 in our study was 30 times higher than that reported for an urban area in Coruña, Spain (1.26 ng/m3) (Salgueiro-Gonzalez et al., 2013). In addition, relatively high concentrations of phthalates were found in PM2.5 in other cities in China, such as Xi'an (445 ng/m3), Chongqing (335 ng/m3), Guangzhou (332 ng/m3), Hangzhou (204 ng/m3), and Nanjing (134 ng/m3) (Wang et al., 2006, 2008). This comparison implies that air quality in China is still an issue, despite recent government policies on clean air. 3.2. Relationship of Particulate Mass, Organic Carbon, and Temperature with Phthalate Concentrations Significant positive correlations were found between the concentrations of total phthalates, DEHP, and BzBP, with mass and OC concentrations of PM of PM2.5 and PM10 (Table 1). The positive correlation of OC with phthalate concentrations suggests that these compounds sorb to organic matter (Ma et al., 2013). Not all phthalate diesters, however, were positively correlated with particle mass or OC, which might be attributed to the differences in gas-particle partitioning of phthalates. Phthalates, especially the low-molecular weight ones (e.g., DMP), are expected to partition preferentially into the vapor phase (Teil et al., 2006). In this study, a significant positive correlation between DEHP concentrations in PM and temperature was found. 3.3. Estimation of Vapor Phase Phthalate Concentrations from PM Once released into the atmosphere, phthalate diesters can be redistributed between gaseous (or vapor) and particulate phases (Teil et al., 2006). The gas-particle partitioning of phthalates can affect their transport, atmospheric residence time, deposition, and chemical transformation (Cousins and Mackay, 2001). We estimated the vapor phase concentrations of phthalate diesters in outdoor air through theoretical derivation of the distribution of compounds between the vapor phase

Table 2 Estimated concentrations of phthalates in gas phase (ng/m3) of ambient air through gasparticle partitioning. Compound

DMP DEP DIBP DBP BzBP DEHP sum

EPI Suite

Estimated gas phase concentration

log PL0 (Pa)a

Min

Max

Mean

−0.27 −0.56 −0.59 −1.80 −2.68 −4.72c -

NAb NA 2.20 2.82 NA 14.0 29.5

12.3 3.35 239 141 21.7 757 1140

1.24 0.57 59.1 25.4 0.89 172 260

Gas phase distribution between gas-particulate fractions 82.5% 80.1% 78.8% 76.3% 63.3% 61.7% 66.3%

a

Estimated by Antoine method. Not available. For DEHP a vapor pressure of PL0=1.9 × 10−5 Pa (log PL0 = −4.72) from Schossler et al., 2011 is used for calculations. b c

and particulate phase, as described by the partitioning coefficients (Kp) (Eq. (1)): K p ¼ ð F=PMÞ=A

ð1Þ

where Kp (m3/μg) is the gas-particle distribution coefficient, which can be estimated from the octanol–air portioning coefficient (KOA) or the vapor pressure of the subcooled liquid. PM is the mass concentration of particulate matter (μg/m3), and F and A are the concentrations of the target analytes in the particulate and vapor phases, respectively (ng/m3). The relationship between Kp and subcooled liquid vapor pressure, P0L (Schossler et al., 2011), of individual phthalate diesters is expressed as follows: 0

log K p ¼ mr log P L þ b

ð2Þ

Concentrations of phthalates in gaseous fraction were estimated using theoretical Kp values. Values of mr = − 0.0738 and b = − 2.74 for Eq. (2) were obtained experimentally by Wang et al. (2008) for phthalates in ambient air in China. Values of sub-cooled liquid vapor pressure of phthalates were estimated by the MPBPWIN v. 1.43 Antoine method from EPI Suite™ (v. 4.0), on the basis of air concentrations near saturation at room temperature (Schossler et al., 2011). Estimated gas phase concentrations of phthalate diesters in ambient air are shown in Table 2. P0L -based concentrations of phthalates in particle fractions ranged from 17% for DMP to 38% for DEHP. The reported concentrations of phthalates in particulate fractions in Paris ranged from 2% for DMP to 20% for DEHP, whereas they ranged from 26% for DMP to 43% for DEHP in an urban area of Thessaloniki, Greece (Teil et al., 2006; Salapasidou et al., 2011). The fraction of phthalates in the particulate phase ranged from 11% for DMP to 23% for DEHP in China (Wang et al., 2008).

Table 1 Relationships of phthalate diesters with particulate mass, organic carbon and temperature in airborne particulate matter in Shanghai, China. Compounds

DMP DEP DIBP DBP BzBP DEHP Total phthalates

PM2.5-bound

PM10-bound

PM

OC

Temp.

PM

OC

Temp.

−0.366⁎,a −0.330⁎ −0.245 −0.250 0.549⁎⁎ 0.712⁎⁎ 0.541⁎⁎

−0.366⁎ −0.312 −0.250 −0.253 0.556⁎⁎ 0.766⁎⁎ 0.557⁎⁎

−0.862⁎⁎ −0.702⁎⁎ −0.084 0.204 0.329⁎ 0.384⁎ 0.410⁎⁎

−0.117 −0.196 −0.154 −0.177 0.393⁎ 0.438⁎⁎ 0.363⁎

−0.089 −0.081 −0.107 −0.151 0.463⁎⁎ 0.502⁎⁎ 0.425⁎⁎

−0.844⁎⁎ −0.652⁎⁎

Correlation coefficient: ⁎⁎p b 0.01 (2-tailed), ⁎p b 0.05 (2-tailed).

a

−0.003 0.206 −0.009 0.545⁎⁎ 0.569⁎⁎

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Table 3 Parameters used in the probabilistic cancer risk assessment of DEHP in airborne particulate matter. Population groups

Gender

Body weight (BW, Kg)

Inhalation rate (IR, m3/d)

Exposure frequency (EF, d/year)

DEHP concentrationa (ng/m3)

Child (1–11 years) Adolescent (12–17 years) Adult (18–70 years)

Boys Girls Male Female Male Female

LNb (17.2, 6.3) LN (16.5, 6.2) LN (47.1, 9.8) LN (44.8, 7.4) LN (60.2, 2.9) LN (53.1, 2.8)

LN (14.1, 1.72)

Uc (200, 365)

LN(211, 190)

a b c

LN (32.13, 1.04) LN (32.73, 1.14)

Considering the DEHP concentrations both in PM and gas phase. LN: lognormal distribution with geometric mean and geometric standard deviation: LN (gm,gsd). U: uniform distribution with minimum and maximum: U (min, max).

3.4. Carcinogenic Risk Assessment for Inhalation Exposure to DEHP in Air When inhaled, PM10 particles can penetrate deep into the respiratory system, while PM2.5 can penetrate farther into the lungs and reach circulation (Marchwinska-Wyrwal et al., 2011). Exposure is expressed in terms of a lifetime average daily dose (LADD) and is calculated for the inhalation pathway. To further understand the potential carcinogenic risks elicited by inhalation of phthalates in ambient air, we estimated incremental lifetime cancer risk (ILCR) as the incremental probability of an individual's developing cancer over a lifetime. Only DEHP exposure was considered for this risk assessment, as this compound has been reported to possess carcinogenic potency (Guyton et al., 2009). The LADD and ILCR models quantitatively estimate the exposure risk for three age-groups: children (1–11 years), adolescents

(12–17 years), and adults (18–70 years), and they were calculated based on the following equations (USEPA, 1997a): LADD ¼

C  IR  EF  ED  cf BW  AT

ð3Þ

1

ILCR ¼ LADD 

CSF 

BW3 70

!! ð4Þ

where LADD is the lifetime average daily dose from inhalation (mg/kg/d); ILCR is the incremental lifetime cancer risk associated with inhalation; C is the DEHP concentration (ng/m3) in air (sum of the concentrations in PM2.5 and gas phase concentrations estimated from PM10, as described

Fig. 3. Cumulative probability of lifetime average daily dose (LADD) associated with inhalation (mg/kg/d) of DEHP in particulate matter by the general population in Shanghai (A: male (M) and female (F) adults; B: male and female adolescents (adole); C: boys and girls); the box and whisker plots are for DEHP-specific LADD (D). x-axis is the LADD value. (For interpretation of the references to colour in this figure, the reader is referred to the web version of this article.)

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above); BW is the body weight (kg) (The Ministry of Health of the People's Republic of China, 2006); IR is the inhalation rate (m3/d) (Liao and Chiang, 2006); EF is the exposure frequency (d/year); ED is the exposure duration (year); AT is the averaging time for carcinogens (365 × 70 = 25550 d); and cf is the conversion factor (10− 6). The cancer slope factor (CSF), which is used to estimate the risk, was normalized to account for extrapolation for different body weights from a standard 70 kg, and the CSF for DEHP inhalation exposure was 0.014 (mg/kg/d)− 1 (USEPA, 1997b). The values of C (for DEHP), EF, and BW applied in Eqs. (3) and (4) were derived probabilistically and presented in Table 3. The LADD and ILCR values were calculated based on a Monte Carlo simulation, which was performed using Crystal Ball software (Version 2002.2, Decisioneering, Inc., Denver, CO, USA) with independent runs of 5,000 trials. The LADD estimates of DEHP for various age-groups of the general population are shown in Fig. 3. The LADDs of DEHP stratified by age and the ranking of exposure dose in decreasing order were: adults (from 4.66 × 10−5 to 8.54 × 10−5 mg/kg/d) N children (from 3.41 × 10−7 to 8.39 × 10−5 mg/kg/d) N adolescents (from 4.23 × 10− 6 to 1.68 × 10− 5 mg/kg/d). Females showed higher exposure doses than did males in adult and adolescent groups, whereas boys and girls had similar exposure doses. The estimated LADD of B[a]Peq through inhalation for temple workers in Taiwan was 10− 5 mg/kg/d (Chiang et al., 2009). In our study, median and mean LADDs of DEHP for adults and children were similar (10−5 mg/kg/d), and this dose is similar to the total daily intake of DEHP through inhalation in the Yangtze River and the Pearl River Delta in China (Chen et al., 2012). The cumulative probability distributions of the calculated ILCR for the general population in a suburban area in Shanghai are presented in Fig. 4. According to the U.S. EPA, a one-in-a-million chance of developing cancer over a 70-year lifetime (ILCR = 10− 6) is considered

acceptable or inconsequential, whereas an additional lifetime cancer risk of one in ten thousand or greater (ILCR = 10−4) is considered serious. The estimated carcinogenic risks of airborne inhalation of DEHP for all population groups were between 1.04 × 10−6 and 8.23 × 10− 9, and these values were below the U.S. EPA's acceptable level of 10− 6, which indicates that the carcinogenic risk associated with inhalation of DEHP in the air in Shanghai is low. The ILCR values were in the decreasing order of adults N children N adolescents, for both males and females. The greater exposure duration of adults than that for children and adolescents contributed to higher ILCR values for that age-group. A lower body weight for children than that for adolescents resulted in higher ILCR values in children. Females showed slightly higher ILCR values than did males. A similar trend also was reported for cancer risk associated with PAH exposure through inhalation (Xia et al., 2013). The sensitivity analysis showed that concentrations of DEHP (C), exposure frequency (EF), and inhalation rate (IR) were the important predictors associated with the model, whereas body weight (BW) was a minor factor. Studies on (lung) cancer risk assessment for airborne phthalates are limited. Phthalates are not chemically bound to products and can be easily released into the indoor environment (Fujii et al., 2003). Carcinogenic risk of DEHP exposure through inhalation has been estimated for various age-groups in China; the ILCR values for children and adolescents (ages of 1 to 21 years) were several times higher than the U.S. EPA's acceptable limit (Pei et al., 2013). The major sources of phthalates in fine particles are diverse and include transportation, industrial processes, and emissions from plastic products used in the indoor environment. Thus, the inclusion of other sources of phthalate exposures, including indoor air, can augment of risk levels. Dietary intake was the dominant route of exposure to DEHP, whereas dermal absorption was a major route to DEP exposure in the Chinese adult population (Guo

Fig. 4. Cumulative probability of incremental lifetime cancer risk (ILCR) from inhalation exposure to DEHP in particulate matter by the general population in Shanghai (A: male (M) and female (F) adults; B: male and female adolescents (adole); C: boys and girls); the box and whisker plots are for DEHP-specific ILCR (D). x-axis is the ILCR value. (For interpretation of the references to colour in this figure, the reader is referred to the web version of this article.)

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and Kannan, 2011; Chen et al., 2012; Wang et al., 2013). Although inhalation accounted for a small percentage of the total intake, the potential for additive or synergistic effects between fine particles and toxic organic compounds (including phthalates, PAHs, ClPAHs, PBDEs, and dioxins) can increase the risk of developing lung cancer. In Shanghai, more than 13 million residents are exposed to a particulate matter level greatly exceeding the normal population exposure level in the Western countries (Zhang et al., 2006). Long-term studies are needed to better understand the sources of airborne fine PM, which may potentially lead to more targeted and effective pollution regulations to improve the quality of air in China. 4. Conclusions The phthalate diesters measured in the present study are ubiquitous in atmospheric PM2.5 and PM10 from a suburban area in Shanghai. DEHP, DBP, and DIBP were the major phthalate diesters found in PM samples. DEHP was found predominantly in coarse particles, whereas DMP, DEP, DBP, DIBP, and BzBP were found predominantly in fine particles. The concentrations of phthalates in PM during warm months were significantly higher than those during cold months. Furthermore, significant positive correlations were found between concentrations of total phthalates, DEHP, and BzBP, with the total mass and organic carbon content of PM. Although the 95% probabilities for the ILCR values for the general population estimated in this study were below the U.S. Environmental Protection Agency (EPA) threshold of 10− 6, further studies are needed to investigate the effects of long-term exposure to air pollution in Shanghai, a rapidly developing economic center in China. Furthermore, potential for additive or synergistic effects between fine particles and phthalates on human health needs to be studied; moreover, the actual health risks should take into consideration of both outdoor and indoor inhalation exposure to airborne organic contaminants. Conflicts of Interests None. Acknowledgements We acknowledge the financial support of the National Natural Science Foundation of China (nos. 21007039 and 31100376) and the Program for Innovative Research Team in University (no. IRT13078); Samples were analyzed at Wadsworth Center, New York State Department of Health. Appendix A. Supplementary Data Supplementary data to this article can be found online at http://dx. doi.org/10.1016/j.scitotenv.2014.08.012. References Abou Chakra OR, Joyeux M, Nerriere E, Strub MP, Zmirou-Navier D. Genotoxicity of organic extracts of urban airborne particulate matter: an assessment within a personal exposure study. Chemosphere 2007;66:1375–81. Akyüz M, Cabuk H. Meteorological variations of PM2.5/PM10 concentrations and particleassociated polycyclic aromatic hydrocarbons in the atmospheric environment of Zonguldak, Turkey. J Hazard Mater 2009;170:13–21. Aristizábal BH, Gonzalez CM, Morales L, Abalos M, Abad E. Polychlorinated dibenzo-pdioxin and dibenzofuran in urban air of an Andean city. Chemosphere 2011;85: 170–8. Chen LY, Zhao Y, Li L, Chen B, Zhang Y. Exposure assessment of phthalates in nonoccupational populations in China. Sci Total Environ 2012;427:60–9. Chiang KC, Chio CP, Chiang YH, Liao CM. Assessing hazardous risks of human exposure to temple airborne polycyclic aromatic hydrocarbons. J Hazard Mater 2009;166:676–85. Clausen PA, Liu Z, Kofoed-Sørensen V, Little J, Wolkoff P. Influence of temperature on the emission of di(2-ethylhexyl)phthalate(DEHP) from PVC flooring in the emission cell FLEC. Environ Sci Technol 2012;46:909–15.

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