Environ. Sci. Technol. 2010, 44, 5188–5194
Polychlorinated Dibenzo-p-dioxins, Dibenzofurans, Biphenyls, and Naphthalenes in Plasma of Workers Deployed at the World Trade Center after the Collapse Y U I C H I H O R I I , †,‡,§ Q I N T I N G J I A N G , | NOBUYASU HANARI,‡ PAUL K. S. LAM,⊥ NOBUYOSHI YAMASHITA,‡ ROBERT JANSING,§ KENNETH M. ALDOUS,§ MATTHEW P. MAUER,¶ GEORGE A. EADON,§ AND K U R U N T H A C H A L A M K A N N A N * ,§ Center for Environmental Science in Saitama, 914 Kamitanadare, Kazo, Saitama 347-0115, Japan, National Institute of Advanced Industrial Science and Technology, 16-1 Onogawa, Tsukuba, Ibaraki 305-8569, Japan, 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, New York 12201-0509, Zhejiang Entry-exit Inspection and Quarantine Bureau of the People’s Republic of China, 2 Wen San Road, Hangzhou, China, Department of Biology and Chemistry, City University of Hong Kong, Tat Chee Avenue, Kowloon, Hong Kong, China, and Center for Environmental Health, New York State Department of Health, 547 River Street, Troy, New York 12180
Received January 26, 2010. Revised manuscript received April 19, 2010. Accepted April 25, 2010.
Blood plasma samples (n ) 43) collected retrospectively from New York State employees and National Guard personnel who had been assigned to work in the vicinity of the World Trade Center (WTC) during the week after the collapse of the buildings were analyzed for polychlorinated dibenzo-pdioxins (PCDDs), polychlorinated dibenzofurans (PCDFs), polychlorinated biphenyls (PCBs), and polychlorinated naphthalenes (PCNs). On the basis of algorithms developed to rank individual exposures to dust and debris and to smoke, we categorized the samples as: more smoke exposure (MSE), more dust exposure (MDE), less smoke exposure (LSE), and less dust exposure (LDE). Mean concentrations of PCDDs were 1070, 223, 3690, and 732 pg/g lipid wt, and mean concentrations of PCDFs were 910, 1520, 230, and 117 pg/g lipid wt, for the MSE, MDE, LSE, and LDE groups, respectively. The concentrations of PCDFs were higher in the two “more exposure” groups * Corresponding author phone: 518-474-0015; fax: 518-473-2895; e-mail:
[email protected]. † Center for Environmental Science in Saitama. ‡ National Institute of Advanced Industrial Science and Technology. § Wadsworth Center, State University of New York at Albany. | Zhejiang Entry-exit Inspection and Quarantine Bureau of the People’s Republic of China. ⊥ City University of Hong Kong. ¶ Center for Environmental Health, New York State Department of Health. 5188
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than in the two “less exposure” groups. Calculated TEQ concentrations of coplanar PCBs and PCDD/Fs in plasma samples were, on average, 1.12 and 41.2 pg WHO-TEQ/g lipid wt, respectively. TEQ concentrations of PCDFs were higher than those of PCDDs in both “more exposure” groups but lower than those of PCDDs in “less exposure” groups. This result is suggestive of exposure of the WTC responders to PCDFs after the WTC collapse. PCDFs contributed the majority of TEQs and are therefore the critical dioxin-like compounds in MSE/ MDE groups, whereas PCDDs are the critical compounds in the LSE/LDE groups.
Introduction Polychlorinated dibenzo-p-dioxins (PCDDs), polychlorinated dibenzofurans (PCDFs), polychlorinated biphenyls (PCBs), and polychlorinated naphthalenes (PCNs) are ubiquitous environmental pollutants. PCDDs, PCDFs, and PCNs are usually produced by the combustion of municipal solid wastes. The collapse of the two towers of the World Trade Center (WTC) on September 11, 2001 resulted in an unprecedented exposure of a human population to complex mixture of toxic chemicals produced by combustion as well as severe environmental effects that will take years to assess. During the disaster, several tens of thousands of computers, tons of PVC materials, plastics, and subutility power stations containing 492 000 L of PCB-containing transformer oil were destroyed (1). As a consequence, elevated concentrations of PCDDs, PCDFs, PCNs, and PCBs were found in the window films (1, 2) and in samples of dust (3), water, sediment, and sewage collected in and around the WTC site after the collapse of the towers (4). Although several studies have monitored air and dust samples, little is known of the exposures of humans to toxic contaminants released during the catastrophe. The initially intense and then prolonged combustion processes associated with the collapse potentially transformed precursor chemicals into new chemical entities, and facilitated their dispersal over a densely populated metropolitan area. The fire-suppression and recovery activities that brought emergency workers into the site could have caused the release of additional chemicals into the environment. In this context, human exposures to a complex mixture of potentially toxic chemicals were inevitable. The groups at greatest risk of exposure were firefighters, police, paramedics, cleaners, and other responders, who inhaled gases and/or dust released during the fire or building collapse. A previous study found higher levels of some metals (particularly urinary antimony), urinary PAH metabolites, and serum PCDD/Fs for firefighters exposed to WTC smoke and dust, as compared to unexposed firefighters (5). The medical monitoring program initiated by the New York State Department of Health (NYSDOH) provided the framework for collection of blood and urine samples from NYS employees and National Guard personnel who had been assigned to work in the vicinity of the WTC during the period between 9/11/2001 and 12/23/2001. Our previous study reported concentrations and profiles of perfluorochemicals in plasma samples from NYS personnel responding to the WTC disaster (6). In this study, we report congener-specific concentrations of PCDDs, PCDFs, PCNs, and PCBs, including coplanar PCBs (CoPCBs), in retrospectively sampled blood plasma from NYS personnel who had responded to the WTC disaster. An algorithm was developed to rank participants based on their exposures to dust and debris generated by the collapse, and another algorithm was developed to rank participants based 10.1021/es100282d
2010 American Chemical Society
Published on Web 05/10/2010
on their exposures to smoke and combustion products (7). The algorithm uses US Environmental Protection Agency’s air monitoring data collected between September 23, 2001 and February 28, 2002, as well as information about duration, location, and time period of work assignment and type and frequency of personal protective equipment use, collected by self-administered mailed questionnaire. These rankings were used to delineate four subset populations: More Dust Exposed (MDE); Less Dust Exposed (LDE); More Smoke Exposed (MSE); and Less Smoke Exposed (LSE). Comparisons between the high- and low-exposure groups in each category should enable us to determine whether specific chemicals are associated with WTC exposures. A chemical marker of exposure identified in this manner should be useful in ongoing and future epidemiological studies of WTC-related health effects, and in monitoring studies in future disaster situations. Intergroup comparisons as described above could also provide indications as to the value of testing archived specimens. Another goal of this study was to identify critical dioxinlike contaminants in plasma from dust- and smoke-exposed WTC responders. Since PCDDs, PCDFs, PCBs, and PCNs elicit toxic effects through a common mechanism of action, that is, activation of the aryl hydrocarbon receptor (AhR) (8, 9), it is possible to evaluate the relative contribution of each compound class to the AhR-mediated toxicity and to calculate their toxic equivalencies (TEQs). That step enables the identification of the most critical dioxin-like contaminant of concern. Accordingly, we determined relative contribution of each contaminant group to the overall dioxin-like (AhRmediated) toxicity in the four exposure groups.
Materials and Methods Blood samples were collected from study subjects who had been WTC responders and were enrolled in a medical monitoring program (10). Institutional Review Board approvals were obtained to collect and analyze blood plasma. Blood samples were collected between May 2002 and November 2003, that is, 5-26 months after the exposures. To harvest plasma, whole blood was centrifuged at 2000 rpm for 10 min in an Eppendorf 5840 centrifuge with swinging bucket head. Specimens were stored in a refrigerator for 2 h and then at -20 °C until analysis. Since this was a pilot study to assess chemical markers of exposure, it entailed analysis of only a subset of the samples for PCDDs, PCDFs, PCBs, and PCNs (n ) 43). As noted earlier, our 43 plasma samples were divided into 4 groups: More Dust Exposed (MDE, n ) 5), Less Dust Exposed (LDE, n ) 6), More Smoke Exposed (MSE, n ) 16), and Less Smoke Exposed (LSE, n ) 16). Demographic information such as age, sex, ethnicity, and body weight was available. PCNs, CoPCBs, and PCDD/Fs were analyzed in blood plasma following the method described elsewhere, with some modifications (11). Details of the sample preparation procedures are given in the Supporting Information. Highresolution gas chromatography/high-resolution mass spectrometry (HRGC/HRMS) analysis was performed with an HP 6890 GC (Agilent Technologies, Foster City, CA) interfaced with a JMS-700D (JEOL, Tokyo, Japan) at a resolution R > 10 000 (10% valley), in the selected ion monitoring (SIM) mode. Each sample was analyzed by two different GC capillary columns. Tetra- to hexa-CDD/Fs were separated and quantified using a SP2331 capillary column (0.25 mm i.d. × 60 m length and 0.20 µm film thickness; Supelco, Bellefonte, PA), while hepta- and octa-CDD/Fs, CoPCBs, and tri- to octa-CNs were separated and quantified on a DB-17 column (0.25 mm i.d. × 30 m length and 0.25 µm film thickness; J&W Scientific). Seventeen 2,3,7,8-substituted
PCDD/F congeners were analyzed in this study. The 12 CoPCB congeners analyzed were IUPAC# 77, 81, 105, 114, 118, 123, 126, 156, 157, 167, 169, and 189. The term total CoPCBs denotes the sum of all 12 non- and mono-ortho PCBs analyzed. The term total PCNs denotes the sum of all trithrough octa-CN congeners analyzed. Quality assurance and quality control (QA/QC) protocols included analysis of matrix spikes and matrix spike duplicates and procedural blanks. Peaks were identified by the corresponding retention times as compared to standards, if the signal-to-noise (S/N) ratio was >3, and they were quantified if target/qualifier ion ratios were within 15% of the theoretical values. 13C-labeled PCB and PCDD/F internal standards (tetra-octa congeners, for isotope dilution method of quantification) were spiked into all samples prior to the extraction step. One sample with recovery below 30% was discarded (this is not included in n ) 43). The recovery rates through the whole analytical procedure were 81 ( 30% for PCDDs, 80 ( 29% for PCDFs, and 78 ( 21% for CoPCBs. The limits of detection (LOD) for Σtotal PCBs, ΣCoPCBs, ΣPCDDs, ΣPCDFs, and ΣPCNs were 69 ng/g lipid wt, 720, 190, 270, and 2500 pg/g lipid wt., respectively (LODs for total are sum of individual congeners). The LOD values for each target chemical were 14-120 pg/g lipid wt for CoPCBs, 16-50 pg/g lipid wt for PCDDs, 9.4-140 pg/g lipid wt for PCDFs, and 15-360 pg/g lipid wt for PCNs. Samples below the LOD were assigned a zero value in the subsequent data analysis. Kruskal-Wallis H and Mann-Whitney U tests were used to examine the differences among the four groups, and the between-group variations. The Spearman rank correlation test was applied to test for the correlation among the concentrations of different compounds and demographic variables. All statistics analyses used were nonparametric tests due to the non-normal distribution of the data, and were performed with the SPSS software (version 13.0, SPSS, Inc., Chicago, IL).
Results Concentrations. Demographic characteristics and concentrations of PCDD/Fs, CoPCBs, and PCNs in the plasma samples (n ) 43) from WTC responders are shown in Table 1. The average age of the subjects was 39, 34, 40, and 46 years, for the MSE, MDE, LSE, and LDE groups, respectively. Overall, 91% of the subjects were males, and 67% were Caucasian. No significant differences in body weight or in creatinine, cholesterol, or triglyceride levels were observed among the four exposure groups (Table 1). Portions of the sample set from the MSE, MDE, LSE, and LDE (i.e., n ) 7, 5, 6, 6, respectively) groups were analyzed for total PCBs. Concentrations of total PCBs in plasma samples ranged from below the LOD to 527 ng/g lipid wt (mean: 205). Statistically significant differences were found for the concentrations of total PCBs (p ) 0.05, Kruskal-Wallis H test) or CoPCBs (p ) 0.02, Kruskal-Wallis H test) and age (p ) 0.05, Kruskal-Wallis H test) among the four exposure groups. Moreover, significant correlations were found between age and total PCB concentration (rs ) 0.767, p < 0.01, Spearman correlation test), and between age and CoPCB concentration in plasma samples (rs ) 0.378, p < 0.05, Spearman correlation test). Distributions of age, total PCB, and CoPCB concentrations among the four exposure groups are shown in Figure 1. The highest mean concentration of total PCBs was observed for the LDE group, which had the highest mean age (mean: 46 year); the lowest mean concentration was found for the MDE group, which had the lowest mean age (mean: 34 year). Concentrations of PCNs in plasma ranged from below the LOD to 38500 pg/g lipid wt (mean: 2740). A few samples contained elevated concentrations of PCNs. VOL. 44, NO. 13, 2010 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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TABLE 1. Demographic Characteristics and Concentrations (Mean ± SD, Median, And Range) of PCDDs, PCDFs, PCBs, and PCNs in Plasma Samples from World Trade Center Responders MSE (n ) 16) Donor Age (year) Gender (%) Male Female Ethnicity (%) African American Caucasian Hispanic Other Weight (lb) Cholesterol (mg/dL) Triglycerides (mg/dL) Fat (%) ΣPCB (ng/g lipid wt)b mean ( SD median (range) ΣcoPCB (pg/g lipid wt)b mean ( SD median (range) ΣPCN (pg/g lipid wt) mean ( SD median (range) ΣPCDD (pg/g lipid wt) mean ( SD median (range) ΣPCDF (pg/g lipid wt) mean ( SD median (range) a
ND: not detected.
b
MDE (n ) 5) 34 ( 5.8
40 ( 8.3
46 ( 7.3
15 (94%) 1 (6%)
5 (100%) -
14 (88%) 2 (12%)
5 (83%) 1 (17%)
2 (13%) 9 (56%) 4 (25%) 1 (6%) 191 ( 23 201 ( 39 171 ( 94 0.60 ( 0.19
4 (80%) 1 (20%) 189 ( 19 180 ( 22 140 ( 48 0.56 ( 0.03
3 (19%) 12 (75%) 1 (6%) 203 ( 46 200 ( 42 173 ( 153 0.64 ( 0.15
2 (33%) 4 (67%) 204 ( 42 209 ( 35 179 ( 110 0.63 ( 0.19
251 ( 170 181 (87.5-527)
93.4 ( 28.6 96.7 (58.5-136)
186 ( 58.7 181 (92-258)
262 ( 114 251 (134-441)
14200 ( 3950 13700 (6120-22700)
6740 ( 4000 5400 (1860-11700)
21900 ( 16800 16200 (755-71300)
32200 ( 19500 30800 (7330-57700)
4178 ( 10300 505 (ND-38500)a
318 ( 167 345 (86.4-518)
1080 ( 961 638 (ND-3160)
5360 ( 10100 1540 (112-25900)
1070 ( 972 915 (ND-3780)
223 ( 345 115 (ND-826)
3690 ( 6934 1490 (ND-27000)
732 ( 641 496 (ND-1560)
910 ( 1350 340 (ND-4630)
1520 ( 2280 176 (ND-5350)
230 ( 198 148 (10.7-674)
117 ( 156 45.2 (ND-372)
p < 0.05 (Kruskal-Wallis Test).
Mean concentrations of PCDDs were 1070, 223, 3690, and 732 pg/g lipid wt, and mean concentrations of PCDFs were 910, 1520, 230, and 117 pg/g lipid wt, for the MSE (n ) 16), MDE (n ) 5), LSE (n ) 16), and LDE (n ) 6) groups, respectively (Table 1). The concentrations of PCDDs in exposure groups decreased in the order: MDE < LDE < MSE < LSE. No significant difference in PCDD concentration was found among the four exposure groups (p ) 0.072, Kruskal-Wallis H test). Concentrations of PCDFs in the two ‘more-exposure’ groups (1060 pg/g lipid wt) were nearly 4to 10-fold greater than the concentrations in the two ‘lessexposure’ groups (199 pg/g lipid wt). The mean concentration of PCDFs in the combined MSE and MDE groups was slightly higher than the concentration in the combined LSE and LDE groups (U ) 155, p ) 0.065, Mann-Whitney U Test). No significant correlation was found between PCDF concentration and age or lipid content of the plasma samples, whereas 9
LDE (n ) 6)
39 ( 7.8
FIGURE 1. Concentrations of coplanar PCBs (CoPCBs) and total PCBs in plasma and age distribution among the four exposure groups. Number of samples for MSE, MDE, LSE, and LDE is 7, 5, 6, and 6, respectively.
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FIGURE 2. Concentrations of PCDDs and PCDFs in plasma of World Trade Center responders compared with concentrations for the general American population, as previously reported. (a) Data from ref 14; whole blood (n ) 100); (b) data from ref 12; whole blood (men ) 100, women ) 100), (c) data from ref 13; plasma (n ) 100). PCDD concentration did significantly correlate with lipid content (rs ) 0.50, p < 0.01, Spearman correlation test). A comparison of the concentrations of PCDDs and PCDFs in plasma samples analyzed in this study, with concentrations previously reported for the US general population, is shown in Figure 2. Concentrations of PCDDs in human blood samples collected in the late 1980s to late 1990s in the US ranged from 627 (12) to 1499 pg/g lipid wt (13), values similar to those found in our study (U ) 8.00, p > 0.05, Mann-Whitney U Test). However, mean concentrations of PCDFs reported in the earlier studies (12-14) were significantly lower than the levels found in our study (U < 0.01, and p < 0.05, Mann-Whitney U Test). The ratios of PCDFs/PCDDs in our
FIGURE 3. Profiles of PCN homologues (pg/g lipid wt) in plasma samples among the four exposure groups of World Trade Center responders.
FIGURE 4. Compositions of (a) PCDD and (b) PCDF homologues in plasma samples in World Trade Center responders. MSE, MDE, LSE, and LDE groups were 1.29 ( 2.15, 3.00 ( 3.02, 0.34 ( 0.54, and 0.34 ( 0.24, respectively, illustrating a trend for higher concentrations of PCDFs in the “moreexposure” groups. Congener Profiles. Hexa- and hepta-CBs were the predominant homologues, together contributing 60% of the total PCB concentration, for all four exposure groups (Figure S1). PCN homologue compositions in the plasma samples are shown in Figure 3. Penta- and tetra-CNs were the major homologues for the MSE group, while tetra- and hexa-CNs were the predominant homologues for the LSE group. Tetraand penta-CNs were the predominant homologues in four individual samples that contained elevated concentrations of PCNs. To our knowledge, this is the first report of PCNs in human blood plasma from the US population. OctaCDD was the predominant congener, contributing >90% of the total PCDD concentration, in all of the exposure categories (Figure 4). OctaCDF was the major congener in both high-exposure groups (i.e., MSE and MDE), while hexaCDF was the predominant homologue in both low-exposure groups. OctaCDF levels were significantly higher in the highexposure groups than in the low-exposure groups (U ) 155, and p ) 0.03, Mann-Whitney U test).
The dioxin-like toxic equivalency (TEQ) was calculated for CoPCBs and PCDD/Fs based on the toxic equivalent factors (TEFs) suggested by the World Health Organization (15). To assess the dioxin-like toxicity of PCN congeners, we used relative potency values reported in earlier studies (16, 17). The TEQs contributed by CoPCBs, PCDD/Fs, and PCNs are shown in Tables 2 and 3. The TEQ concentration for CoPCBs in plasma samples was, on average, 1.12 pg WHOTEQ/g lipid wt. The TEQ concentrations for total of PCDDs and PCDFs averaged 41.2 pg WHO-TEQ/g lipid wt. Furthermore, the TEQ concentration of PCDFs was higher than that of PCDDs in both high-exposure groups, but lower than that of PCDDs in both low-exposure groups. Overall, the most prevalent congeners in plasma were 2,3,4,7,8-pentaCDF, 2,3,4,6,7,8-hexaCDF, and 1,2,3,7,8-pentaCDD. These three congeners accounted for ∼74% of the total PCDD/F-TEQs. PCN-TEQ (1.96 pg/g lipid wt) values were similar to CoPCB TEQ values (Tables 2 and 3).
Discussion Although PCBs were banned in electrical transformers manufactured after 1977, transformers containing PCBs, often in combination with chlorinated benzenes, have remained in operation throughout the US (18). The average plasma levels of total PCBs of 200 ng/g lipid wt found in our study are lower than the total PCB levels that were previously reported in a study of male Lake Ontario sportfish consumers (781 ng/g lipid wt) (19), and in a study of native American population from Mohawks in New York State (732 ng/g lipid wt; converted from 4.39 ng/g wet wt) (20). In 1999-2000 subsamples in the National Health and Nutrition Examination Survey (NHANES), the 95th percentile of serum concentration of 25 PCB congeners was 436 ng/g lipid wt (21). Comparable to that value, the highest concentration of total PCBs found in our study was 527 ng/g lipid wt. Although we found significant differences in the concentration of total PCBs and CoPCBs among the four exposure groups, further correlation analysis showed that the differences were ascribable to age rather than to differences in levels of exposures. We believe the plasma PCB levels measured in this study to have been due to dietary exposures because PCB concentrations were similar to those seen for the general population, and because the homologue composition that we determined was similar across the four exposure groups. An interesting finding in our study was that the levels of PCDFs for the MSE and MDE groups (mean ) 1060 pg/g lipid wt) were significantly higher than those for the LSE and LDE groups (mean ) 199 pg/g lipid wt). Furthermore, the concentrations of total PCDFs in the present study were significantly higher than those that have been reported for the US general population (12-14). It is conceivable, therefore, that PCDFs were produced during the fires at the WTC site. In contrast, the mean concentrations of PCDDs were comparable not only between the high and the low exposure groups, but they also compare to values reported previously for the US general population. The PCDD concentrations were significantly correlated with lipid content in our plasma samples. Combustion of PVC plastics and PCB and chlorinated benzene-contained transformer oil can generate PCDFs (22). Yasuhara et al. (23) reported that the total amount of PCDDs, PCDFs, and CoPCBs formed during combustion was proportional to the chlorine content in the feedstock samples and the temperature. That study found that when the combustion temperature was between 400 and 600 °C, PCDFs were the predominant contaminants produced. Similarly, high levels of PCBs (50 000 ppb) and PCDFs (2 100 000 ppb) were found in soot samples after a transformer fire in Binghamton, New York (18). Although PCDDs and PCDFs are both produced during combustion, VOL. 44, NO. 13, 2010 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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TABLE 2. Mean TEQ Levels of Coplanar PCBs (CoPCBs), and PCDD/Fs (pg WHO-TEQ/g lipid wt) in Plasma Samples from World Trade Center Responders WHO-TEF (2005)
MSE (n ) 16)
MDE (n ) 5)
LSE (n ) 16)
LDE (n ) 6)
average
77 81 126 169 105 114 118 123 156 157 167 189
0.0001 0.0003 0.1 0.03 0.00003 0.00003 0.00003 0.00003 0.00003 0.00003 0.00003 0.00003
0.00379 NDa 0.479 0.357 0.045 0.011 0.169 0.0055 0.127 0.0323 0.024 0.011
CoPCBs 0.0114 ND ND 0.837 0.0288 0.0031 0.0764 0.0035 0.0596 0.0149 0.0076 0.0039
0.00108 ND ND 0.0657 0.0484 0.0289 0.238 0.0080 0.229 0.0523 0.0396 0.0137
0.134 ND ND 0.778 0.145 0.0303 0.349 0.0414 0.238 0.0558 0.0541 0.0103
0.0218 ND 0.178 0.363 0.0582 0.0193 0.209 0.0112 0.173 0.0410 0.0321 0.0109
2378 12378 123478 123678 123789 1234678 12346789
1 1 0.1 0.1 0.1 0.01 0.0003
4.98 13.4 ND 1.65 0.815 0.456 0.295
PCDDs ND 3.52 ND ND ND 0.122 0.0623
4.40 9.91 ND 2.66 2.41 0.656 1.07
ND 40.5 ND 1.93 ND ND 0.202
3.49 14.7 ND 1.87 1.20 0.428 0.543
2378 0.1 12378 0.03 23478 0.3 123478 0.1 123678 0.1 123789 0.1 234678 0.1 1234678 0.01 1234789 0.01 12346789 0.0003 Total CoPCBs Total PCDDs Total PCDFs Total PCDD/Fs Total CoPCBs and PCDD/Fs
0.671 0.734 13.3 0.850 0.750 1.17 6.48 0.217 ND 0.216 1.26 21.6 24.4 46.0 47.2
PCDFs ND 0.705 9.43 0.565 0.330 0.657 4.24 ND ND 0.423 1.05 3.70 16.3 20.0 21.1
0.170 0.459 8.27 0.939 0.657 0.358 3.93 0.216 ND 0.031 0.724 21.1 15.0 36.1 36.9
ND 0.714 10.2 1.24 ND ND 4.65 ND ND ND 1.84 42.6 16.8 59.4 61.2
0.313 0.626 10.6 0.905 0.562 0.645 5.02 0.161 ND 0.141 1.12 22.2 18.9 41.2 42.3
congener
a
ND: not detected.
TABLE 3. Relative Potencies (REPs) and TEQ Levels of Dioxin-like PCNs (pg-TEQ/g lipid wt) in Plasma Samples from World Trade Center Responders congener 12367 12456 12378 123467, 123567 123457, 123568 123578 123456 1234567 Total PCNs a
REP 5.0 5.0 5.0 5.0 5.0 5.0 5.0 5.0
× × × × × × × ×
10-4 10-6 10-5 10-3 10-3 10-3 10-3 10-3
MSE (n ) 16)
MDE (n ) 5)
LSE (n ) 16)
LDE (n ) 6)
average
NDa 7.27 × 10-4 ND 0.613 0.204 0.433 0.161 0.885 2.30
ND ND ND ND ND ND ND 0.229 0.229
ND 3.96 × 10-5 ND 0.894 ND 0.259 0.032 0.349 1.53
0.160 5.64 × 10-4 ND ND ND 0.329 2.54 0.602 3.63
0.022 3.64 × 10-4 ND 0.561 0.076 0.304 0.426 0.570 1.96
ND: not detected.
the patterns of congeners depend on the substrates, the temperature, and what other catalysts are present. Differences in the levels of chlorinated contaminants present in plasma are in part due to exposure but may also result from differences in absorption, tissue distribution, metabolism, and elimination. The half-life of PCDFs in humans ranges from 2.9 to 7.7 years (24). Plasma samples were collected between 5 and 26 months after exposure, and therefore, the measured concentrations are expected to reflect exposures 5192
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at the WTC site, along with other exposures prior to or since work at the WTC. The elevated levels of total PCDFs in both high-exposure groups are attributable to the high concentration of octaCDF (mean ) 884 pg/g lipid wt), which accounted for >80% of the total PCDFs. Moreover, concentrations of octaCDF in the high-exposure groups are much higher than those reported for the US general population (21). Concentrations of octaCDD in both high- and low-exposure groups were lower
than those reported for the US general population (13, 21), which may indicate that octaCDF is elevated here due to specific exposure to smoke/dust at the WTC site. Concentrations of 1,2,3,4,6,7,8-heptaCDD in the MSE (45.6 pg/g lipid wt) and MDE groups (12.2 pg/g lipid wt) were comparable to the concentrations (22 pg/g lipid wt) previously reported for the plasma of pregnant women in New York City after the WTC collapse (25). Our PCDD/F results are consistent with the reported high blood levels of 1,2,3,4,6,7,8-heptaCDF, 1,2,3,4,6,7,8-heptaCDD, octaCDF, and octaCDD in firefighters after exposure to a transformer-fire in Binghamton, New York (18). However, we did not find high plasma concentrations of heptaCDFs, in contrast to what was previously reported for plasma samples from firefighters who responded to the WTC collapse (5). The differences in congener levels and profiles in the above sets of human blood samples may be due to different sampling times, locations, and sample matrix. The plasma samples in the current study were collected from WTC responders between May 2002 and November 2003, 5-26 months after potential exposures, whereas the WTC firefighter samples were obtained within a month after the collapse of the towers (i.e., in October 2001) (5). In addition, we analyzed plasma samples in this study, whereas whole blood samples were analyzed in the study of the firefighters. Human exposures to PCNs are not well documented. Production of PCNs in the US ceased in 1980; however, PCNs are still found in the environment and are released from combustion of municipal solid wastes (1). PCNs can be detected in body fluids and adipose tissue samples (26). However, few data are available for the US population. Tetrato hexa-CNs were the most abundant congeners in our plasma samples, while penta- and hexa-CNs were dominant in human adipose tissues from New York City residents (26). We also found high levels of octaCN in our MSE group, similar to that reported for Halowax 1051 (27). The pharmacokinetics and half-life of PCNs in humans are not known. The CoPCB-TEQs values in our plasma samples (mean: 1.1 pg WHO-TEQ/g lipid wt) were lower than those reported for the US general population (5.2 pg WHO-TEQ/g lipid wt; 14). PCNs contributed less than 5% of the total TEQs, but PCN-TEQs are similar in magnitude to the CoPCB-TEQs. Overall, PCDDs and PCDFs together contributed >90% of the total TEQs. The total PCDD/F-TEQs measured in this study (41 pg WHO-TEQ/g lipid wt) were similar to the average serum TEQs previously reported for New York City firefighters (39 pg/g) (18). PCDD/F-TEQs measured in this study were similar to the levels previously reported for New York residents (13). The main congeners that contributed to the PCDD/F-TEQinourstudywere2,3,4,7,8-pentaCDF,2,3,4,6,7,8hexaCDF, and 1,2,3,7,8-pentaCDD. The CDC’s NHANES study (21) in 1999-2000 showed that more highly chlorinated dioxin and furan congeners, and CoPCBs, were the main contributors to TEQs. The mean PCDF-TEQ in our MSE group was 24.4 pg/g lipid wt, a value accounting for half of total TEQs. This proportion suggests that the smoke from the WTC was a source of PCDF exposure. Although PCDF concentrations in MDE samples were higher than those in LDE samples, the TEQs were higher for LDE samples than for MDE samples; this is because the congeners that contributed to elevated concentrations in MDE group (i.e., OCDF, HeptaCDF) have low TEFs. In summary, the plasma levels of PCDFs in more smoke exposure and more dust exposure groups were higher than the levels found for less smoke- and less dust-exposure groups, suggesting exposure of the WTC responders to PCDFs after the collapse of WTC. On the basis of TEQs, we conclude that PCDFs are the critical dioxin-like compounds in the MSE/MDE groups, whereas PCDDs are the critical contaminants in the LSE/LDE groups.
Acknowledgments We would like to thank Richard Ciulla, M.D., and the staff of the NYS Department of Civil Service Employee Health Service for collecting the biological samples as part of the WTC Medical Monitoring program. We would also like to thank Karen Cummings, MPH, for her assistance in study coordination, Michele Herdt-Losavio, Ph.D., MPH, for her assistance in developing the exposure assessment method used, and Rebecca Hoen, MS, for her assistance with data review. This study was supported by a grant (UIQ/CCU22115904) from the Centers for Disease Control and Prevention (CDC). Its contents are solely the responsibility of the authors and do not necessarily represent the official views of CDC.
Supporting Information Available Detailed analytical methods and a figure showing composition of total PCB homologues in plasma samples. This material is available free of charge via the Internet at http:// pubs.acs.org.
Literature Cited (1) Butt, C. M.; Diamond, M. L.; Truong, J.; Ikonomou, M. G.; Helm, P. A.; Stern, G. A. Semivolatile organic compounds in window films from lower Manhattan after the September 11th World Trade Center attacks. Environ. Sci. Technol. 2004, 38, 3514– 3524. (2) Rayne, S.; Ikonomou, M. G.; Butt, C. M.; Diamond, M. L.; Truong, J. Polychlorinated dioxins and furans from the World Trade Center attacks in exterior window films from lower Manhattan in New York City. Environ. Sci. Technol. 2005, 39, 1995–2003. (3) Offenberg, J. H.; Eisenreich, S. J.; Gigliotti, C. L.; Chen, L. C.; Xiong, J. Q.; Quan, C.; et al. Persistent organic pollutants in dusts that settled indoors in lower Manhattan after September 11, 2001. J. Exposure Anal. Environ. Epidemiol. 2004, 14, 164– 172. (4) Litten, S.; McChesney, D. J.; Hamilton, M. C.; Fowler, B. Destruction of the World Trade Center and PCBs, PBDEs, PCDD/ Fs, PBDD/Fs, and chlorinated biphenylenes in water, sediment, and sewage sludge. Environ. Sci. Technol. 2003, 37, 5502–5510. (5) Edelman, P.; Osterloh, J.; Pirkle, J.; Caudill, S. P.; Grainger, J.; Jones, R.; et al. Biomonitoring of chemical exposure among New York City firefighters responding to the World Trade Center fire and collapse. Environ. Health Perspect. 2003, 111, 1906– 1911. (6) Tao, L.; Kannan, K.; Aldous, K. M.; Mauer, M. P.; Eadon, G. A. Biomonitoring of perfluorochemicals in plasma of New York State personnel responding to the World Trade Center disaster. Environ. Sci. Technol. 2008, 42, 3472–3478. (7) Herdt-Losavio, M. L.; Mauer, M. P.; Carlson, G. A. Development of an exposure assessment method for epidemiological studies of New York State personnel who responded to the World Trade Center disaster. Ann. Occup. Hyg. 2008, 52, 83–93. (8) Hilscherova, K.; Machala, M.; Kannan, K.; Blankenship, A. L.; Giesy, J. P. Cell bioassays for detection of aryl hydrocarbon (AhR) and estrogen receptor (ER) mediated activity in environmental samples. Environ. Sci. Pollut. Res. 2000, 7, 159–171. (9) Kannan, K.; Yamashita, N.; Imagawa, T.; Decoen, W.; Khim, J. S.; Day, R. M.; et al. Polychlorinated naphthalenes and polychlorinated biphenyls in fishes from Michigan waters including the Great Lakes. Environ. Sci. Technol. 2000, 34, 566– 572. (10) Mauer, M. P.; Cummings, K. R.; Carlson, G. A. Health effects in New York State personnel who responded to the World Trade Center disaster. J. Occup. Environ. Med. 2007, 49, 1197–1205. (11) Hanari, N.; Horii, Y.; Okazawa, T.; Falandysz, J.; Bochentin, I.; Orlikowska, A.; et al. Dioxin-like compounds in pine needles around Tokyo Bay, Japan in 1999. J. Environ. Monit. 2004, 6, 305–312. (12) Schecter, A.; Pa¨pke, O. Comparison of blood dioxin, dibenzofuran, and coplaner PCB levels in strict vegetarians (vegans) and the general United States population. Organohalogen Compd. 1998, 38, 179–182. (13) Schecter, A.; Fu ¨ rst, P.; Fu ¨ rst, C.; Pa¨pke, O.; Ball, M.; Dai, L. C.; et al. Dioxins, dibenzofurans and selected chlorinated organic compounds in human milk and blood from Cambodia, Germany, Thailand, the U.S.A., the U.S.S.R., and Vietnam. Chemosphere 1991, 23, 1903–1912. VOL. 44, NO. 13, 2010 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
9
5193
(14) Schecter, A.; Pa¨pke, O. Dioxins, dibenzofurans, and coplaner and marker PCBs in blood of persons near a PCB manufacturing facility in the United States. Organohalogen Compd. 1998, 38, 175–178. (15) Van den Berg, M.; Birnbaum, L. S.; Denison, M.; De Vito, M.; Farland, W.; Feeley, M.; et al. The 2005 World Health Organization reevaluation of human and Mammalian toxic equivalency factors for dioxins and dioxin-like compounds. Toxicol. Sci. 2006, 93, 223–241. (16) Blankenship, A. L.; Kannan, K.; Villalobos, S. A.; Villeneuve, D. L.; Falandysz, J.; Imagawa, T.; et al. Relative potencies of individual polychlorinated naphthalenes and halowax mixtures to induce Ah receptor-mediated responses. Environ. Sci. Technol. 2000, 34, 3153–3158. (17) Villeneuve, D. L.; Kannan, K.; Khim, J. S.; Falandysz, J.; Nikiforov, V. A.; Blankenship, A. L.; et al. Relative potencies of individual polychlorinated naphthalenes to induce dioxin-like responses in fish and mammalian in vitro bioassays. Arch. Environ. Contam. Toxicol. 2000, 39, 273–281. (18) Kelly, K. J.; Connelly, E.; Reinhold, G. A.; Byrne, M.; Prezant, D. J. Assessment of health effects in New York City firefighters after exposure to polychlorinated biphenyls (PCBs) and polychlorinated dibenzofurans (PCDFs): the Staten Island Transformer Fire Health Surveillance Project. Arch. Environ. Health 2002, 57, 282–293. (19) Bloom, M. S.; Vena, J. E.; Swanson, M. K.; Moysich, K. B.; Olson, J. R. Profiles of ortho-polychlorinated biphenyl congeners, dichlorodiphenyldichloroethylene, hexachlorobenzene, and Mirex among male Lake Ontario sportfish consumers: the New York State Angler cohort study. Environ. Res. 2005, 97, 178–194. (20) DeCaprio, A. P.; Johnson, G. W.; Tarbell, A. M.; Carpenter, D. O.; Chiarenzelli, J. R.; Morse, G. S.; et al. Polychlorinated biphenyl
5194
9
ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 44, NO. 13, 2010
(21) (22)
(23)
(24) (25)
(26)
(27)
(PCB) exposure assessment by multivariate statistical analysis of serum congener profiles in an adult Native American population. Environ. Res. 2005, 98, 284–302. CDC. Second National Report on Human Exposure to Environmental Chemicals. NCEH Pub No 02-0716; Centers for Disease Control and Prevention: Atlanta, GA, 2003. Austin, C. C.; Wang, D.; Ecobichon, D. J.; Dussault, G. Characterization of volatile organic compounds in smoke at municipal structural fires. J. Toxicol. Environ. Health 2001, 63, 437– 458. Yasuhara, A.; Katami, T.; Shibamoto, T. Formation of PCDDs, PCDFs, and coplanar PCBs from incineration of various woods in the presence of chlorides. Environ. Sci. Technol. 2003, 37, 1563–1567. Masuda, Y. Fate of PCDF/PCB congeners and change of clinical symptoms in patients with Yusho PCB poisoning for 30 years. Chemosphere 2001, 43, 925–930. Wolff, M. S.; Teitelbaum, S. L.; Lioy, P. J.; Santella, R. M.; Georgopoulos, P.; Li, W.; et al. Exposures among pregrant women near the World Trade Center site on 9/11. Epidemiology 2004, 15, S120. Kunisue, T.; Johnson-Restrepo, B.; Hilker, D. R.; Aldous, K. M.; Kannan, K. Polychlorinated naphthalenes in human adipose tissue from New York, USA. Environ. Pollut. 2009, 157, 910– 915. Kannan, K.; Imagawa, T.; Blankenship, A. L.; Giesy, J. P. Isomerspecific analysis and toxic evaluation of polychlorinated naphthalenes in soil, sediment, and biota collected near the site of a former chlor-alkali plant. Environ. Sci. Technol. 1998, 32, 2507–2514.
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