Science of the Total Environment

Phthalate diesters in Airborne PM

_2.5

and PM

₁₀

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,

⁎

aSchool of Environmental and Chemical Engineering, Shanghai University, Shanghai 200444, China

bWadsworth Center, New York State Department of Health, Albany, NY 12201-0509, USA

cDepartment of Environmental Health Sciences, School of Public Health, State University of New York at Albany, Albany, NY 12201-0509, USA

dBiochemistry 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

•Phthalate diesters are ubiquitous in atmospheric PM2.5and PM10

•High concentrations of phthalates were found on PM2.5in summer

•Estimated cancer risk from DEHP in PM was below the USEPA's acceptable limit

a b s t r a c t 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

Concentrations of nine phthalate diesters in 24-h airborne PM2.5and PM10were 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(2- ethylhexyl) 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/m³in PM2.5, and from 10.1 to 445 ng/m³, with an average value of 132 ng/m³in PM10. DEHP, DBP, and DIBP were the major phthalate diesters found in PM samples. DEHP was found predominantly in coarse (size fraction of between PM2.5and PM10) particles, whereas DMP, DEP, DBP, DIBP, and BzBP were found predominantly infine (PM2.5) particles. The concentrations of phthalates in PM during warm months (207 ng/m³for PM10and 71.9 ng/m³ for PM2.5, on average) were significantly higher than those during cold months (76.9 ng/m³for PM10and 50.4 ng/m³for 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 simula- tion. Although the 95% probabilities for the ILCR values for the general population were below the U.S. Environ- mental 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, especiallyfine particles (PM2.5, particle size below 2.5μm), due to their small size and abundance, can be inhaled through the nasal pharynx and mouth, reach the lungs, and be deposited in the

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 ad- dressing 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 thefine particles present in the air (Straif et al., 2013). The exact mechanisms of injury and the chronic/acute health risks instigated by airbornefine PM have not been fully under- stood. Further, morphological properties, chemical composition, mineral content, or microbialflora associated with PM have not been adequately

⁎ 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:kkannan@wadsworth.org(K. Kannan).

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

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characterized. Currently, the general consensus is that harmful contami- nants, 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 airbornefine 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 plasti- cizers 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 inges- tion (Wensing et al., 2005; Guo and Kannan, 2011; Chen et al., 2012).

Studies with regard to carcinogenic risk of phthalates through inhala- tion 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 PM10and PM2.5in suburban air collected from Shanghai during the summer and winter seasons and to evaluate the factors (PM mass and organic carbon [OC]) that influ- ence the concentrations in PM. Moreover, exposure dose and incremen- tal 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.

2. Materials and Methods 2.1. Sample Collection and Standards

Atmospheric PM10and PM2.5were collected at the rooftop (approx- imately 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 high- way, 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 quartzfiberfilters (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 2.5μm and 10μm particle sizes. The samplers were operated at a constantflow rate of 1.13 m³/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 quartzfilters 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, thefilters were wrapped in pre-cleaned aluminum foil, sealed in polyethylene bags, and stored at−29 °C until extraction. Thefield blanks comprising quartzfilters that had been maintained at 40% relative humidity and at 20 °C for over 48 h were weighed before and after sampling, sealed in polyethyl- ene 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 correspondingd4(deuterated) internal standards (except for BzBP) were purchased from AccuStandard, Inc. (New Haven, CT, USA), with a purity ofN99%.

2.2. Chemical and Instrumental Analysis

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 quartzfilter 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 ofn-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., 0.25μmfilm thickness). Aliquots of 1μL 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 in- creased to 270 °C at 8 °C/min (2 min), andfinally 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. Ionsm/z163, 279, and 149 were monitored for the identification and quantification of DMP, DNOP, and seven other phthalates, respectively. The fragment ionm/z 177 was monitored for confirmation of DEP,m/z223 for DIBP and DBP,m/z223 and 206 for BzBP, 167 for DCHP,m/z167 and 279 for DEHP, andm/z279 for DNHP.

2.3. Quality Assurance and Quality Control

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 quartzfilter, n= 7), and afield blank (cleanfilters exposed to the samefield condi- tions 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% ford-DMP, 82 ± 5% ford-DEP, 84 ± 7% ford-DIBP, 85 ± 7%

ford-DBP, 86 ± 8% ford-DNHP, 89 ± 9% ford-BzBP, 87 ± 8% for d-DCHP, 87 ± 11% ford-DEHP, and 94 ± 16% ford-DNOP. Trace con- centrations of DMP, DEP, DIBP, DBP, BzBP, and DEHP were detected in laboratory andfield 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/m³for 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 atpb0.05.

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 associ- ated with airborne PM2.5and PM10are illustrated inFig. 1(additional details are presented in Table S1 and Table S2 in the Supplementary

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 PM2.5and 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 PM10were 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 PM2.5were 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(pb0.01, one samplet-test). The concentrations of total and individual phthalates in PM10and PM2.5were log-normally distributed (Kolmogorov–Smirnov test,pN0.05). Among the nine phthalates analyzed, DEHP, DBP, and DIBP were the dominant com- pounds found in PM. The average concentrations of these three com- pounds were 125–900 times higher than the concentrations of the next three major phthalate diesters (DMP, DEP, and BzBP). Concentra- tions of DEHP were 7 and 3 times higher than the concentrations of DIBP in PM10and PM2.5, respectively, and were 14 and 6 times higher than the concentrations of DBP in PM10and PM2.5, respectively. On average, 63% of DEHP concentrations were associated with coarse (size distribution between PM_2.5and 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 offine particles, which can be attributed to large specific surface area offine particles. The profile of concentrations of phthalates in PM, DEHPNDIBPNDBP, is consistent with the data re- ported 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/m³in PM10and 71.9 ng/m³in PM2.5) were significantly higher than those in winter months (76.9 ng/m³in PM10and 50.4 ng/m³in 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 poly- meric 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. 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 thisfigure, the reader is referred to the web version of this article.)

Fig. 2.Concentrations of phthalate diesters (ng/m³; sum of nine diesters) in PM2.5during winter months (A,n= 22) and summer months (B,n= 17); in PM10during 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-samplet-test) higher concentrations in warmer months than in colder months both for PM2.5and PM10. (For interpretation of the references to colour in thisfigure, the reader is referred to the web version of this article.)

that the concentrations of phthalates decreased significantly with in- creasing 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 air- borne 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 PM_2.5in 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 concentra- tions of phthalates were found in PM2.5in 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 concentra- tions of total phthalates, DEHP, and BzBP, with mass and OC concentra- tions of PM of PM2.5and 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 trans- formation (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

and particulate phase, as described by the partitioning coefficients (Kp) (Eq.(1)):

K_p¼ðF=PMÞ=A ð1Þ

whereKp(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), andFandAare the concentrations of the target analytes in the particulate and vapor phases, respectively (ng/m³).

The relationship betweenKpand subcooled liquid vapor pressure,PL0

(Schossler et al., 2011), of individual phthalate diesters is expressed as follows:

logK_p¼m_rlogP_L⁰þb ð2Þ

Concentrations of phthalates in gaseous fraction were estimated using theoreticalKpvalues. Values ofmr=−0.0738 andb=−2.74 for Eq.(2)were obtained experimentally byWang 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.PL0-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 PM2.5-bound PM10-bound

PM OC Temp. PM OC Temp.

DMP −0.366⁎,a −0.366⁎ −0.862⁎⁎ −0.117 −0.089 −0.844⁎⁎

DEP −0.330⁎ −0.312 −0.702⁎⁎ −0.196 −0.081 −0.652⁎⁎

DIBP −0.245 −0.250 −0.084 −0.154 −0.107 −0.003

DBP −0.250 −0.253 0.204 −0.177 −0.151 0.206

BzBP 0.549⁎⁎ 0.556⁎⁎ 0.329⁎ 0.393⁎ 0.463⁎⁎ −0.009

DEHP 0.712⁎⁎ 0.766⁎⁎ 0.384⁎ 0.438⁎⁎ 0.502⁎⁎ 0.545⁎⁎

Total phthalates 0.541⁎⁎ 0.557⁎⁎ 0.410⁎⁎ 0.363⁎ 0.425⁎⁎ 0.569⁎⁎

aCorrelation coefficient:⁎⁎pb0.01 (2-tailed),⁎pb0.05 (2-tailed).

Table 2

Estimated concentrations of phthalates in gas phase (ng/m³) of ambient air through gas- particle partitioning.

Compound EPI Suite Estimated gas phase concentration

Gas phase distribution between gas-particulate fractions

logPL0

(Pa)^a Min Max Mean

DMP −0.27 NA^b 12.3 1.24 82.5%

DEP −0.56 NA 3.35 0.57 80.1%

DIBP −0.59 2.20 239 59.1 78.8%

DBP −1.80 2.82 141 25.4 76.3%

BzBP −2.68 NA 21.7 0.89 63.3%

DEHP −4.72^c 14.0 757 172 61.7%

sum - 29.5 1140 260 66.3%

aEstimated by Antoine method.

b Not available.

c For DEHP a vapor pressure ofPL0

=1.9 × 10⁻⁵Pa (logPL0

=−4.72) fromSchossler et al., 2011is used for calculations.

3.4. Carcinogenic Risk Assessment for Inhalation Exposure to DEHP in Air

When inhaled, PM10particles can penetrate deep into the respira- tory system, while PM2.5can 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 calcu- lated 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 com- pound 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):

LADD¼CIREFED

BWAT cf ð3Þ

ILCR¼LADD CSF BW 70

1 3

!!

ð4Þ

where LADD is the lifetime average daily dose from inhalation (mg/kg/d);

ILCR is the incremental lifetime cancer risk associated with inhalation;

Cis the DEHP concentration (ng/m³) in air (sum of the concentrations in PM2.5and gas phase concentrations estimated from PM10,as described 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 concentration^a (ng/m³)

Child (1–11 years)

Boys LN^b(17.2, 6.3) LN (14.1, 1.72) U^c(200, 365) LN(211, 190)

Girls LN (16.5, 6.2)

Adolescent (12–17 years)

Male LN (47.1, 9.8) LN (32.13, 1.04)

Female LN (44.8, 7.4)

Adult (18–70 years)

Male LN (60.2, 2.9) LN (32.73, 1.14)

Female LN (53.1, 2.8)

aConsidering the DEHP concentrations both in PM and gas phase.

b LN: lognormal distribution with geometric mean and geometric standard deviation: LN (gm,gsd).

c U: uniform distribution with minimum and maximum: U (min, max).

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 interpre- tation of the references to colour in thisfigure, the reader is referred to the web version of this article.)

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 carcin- ogens (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 inTable 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 inFig. 3. The LADDs of DEHP stratified by age and the ranking of exposure dose in decreasing order were: adults (from 4.66 × 10⁻⁵to 8.54 × 10⁻⁵mg/kg/d)Nchildren (from 3.41 × 10⁻⁷to 8.39 × 10⁻⁵mg/kg/d)Nadolescents (from 4.23 × 10⁻⁶to 1.68 × 10⁻⁵mg/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]Peqthrough inhala- tion for temple workers in Taiwan was 10⁻⁵mg/kg/d (Chiang et al., 2009). In our study, median and mean LADDs of DEHP for adults and children were similar (10⁻⁵mg/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 inFig. 4. According to the U.S. EPA, a one-in-a-million chance of devel- oping 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 × 10⁻⁶and 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 adultsNchildrenNadolescents, 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 adoles- cents 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). Carcino- genic risk of DEHP exposure through inhalation has been estimated for various age-groups in China; the ILCR values for children and adoles- cents (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 infine particles are diverse and include transportation, industrial processes, and emissions from plastic products used in the indoor envi- ronment. 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 thisfigure, the reader is referred to the web version of this article.)

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 betweenfine 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 airbornefine PM, which may potentially lead to more targeted and effective pollution regula- tions to improve the quality of air in China.

4. Conclusions

The phthalate diesters measured in the present study are ubiquitous in atmospheric PM2.5and PM10from 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 infine par- ticles. 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 thefinancial 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 Depart- ment of Health.

Appendix A. Supplementary Data

Supplementary data to this article can be found online athttp://dx.

doi.org/10.1016/j.scitotenv.2014.08.012.

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