- Email: [email protected]
Per- and polyfluoroalkyl substance (PFAS) exposure assessment in a community exposed to contaminated drinking water, New Hampshire, 2015
International Journal of Hygiene and Environmental Health xxx (xxxx) xxx–xxx
Contents lists available at ScienceDirect
International Journal of Hygiene and Environmental Health journal homepage: www.elsevier.com/locate/ijheh
Per- and polyfluoroalkyl substance (PFAS) exposure assessment in a community exposed to contaminated drinking water, New Hampshire, 2015 ⁎
⁎
Elizabeth R. Dalya, , Benjamin P. Chana, , Elizabeth A. Talbota,b, Julianne Nassifa,1, Christine Beana, Steffany J. Cavalloa,2, Erin Metcalfa, Karen Simonec,g, Alan D. Woolfd,e,f a
New Hampshire Department of Health and Human Services, Concord, NH, United States Geisel School of Medicine at Dartmouth, Hanover, NH, United States c Northern New England Poison Center, Portland, ME, United States d Region 1 New England Pediatric Environmental Health Specialty Unit, Boston, MA, United States e Pediatric Environmental Health Center, Division of General Pediatrics, Department of Medicine, Boston Children’s Hospital, Boston, MA, United States f Harvard Medical School, Boston, MA, United States g School of Medicine, Tufts University, Boston, MA, United States b
A R T I C L E I N F O
A B S T R A C T
Keywords: Perfluoroalkyl substances Polyfluoroalkyl substances PFAS Biomonitoring Chemical Drinking water contamination
Background: Per- and polyfluoroalkyl substances (PFAS) are synthetic chemicals used in manufacturing that resist environmental degradation, can leach into drinking water, and bioaccumulate in tissues. Some studies have shown associations with negative health outcomes. In May 2014, a New Hampshire public drinking water supply was found to be contaminated with PFAS from a former U.S. Air Force base. Objectives: We established a serum testing program to assess PFAS exposure in the affected community. Methods: Serum samples and demographic and exposure information were collected from consenting eligible participants. Samples were tested for PFAS at three analytical laboratories. Geometric means and 95% confidence intervals were calculated and analyzed by age and exposure variables. Results: A total of 1578 individuals provided samples for PFAS testing; > 94% were found to have perfluorooctane sulfonic acid (PFOS), perfluorooctanoic acid (PFOA), and perfluorohexane sulfonic acid (PFHxS) detectable in serum. Geometric mean serum concentrations of PFOS, PFOA, and PFHxS were 8.6 μg/L (95% CI:8.3–8.9), 3.1 μg/L (95% CI: 3.0–3.2), and 4.1 μg/L (95% CI: 3.9–4.3), respectively, which were statistically higher than the general U.S. population. Significant associations were observed between PFAS serum concentrations and age, time spent in the affected community, childcare attendance, and water consumption. Conclusions: PFOS, PFOA, and PFHxS were found in significantly higher levels in the affected population, consistent with PFAS drinking water contamination. Given increased recognition of PFAS contamination in the U.S, a coordinated national response is needed to improve access to biomonitoring and understand health impacts.
1. Introduction Per- and polyfluoroalkyl substances (PFAS) are a diverse group of synthetic chemicals first produced by the 3 M Company in the 1940’s (Lindstrom et al., 2011). Their water-, stain-, and grease-resistant properties are exploited for multiple different commercial and industrial products and applications. Unfortunately, these same properties contribute to slow environmental degradation, which has resulted
in widespread environmental contamination of soil and water (Giesy and Kannan 2001; Yamashita et al., 2005), and detectable serum levels of PFAS in most people around the world, including the United States (Kannan et al., 2004; Calafat et al., 2007; Olsen et al., 2008; Kato et al., 2011). Individuals are exposed to these chemicals primarily through ingestion of contaminated food, water, and dust; however, young children may ingest them through hand-to-mouth behavior after touching surfaces treated with PFAS in the home environment (Trudel
Abbreviations: LOD, limit of detection; NHANES, National Health and Nutrition Examination Survey; NHDHHS, New Hampshire Department of Health and Human Services; PFAS, Perand polyfluoroalkyl substance; PFOS, perfluorooctane sulfonic acid; PFOA, perfluorooctanoic acid; PFHxS, perfluorohexane sulfonic acid; PFNA, perfluorononanoic acid ⁎ Corresponding authors. E-mail address: [email protected] (E.R. Daly). 1 Present address: Association of Public Health Laboratories, Silver Spring, Maryland, United States. 2 Present address: Tennessee Department of Health, Nashville, Tennessee United States. https://doi.org/10.1016/j.ijheh.2018.02.007 Received 22 November 2017; Received in revised form 30 January 2018; Accepted 14 February 2018 1438-4639/ © 2018 Elsevier GmbH. All rights reserved.
Please cite this article as: Daly, E.R., International Journal of Hygiene and Environmental Health (2018), https://doi.org/10.1016/j.ijheh.2018.02.007
International Journal of Hygiene and Environmental Health xxx (xxxx) xxx–xxx
E.R. Daly et al.
consumed contaminated drinking water while working on, living on, or attending childcare at the former Air Force base, while it was an active base or in the civilian community of Pease after the base closure. Infants or children who were exposed in-utero, or by breastfeeding, through their mother’s consumption of contaminated drinking water were also eligible. Enrollment and sample collection began in April 2015 and ended in October 2015. The serum testing program was submitted to the Committee for the Protection of Human Subjects at Dartmouth College and designated as public health surveillance, not research, and therefore exempt from Institutional Review Board (IRB) review. Individuals interested in participating in the serum testing program were asked to call a NH DHHS public inquiry line to determine eligibility and register for testing. Eligible participants were sent educational material about PFAS and serum testing, including information about the inability to correlate a person’s PFAS serum levels with any health outcomes. Individuals were also sent a consent form and questionnaire that collected demographic information and self-reported information about water consumption on Pease, time spent on Pease, time since last on Pease, and childcare attendance. The questionnaire did not assess most other potential sources of PFAS exposure.
et al., 2008; Lorber and Egeghy 2011; Gebbink et al., 2015). In the body, certain PFAS, including perfluorooctanoic acid (PFOA), perfluorooctane sulfonic acid (PFOS), and perfluorohexane sulfonic acid (PFHxS) have long half-lives. Initial half-life estimates in occupational workers for PFOA, PFOS, and PFHxS were 3.8 years, 5.4 years, and 8.5 years (arithmetic mean), respectively (Olsen et al., 2007); however, a more recent study in a Swedish community exposed to PFAS through drinking water contamination have shown shorter half-lives of 2.7 years, 3.4 years, and 5.3 years, respectively (Li et al., 2018). Because of their widespread use, their persistence in the environment, and the concern for possible health impact, the Environmental Protection Agency (EPA) has worked with manufacturers of PFOS and PFOA to eliminate these compounds from emissions and products since 2002 (EPA, 2016a), and overall exposure has been declining in the United States human population over the past 15 years (CDC, 2017). Identification of PFAS contaminated drinking water supplies, however, will likely be an issue of increasing concern for many communities in the United States in the future. Though PFAS are not currently regulated under the Safe Drinking Water Act, the EPA conducts a national monitoring program for unregulated drinking water contaminants; every five years the EPA publishes a list of unregulated contaminants to be monitored in public drinking water systems (SDWA, 1996). In 2012, PFOS and PFOA were added to the third Unregulated Contaminant Monitoring Rule (UCMR 3), which required all public drinking water systems serving more than 10,000 people to monitor for these contaminants by December 2015 (EPA, 2016a,b). Pease Air Force Base in New Hampshire closed in 1991 under the U.S. Base Realignment and Closure Act, and the site was transitioned to a civilian business and aviation community employing more than 9500 individuals to support its more than 250 businesses, public offices, restaurants, and childcare facilities. The public water system was comprised of three different wells blended together prior to distribution. In May 2014, one of the three drinking water wells was identified to have PFAS contamination with various PFAS, including PFOA (0.35 μg/L), PFOS (2.50 μg/L), and PFHxS (0.83 μg/L) (NH DHHS, n.d.). The levels of PFOA and PFOS were near or above the Provisional Health Advisory (PHA) set by the EPA in 2009 for PFOA and PFOS, (0.4 ug/L and 0.2 ug/L respectively); however, there was no health advisory level for PFHxS (EPA, 2009). In 2016, the EPA revised its drinking water PHA to a lifetime Health Advisory for PFOA and PFOS recommending that levels of PFOA and PFOS, either individually or combined, not exceed 0.07 ug/L, a value that has also been adopted by New Hampshire (EPA, 2016a,b). The contamination likely occurred as a result of the use of aqueous film-forming foam (AFFF) to combat and prevent fuel-based fires and to train military firefighting personnel while the U.S. Air Force base was operational. The contaminated well was shut down and the New Hampshire Department of Health and Human Services (NH DHHS) initiated a PFAS serum testing program to address public concerns about human exposure. The purpose of the testing program was to provide community members with more information about their individual and collective levels of exposure. The results of this testing program are among the first from a state public health response to PFAS exposure from drinking water contamination related to use of AFFF on a U.S. military base.
2.2. Laboratory analyses Individuals who returned a completed questionnaire and consent form were mailed a laboratory requisition and instructions for blood draw. Serum samples were collected at a local partnering hospital and transported to the NH DHHS Public Health Laboratories where the specimens were processed, de-identified, labeled with a unique patient identification number, and shipped in batches to one of three out-ofstate testing laboratories, including the U.S. Centers for Disease Control and Prevention (CDC, Atlanta, Georgia), AXYS Analytical (Sidney, British Columbia, Canada), and the California State biomonitoring laboratories (Richmond, California). Multiple laboratories were required due to a high demand for clinical testing, and limited testing capacity at each laboratory. Each laboratory tested for a different panel of PFAS, but a common subset of seven PFAS was included by all three laboratories (Table 1). All laboratories used the same testing methodology that separated, identified, and measured PFAS present in the serum specimens by liquid chromatography tandem mass spectrometry. (LC/ MS/MS) following solid-phase extraction. Each laboratory used an approved quality management system that included method validation with acceptable precision and accuracy, instrument calibration, quality indicators for acceptable performance, standard operating procedures for analysis and data review, and successful participation in an external proficiency testing program (CTQ, n.d.). Table 1 lists the PFAS tested at each laboratory and the corresponding limits of detection, which varied by laboratory and analyte. Collection, processing and transport of specimens from eligible participants who lived outside of the hospital catchment area were facilitated through the public health laboratories in their home states, in consultation with study investigators. 2.3. Statistical analyses For all statistical analyses, test results below each laboratory’s limit of detection were assigned a value equal to the laboratory’s respective limit of detection divided by the square root of two (CDC, 2017). Summary test statistics were calculated including medians, geometric means, 95th percentiles, maximums, and detection frequencies for each PFAS and compared to National Health and Nutrition Examination Survey (NHANES) data (CDC, 2017, Ye et al., 2018). Consistent with statistical methods for NHANES analyses, summary statistics for each PFAS are shown only if 60% or more of samples tested above the limit of detection for that PFAS in order to provide a valid result. Nonoverlapping confidence intervals were considered statistically different. An assessment of relationships between each individual demographic and exposure characteristic and PFAS serum concentration was
2. Material and methods 2.1. Enrollment and exposure assessment The serum testing program was designed and implemented with input from the community and with direction from elected officials. Eligibility criteria and instructions for participation were posted in public places, reported through press releases and via letters to employees of affected businesses. Individuals self-identified as eligible to participate in the serum testing program if they had, at any time, 2
International Journal of Hygiene and Environmental Health xxx (xxxx) xxx–xxx
E.R. Daly et al.
Table 1 Per- and polyfluoroalkyl substance testing panel and corresponding limits of detection by testing laboratory, Pease PFAS Serum Testing Program, New Hampshire, 2015. PFAS Name
Perfluorooctane sulfonic acid Perfluorooctanoic acid Perfluorohexane sulfonic acid Perfluorononanoic acid Perfluorodecanoic acid Perfluoroundecanoic acid Perfluorooctane sulfonamide 2-(N-methyl-perfluorooctane sulfonamido) acetic acid 2-(N-ethyl-perfluorooctane sulfonamido) acetic acid Perfluorobutane sulfonic acid Perfluoorododecanoic acid Perfluoroheptanoic acid
PFAS Abbreviation
PFOS PFOA PFHxS PFNA PFDeA PFUA PFOSA Me-PFOSA-AcOH Et-PFOSA-AcOH PFBuS PFDoA PFHpA
Limit of Detection (LOD) (ug/L) CDC
AXYS
CA State
0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 not tested not tested not tested
1.0 0.5 1.0 0.5 0.5 0.5 0.5 not not not not not
0.144 0.072 0.019 0.045 0.073 0.030 0.016 0.020 0.028 0.050 0.115 0.100
tested tested tested tested tested
Number of Samples Tested
Number Above LOD n (%)
1578 1578 1578 1578 1578 1578 1578 878 878 107 107 107
1574 (99.8) 1566 (99.2) 1487 (94.2) 1345 (85.2) 664 (42.1) 474 (30.0) 31 (2.0) 317 (36.1) 23 (2.6) 20 (18.7) 5 (4.7) 1 (0.9)
LOD: limits of detection PFAS: per- and polyfluoroalkyl substance; CDC: U.S. Centers for Disease Control and Prevention (Atlanta, GA); AXYS: AXYS Analytical (Sidney, British Columbia, Canada); CA State: California State biomonitoring laboratories (Richmond, CA).
2.9–3.1, respectively) but not for PFOS (8.1 μg/L, 95% CI: 7.6–8.7 vs. 8.7 μg/L, 95% CI: 8.4–9.1, respectively) and PFHxS (3.8 μg/L, 95% CI: 3.5–4.2 vs. 4.2 μg/L, 95% CI: 4.0–4.5, respectively). Differences were identified when stratifying further by age group and gender (Table 3). The geometric mean for each age group was compared with the youngest age group (0–2 year olds), which served as a reference group for the statistical comparison. Mean serum concentrations of PFOS and PFHxS showed a bimodal distribution, with significantly higher levels found in 3–5 year old children and adults over 40 years of age when compared with the youngest group (Fig. 1, Table 3). Levels of PFOS, PFOA, and PFHxS declined in later childhood and adolescence before increasing starting at 20 years of age. Males had significantly higher PFOS, PFOA, and PFHxS serum concentrations compared with females. To further explore the observation that 3–5 year olds demonstrated higher serum PFAS concentrations than other children, we evaluated attendance at either of the two childcare facilities on the base, which primarily accommodate children 6 weeks up to 5 years of age. As compared to children that did not attend childcare on the base (i.e. children exposure through breastfeeding or in-utero), childcare attendees were observed to have significantly higher PFOS (8.8 μg/L vs. 5.4 μg/L, p < 0.0001), PFOA (3.6 μg/L vs. 2.7 μg/L, p = .0012), and PFHxS (4.6 μg/L vs. 1.5 μg/L, p < 0.0001) serum concentrations. This finding was observed for all age groups of children but was most pronounced for children 3–5 years old (Fig. 2). When comparing serum levels by reported water consumption on Pease, only PFHxS showed significantly higher geometric mean serum concentrations for participants that consumed 4–7 or 8+ cups of water per day on Pease compared with those who drank only 0–3 cups per day (Table 3). PFOS, PFOA, and PFHxS serum concentrations increased with increasing time spent on Pease, which was most pronounced for PFOS and PFHxS (Table 3). Interestingly, those who had last been on Pease 20+ years prior had the highest serum concentrations of PFOS, PFOA, and PFHxS (Table 3).
conducted using non-parametric analysis of variance with post-hoc testing. Only results for PFOS, PFOA, and PFHxS are provided in this report because more than 90% of participants had these PFAS detected in their serum and geometric means were significantly higher compared with the general U.S. population for these three PFAS. For participants who reported a range for volume of water consumption on Pease (approximately 30% of respondents), the average of the range was calculated and used in all water consumption analyses. The Kruskal-Wallis test was used to assess individual relationships between PFAS serum concentration and age, sex, water consumption, time spent on Pease, time since last on Pease, and childcare attendance. Where significant relationships existed, post-hoc analyses of ranked data were performed using a Bonferroni adjustment for multiple comparisons to identify which groups were significantly different from a reference group. SAS version 9.3 (SAS Institute Inc., Cary, NC) was used to analyze data; pvalues less than 0.05 were considered statistically significant. 3. Results 3.1. Serum testing results A total of 1578 eligible individuals provided serum samples for testing between April and October 2015. In total, 771 samples (49%) were tested at the CDC laboratory, 700 (44%) at AXYS, and 107 (7%) at the CA State laboratory. Most serum specimens had detectable levels of PFOS (99.8%), PFOA (99.2%), PFHxS (94.2%), and PFNA (85.2%). Summary statistics are not presented for the other PFAS because too high a proportion of samples were below the testing laboratory’s limit of detection to provide a valid result. In comparison to NHANES U.S. population data (CDC, 2017, Ye et al., 2018), geometric means for three PFAS (PFOS, PFOA, PFHxS) were found to be significantly higher (Table 2). In comparison to corresponding age-stratified NHANES data, geometric means for PFOS, PFOA, and PFHxS were significantly higher in all age groups except for the 12–19 years age group, which only observed a higher PFOS level; comparison data were not available for 0–2 year olds (Table 2).
4. Discussion PFAS may be linked to adverse health outcomes in humans. Reviews of epidemiological studies suggest that there may be changes in uric acid levels, liver function tests, effects on lipid metabolism, thyroid function, growth and development, immune function, and certain types of cancers attributable to exposure to sources of PFAS (ATSDR, 2015; EPA, 2016a,b; NTP, 2016; IARC, 2016). For this reason, people living in communities in which PFAS contamination of drinking water has been confirmed have called for this source of exposure to be addressed as a public health issue. Most participants in the 2015 NH Pease PFAS serum
3.2. Participant characteristics and exposure assessment The majority of participants were female (n = 856, 57.3%), aged 20 years or older (n = 1181, 74.8%), had spent fewer than 10 years on Pease (n = 882, 68.5%), and had recent exposure (within the previous year) to drinking water on Pease (n = 948, 73.6%) (Table 3). When comparing overall levels for children (age 11 and younger) with adolescents and adults (age 12 and older), mean serum levels of PFOA were significantly higher (3.4 μg/L, 95% CI: 3.2–3.6 vs. 3.0 μg/L, 95% CI: 3
International Journal of Hygiene and Environmental Health xxx (xxxx) xxx–xxx
E.R. Daly et al.
Table 2 Summary of per- and polyfluoroalkyl substance serum concentrations in the exposed testing population compared with NHANES, New Hampshire, 2015. CDC, 2017; Ye et al., 2018. PFAS
PFOS Total Age Groups: 0-2 years 3–5 years 6–11 years 12–19 years 20+ years PFOA Total Age Groups: 0-2 years 3–5 years 6–11 years 12–19 years 20+ years PFHxS Total Age Groups: 0-2 years 3–5 years 6–11 years 12–19 years 20+ years PFNA Total Age Groups: 0-2 years 3–5 years 6–11 years 12–19 years 20+ years
n
Pease Testing Population (μg/L)
NHANES 2013–2014 Data (μg/L)
Median
Geometric Mean
95% CI
95th Percentile
Max
n
Geometric Mean
95% CI
95th Percentile
1578
8.90
8.59a
8.28−8.91
27.40
95.60
2165
4.99
4.50−5.52
18.50
75 164 127 31 1181
6.47 10.10 7.58 5.20 9.30
6.25 9.81a 7.41a 5.39a 8.85a
5.29−7.38 8.98−10.72 6.65−8.25 4.42−6.57 8.47−9.25
18.40 24.40 20.70 12.90 30.00
28.50 30.80 29.30 18.10 95.60
– 181 458 401 1764
– 3.38 4.15 3.54 5.22
– 3.04−3.77 3.76−4.58 3.17−3.96 4.70−5.81
– 8.82 12.4 9.30 19.5
1578
3.20
3.09a
2.99−3.19
8.65
32.00
2165
1.94
1.76−2.14
5.57
75 164 127 31 1181
3.83 4.31 2.56 1.60 3.16
3.47 4.12a 2.69a 1.62 3.04a
2.98−4.05 3.83−4.44 2.44−2.98 1.29−2.03 2.92−3.16
10.60 8.70 6.50 4.74 9.00
12.00 11.60 9.29 5.73 32.00
– 181 458 401 1764
– 2.00 1.89 1.66 1.98
– 1.75−2.29 1.72−2.07 1.50−1.84 1.79−2.19
– 5.58 3.84 3.47 5.60
1578
4.20
4.12a
3.92−4.33
20.00
116.00
2168
1.35
1.20−1.52
5.60
75 164 127 31 1181
2.60 6.06 3.70 2.30 4.25
2.63 5.11a 3.30a 1.92 4.30a
2.08−3.33 4.47−5.84 2.84−3.84 1.49−2.49 4.06−4.55
12.50 15.60 11.40 4.80 21.80
19.70 31.70 19.50 7.50 116.00
– 181 458 402 1766
– 0.72 0.91 1.27 1.36
– 0.62−0.83 0.80−1.04 1.06−1.53 1.21−1.53
– 1.62 4.14 6.30 5.50
1578
0.74
0.73
0.70−0.75
1.96
5.20
2168
0.68
0.61−0.74
2.00
75 164 127 31 1181
0.74 1.03 0.90 0.40 0.70
0.76 1.01 0.90 0.49 0.68
0.65−0.90 0.92−1.12 0.80−1.01 0.38−0.63 0.66−0.71
2.60 2.58 3.49 1.82 1.66
5.16 5.20 4.46 1.98 4.90
– 181 458 402 1766
– 0.76 0.81 0.60 0.69
– 0.63−0.93 0.68−0.96 0.49−0.73 0.63−0.75
– 3.49 3.19 2.00 2.00
CI = confidence interval, NHANES=National Health and Nutrition Examination Survey, PFAS = Per- and polyfluoroalkyl substance, PFOS = Perfluorooctane sulfonic acid, PFOA = Perfluorooctanoic acid, PFHxS = Perfluorohexane sulfonic acid, PFNA = Perfluorononanoic acid. Note: Only PFAS detected in at least 60% of samples tested are shown. a Geometric mean is significantly higher than NHANES comparison data – Comparison data not available.
These sex-related differences in PFAS levels may be due to difference in clearances related to elimination through menstrual blood losses, transfers during lactation, or transplacental transfer during pregnancy (Papadopoulou et al., 2016; Wong et al., 2014). The two PFAS that were found in the highest levels in the contaminated well (PFOS and PFHxS) were found in significantly higher concentrations in the 3–5 and 40+ year old age groups compared with the youngest age group. PFOS, PFOA, and PFHxS levels all declined in late childhood and adolescence and then increased after age 20. A significant relationship between childcare attendance on Pease and serum concentrations for PFOS, PFOA, and PFHxS was observed for children under the age 12 years old, and especially for 3–5 year olds. This finding suggests that exposure on Pease likely represents a significant source of PFAS for these children. Studies of the general U.S. adolescent and adult population have shown conflicting results when assessing differences in PFAS levels by age. Some studies have found no difference in PFAS levels by age (Olsen et al., 2008; Calafat et al., 2007) but a more recent study found significant increases in PFOS, PFOA, and PFNA with increasing age (Kato et al., 2011). Studies of children have also shown conflicting results (Schecter et al., 2012; Olsen et al., 2004). The differences likely illustrate the complex pattern of age, behavior, and PFAS exposure. Age may play a significant role in exposure because childhood behaviors can predispose to PFAS exposure, including hand-to-mouth behavior, which is most prominent in younger children and decreases with age (Trudel et al., 2008). While drinking water exposure likely contributed to the elevation of PFOS, PFOA, and PFHxS levels in the 3–5 year old
testing program (more than 94%) were found to have PFOS, PFOA, and PFHxS detectable in their serum; this is consistent with other studies of children, adolescents, and adults (Kato et al., 2011; Olsen et al., 2008; Calafat et al., 2007; Schecter et al., 2012). Average levels of three PFAS compounds (PFOS, PFOA, and PFHxS) in the exposed Pease community were higher than levels found in the general U.S. adult and adolescent population (CDC, 2017). Levels of all three PFAS in this community were substantially lower than those found in other occupationally- and environmentally-exposed populations (Fig. 3) (Olsen et al., 2003, 2007; Sakr et al., 2007; Frisbee et al., 2009; ATSDR, 2013; Landsteiner et al., 2014; NYSDOH, 2016; VTDOH, 2016; CDC, 2017). Drinking water consumption on Pease is likely a primary source of exposure to these PFAS, which is supported by the increasing trend in serum concentrations with increasing time spent on Pease. This trend was most notable for PFOS and PFHxS, which have longer half-lives and were found at higher concentrations in the affected well (City of Portsmouth New Hampshire, 2018). Self-reported water consumption only showed increasing PFHxS levels with increasing water consumption, and not with PFOA and PFOS, suggesting lack of precision in selfreported retrospective water consumption, which required averaging of reported ranges of water consumption in almost a third of participants. Males were found to have higher geometric mean serum levels of PFOS, PFOA, and PFHxS compared with females. This finding is consistent with other U.S. studies of PFAS levels and may represent differences in exposure between the sexes (Kato et al., 2011; Olsen et al., 2004, 2008; Calafat et al., 2007; Schecter et al., 2012; CDC, 2017). 4
International Journal of Hygiene and Environmental Health xxx (xxxx) xxx–xxx
E.R. Daly et al.
Table 3 Association between characteristics of the exposed testing population and serum per- and polyfluoroalkyl substance concentrations (μg/L), New Hampshire, 2015. Characteristics
n (%)
PFOS Geometric Mean
Age group
n = 1578 median = 40 75 (4.8) 164 (10.4) 91 (5.8) 36 (2.3) 31 (2.0) 369 (23.4) 611 (38.7) 201 (12.7)
6.25 9.81 7.89 6.31 5.39 6.94 9.35 11.72
Sex Female Male
n = 1495 856 (57.3) 639 (42.7)
7.46 10.45
Water consumption (cups per day) 0−3 4–7 8+
n = 1338 median = 4 572 (42.8) 539 (40.3) 227 (17.0)
Time spent on base (years) <1 1–4 5–9 10–19 20+
n = 1288 median = 6.5 75 (5.8) 429 (33.3) 378 (29.3) 318 (24.7) 88 (6.8)
Time since last on base (years) <1 1–4 5–9 10–19 20+
n = 1288 median = 0.0 948 (73.6) 144 (11.1) 88 (6.8) 74 (5.7) 34 (2.6)
Childcare Attendance (age < 12 only) No Yes
n = 366
0−2 3–5 6–8 9–11 12–19 20–39 40–59 60+
61 (16.7) 305 (83.3)
PFOA p-valueŦ
Post-Hoc Multiple Comparison Testing¥
Geometric Mean
< 0.0001
p-valueŦ
Post-Hoc Multiple Comparison Testing¥
3.47 4.12 2.94 2.16 1.62 2.47 3.20 3.80
N/A
ref 0.1652 0.4975 < 0.0001 < 0.0001 < 0.0001 1.0 1.0 < 0.0001
N/A
8.40 9.10 9.01
N/A
< 0.0001
ref 1.0000 0.5582 0.0212 0.0094
3.14 2.68 2.80 2.93 4.04
N/A
2.37 3.16 4.66 5.68 7.91
5.41 8.80
2.75 3.59
ref 0.0466 < 0.0001 < 0.0001 < 0.0001 < 0.0001
0.2279 0.0051 0.0225 0.1525 ref 0.0012
ref < 0.0001 0.0023 < 0.0001
0.0014 0.0043 < 0.0001 0.0210 0.0013 ref
N/A
< 0.0001 3.77 4.76 4.90
2.75 2.75 3.08 3.42 3.75
< 0.0001
ref < 0.0001 0.1048 1.0000 0.4365 1.0000 < 0.0001 < 0.0001 < 0.0001
< 0.0001 ref 0.7065 0.0003 < 0.0001 < 0.0001
8.94 7.40 9.03 7.87 13.99
2.63 5.11 3.80 2.31 1.92 3.10 4.79 5.64
N/A
2.98 3.17 3.22
6.61 7.45 9.30 10.18 11.79
Post-Hoc Multiple Comparison Testing¥
3.41 5.36 0.1102
< 0.0001
p-valueŦ
< 0.0001
2.85 3.45 0.1115
Geometric Mean
< 0.0001 ref < 0.0001 0.3406 1.0000 1.0000 1.0000 < 0.0001 < 0.0001
< 0.0001
PFHxS
4.47 3.07 4.09 3.86 8.11
N/A
0.0041 < 0.0001 0.0018 0.0028 ref < 0.0001
N/A
1.49 4.63
PFAS = Per- and polyfluoroalkyl substance, PFOS = Perfluorooctane sulfonic acid, PFOA = Perfluorooctanoic acid, PFHxS = Perfluorohexane sulfonic acid N/A: Not applicable because post-hoc testing wasn’t performed. Multiple comparison testing was only performed for statistically significant variables in the Kruskal-Wallis analysis with more than two categories. Ŧ Kruskal-Wallis test. ¥ Comparing ranked data using Bonferroni adjustment.
suspected levels of exposure would also be those who would be most worried and therefore most likely to seek testing. It was not a scientifically designed random sampling exposure assessment, which limits its generalizability and conclusions that can be drawn about exposure in the Pease population as a whole. Given the need to most responsibly use limited public health resources and the uncertainty surrounding health–related end-points, PFAS biomonitoring of affected communities should be conducted in the context of scientific studies designed to answer specific clinical questions. A consistent scientific approach is important and necessary as communities exposed to PFAS are being identified around the country. Secondly, the participant questionnaire collected information on a limited number of exposures that related to the affected community and drinking water exposure. Therefore, while the Pease serum testing results suggest drinking water exposure as a contributor, the serum PFAS levels actually represent exposure from all sources, including exposures in the home and work environments. Because PFAS have been widely used in home products and industry, there are likely other significant
age group in this community, additional exposure from home sources of PFAS through hand-to-mouth behavior, cannot be excluded. Breastfeeding can also contribute to PFAS exposure in infants since PFAS compounds can be excreted in breast milk in varying amounts depending on the compound (Mondal et al., 2014). One study showed that infant serum concentrations of PFOS and PFOA increased during the period of exclusive or partial breastfeeding; however, levels appeared to peak around 12 months of age, which is different from our described findings where average childhood PFOS and PFOA levels peaked between 3 and 5 years of age (Mogensen et al., 2015). We did not collect information on breastfeeding, and so were unable to assess its role in elevated childhood serum concentrations in the Pease population. The results of this serum testing program have several notable limitations. First, it was intentionally designed to be a convenience sample of self-selecting individuals who wanted to know their own, or their child’s, PFAS serum levels. This self-selection might have resulted in an overestimation of exposure, as the people with the highest 5
International Journal of Hygiene and Environmental Health xxx (xxxx) xxx–xxx
E.R. Daly et al.
The Pease serum testing program was not designed to be a health study and did not collect comprehensive exposure or any health outcome related information. PFAS serum testing provided affected individuals and health officials with further information about levels of exposure to PFAS from all sources of exposure, but there is not a PFAS serum level at which health effects are known or expected to occur, and the potential long term health implications from the elevated levels of exposure seen at Pease remain unclear ATSDR, 2016. Helping participants understand their test results as they relate to their health was the greatest challenge in this response. We attempted to make relative comparisons to other tested communities, but serum testing ultimately provides little actionable healthcare information. Given the uncertainty around health impact from PFAS exposure, addressing health concerns requires a multiagency coordinated response. Others have noted previously that a coordinated communication plan must be developed when conveying results of biomonitoring of PFAS to the general public (Hernick et al., 2011). NH DHHS has worked closely with the regional poison control center (Northern New England Poison Center), CDC and the Agency for Toxic Substances & Disease Registry (ATSDR), the Region 1 Pediatric Environmental Health Specialty Unit (Region 1 PEHSU), and other local environmental health physicians to try and respond to and address community and healthcare provider questions and concerns about health impacts from PFAS exposure. 5. Conclusions Biomonitoring can provide affected communities and local health departments with more information about levels of PFAS exposure, but fully understanding sources and duration of exposure is challenging given the widespread use of these chemicals in our home and work environments. The serum testing program described here was one of the first public health responses in the nation to try and address concerns from PFAS exposure related to a U.S. Department of Defense site of contamination. It was an active public health response that was designed to address community concerns and was developed with input from the community and at the behest of elected officials. While we were able to provide PFAS testing to all affected individuals who wanted it, this public health response presented many challenges including identifying funds to support the testing program, prolonged (greater than one year) activation of the public health incident response team, defining the appropriate roles and responsibilities of the various federal, state, and local entities involved, and public and provider communication. The scenario described in this report is beginning to play out across the United States in other jurisdictions as PFAS drinking water contamination is identified related to military or industry contamination. Communicating exposure risk, test results, and uncertainty regarding health effects requires a national coordinated response from federal and state agencies to address health concerns through additional research and consistent messaging and recommendations to communities, public health agencies, and healthcare providers.
Fig. 1. Per- and polyfluoroalkyl substance serum concentrations in the exposed testing population by age group in years, New Hampshire, 2015 (n = 1578). PFAS = Per- and polyfluoroalkyl substance, PFOS = Perfluorooctane sulfonic acid, PFOA = Perfluorooctanoic acid, PFHxS = Perfluorohexane sulfonic acid. Note: The box represents the interquartile range, which is intersected by a line representing the median. The circle represents the geometric mean.
sources of PFAS exposure that were not evaluated in this serum testing program. Due to a lack of complete exposure information resulting in validity concerns, the data presented in this report are univariate analyses that do not take into account, using multivariate analysis techniques, the relationships between all potential factors that contribute to PFAS serum levels. Ideally any biomonitoring assessment should assess other sources of exposure as a way to inform and educate communities about PFAS exposure and to help interpret PFAS serum levels, which is very challenging because serum PFAS test results represent exposure from multiple sources over years of exposure and not just drinking water contamination. Thirdly, because of logistical considerations in such a large community-based testing program, serum samples were analyzed at three separate certified laboratories. Although their analytical techniques, limits of detection, and quality control protocols were similar, sources of measurement variation may still have contributed to minor systematic differences in the results of serum assays.
Funding and disclaimer The work conducted at the New Hampshire Department of Health and Human Services was supported, in part, by the Centers for Disease Control and Prevention (CDC), Biomonitoring cooperative agreement [grant number 5U88EH001142-01] and Public Health Emergency Preparedness cooperative agreement [grant number 5U90TP00053504]. The findings and conclusions in this report are solely the responsibility of the authors and do not necessarily represent the official views of the CDC or the Assistant Secretary for Preparedness and Response. ADW is supported by the Agency for Toxic Substances and Disease Registry (ATSDR) cooperative agreement award number 1U61TS000238-01 (to the Region 1 New England Pediatric Environmental Health Specialty Unit). The contents of this manuscript 6
International Journal of Hygiene and Environmental Health xxx (xxxx) xxx–xxx
E.R. Daly et al.
Fig. 2. Per- and polyfluoroalkyl substance serum concentrations in the exposed testing population by participant childcare attendance, New Hampshire, 2015 (n = 1578). PFAS = Per- and polyfluoroalkyl substance, PFOS = Perfluorooctane sulfonic acid, PFOA = Perfluorooctanoic acid, PFHxS = Perfluorohexane sulfonic acid. Note: Circle denotes geometric mean with corresponding 95% confidence interval.
this report, or the decision to submit this manuscript for publication.
are the responsibility of the authors and do not necessarily represent the official views of ATSDR. The U.S. Environmental Protection Agency (EPA) supports the Pediatric Environmental Health Specialty Units (PEHSU) by providing funds to ATSDR under Inter-Agency Agreement number DW-75- 92301-05. Neither EPA nor ATSDR endorse the purchase of any commercial products or services mentioned in PEHSU publications. CDC, ATSDR, and EPA did not play any role in the design of the study, the collection and interpretation of the data, the writing of
Disclosure statement The authors declare they have no actual or potential competing financial interests.
7
International Journal of Hygiene and Environmental Health xxx (xxxx) xxx–xxx
E.R. Daly et al.
Fig. 3. Mean per- and polyfluoroalkyl substance serum concentrations comparing the exposed New Hampshire Pease population with the general United States population, environmentally exposed communities, and occupationally exposed workers. PFAS = Per- and polyfluoroalkyl substance, PFOS = Perfluorooctane sulfonic acid, PFOA = Perfluorooctanoic acid, PFHxS = Perfluorohexane sulfonic acid Note: All means are geometric means except the 3M 2004 study, which is an arithmetic mean. Olsen et al., 2003, 2007; Sakr et al., 2007; Frisbee et al., 2009; ATSDR, 2013; Landsteiner et al., 2014; NYSDOH, 2016; VTDOH, 2016; CDC, 2017.
Acknowledgements
Agency for Toxic Substances & Disease Registry (ATSDR), 2015. Draft Toxicological Profile for Perfluoroalkyls. Available: https://www.atsdr.cdc.gov/toxprofiles/tp200. pdf (Accessed 18 January 2018). Agency for Toxic Substances & Disease Registry (ATSDR), 2016. Perfluoroalkyl Substances and Your Health: Health Effects of PFAS. Available: http://www.atsdr. cdc.gov/pfc/health_effects_pfcs.html (Accessed 13 February 2017). Centers for Disease Control and Prevention (CDC), 2017. Fourth National Report on Human Exposure to Environmental Chemicals: Updated Tables January 2017. . Available: https://www.cdc.gov/exposurereport/ (Accessed 22 July 2017). Centre de Toxicologie du Quebec (CTQ), 2018. AMAP: AMAP Ring Test for Persistent Organic Pollutants in Human Serum. (n.d. Available: https://www.inspq.qc.ca/en/ ctq/eqas/amap/description (Accessed 13 February 2017)). Calafat, A.M., Wong, L.-Y., Kuklenyik, Z., Reidy, J.A., Needham, L.L., 2007. Polyfluoroalkyl chemicals in the U.S. population: data from the national health and nutrition examination survey (NHANES) 2003–2004 and comparisons with NHANES 1999–2000. Environ. Health Perspect. 115, 1596–1602. City of Portsmouth, New Hampshire, 2018. Pease Well Monitoring and Sampling Results. (n.d. Available: https://www.cityofportsmouth.com/publicworks/water/pease-
We wish to thank Christine Adamski, formerly of the New Hampshire Department of Health and Human Services, and the U.S. Centers for Disease Control and Prevention, National Center for Environmental Health, Division of Laboratory Sciences and the Agency for Toxic Substances and Disease Registry for technical guidance and assistance. References Agency for Toxic Substances & Disease Registry (ATSDR), 2013. Exposure Investigation Report: PFC Serum Sampling in the Vicinity of Decatur, AL, Morgan, Lawrence, and Limestone Counties. . Available: http://www.atsdr.cdc.gov/HAC/pha/Decatur/ Perfluorochemical_Serum%20Sampling.pdf (Accessed 22 July 2017).
8
International Journal of Hygiene and Environmental Health xxx (xxxx) xxx–xxx
E.R. Daly et al.
with Exposure to Perfluorooctanoic Acid or Perfluorooctane Sulfonate. Available: https://ntp.niehs.nih.gov/ntp/ohat/pfoa_pfos/pfoa_pfosmonograph_508.pdf (Accessed 1 December 2017). New York State Department of Health (NYSOH), 2016. PFOA in Drinking Water in the Village of Hoosick Falls and Town of Hoosick, Preliminary Participant Results. Available: https://www.health.ny.gov/environmental/investigations/hoosick/ (Accessed 22 July 2017). New Hampshire Department of Health Human Services, 2018. Pease Tradeport Water System Investigation. (n.d. Available: http://www.dhhs.nh.gov/dphs/investigationpease.htm Accessed 31 July 2017). Olsen, G.W., Burris, J.M., Burlew, M.M., Mandel, J.H., 2003. Epidemiologic assessment of worker serum perfluorooctanesulfonate (PFOS) and perfluorooctanoate (PFOA) concentrations and medical surveillance examinations. J. Occup. Environ. Med. 45, 260–270. Olsen, G.W., Church, T.R., Hansen, K.J., Burris, J.M., Butenhoff, J.L., Mandel, J.H., et al., 2004. Quantitative evaluation of perfluorooctanesulfonate (PFOS) and other fluorochemicals in the serum of children. J. Child Health 2, 53–76. Olsen, G.W., Burris, J.M., Ehresman, D.J., Froehlich, J.W., Seacat, A.M., Butenhoff, J.L., et al., 2007. Half-life of serum elimination of perfluorooctanesulfonate, perfluorohexanesulfonate, and perfluorooctaneoate in retired fluorochemicals production workers. Environ. Health Perspec. 115, 1298–1305. Olsen, G.W., Mair, D.C., Church, T.R., Ellefson, M.E., Reagen, W.K., Boyd, T.M., et al., 2008. Decline in perfluorooctanesulfonate and other polyfluoroalkyl chemicals in American Red Cross adult blood donors, 2000–2006. Environ. Sci. Technol. 42, 4989–4995. Papadopoulou, E., Sabaredzovic, A., Namork, E., Nygaard, U.C., Granum, B., Haug, L.S., 2016. Exposure of Norwegian toddlers to perfluoroalkyl substances (PFAS): the association with breastfeeding and maternal PFAS concentrations. Environ. Int. 94, 687–694. Safe Drinking Water Act Amendments of 1996, 1996. 42 USC 300f. Sakr, C.J., Kreckmann, K.H., Green, J.W., Gillies, P.J., Reynolds, J.L., Leonard, R.C., 2007. Cross-sectional study of lipids and liver enzymes related to a serum biomarker of exposure (ammonium perfluorooctanoate or APFO) as part of a general health survey in a cohort of occupationally exposed workers. J. Occup. Environ. Med. 49, 1086–1096. Schecter, A., Malik-Bass, N., Calafat, A.M., Kato, K., Colacino, J.A., Gent, T.L., et al., 2012. Polyfluoroalkyl compounds in Texas children from birth through 12 years of age. Environ. Health Perspec. 120, 590–594. Trudel, D., Horowitz, L., Wormuth, M., Scheringer, M., Cousins, I.T., Hungerbuhler, K., 2008. Estimating consumer exposure to PFOS and PFOA. Risk Anal. 28, 251–269. Vermont Department of Health (VTDOH), 2016. PFOA Blood Test Results for Bennington/ North Bennington. Available: http://healthvermont.gov/enviro/pfoa_clinics.aspx# info (Accessed 22 July 2017). Wong, F., MacLeod, M., Mueller, J.F., Cousins, I.T., 2014. Enhanced elimination of perfluorooctane sulfonic acid by menstruating women: evidence from population-based pharmacokinetic modeling. Environ. Sci. Technol. 48 (15), 8807–8814. Yamashita, N., Kannan, K., Taniyasu, S., Horii, Y., Petrick, G., Gamo, T., 2005. A global survey of perfluorinated acids in oceans. Mar. Pollut. Bull. 51, 658–668. Ye, X., Kato, K., Wong, L.Y., Jia, T., Kalathil, A., Latremouille, J., Calafat, A.M., 2018. Perand polyfluoroalkyl substances in sera from children 3–11 years of age participating in the National Health and Nutrition Examination Survey 2013–2014. Int. J. Hyg. Environ. Health 221, 9–16.
tradeport-water-system#wellmonitoring (Accessed 1 September 2017)). Environmental Protection Agency (EPA), 2009. Provisional Health Advisories for Perfluorooctanoic Acid (PFOA) and Perfluorooctane Sulfonate (PFOS). Available: https://www.epa.gov/dwstandardsregulations/provisional-health-advisoriesperfluorooctanoic-acid-pfoa-and-perfluorooctane (Accessed 9 August 2016). Environmental Protection Agency (EPA), 2016a. Drinking Water Health Advisory for Perfluorooctanoic Acid (PFOA). Available: https://www.epa.gov/sites/production/ files/2016-05/documents/pfos_health_advisory_final_508.pdf (Accessed 13 February 2017). Environmental Protection Agency (EPA), 2016b. Drinking Water Health Advisory for Perfluorooctane Sulfonate (PFOS). Available: https://www.epa.gov/sites/ production/files/2016-05/documents/pfos_health_advisory_final_508.pdf (Accessed 13 February 2017). Frisbee, S.J., Brooks, A.P., Maher, A., Flensborg, P., Arnold, S., Fletcher, T., et al., 2009. The C8 Health Project: design, methods, and participants. Env Health Persp 117, 1873–1882. Gebbink, W.A., Berger, U., Cousins, I.T., 2015. Estimating human exposure to PFOS isomers and PFCA homologues: the relative importance of direct and indirect (precursor) exposure. Environ. Int. 74, 160–169. Giesy, J.P., Kannan, K., 2001. Global distribution of perfluorooctane sulfonate in wildlife. Environ. Sci. Technol. 35, 1339–1342. Hernick, A.D., Brown, K., Piinney, S.M., Biro, F.M., Ball, K.M., Bornschein, R.L., 2011. Sharing unexpected biomarker results with study participants. Environ. Heal. Persp. 119, 1–5. International Agency for Research on Cancer (IARC), 2016. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, Volume 110: Perfluorooctanoic Acid. Available at: http://monographs.iarc.fr/ENG/Monographs/vol110/mono110-01.pdf (Accessed 14 September 2017). Kannan, K., Corsolini, S., Falandysz, J., Fillmann, G., Kumar, K.S., Loganathan, B.G., et al., 2004. Perfluorooctanesulfonate and related fluorochemicals in human blood from several countries. Environ. Sci. Technol. 38, 4489–4495. Kato, K., Wong, L.-Y., Jia, L.T., Kuklenyik, Z., Calafat, A.M., 2011. Trends in exposure to polyfluoroalkyl chemicals in the U.S. population: 1999–2008. Environ. Sci. Technol. 45, 8037–8045. Landsteiner, A., Huset, C., Johnson, J., Williams, A., 2014. Biomonitoring for perfluorochemicals in a Minnesota community with known drinking water contamination. J. Environ. Health 77, 14–19. Li, Y., Fletcher, T., Mucs, D., Scott, K., Lindh, C.H., Tallving, P., et al., 2018. 2018 Halflives of PFOS, PFHxS and PFOA after end of exposure to contaminated drinking water. Occup. Environ. Med. 75, 46–51. Lindstrom, A.B., Stynar, M.J., Libelo, E.L., 2011. Polyfluorinated compounds: past, present, and future. Environ. Sci. Technol. 45, 1954–1961. Lorber, M., Egeghy, P.P., 2011. Simple intake and pharmacokinetic modeling to characterize exposure of Americans to perfluoroctanoic acid, PFOA. Environ. Sci. Technol. 45, 8006–8014. Mogensen, U.B., Grandjean, P., Nielsen, F., Weihe, P., Budtz-Jørgensen, E., 2015. Breastfeeding as an exposure pathway for perfluorinated alkylates. Environ. Sci. Technol. 49, 10466–10473. Mondal, D., Weldon, R.H., Armstrong, B.G., Gibson, L.J., Lopez-Espinosa, M.J., Shin, H.M., et al., 2014. Breastfeeding: a potential excretion route for mothers and implications for infant exposure to perfluoroalkyl acids. Environ. Health Perspect. 122, 187–192. National Toxicology Program (NTP), 2016. NTP Monograph: Immunotoxicity Associated
9
Contents lists available at ScienceDirect
International Journal of Hygiene and Environmental Health journal homepage: www.elsevier.com/locate/ijheh
Per- and polyfluoroalkyl substance (PFAS) exposure assessment in a community exposed to contaminated drinking water, New Hampshire, 2015 ⁎
⁎
Elizabeth R. Dalya, , Benjamin P. Chana, , Elizabeth A. Talbota,b, Julianne Nassifa,1, Christine Beana, Steffany J. Cavalloa,2, Erin Metcalfa, Karen Simonec,g, Alan D. Woolfd,e,f a
New Hampshire Department of Health and Human Services, Concord, NH, United States Geisel School of Medicine at Dartmouth, Hanover, NH, United States c Northern New England Poison Center, Portland, ME, United States d Region 1 New England Pediatric Environmental Health Specialty Unit, Boston, MA, United States e Pediatric Environmental Health Center, Division of General Pediatrics, Department of Medicine, Boston Children’s Hospital, Boston, MA, United States f Harvard Medical School, Boston, MA, United States g School of Medicine, Tufts University, Boston, MA, United States b
A R T I C L E I N F O
A B S T R A C T
Keywords: Perfluoroalkyl substances Polyfluoroalkyl substances PFAS Biomonitoring Chemical Drinking water contamination
Background: Per- and polyfluoroalkyl substances (PFAS) are synthetic chemicals used in manufacturing that resist environmental degradation, can leach into drinking water, and bioaccumulate in tissues. Some studies have shown associations with negative health outcomes. In May 2014, a New Hampshire public drinking water supply was found to be contaminated with PFAS from a former U.S. Air Force base. Objectives: We established a serum testing program to assess PFAS exposure in the affected community. Methods: Serum samples and demographic and exposure information were collected from consenting eligible participants. Samples were tested for PFAS at three analytical laboratories. Geometric means and 95% confidence intervals were calculated and analyzed by age and exposure variables. Results: A total of 1578 individuals provided samples for PFAS testing; > 94% were found to have perfluorooctane sulfonic acid (PFOS), perfluorooctanoic acid (PFOA), and perfluorohexane sulfonic acid (PFHxS) detectable in serum. Geometric mean serum concentrations of PFOS, PFOA, and PFHxS were 8.6 μg/L (95% CI:8.3–8.9), 3.1 μg/L (95% CI: 3.0–3.2), and 4.1 μg/L (95% CI: 3.9–4.3), respectively, which were statistically higher than the general U.S. population. Significant associations were observed between PFAS serum concentrations and age, time spent in the affected community, childcare attendance, and water consumption. Conclusions: PFOS, PFOA, and PFHxS were found in significantly higher levels in the affected population, consistent with PFAS drinking water contamination. Given increased recognition of PFAS contamination in the U.S, a coordinated national response is needed to improve access to biomonitoring and understand health impacts.
1. Introduction Per- and polyfluoroalkyl substances (PFAS) are a diverse group of synthetic chemicals first produced by the 3 M Company in the 1940’s (Lindstrom et al., 2011). Their water-, stain-, and grease-resistant properties are exploited for multiple different commercial and industrial products and applications. Unfortunately, these same properties contribute to slow environmental degradation, which has resulted
in widespread environmental contamination of soil and water (Giesy and Kannan 2001; Yamashita et al., 2005), and detectable serum levels of PFAS in most people around the world, including the United States (Kannan et al., 2004; Calafat et al., 2007; Olsen et al., 2008; Kato et al., 2011). Individuals are exposed to these chemicals primarily through ingestion of contaminated food, water, and dust; however, young children may ingest them through hand-to-mouth behavior after touching surfaces treated with PFAS in the home environment (Trudel
Abbreviations: LOD, limit of detection; NHANES, National Health and Nutrition Examination Survey; NHDHHS, New Hampshire Department of Health and Human Services; PFAS, Perand polyfluoroalkyl substance; PFOS, perfluorooctane sulfonic acid; PFOA, perfluorooctanoic acid; PFHxS, perfluorohexane sulfonic acid; PFNA, perfluorononanoic acid ⁎ Corresponding authors. E-mail address: [email protected] (E.R. Daly). 1 Present address: Association of Public Health Laboratories, Silver Spring, Maryland, United States. 2 Present address: Tennessee Department of Health, Nashville, Tennessee United States. https://doi.org/10.1016/j.ijheh.2018.02.007 Received 22 November 2017; Received in revised form 30 January 2018; Accepted 14 February 2018 1438-4639/ © 2018 Elsevier GmbH. All rights reserved.
Please cite this article as: Daly, E.R., International Journal of Hygiene and Environmental Health (2018), https://doi.org/10.1016/j.ijheh.2018.02.007
International Journal of Hygiene and Environmental Health xxx (xxxx) xxx–xxx
E.R. Daly et al.
consumed contaminated drinking water while working on, living on, or attending childcare at the former Air Force base, while it was an active base or in the civilian community of Pease after the base closure. Infants or children who were exposed in-utero, or by breastfeeding, through their mother’s consumption of contaminated drinking water were also eligible. Enrollment and sample collection began in April 2015 and ended in October 2015. The serum testing program was submitted to the Committee for the Protection of Human Subjects at Dartmouth College and designated as public health surveillance, not research, and therefore exempt from Institutional Review Board (IRB) review. Individuals interested in participating in the serum testing program were asked to call a NH DHHS public inquiry line to determine eligibility and register for testing. Eligible participants were sent educational material about PFAS and serum testing, including information about the inability to correlate a person’s PFAS serum levels with any health outcomes. Individuals were also sent a consent form and questionnaire that collected demographic information and self-reported information about water consumption on Pease, time spent on Pease, time since last on Pease, and childcare attendance. The questionnaire did not assess most other potential sources of PFAS exposure.
et al., 2008; Lorber and Egeghy 2011; Gebbink et al., 2015). In the body, certain PFAS, including perfluorooctanoic acid (PFOA), perfluorooctane sulfonic acid (PFOS), and perfluorohexane sulfonic acid (PFHxS) have long half-lives. Initial half-life estimates in occupational workers for PFOA, PFOS, and PFHxS were 3.8 years, 5.4 years, and 8.5 years (arithmetic mean), respectively (Olsen et al., 2007); however, a more recent study in a Swedish community exposed to PFAS through drinking water contamination have shown shorter half-lives of 2.7 years, 3.4 years, and 5.3 years, respectively (Li et al., 2018). Because of their widespread use, their persistence in the environment, and the concern for possible health impact, the Environmental Protection Agency (EPA) has worked with manufacturers of PFOS and PFOA to eliminate these compounds from emissions and products since 2002 (EPA, 2016a), and overall exposure has been declining in the United States human population over the past 15 years (CDC, 2017). Identification of PFAS contaminated drinking water supplies, however, will likely be an issue of increasing concern for many communities in the United States in the future. Though PFAS are not currently regulated under the Safe Drinking Water Act, the EPA conducts a national monitoring program for unregulated drinking water contaminants; every five years the EPA publishes a list of unregulated contaminants to be monitored in public drinking water systems (SDWA, 1996). In 2012, PFOS and PFOA were added to the third Unregulated Contaminant Monitoring Rule (UCMR 3), which required all public drinking water systems serving more than 10,000 people to monitor for these contaminants by December 2015 (EPA, 2016a,b). Pease Air Force Base in New Hampshire closed in 1991 under the U.S. Base Realignment and Closure Act, and the site was transitioned to a civilian business and aviation community employing more than 9500 individuals to support its more than 250 businesses, public offices, restaurants, and childcare facilities. The public water system was comprised of three different wells blended together prior to distribution. In May 2014, one of the three drinking water wells was identified to have PFAS contamination with various PFAS, including PFOA (0.35 μg/L), PFOS (2.50 μg/L), and PFHxS (0.83 μg/L) (NH DHHS, n.d.). The levels of PFOA and PFOS were near or above the Provisional Health Advisory (PHA) set by the EPA in 2009 for PFOA and PFOS, (0.4 ug/L and 0.2 ug/L respectively); however, there was no health advisory level for PFHxS (EPA, 2009). In 2016, the EPA revised its drinking water PHA to a lifetime Health Advisory for PFOA and PFOS recommending that levels of PFOA and PFOS, either individually or combined, not exceed 0.07 ug/L, a value that has also been adopted by New Hampshire (EPA, 2016a,b). The contamination likely occurred as a result of the use of aqueous film-forming foam (AFFF) to combat and prevent fuel-based fires and to train military firefighting personnel while the U.S. Air Force base was operational. The contaminated well was shut down and the New Hampshire Department of Health and Human Services (NH DHHS) initiated a PFAS serum testing program to address public concerns about human exposure. The purpose of the testing program was to provide community members with more information about their individual and collective levels of exposure. The results of this testing program are among the first from a state public health response to PFAS exposure from drinking water contamination related to use of AFFF on a U.S. military base.
2.2. Laboratory analyses Individuals who returned a completed questionnaire and consent form were mailed a laboratory requisition and instructions for blood draw. Serum samples were collected at a local partnering hospital and transported to the NH DHHS Public Health Laboratories where the specimens were processed, de-identified, labeled with a unique patient identification number, and shipped in batches to one of three out-ofstate testing laboratories, including the U.S. Centers for Disease Control and Prevention (CDC, Atlanta, Georgia), AXYS Analytical (Sidney, British Columbia, Canada), and the California State biomonitoring laboratories (Richmond, California). Multiple laboratories were required due to a high demand for clinical testing, and limited testing capacity at each laboratory. Each laboratory tested for a different panel of PFAS, but a common subset of seven PFAS was included by all three laboratories (Table 1). All laboratories used the same testing methodology that separated, identified, and measured PFAS present in the serum specimens by liquid chromatography tandem mass spectrometry. (LC/ MS/MS) following solid-phase extraction. Each laboratory used an approved quality management system that included method validation with acceptable precision and accuracy, instrument calibration, quality indicators for acceptable performance, standard operating procedures for analysis and data review, and successful participation in an external proficiency testing program (CTQ, n.d.). Table 1 lists the PFAS tested at each laboratory and the corresponding limits of detection, which varied by laboratory and analyte. Collection, processing and transport of specimens from eligible participants who lived outside of the hospital catchment area were facilitated through the public health laboratories in their home states, in consultation with study investigators. 2.3. Statistical analyses For all statistical analyses, test results below each laboratory’s limit of detection were assigned a value equal to the laboratory’s respective limit of detection divided by the square root of two (CDC, 2017). Summary test statistics were calculated including medians, geometric means, 95th percentiles, maximums, and detection frequencies for each PFAS and compared to National Health and Nutrition Examination Survey (NHANES) data (CDC, 2017, Ye et al., 2018). Consistent with statistical methods for NHANES analyses, summary statistics for each PFAS are shown only if 60% or more of samples tested above the limit of detection for that PFAS in order to provide a valid result. Nonoverlapping confidence intervals were considered statistically different. An assessment of relationships between each individual demographic and exposure characteristic and PFAS serum concentration was
2. Material and methods 2.1. Enrollment and exposure assessment The serum testing program was designed and implemented with input from the community and with direction from elected officials. Eligibility criteria and instructions for participation were posted in public places, reported through press releases and via letters to employees of affected businesses. Individuals self-identified as eligible to participate in the serum testing program if they had, at any time, 2
International Journal of Hygiene and Environmental Health xxx (xxxx) xxx–xxx
E.R. Daly et al.
Table 1 Per- and polyfluoroalkyl substance testing panel and corresponding limits of detection by testing laboratory, Pease PFAS Serum Testing Program, New Hampshire, 2015. PFAS Name
Perfluorooctane sulfonic acid Perfluorooctanoic acid Perfluorohexane sulfonic acid Perfluorononanoic acid Perfluorodecanoic acid Perfluoroundecanoic acid Perfluorooctane sulfonamide 2-(N-methyl-perfluorooctane sulfonamido) acetic acid 2-(N-ethyl-perfluorooctane sulfonamido) acetic acid Perfluorobutane sulfonic acid Perfluoorododecanoic acid Perfluoroheptanoic acid
PFAS Abbreviation
PFOS PFOA PFHxS PFNA PFDeA PFUA PFOSA Me-PFOSA-AcOH Et-PFOSA-AcOH PFBuS PFDoA PFHpA
Limit of Detection (LOD) (ug/L) CDC
AXYS
CA State
0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 not tested not tested not tested
1.0 0.5 1.0 0.5 0.5 0.5 0.5 not not not not not
0.144 0.072 0.019 0.045 0.073 0.030 0.016 0.020 0.028 0.050 0.115 0.100
tested tested tested tested tested
Number of Samples Tested
Number Above LOD n (%)
1578 1578 1578 1578 1578 1578 1578 878 878 107 107 107
1574 (99.8) 1566 (99.2) 1487 (94.2) 1345 (85.2) 664 (42.1) 474 (30.0) 31 (2.0) 317 (36.1) 23 (2.6) 20 (18.7) 5 (4.7) 1 (0.9)
LOD: limits of detection PFAS: per- and polyfluoroalkyl substance; CDC: U.S. Centers for Disease Control and Prevention (Atlanta, GA); AXYS: AXYS Analytical (Sidney, British Columbia, Canada); CA State: California State biomonitoring laboratories (Richmond, CA).
2.9–3.1, respectively) but not for PFOS (8.1 μg/L, 95% CI: 7.6–8.7 vs. 8.7 μg/L, 95% CI: 8.4–9.1, respectively) and PFHxS (3.8 μg/L, 95% CI: 3.5–4.2 vs. 4.2 μg/L, 95% CI: 4.0–4.5, respectively). Differences were identified when stratifying further by age group and gender (Table 3). The geometric mean for each age group was compared with the youngest age group (0–2 year olds), which served as a reference group for the statistical comparison. Mean serum concentrations of PFOS and PFHxS showed a bimodal distribution, with significantly higher levels found in 3–5 year old children and adults over 40 years of age when compared with the youngest group (Fig. 1, Table 3). Levels of PFOS, PFOA, and PFHxS declined in later childhood and adolescence before increasing starting at 20 years of age. Males had significantly higher PFOS, PFOA, and PFHxS serum concentrations compared with females. To further explore the observation that 3–5 year olds demonstrated higher serum PFAS concentrations than other children, we evaluated attendance at either of the two childcare facilities on the base, which primarily accommodate children 6 weeks up to 5 years of age. As compared to children that did not attend childcare on the base (i.e. children exposure through breastfeeding or in-utero), childcare attendees were observed to have significantly higher PFOS (8.8 μg/L vs. 5.4 μg/L, p < 0.0001), PFOA (3.6 μg/L vs. 2.7 μg/L, p = .0012), and PFHxS (4.6 μg/L vs. 1.5 μg/L, p < 0.0001) serum concentrations. This finding was observed for all age groups of children but was most pronounced for children 3–5 years old (Fig. 2). When comparing serum levels by reported water consumption on Pease, only PFHxS showed significantly higher geometric mean serum concentrations for participants that consumed 4–7 or 8+ cups of water per day on Pease compared with those who drank only 0–3 cups per day (Table 3). PFOS, PFOA, and PFHxS serum concentrations increased with increasing time spent on Pease, which was most pronounced for PFOS and PFHxS (Table 3). Interestingly, those who had last been on Pease 20+ years prior had the highest serum concentrations of PFOS, PFOA, and PFHxS (Table 3).
conducted using non-parametric analysis of variance with post-hoc testing. Only results for PFOS, PFOA, and PFHxS are provided in this report because more than 90% of participants had these PFAS detected in their serum and geometric means were significantly higher compared with the general U.S. population for these three PFAS. For participants who reported a range for volume of water consumption on Pease (approximately 30% of respondents), the average of the range was calculated and used in all water consumption analyses. The Kruskal-Wallis test was used to assess individual relationships between PFAS serum concentration and age, sex, water consumption, time spent on Pease, time since last on Pease, and childcare attendance. Where significant relationships existed, post-hoc analyses of ranked data were performed using a Bonferroni adjustment for multiple comparisons to identify which groups were significantly different from a reference group. SAS version 9.3 (SAS Institute Inc., Cary, NC) was used to analyze data; pvalues less than 0.05 were considered statistically significant. 3. Results 3.1. Serum testing results A total of 1578 eligible individuals provided serum samples for testing between April and October 2015. In total, 771 samples (49%) were tested at the CDC laboratory, 700 (44%) at AXYS, and 107 (7%) at the CA State laboratory. Most serum specimens had detectable levels of PFOS (99.8%), PFOA (99.2%), PFHxS (94.2%), and PFNA (85.2%). Summary statistics are not presented for the other PFAS because too high a proportion of samples were below the testing laboratory’s limit of detection to provide a valid result. In comparison to NHANES U.S. population data (CDC, 2017, Ye et al., 2018), geometric means for three PFAS (PFOS, PFOA, PFHxS) were found to be significantly higher (Table 2). In comparison to corresponding age-stratified NHANES data, geometric means for PFOS, PFOA, and PFHxS were significantly higher in all age groups except for the 12–19 years age group, which only observed a higher PFOS level; comparison data were not available for 0–2 year olds (Table 2).
4. Discussion PFAS may be linked to adverse health outcomes in humans. Reviews of epidemiological studies suggest that there may be changes in uric acid levels, liver function tests, effects on lipid metabolism, thyroid function, growth and development, immune function, and certain types of cancers attributable to exposure to sources of PFAS (ATSDR, 2015; EPA, 2016a,b; NTP, 2016; IARC, 2016). For this reason, people living in communities in which PFAS contamination of drinking water has been confirmed have called for this source of exposure to be addressed as a public health issue. Most participants in the 2015 NH Pease PFAS serum
3.2. Participant characteristics and exposure assessment The majority of participants were female (n = 856, 57.3%), aged 20 years or older (n = 1181, 74.8%), had spent fewer than 10 years on Pease (n = 882, 68.5%), and had recent exposure (within the previous year) to drinking water on Pease (n = 948, 73.6%) (Table 3). When comparing overall levels for children (age 11 and younger) with adolescents and adults (age 12 and older), mean serum levels of PFOA were significantly higher (3.4 μg/L, 95% CI: 3.2–3.6 vs. 3.0 μg/L, 95% CI: 3
International Journal of Hygiene and Environmental Health xxx (xxxx) xxx–xxx
E.R. Daly et al.
Table 2 Summary of per- and polyfluoroalkyl substance serum concentrations in the exposed testing population compared with NHANES, New Hampshire, 2015. CDC, 2017; Ye et al., 2018. PFAS
PFOS Total Age Groups: 0-2 years 3–5 years 6–11 years 12–19 years 20+ years PFOA Total Age Groups: 0-2 years 3–5 years 6–11 years 12–19 years 20+ years PFHxS Total Age Groups: 0-2 years 3–5 years 6–11 years 12–19 years 20+ years PFNA Total Age Groups: 0-2 years 3–5 years 6–11 years 12–19 years 20+ years
n
Pease Testing Population (μg/L)
NHANES 2013–2014 Data (μg/L)
Median
Geometric Mean
95% CI
95th Percentile
Max
n
Geometric Mean
95% CI
95th Percentile
1578
8.90
8.59a
8.28−8.91
27.40
95.60
2165
4.99
4.50−5.52
18.50
75 164 127 31 1181
6.47 10.10 7.58 5.20 9.30
6.25 9.81a 7.41a 5.39a 8.85a
5.29−7.38 8.98−10.72 6.65−8.25 4.42−6.57 8.47−9.25
18.40 24.40 20.70 12.90 30.00
28.50 30.80 29.30 18.10 95.60
– 181 458 401 1764
– 3.38 4.15 3.54 5.22
– 3.04−3.77 3.76−4.58 3.17−3.96 4.70−5.81
– 8.82 12.4 9.30 19.5
1578
3.20
3.09a
2.99−3.19
8.65
32.00
2165
1.94
1.76−2.14
5.57
75 164 127 31 1181
3.83 4.31 2.56 1.60 3.16
3.47 4.12a 2.69a 1.62 3.04a
2.98−4.05 3.83−4.44 2.44−2.98 1.29−2.03 2.92−3.16
10.60 8.70 6.50 4.74 9.00
12.00 11.60 9.29 5.73 32.00
– 181 458 401 1764
– 2.00 1.89 1.66 1.98
– 1.75−2.29 1.72−2.07 1.50−1.84 1.79−2.19
– 5.58 3.84 3.47 5.60
1578
4.20
4.12a
3.92−4.33
20.00
116.00
2168
1.35
1.20−1.52
5.60
75 164 127 31 1181
2.60 6.06 3.70 2.30 4.25
2.63 5.11a 3.30a 1.92 4.30a
2.08−3.33 4.47−5.84 2.84−3.84 1.49−2.49 4.06−4.55
12.50 15.60 11.40 4.80 21.80
19.70 31.70 19.50 7.50 116.00
– 181 458 402 1766
– 0.72 0.91 1.27 1.36
– 0.62−0.83 0.80−1.04 1.06−1.53 1.21−1.53
– 1.62 4.14 6.30 5.50
1578
0.74
0.73
0.70−0.75
1.96
5.20
2168
0.68
0.61−0.74
2.00
75 164 127 31 1181
0.74 1.03 0.90 0.40 0.70
0.76 1.01 0.90 0.49 0.68
0.65−0.90 0.92−1.12 0.80−1.01 0.38−0.63 0.66−0.71
2.60 2.58 3.49 1.82 1.66
5.16 5.20 4.46 1.98 4.90
– 181 458 402 1766
– 0.76 0.81 0.60 0.69
– 0.63−0.93 0.68−0.96 0.49−0.73 0.63−0.75
– 3.49 3.19 2.00 2.00
CI = confidence interval, NHANES=National Health and Nutrition Examination Survey, PFAS = Per- and polyfluoroalkyl substance, PFOS = Perfluorooctane sulfonic acid, PFOA = Perfluorooctanoic acid, PFHxS = Perfluorohexane sulfonic acid, PFNA = Perfluorononanoic acid. Note: Only PFAS detected in at least 60% of samples tested are shown. a Geometric mean is significantly higher than NHANES comparison data – Comparison data not available.
These sex-related differences in PFAS levels may be due to difference in clearances related to elimination through menstrual blood losses, transfers during lactation, or transplacental transfer during pregnancy (Papadopoulou et al., 2016; Wong et al., 2014). The two PFAS that were found in the highest levels in the contaminated well (PFOS and PFHxS) were found in significantly higher concentrations in the 3–5 and 40+ year old age groups compared with the youngest age group. PFOS, PFOA, and PFHxS levels all declined in late childhood and adolescence and then increased after age 20. A significant relationship between childcare attendance on Pease and serum concentrations for PFOS, PFOA, and PFHxS was observed for children under the age 12 years old, and especially for 3–5 year olds. This finding suggests that exposure on Pease likely represents a significant source of PFAS for these children. Studies of the general U.S. adolescent and adult population have shown conflicting results when assessing differences in PFAS levels by age. Some studies have found no difference in PFAS levels by age (Olsen et al., 2008; Calafat et al., 2007) but a more recent study found significant increases in PFOS, PFOA, and PFNA with increasing age (Kato et al., 2011). Studies of children have also shown conflicting results (Schecter et al., 2012; Olsen et al., 2004). The differences likely illustrate the complex pattern of age, behavior, and PFAS exposure. Age may play a significant role in exposure because childhood behaviors can predispose to PFAS exposure, including hand-to-mouth behavior, which is most prominent in younger children and decreases with age (Trudel et al., 2008). While drinking water exposure likely contributed to the elevation of PFOS, PFOA, and PFHxS levels in the 3–5 year old
testing program (more than 94%) were found to have PFOS, PFOA, and PFHxS detectable in their serum; this is consistent with other studies of children, adolescents, and adults (Kato et al., 2011; Olsen et al., 2008; Calafat et al., 2007; Schecter et al., 2012). Average levels of three PFAS compounds (PFOS, PFOA, and PFHxS) in the exposed Pease community were higher than levels found in the general U.S. adult and adolescent population (CDC, 2017). Levels of all three PFAS in this community were substantially lower than those found in other occupationally- and environmentally-exposed populations (Fig. 3) (Olsen et al., 2003, 2007; Sakr et al., 2007; Frisbee et al., 2009; ATSDR, 2013; Landsteiner et al., 2014; NYSDOH, 2016; VTDOH, 2016; CDC, 2017). Drinking water consumption on Pease is likely a primary source of exposure to these PFAS, which is supported by the increasing trend in serum concentrations with increasing time spent on Pease. This trend was most notable for PFOS and PFHxS, which have longer half-lives and were found at higher concentrations in the affected well (City of Portsmouth New Hampshire, 2018). Self-reported water consumption only showed increasing PFHxS levels with increasing water consumption, and not with PFOA and PFOS, suggesting lack of precision in selfreported retrospective water consumption, which required averaging of reported ranges of water consumption in almost a third of participants. Males were found to have higher geometric mean serum levels of PFOS, PFOA, and PFHxS compared with females. This finding is consistent with other U.S. studies of PFAS levels and may represent differences in exposure between the sexes (Kato et al., 2011; Olsen et al., 2004, 2008; Calafat et al., 2007; Schecter et al., 2012; CDC, 2017). 4
International Journal of Hygiene and Environmental Health xxx (xxxx) xxx–xxx
E.R. Daly et al.
Table 3 Association between characteristics of the exposed testing population and serum per- and polyfluoroalkyl substance concentrations (μg/L), New Hampshire, 2015. Characteristics
n (%)
PFOS Geometric Mean
Age group
n = 1578 median = 40 75 (4.8) 164 (10.4) 91 (5.8) 36 (2.3) 31 (2.0) 369 (23.4) 611 (38.7) 201 (12.7)
6.25 9.81 7.89 6.31 5.39 6.94 9.35 11.72
Sex Female Male
n = 1495 856 (57.3) 639 (42.7)
7.46 10.45
Water consumption (cups per day) 0−3 4–7 8+
n = 1338 median = 4 572 (42.8) 539 (40.3) 227 (17.0)
Time spent on base (years) <1 1–4 5–9 10–19 20+
n = 1288 median = 6.5 75 (5.8) 429 (33.3) 378 (29.3) 318 (24.7) 88 (6.8)
Time since last on base (years) <1 1–4 5–9 10–19 20+
n = 1288 median = 0.0 948 (73.6) 144 (11.1) 88 (6.8) 74 (5.7) 34 (2.6)
Childcare Attendance (age < 12 only) No Yes
n = 366
0−2 3–5 6–8 9–11 12–19 20–39 40–59 60+
61 (16.7) 305 (83.3)
PFOA p-valueŦ
Post-Hoc Multiple Comparison Testing¥
Geometric Mean
< 0.0001
p-valueŦ
Post-Hoc Multiple Comparison Testing¥
3.47 4.12 2.94 2.16 1.62 2.47 3.20 3.80
N/A
ref 0.1652 0.4975 < 0.0001 < 0.0001 < 0.0001 1.0 1.0 < 0.0001
N/A
8.40 9.10 9.01
N/A
< 0.0001
ref 1.0000 0.5582 0.0212 0.0094
3.14 2.68 2.80 2.93 4.04
N/A
2.37 3.16 4.66 5.68 7.91
5.41 8.80
2.75 3.59
ref 0.0466 < 0.0001 < 0.0001 < 0.0001 < 0.0001
0.2279 0.0051 0.0225 0.1525 ref 0.0012
ref < 0.0001 0.0023 < 0.0001
0.0014 0.0043 < 0.0001 0.0210 0.0013 ref
N/A
< 0.0001 3.77 4.76 4.90
2.75 2.75 3.08 3.42 3.75
< 0.0001
ref < 0.0001 0.1048 1.0000 0.4365 1.0000 < 0.0001 < 0.0001 < 0.0001
< 0.0001 ref 0.7065 0.0003 < 0.0001 < 0.0001
8.94 7.40 9.03 7.87 13.99
2.63 5.11 3.80 2.31 1.92 3.10 4.79 5.64
N/A
2.98 3.17 3.22
6.61 7.45 9.30 10.18 11.79
Post-Hoc Multiple Comparison Testing¥
3.41 5.36 0.1102
< 0.0001
p-valueŦ
< 0.0001
2.85 3.45 0.1115
Geometric Mean
< 0.0001 ref < 0.0001 0.3406 1.0000 1.0000 1.0000 < 0.0001 < 0.0001
< 0.0001
PFHxS
4.47 3.07 4.09 3.86 8.11
N/A
0.0041 < 0.0001 0.0018 0.0028 ref < 0.0001
N/A
1.49 4.63
PFAS = Per- and polyfluoroalkyl substance, PFOS = Perfluorooctane sulfonic acid, PFOA = Perfluorooctanoic acid, PFHxS = Perfluorohexane sulfonic acid N/A: Not applicable because post-hoc testing wasn’t performed. Multiple comparison testing was only performed for statistically significant variables in the Kruskal-Wallis analysis with more than two categories. Ŧ Kruskal-Wallis test. ¥ Comparing ranked data using Bonferroni adjustment.
suspected levels of exposure would also be those who would be most worried and therefore most likely to seek testing. It was not a scientifically designed random sampling exposure assessment, which limits its generalizability and conclusions that can be drawn about exposure in the Pease population as a whole. Given the need to most responsibly use limited public health resources and the uncertainty surrounding health–related end-points, PFAS biomonitoring of affected communities should be conducted in the context of scientific studies designed to answer specific clinical questions. A consistent scientific approach is important and necessary as communities exposed to PFAS are being identified around the country. Secondly, the participant questionnaire collected information on a limited number of exposures that related to the affected community and drinking water exposure. Therefore, while the Pease serum testing results suggest drinking water exposure as a contributor, the serum PFAS levels actually represent exposure from all sources, including exposures in the home and work environments. Because PFAS have been widely used in home products and industry, there are likely other significant
age group in this community, additional exposure from home sources of PFAS through hand-to-mouth behavior, cannot be excluded. Breastfeeding can also contribute to PFAS exposure in infants since PFAS compounds can be excreted in breast milk in varying amounts depending on the compound (Mondal et al., 2014). One study showed that infant serum concentrations of PFOS and PFOA increased during the period of exclusive or partial breastfeeding; however, levels appeared to peak around 12 months of age, which is different from our described findings where average childhood PFOS and PFOA levels peaked between 3 and 5 years of age (Mogensen et al., 2015). We did not collect information on breastfeeding, and so were unable to assess its role in elevated childhood serum concentrations in the Pease population. The results of this serum testing program have several notable limitations. First, it was intentionally designed to be a convenience sample of self-selecting individuals who wanted to know their own, or their child’s, PFAS serum levels. This self-selection might have resulted in an overestimation of exposure, as the people with the highest 5
International Journal of Hygiene and Environmental Health xxx (xxxx) xxx–xxx
E.R. Daly et al.
The Pease serum testing program was not designed to be a health study and did not collect comprehensive exposure or any health outcome related information. PFAS serum testing provided affected individuals and health officials with further information about levels of exposure to PFAS from all sources of exposure, but there is not a PFAS serum level at which health effects are known or expected to occur, and the potential long term health implications from the elevated levels of exposure seen at Pease remain unclear ATSDR, 2016. Helping participants understand their test results as they relate to their health was the greatest challenge in this response. We attempted to make relative comparisons to other tested communities, but serum testing ultimately provides little actionable healthcare information. Given the uncertainty around health impact from PFAS exposure, addressing health concerns requires a multiagency coordinated response. Others have noted previously that a coordinated communication plan must be developed when conveying results of biomonitoring of PFAS to the general public (Hernick et al., 2011). NH DHHS has worked closely with the regional poison control center (Northern New England Poison Center), CDC and the Agency for Toxic Substances & Disease Registry (ATSDR), the Region 1 Pediatric Environmental Health Specialty Unit (Region 1 PEHSU), and other local environmental health physicians to try and respond to and address community and healthcare provider questions and concerns about health impacts from PFAS exposure. 5. Conclusions Biomonitoring can provide affected communities and local health departments with more information about levels of PFAS exposure, but fully understanding sources and duration of exposure is challenging given the widespread use of these chemicals in our home and work environments. The serum testing program described here was one of the first public health responses in the nation to try and address concerns from PFAS exposure related to a U.S. Department of Defense site of contamination. It was an active public health response that was designed to address community concerns and was developed with input from the community and at the behest of elected officials. While we were able to provide PFAS testing to all affected individuals who wanted it, this public health response presented many challenges including identifying funds to support the testing program, prolonged (greater than one year) activation of the public health incident response team, defining the appropriate roles and responsibilities of the various federal, state, and local entities involved, and public and provider communication. The scenario described in this report is beginning to play out across the United States in other jurisdictions as PFAS drinking water contamination is identified related to military or industry contamination. Communicating exposure risk, test results, and uncertainty regarding health effects requires a national coordinated response from federal and state agencies to address health concerns through additional research and consistent messaging and recommendations to communities, public health agencies, and healthcare providers.
Fig. 1. Per- and polyfluoroalkyl substance serum concentrations in the exposed testing population by age group in years, New Hampshire, 2015 (n = 1578). PFAS = Per- and polyfluoroalkyl substance, PFOS = Perfluorooctane sulfonic acid, PFOA = Perfluorooctanoic acid, PFHxS = Perfluorohexane sulfonic acid. Note: The box represents the interquartile range, which is intersected by a line representing the median. The circle represents the geometric mean.
sources of PFAS exposure that were not evaluated in this serum testing program. Due to a lack of complete exposure information resulting in validity concerns, the data presented in this report are univariate analyses that do not take into account, using multivariate analysis techniques, the relationships between all potential factors that contribute to PFAS serum levels. Ideally any biomonitoring assessment should assess other sources of exposure as a way to inform and educate communities about PFAS exposure and to help interpret PFAS serum levels, which is very challenging because serum PFAS test results represent exposure from multiple sources over years of exposure and not just drinking water contamination. Thirdly, because of logistical considerations in such a large community-based testing program, serum samples were analyzed at three separate certified laboratories. Although their analytical techniques, limits of detection, and quality control protocols were similar, sources of measurement variation may still have contributed to minor systematic differences in the results of serum assays.
Funding and disclaimer The work conducted at the New Hampshire Department of Health and Human Services was supported, in part, by the Centers for Disease Control and Prevention (CDC), Biomonitoring cooperative agreement [grant number 5U88EH001142-01] and Public Health Emergency Preparedness cooperative agreement [grant number 5U90TP00053504]. The findings and conclusions in this report are solely the responsibility of the authors and do not necessarily represent the official views of the CDC or the Assistant Secretary for Preparedness and Response. ADW is supported by the Agency for Toxic Substances and Disease Registry (ATSDR) cooperative agreement award number 1U61TS000238-01 (to the Region 1 New England Pediatric Environmental Health Specialty Unit). The contents of this manuscript 6
International Journal of Hygiene and Environmental Health xxx (xxxx) xxx–xxx
E.R. Daly et al.
Fig. 2. Per- and polyfluoroalkyl substance serum concentrations in the exposed testing population by participant childcare attendance, New Hampshire, 2015 (n = 1578). PFAS = Per- and polyfluoroalkyl substance, PFOS = Perfluorooctane sulfonic acid, PFOA = Perfluorooctanoic acid, PFHxS = Perfluorohexane sulfonic acid. Note: Circle denotes geometric mean with corresponding 95% confidence interval.
this report, or the decision to submit this manuscript for publication.
are the responsibility of the authors and do not necessarily represent the official views of ATSDR. The U.S. Environmental Protection Agency (EPA) supports the Pediatric Environmental Health Specialty Units (PEHSU) by providing funds to ATSDR under Inter-Agency Agreement number DW-75- 92301-05. Neither EPA nor ATSDR endorse the purchase of any commercial products or services mentioned in PEHSU publications. CDC, ATSDR, and EPA did not play any role in the design of the study, the collection and interpretation of the data, the writing of
Disclosure statement The authors declare they have no actual or potential competing financial interests.
7
International Journal of Hygiene and Environmental Health xxx (xxxx) xxx–xxx
E.R. Daly et al.
Fig. 3. Mean per- and polyfluoroalkyl substance serum concentrations comparing the exposed New Hampshire Pease population with the general United States population, environmentally exposed communities, and occupationally exposed workers. PFAS = Per- and polyfluoroalkyl substance, PFOS = Perfluorooctane sulfonic acid, PFOA = Perfluorooctanoic acid, PFHxS = Perfluorohexane sulfonic acid Note: All means are geometric means except the 3M 2004 study, which is an arithmetic mean. Olsen et al., 2003, 2007; Sakr et al., 2007; Frisbee et al., 2009; ATSDR, 2013; Landsteiner et al., 2014; NYSDOH, 2016; VTDOH, 2016; CDC, 2017.
Acknowledgements
Agency for Toxic Substances & Disease Registry (ATSDR), 2015. Draft Toxicological Profile for Perfluoroalkyls. Available: https://www.atsdr.cdc.gov/toxprofiles/tp200. pdf (Accessed 18 January 2018). Agency for Toxic Substances & Disease Registry (ATSDR), 2016. Perfluoroalkyl Substances and Your Health: Health Effects of PFAS. Available: http://www.atsdr. cdc.gov/pfc/health_effects_pfcs.html (Accessed 13 February 2017). Centers for Disease Control and Prevention (CDC), 2017. Fourth National Report on Human Exposure to Environmental Chemicals: Updated Tables January 2017. . Available: https://www.cdc.gov/exposurereport/ (Accessed 22 July 2017). Centre de Toxicologie du Quebec (CTQ), 2018. AMAP: AMAP Ring Test for Persistent Organic Pollutants in Human Serum. (n.d. Available: https://www.inspq.qc.ca/en/ ctq/eqas/amap/description (Accessed 13 February 2017)). Calafat, A.M., Wong, L.-Y., Kuklenyik, Z., Reidy, J.A., Needham, L.L., 2007. Polyfluoroalkyl chemicals in the U.S. population: data from the national health and nutrition examination survey (NHANES) 2003–2004 and comparisons with NHANES 1999–2000. Environ. Health Perspect. 115, 1596–1602. City of Portsmouth, New Hampshire, 2018. Pease Well Monitoring and Sampling Results. (n.d. Available: https://www.cityofportsmouth.com/publicworks/water/pease-
We wish to thank Christine Adamski, formerly of the New Hampshire Department of Health and Human Services, and the U.S. Centers for Disease Control and Prevention, National Center for Environmental Health, Division of Laboratory Sciences and the Agency for Toxic Substances and Disease Registry for technical guidance and assistance. References Agency for Toxic Substances & Disease Registry (ATSDR), 2013. Exposure Investigation Report: PFC Serum Sampling in the Vicinity of Decatur, AL, Morgan, Lawrence, and Limestone Counties. . Available: http://www.atsdr.cdc.gov/HAC/pha/Decatur/ Perfluorochemical_Serum%20Sampling.pdf (Accessed 22 July 2017).
8
International Journal of Hygiene and Environmental Health xxx (xxxx) xxx–xxx
E.R. Daly et al.
with Exposure to Perfluorooctanoic Acid or Perfluorooctane Sulfonate. Available: https://ntp.niehs.nih.gov/ntp/ohat/pfoa_pfos/pfoa_pfosmonograph_508.pdf (Accessed 1 December 2017). New York State Department of Health (NYSOH), 2016. PFOA in Drinking Water in the Village of Hoosick Falls and Town of Hoosick, Preliminary Participant Results. Available: https://www.health.ny.gov/environmental/investigations/hoosick/ (Accessed 22 July 2017). New Hampshire Department of Health Human Services, 2018. Pease Tradeport Water System Investigation. (n.d. Available: http://www.dhhs.nh.gov/dphs/investigationpease.htm Accessed 31 July 2017). Olsen, G.W., Burris, J.M., Burlew, M.M., Mandel, J.H., 2003. Epidemiologic assessment of worker serum perfluorooctanesulfonate (PFOS) and perfluorooctanoate (PFOA) concentrations and medical surveillance examinations. J. Occup. Environ. Med. 45, 260–270. Olsen, G.W., Church, T.R., Hansen, K.J., Burris, J.M., Butenhoff, J.L., Mandel, J.H., et al., 2004. Quantitative evaluation of perfluorooctanesulfonate (PFOS) and other fluorochemicals in the serum of children. J. Child Health 2, 53–76. Olsen, G.W., Burris, J.M., Ehresman, D.J., Froehlich, J.W., Seacat, A.M., Butenhoff, J.L., et al., 2007. Half-life of serum elimination of perfluorooctanesulfonate, perfluorohexanesulfonate, and perfluorooctaneoate in retired fluorochemicals production workers. Environ. Health Perspec. 115, 1298–1305. Olsen, G.W., Mair, D.C., Church, T.R., Ellefson, M.E., Reagen, W.K., Boyd, T.M., et al., 2008. Decline in perfluorooctanesulfonate and other polyfluoroalkyl chemicals in American Red Cross adult blood donors, 2000–2006. Environ. Sci. Technol. 42, 4989–4995. Papadopoulou, E., Sabaredzovic, A., Namork, E., Nygaard, U.C., Granum, B., Haug, L.S., 2016. Exposure of Norwegian toddlers to perfluoroalkyl substances (PFAS): the association with breastfeeding and maternal PFAS concentrations. Environ. Int. 94, 687–694. Safe Drinking Water Act Amendments of 1996, 1996. 42 USC 300f. Sakr, C.J., Kreckmann, K.H., Green, J.W., Gillies, P.J., Reynolds, J.L., Leonard, R.C., 2007. Cross-sectional study of lipids and liver enzymes related to a serum biomarker of exposure (ammonium perfluorooctanoate or APFO) as part of a general health survey in a cohort of occupationally exposed workers. J. Occup. Environ. Med. 49, 1086–1096. Schecter, A., Malik-Bass, N., Calafat, A.M., Kato, K., Colacino, J.A., Gent, T.L., et al., 2012. Polyfluoroalkyl compounds in Texas children from birth through 12 years of age. Environ. Health Perspec. 120, 590–594. Trudel, D., Horowitz, L., Wormuth, M., Scheringer, M., Cousins, I.T., Hungerbuhler, K., 2008. Estimating consumer exposure to PFOS and PFOA. Risk Anal. 28, 251–269. Vermont Department of Health (VTDOH), 2016. PFOA Blood Test Results for Bennington/ North Bennington. Available: http://healthvermont.gov/enviro/pfoa_clinics.aspx# info (Accessed 22 July 2017). Wong, F., MacLeod, M., Mueller, J.F., Cousins, I.T., 2014. Enhanced elimination of perfluorooctane sulfonic acid by menstruating women: evidence from population-based pharmacokinetic modeling. Environ. Sci. Technol. 48 (15), 8807–8814. Yamashita, N., Kannan, K., Taniyasu, S., Horii, Y., Petrick, G., Gamo, T., 2005. A global survey of perfluorinated acids in oceans. Mar. Pollut. Bull. 51, 658–668. Ye, X., Kato, K., Wong, L.Y., Jia, T., Kalathil, A., Latremouille, J., Calafat, A.M., 2018. Perand polyfluoroalkyl substances in sera from children 3–11 years of age participating in the National Health and Nutrition Examination Survey 2013–2014. Int. J. Hyg. Environ. Health 221, 9–16.
tradeport-water-system#wellmonitoring (Accessed 1 September 2017)). Environmental Protection Agency (EPA), 2009. Provisional Health Advisories for Perfluorooctanoic Acid (PFOA) and Perfluorooctane Sulfonate (PFOS). Available: https://www.epa.gov/dwstandardsregulations/provisional-health-advisoriesperfluorooctanoic-acid-pfoa-and-perfluorooctane (Accessed 9 August 2016). Environmental Protection Agency (EPA), 2016a. Drinking Water Health Advisory for Perfluorooctanoic Acid (PFOA). Available: https://www.epa.gov/sites/production/ files/2016-05/documents/pfos_health_advisory_final_508.pdf (Accessed 13 February 2017). Environmental Protection Agency (EPA), 2016b. Drinking Water Health Advisory for Perfluorooctane Sulfonate (PFOS). Available: https://www.epa.gov/sites/ production/files/2016-05/documents/pfos_health_advisory_final_508.pdf (Accessed 13 February 2017). Frisbee, S.J., Brooks, A.P., Maher, A., Flensborg, P., Arnold, S., Fletcher, T., et al., 2009. The C8 Health Project: design, methods, and participants. Env Health Persp 117, 1873–1882. Gebbink, W.A., Berger, U., Cousins, I.T., 2015. Estimating human exposure to PFOS isomers and PFCA homologues: the relative importance of direct and indirect (precursor) exposure. Environ. Int. 74, 160–169. Giesy, J.P., Kannan, K., 2001. Global distribution of perfluorooctane sulfonate in wildlife. Environ. Sci. Technol. 35, 1339–1342. Hernick, A.D., Brown, K., Piinney, S.M., Biro, F.M., Ball, K.M., Bornschein, R.L., 2011. Sharing unexpected biomarker results with study participants. Environ. Heal. Persp. 119, 1–5. International Agency for Research on Cancer (IARC), 2016. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, Volume 110: Perfluorooctanoic Acid. Available at: http://monographs.iarc.fr/ENG/Monographs/vol110/mono110-01.pdf (Accessed 14 September 2017). Kannan, K., Corsolini, S., Falandysz, J., Fillmann, G., Kumar, K.S., Loganathan, B.G., et al., 2004. Perfluorooctanesulfonate and related fluorochemicals in human blood from several countries. Environ. Sci. Technol. 38, 4489–4495. Kato, K., Wong, L.-Y., Jia, L.T., Kuklenyik, Z., Calafat, A.M., 2011. Trends in exposure to polyfluoroalkyl chemicals in the U.S. population: 1999–2008. Environ. Sci. Technol. 45, 8037–8045. Landsteiner, A., Huset, C., Johnson, J., Williams, A., 2014. Biomonitoring for perfluorochemicals in a Minnesota community with known drinking water contamination. J. Environ. Health 77, 14–19. Li, Y., Fletcher, T., Mucs, D., Scott, K., Lindh, C.H., Tallving, P., et al., 2018. 2018 Halflives of PFOS, PFHxS and PFOA after end of exposure to contaminated drinking water. Occup. Environ. Med. 75, 46–51. Lindstrom, A.B., Stynar, M.J., Libelo, E.L., 2011. Polyfluorinated compounds: past, present, and future. Environ. Sci. Technol. 45, 1954–1961. Lorber, M., Egeghy, P.P., 2011. Simple intake and pharmacokinetic modeling to characterize exposure of Americans to perfluoroctanoic acid, PFOA. Environ. Sci. Technol. 45, 8006–8014. Mogensen, U.B., Grandjean, P., Nielsen, F., Weihe, P., Budtz-Jørgensen, E., 2015. Breastfeeding as an exposure pathway for perfluorinated alkylates. Environ. Sci. Technol. 49, 10466–10473. Mondal, D., Weldon, R.H., Armstrong, B.G., Gibson, L.J., Lopez-Espinosa, M.J., Shin, H.M., et al., 2014. Breastfeeding: a potential excretion route for mothers and implications for infant exposure to perfluoroalkyl acids. Environ. Health Perspect. 122, 187–192. National Toxicology Program (NTP), 2016. NTP Monograph: Immunotoxicity Associated
9