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Temporal Changes in the Levels of Perfluorinated Compounds in California Women’s Serum over the Past 50 Years Miaomiao Wang,* June-Soo Park, and Myrto Petreas Department of Toxic Substances Control, California Environmental Protection Agency, Berkeley, California 94710, United States
bS Supporting Information ABSTRACT: Serum samples collected from California women at different time periods: 1960s (n = 40), 1980s (n = 30), and 2009 (n = 35) were examined for the presence of 12 perfluorinated compounds (PFCs) using an online SPE-HPLC-MS/MS method. At each time period, perfluorooctane sulfonate (PFOS) was present at the highest concentration, followed by perfluorooctanoic acid (PFOA, except in the 1960s). We found the highest levels of PFOS (median = 42.1 ng/ mL) and perfluorohexane sulfonate (PFHxS, median = 1.56 ng/mL) in the 1960s samples, possibly reflecting widespread use of precursor PFCs. PFOS showed a statistically significant drop from the 1960s to the 1980s (28.8 ng/mL ) and to 2009 (9.0 ng/mL ), the latter being in agreement with national data. For PFOA, there was an approximately 10-fold increase in median concentrations from the 1960s (0.27 ng/ mL) to the1980s (2.71 ng/mL), and a slight drop in the 2009 samples (2.08 ng/mL). For longer chain perfluorocarboxylic acids (PFCAs), there was a continuous build-up in serum from the 1960s to 2009. To our knowledge, this is the first study to investigate temporal changes of PFCs over the past 50 years.
’ INTRODUCTION Perfluorinated compounds (PFCs) are of particular interest as emerging environmental contaminants. They are found in the environment and in biota due to the manufacturing of PFCs, their industrial application practices and their widespread use in consumer products.1 3 They have been widely used as protective coatings in a variety of industrial applications, such as in textiles and paper and as surfactants for more than 50 years. The detection of certain PFCs, particularly perfluorooctane sulfonate (PFOS) and perfluorooctanoic acid (PFOA) in water systems, house dust, and wildlife,4 13 has raised concerns about their persistence and bioaccumulation in the environment. Among the various PFCs, PFOS and PFOA are found in the highest concentration ranges in the environment and have been found in human serum around the world.14 28 Both PFOS and PFOA have demonstrated toxicity in lab animals (adverse effects on reproductive and developmental systems, fatty acid metabolism and liver damage) as well as adverse effects on human health.29 31 Recent studies have shown the presence of certain PFCs in breast milk,32 34 and their placental transport.32,35 Due to its persistence and bioaccumulative properties, PFOS has been added to the 2009 Stockholm Convention list of POPs (persistent organic pollutants). PFCs may enter the environment from several sources such as the manufacturing of perfluoralkylsulfonyl-based substances by electrochemical fluorination (ECF),36 telomerization of pentafluoroiodoethane with tetrafluoroethylene oligomers,1 the environmental degradation of perfluorooctanesulfonyl fluoride (POSF) r 2011 American Chemical Society
and related products,37 39 and from various industrial applications, such as water- and oil-repellant coatings.40,41 Although PFCs (particularly PFOS, PFOA, and perfluorohexane sulfonate or PFHxS) have been widely detected in environmental samples, there are only a few studies on time trends in humans and other biota,12,15,28,33,42 45 and fewer still in human milk or serum.15,28,42,43 Temporal trend studies are valuable tools for evaluating the contaminants’ status, their persistence, changes in sources of exposure and the efficacy of environmental regulations. Data from the National Health and Nutrition Examination Survey (NHANES) from 1999 to 2000 and 2003 2004 showed a decrease in PFOS concentrations in the U.S. population, consistent with the phase out by 3M of manufacturing processes based on POSF chemistry, and with more strict regulations overall. However, to our knowledge, there is no report on PFC levels in human serum samples as early as the 1960s, neither on human population time trend studies from the 1960s to the present. Such data would expand the present knowledge on PFCs and would provide valuable information on the early contamination profiles of PFCs, since the manufacturing practice based on POSF chemistry started as early as 1949.1 Here we report on how we adapted and validated an online SPE-HPLCMS/MS method based on the Center for Disease Control Received: April 11, 2011 Accepted: July 6, 2011 Revised: June 29, 2011 Published: July 06, 2011 7510
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Table 1. Summary of PFCs Concentration (ng/mL) Detected in the Serum Samples, Detection Frequency, And Limit of Detection (LOD) for Each Analytea
a
NA, not applicable. SE, standard error. DF, detection frequency. NR, not reported.
(CDC) protocol,27,46 and examined the concentrations of PFCs in serum samples from California women collected from the 1960s, the 1980s, and 2009. The data trends are compared with U.S. data and data from other geographic locations.
’ MATERIALS AND METHODS Sample Populations. Samples were collected from three different time periods. The 1960s samples (n = 40, drawn between 1960 and 1963) were randomly selected among over 500 archived samples of pregnant women participating in a study of reproductive outcomes nested within the historic Child Health and Development Studies (CHDS) cohort. The CHDS47 is a longitudinal study of over 20 000 pregnancies among Northern California Kaiser Foundation Health Plan members, with subjects enrolled between 1959 and 1966. The 1980s samples (n = 30, drawn between 1981 and 1986) were randomly selected among archived serum samples from cancer-free women (controls) participating in a breast cancer study.48 The 2009 samples (n = 35) were from a pilot study for the California Environmental Contaminants Biomonitoring Program.49 All serum samples were from California women49 and were obtained with informed consent processes. All samples were stored at 80 °C or 20 °C prior to analysis. Standards and Materials. The following labeled compounds and native PFC standards were purchased from Wellington Laboratories (Guelph, Ontario, Canada): PFOS (perfluorooctane sulfonate), PFHxS (perfluorohexane sulfonate), PFBS (perfluorobutane sulfonate), PFOA(perfluorooctanoic acid), PFNA (perfluoronanonoic acid), PFHpA (perfluoroheptanoic acid), PFDA (perfluorodecanoic acid), PFUA (perfluoroundecanoic acid),
PFDoA (perfluorododecanoic acid), PFOSA (perfluooctane sulfonamide), Et-PFOSA-AcOH (2-(N-ethyl-perfluorooctane sulfoamido) acetic acid), and Me-PFOSA-AcOH (2-(N-methyl-perfluorooctane sulfoamido) acetic acid). Reagents (including methanol and water (both HPLC grade), glacial acetic acid, ammonia, formic acid) were purchased from Mallinckrodt Baker (formerly J.T. Baker, Phillipsburg, NJ) Sample Preparation and Analysis. Our method is based on an online SPE-HPLC-MS/MS method,46 with details described in the Supporting Information (SI). Briefly, 100 μL of serum were mixed with 0.1 M formic acid, and internal standards were added (13C2-PFOA and 13C4-PFOS), then injected by an online SPE-HPLC system (Symbiosis Pharma system with Mistral CS Cool, Spark Holland Inc.) to a C18 cartridge (HySphere C18 HD, 7 μm, 10 2 mm). After washing, the target analytes were eluted to a C8 HPLC column (BETASIL C8 column, Thermo Fisher Scientific) for separation. The eluate was then introduced to the MS/MS (ABSciex 4000 QTrap) for multiple-reaction-monitoring (MRM) analysis. The area of the Q1/Q3 ion pairs was used in the analysis. Regression coefficients of 0.98 to 0.99 were generally obtained. Quality Control. The method was validated by repeatedly analyzing blank calf serum spiked with unlabeled PFC standards at two different levels (low and high). Furthermore, standard reference materials (SRM 1958) from the National Institute of Standards and Technology, as well as PFC-spiked samples of known concentration from the CDC were used as reference materials.50 A summary chart of interlaboratory comparison studies is shown in the SI (Figure S1 A and B). Blank samples (bovine serum) were also processed with each batch of samples, and no PFCs were detected above the respective LODs (defined as 3 times the standard deviation of the blank and listed in Table 1). 7511
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Figure 1. A and B. Concentrations (mean and standard error) in ng/ mL of PFOS and PFHxS in serum samples from the three time periods. NHANES data for female serum (Geometric mean value (GM)) are plotted as references.
Statistical Analysis. As the data were not normally distributed, we used the nonparametric test for trend across ordered groups developed by Cuzick51 and the Kruskal Wallis equality of populations rank test (STATA, Statistical data analysis software, 11th edition. StataCorp., College Station, TX) to compare the concentrations of each chemical across the three time periods. The Spearman rank correlation coefficient was used to assess the relationship between individual PFCs in the samples.
’ RESULTS AND DISCUSSION Individual PFC levels in serum from the 1960s, 1980s and 2009 are shown in the SI, Tables S1 A, B, and C, respectively. Summary statistics are shown in Table 1. PFOS and PFHxS were detected in all the serum samples, whereas PFOA, PFDA, EtPFOSA-AcOH, and PFOSA were detected in the majority of the samples. Neither PFBS nor PFDoA were measured above the detection limit in any of the serum samples. Perfluorosulfonates. PFOS showed decreasing trends from the 1960s to 2009 (Figure 1 A and B) that were statistically significant (p < 0.001). Given our sampling times, in the current study we have no data on whether concentrations might have increased between the 1980s to early 2000 as others have reported.28 The decreasing trends of PFOS and PFHxS from the 1980s to 2009, in general, are consistent with the phase out of the perfluorooctyl manufacturing practice in 2002.43 They also agree well with the NHANES data, as shown in Figure 1. However, the levels of PFOS and PFHxS in the 1960s serum
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samples were unexpectedly high. To our knowledge, there are no reports on human serum samples as early as the 1960s: while there is one report on organic fluorine in human blood from the 1960s (∼1 μM organic fluorine in serum), due to technical restrictions at that time, it is not clear which specific compound was the major component.52 Based on our QC and interlaboratory studies (SI Figure S1), we believe that the presence of PFOS and PFHxS in the 1960s samples was not an artifact introduced either through laboratory background or detection error, nor was it likely a systematic contamination attributable to materials used for sample collection and storage. Our belief is, in part, based on the wide range of PFOS concentrations detected (8.3 124 ng/mL). To our knowledge, the samples were collected and stored using the same protocol and, therefore, the wide range of PFOS concentrations within this batch can only be attributed to the wide differences among individual samples. PFOS results reported from global populations in the 1970s were not consistent. In one study, only 3.8 ng/mL of PFOS were detected in pooled serum samples that were collected in 1977 in Norway.42 In another study, a median value of 29.5 ng/mL PFOS was detected in archived serum samples that were collected from Maryland, U.S. in 1974 (n = 178).28 This is the earliest report on U.S. serum and it is, therefore, likely that PFOS was present in high concentrations in human serum as early as the 1960s in the U.S. When we examined the 1960s concentrations by the year of sample collection we found statistically significant increasing trends from 1960 to 1963 for PFOS (p < 0.001) and PFHxS (p < 0.001). This may reflect increasing use of Scotchgard-containing products in the early 1960s. Furthermore, there are interesting, and statistically significant, correlations observed between PFOS and PFHxS. PFHxS, also a key ingredient in the Scotchgard line, showed similarly high concentrations in our 1960s serum samples (Figure 1B). The detection of both octa- and hexa- forms of perfluorosulfonates strongly confirms the presence of these compounds as early as the 1960s. The strongest correlations were observed for samples collected in the 1960s (r = 0.92, Table 2a), again confirming the presence of high PFOS in serum as early as 1960s. There was a similar correlation in the 1980s samples (r = 0.83, Table 2b), but not in the 2009 samples (r = 0.27, Table 2c). These correlations indicate that both PFOS and PFHxS have significant overlap in sources that contribute to their environmental presence. The reduced correlation in 2009 might be due to their different halflives (5.4 years for PFOS, and 8.5 years for PFHxS),53 and thus different persistence in biota, or might be indicative of new and different sources that contribute to contemporary levels of PFOS and PFHxS. Perfluorooctanesulfonamide. PFOSA, Me-PFOSA acetic acid, and Et-PFOSA acetic acid showed trends similar to one another: an increase until the 1980s and a decrease since then. PFOSA is also the product of the ECF chemistry and a degradation precursor of PFOS. However, the strongest correlation was found between PFOS and PFOSA in serum samples from the 1960s (r = 0.69, Table 2a), and deceased in 1980s (r = 0.21, Table 2b), and 2009 (r = 0.41, Table 2c), indicating that more recently, there are multiple sources of PFOS in the environment other than PFOSA degradation. There is a quite strong correlation between PFOSA and Et-PFOSA in the 2009 serum samples (r = 0.59, Table 2c), suggesting that Et-PFOSA is a precursor and significant source of environmental PFOSA. The time trend of 7512
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Table 2. Spearman Rank Correlation Coefficients between Concentrations of PFCs in Serum Samples from Each of the Three Time Periodsa
a
NA: not applicable.
Figure 2. Concentrations (mean and standard error) in ng/mL of PFOSA in serum samples from the 3 time periods. NHANES data for female serum (GM) from 1999 to 2000 and from 2003 to 2004 are plotted as references.
PFOSA (Figure 2) clearly indicates the build up of PFOSA in serum from the 1960s to the 1980s, and its decrease by 2009. This decrease of PFOSA down to around the limit of detection levels in the 2009 samples indicates that exposure to PFOSA has been effectively decreased by the regulation of ECF chemistry, by PFOSA’s degradation in the environment and the elimination from the human body. Interestingly, a study of 84 pooled serum
samples (from 2420 individuals) in Australia collected in 2006 2007 has shown similar levels for PFOSAs16 compared to our 2009 serum samples: while Me-PFOSA was still detected in 94% of the samples, there was a detection frequency of only 24% in all the samples for PFOSA, and Et-PFOSA was detected in only 1% of the samples, again reflecting a clear impact of the phase out of the POSF chemistry. Perfluorocarboxylic Acid. PFOA showed an increase of approximately 10-fold from the 1960s to the 1980s, followed by a slight decrease. However, as we had no samples collected in the early 2000s, we may have missed the peaking period of PFOA’s presence. Furthermore, compared to PFOS and PFOSA, PFOA does not show such a big decrease from the 1980s to 2009, as shown in Figure 3. PFOS has a three- fold decrease (about 31%), while PFOA has only decreased to about 77% of the original value from the 1980s to 2009. This might indicate alternate sources of PFOA in the environment other than the ECF manufacturing that was phased out during this time period. For example, fluorotelomer alcohol degradation can contribute to PFCAs of various chain lengths.37,38 Furthermore, the levels of PFNA, PFDA and PFUA in our study showed increases from the 1960s to 2009 (Figure 4 and SI Figure S3), although PFDA and PFUA were either not present or below the detection limit in the NHANES data. These differences might indicate differences in exposures between California and the U.S. in general, although our limited sample size and the lack of statistical representativeness 7513
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Figure 3. Concentrations (mean and standard error) in ng/mL of PFOA in serum samples from the three time periods. NHANES data for female serum (GM) are plotted as references.
Figure 4. A and B. Concentrations (mean and standard error) in ng/ mL of PFNA and PFDA in serum samples from the three time periods. For values lower than LOD, half of the LOD value was used in the plots. NHANES data for female serum (GM) (for PFNA only) are plotted as references. PFDA was either not detected or lower than LOD in the 1999 and 2003 NHANES data.
should be taken into account. As shown in Figure 4B, PFDA has an approximately 6-fold increase from the 1960s to 2009 (medians from 0.06 to 0.37 ng/mL in serum), while PFUA was below the detection limit in the 1960s, but was detected with a median of 0.17 ng/mL in our 2009 serum (SI Figure S3). These trends were statistically significant for both PFDA and PFUA.
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These longer chain PFCAs have also been detected globally recently: PFDA was detected in 2006 2007 Australian serum samples (0.3 ng/mL),16 PFDA and PFUA in contemporary Chinese serum samples (0.38 and 0.76 ng/mL, respectively),19 and in Swedish serum samples collected between 1996 and 2004 (0.53 and 0.40 ng/mL, respectively).26 Globally, it appears that the longer chain PFCAs have been building-up in human serum. Possible reasons for such a build-up include the persistence of the sources and the longer half-lives of these compounds compared to PFOA.54,55 It would be interesting to keep monitoring these compounds in biota samples. Correlation Trends between PFCs. Statistically significant correlations existed not only for the closely related PFOS PFHxS pair, but also for other related PFCs, including PFOS and PFOA, PFOS and PFOSA, PFOSA and Et-PFOSA, and PFHxS and PFOA (Table 2a c). Moreover, there was a decreasing trend in the correlation between these compounds from the 1960s to 2009. As mentioned above, the longer exposure time, multiple exposure sources and different half-lives for these compounds contribute to the decreasing trend in correlation. Interestingly, however, there was an increasing trend in the correlation between long chain PFCA compounds. Most of these compounds were not detected in the 1960s, and, therefore, only data from the 1980s and 2009 were available for comparison. Correlation coefficients for PFNA and PFDA increased from 0.28 to 0.74; for PFNA and PFOA from 0.30 to 0.72; and for PFDA and PFUA from 0.21 to 0.68 (Table 2b and 2c). One reason for the change might be the changes of PFCA sources: the manufacturing of ammonium perfluorooctanoate (APFO) by the ECF process ceased by 2002 in the U.S.2 whereas the fluoropolymer manufacturing process of APFO and APFN (ammonium perfluorononanoate) became the major source of PFCAs. It would be interesting to observe whether or not the trend continues in the future. A limitation of our study is the fact that it was based on a convenience sample of three discrete populations of California women that was not selected in any statistically based way. The 1960s group was comprised of pregnant women who were younger than the other two groups. Metabolic changes and blood volume expansion during pregnancy are known to alter body burdens of many chemical contaminants. In particular, albumin levels are lower during pregnancy56 and PFCs bind to it.57 Interestingly, in a study using NHANES data, pregnant women had lower PFOS levels than nonpregnant women.56 Therefore, the 1960s PFOS levels could have been even higher if nonpregnant women had been sampled, further supporting the downward trend we observed. Our study is the first to report time trends of PFCs in California women over the last 50 years. The changes in the concentrations of the PFCs in serum samples from the 1960s to 2009 indicate increasing exposure during the time of wide usage of these chemicals and then decreasing exposure once the contaminant sources were reduced or removed. While contemporary levels seem to be in agreement with NHANES, we found unexpectedly high levels of PFOS and PFHxS in the 1960s samples. We are currently exploring these chemicals as risk factors in our original epidemiologic study of thyroid effects. The relative profiles of PFCs have changed over time, probably reflecting patterns of use and contemporary patterns are similar to NHANES. In addition, we found increasing trends in levels of longer chain PFCAs which were present in the majority of the contemporary serum samples. 7514
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’ ASSOCIATED CONTENT
bS
Supporting Information. Descriptions of methods and PFC concentrations for individual samples. This material is available free of charge via the Internet at http://pubs.acs.org.
’ AUTHOR INFORMATION Corresponding Author
*Phone: (510) 540-2925; fax: (510) 540-2305; e-mail: mwang@ dtsc.ca.gov.
’ ACKNOWLEDGMENT We thank W. Guo, F.R. Brown, S. Harwani (ECL, DTSC); A. Calafat, M. Davis (CDC); K. Kannan (NYDPH); C. Huset (MN DPH) for their support and help in sharing samples, interlaboratory reference materials, and discussion. We thank Drs. Mary A. Kaiser and Barbara S. Larsen of DuPont Corporate Center for Analytical Sciences for reviewing an early draft and providing us with insightful comments. The ideas and opinions expressed herein are those of the authors and do not necessarily reflect the official position of the California Department of Toxic Substances Control. ’ REFERENCES (1) Houde, M.; Martin, J. W.; Letcher, R. J.; Solomon, K. R.; Muir, D. C. G. Biological monitoring of polyfluoroalkyl substances: A review. Environ. Sci. Technol. 2006, 40 (11), 3463–3473. (2) Prevedouros, K.; Cousins, I. T.; Buck, R. C.; Korzeniowski, S. H. Sources, fate and transport of perfluorocarboxylates. Environ. Sci. Technol. 2006, 40 (1), 32–44. (3) Giesy, J. P.; Kannan, K. Global distribution of perfluorooctane sulfonate in wildlife. Environ. Sci. Technol. 2001, 35 (7), 1339–1342. (4) Kato, K.; Calafat, A. M.; Needham, L. L. Polyfluoroalkyl chemicals in house dust. Environ. Res. 2009, 109 (5), 518–523. (5) Jin, Y. H.; Liu, W.; Sato, I.; Nakayama, S. F.; Sasaki, K.; Saito, N.; Tsuda, S. PFOS and PFOA in environmental and tap water in China. Chemosphere 2009, 77 (5), 605–611. (6) Martin, J. W.; Smithwick, M. M.; Braune, B. M.; Hoekstra, P. F.; Muir, D. C. G.; Mabury, S. A. Identification of long-chain perfluorinated acids in biota from the Canadian Arctic. Environ. Sci. Technol. 2003, 38 (2), 373–380. (7) Martin, J. W.; Whittle, D. M.; Muir, D. C. G.; Mabury, S. A. Perfluoroalkyl contaminants in a food web from Lake Ontario. Environ. Sci. Technol. 2004, 38 (20), 5379–5385. (8) Brede, E.; Wilhelm, M.; G€oen, T.; M€uller, J.; Rauchfuss, K.; Kraft, M.; H€olzer, J. Two-year follow-up biomonitoring pilot study of residents’ and controls’ PFC plasma levels after PFOA reduction in public water system in Arnsberg, Germany. Int. J. Hygiene Environ. Health 2010, 213 (3), 217–223. (9) De Silva, A. O.; Mabury, S. A. Isolating isomers of perfluorocarboxylates in polar bears (Ursus maritimus) from two geographical locations. Environ. Sci. Technol. 2004, 38 (24), 6538–6545. (10) Delinsky, A. D.; Strynar, M. J.; McCann, P. J.; Varns, J. L.; McMillan, L.; Nakayama, S. F.; Lindstrom, A. B. Geographical distribution of perfluorinated compounds in fish from Minnesota lakes and rivers. Environ. Sci. Technol. 2010, 44 (7), 2549–2554. (11) Houde, M.; Czub, G.; Small, J. M.; Backus, S.; Wang, X.; Alaee, M.; Muir, D. C. G. Fractionation and bioaccumulation of perfluorooctane sulfonate (PFOS) isomers in a Lake Ontario food web. Environ. Sci. Technol. 2008, 42 (24), 9397–9403. (12) Smithwick, M.; Norstrom, R. J.; Mabury, S. A.; Solomon, K.; Evans, T. J.; Stirling, I.; Taylor, M. K.; Muir, D. C. G. Temporal trends of perfluoroalkyl contaminants in polar bears (Ursus maritimus) from two
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