Residential Proximity to Metal-Containing Superfund Sites and Their Potential as a Source of Disparities in Metal Exposure among US Women

Vol. 131, No. 3 Research LetterOpen AccessResidential Proximity to Metal-Containing Superfund Sites and Their Potential as a Source of Disparities in Metal Exposure among U.S. Women Brittany A. Trottier, Nicole M. Niehoff, Alexander P. Keil, Rena R. Jones, Keith E. Levine, Nathaniel S. MacNell, and Alexandra J. White Brittany A. Trottier Hazardous Substances Research Branch, Division of Extramural Research and Training, National Institute of Environmental Health Sciences, Research Triangle Park, North Carolina, USA Department of Epidemiology, Gillings School of Global Public Health, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA Search for more papers by this author , Nicole M. Niehoff Epidemiology Branch, Division of Intramural Research, National Institute of Environmental Health Sciences, Research Triangle Park, North Carolina, USA Search for more papers by this author , Alexander P. Keil Department of Epidemiology, Gillings School of Global Public Health, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA Epidemiology Branch, Division of Intramural Research, National Institute of Environmental Health Sciences, Research Triangle Park, North Carolina, USA Search for more papers by this author , Rena R. Jones Occupational and Environmental Epidemiology Branch, Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, Maryland, USA Search for more papers by this author , Keith E. Levine RTI International, Research Triangle Park, North Carolina, USA Search for more papers by this author , Nathaniel S. MacNell Social & Scientific Systems, Inc., Durham, North Carolina, USA Search for more papers by this author , and Alexandra J. White https://orcid.org/0000-0003-2455-2945 Epidemiology Branch, Division of Intramural Research, National Institute of Environmental Health Sciences, Research Triangle Park, North Carolina, USA Search for more papers by this author Published:14 March 2023CID: 037701https://doi.org/10.1289/EHP11045AboutSectionsPDF ToolsDownload CitationsTrack Citations ShareShare onFacebookTwitterLinked InReddit IntroductionMore than 73 million people in the United States live within 3 mi (5 km) of a Superfund site,1 which can be sources of uncontrolled hazardous waste. These sites tend to be in areas of lower socioeconomic status or with higher proportions of people of color.2 Many Superfund sites release metals into different environmental media,3 making the sites plausible sources of exposure for nearby communities. We aimed to evaluate associations between residential proximity to metal-containing Superfund sites and toenail metal biomarker concentrations, with consideration of how these associations varied by race to assess the potential for unequal burden of exposure.MethodsAmong participants in the Sister Study, a nationwide prospective cohort study of U.S. women recruited between 2003–2009, we used a nested case–cohort design that oversampled non-Hispanic Black participants.4 We measured toenail metal concentrations in 1,499 women with breast cancer (1,254 non-Hispanic White, 245 non-Hispanic Black) and 1,500 randomly selected women (1,000 non-Hispanic White, 500 non-Hispanic Black). Sample weights were used to weight back to the full cohort. We excluded women whose enrollment address could not be geocoded (lowercase italic n equals 8n=8), whose toenails could not be processed (lowercase italic n equals 3n=3), or who were missing covariate data (lowercase italic n equals 6n=6). The final analytic sample was 2,982 women.As previously described,4 toenail metal concentrations were analyzed using a Thermo iCAP Q quadrupole inductively coupled plasma mass spectrometer. Single-element 1000 micrograms per liter1,000μg/mL National Institute of Standards and Technology-traceable solutions from High Purity Standards for each analyte were used to prepare calibration standards. Quality control samples were processed with each batch to monitor performance. Toenail metal concentrations were natural log-transformed to improve approximate homoskedasticity and normality of model residuals. Arsenic, cadmium, lead, and antimony were selected due to their inclusion on the Agency for Toxic Substances and Disease Registry Substance Priority List, which prioritizes 275 Superfund chemicals.3 Arsenic, cadmium, and lead rank within the top ten, and antimony ranks 244; all are nonessential metals that have no biological function in humans.Superfund sites were identified from the U.S. Environmental Protection Agency Superfund Enterprise Management System Public User Database5 and were subset to sites that were actively releasing (i.e., cleanup had not been completed) one or more metals of interest during Sister Study biospecimen collection (2003–2009). Of 1,139 active sites, 240 were included.We calculated the sum of the inverse-distance weighted (IDW) number of sites within 20 mi (32 km) of participants’ residences (IDW score, summation from lowercase italic j of uppercase italic i open parenthesis lowercase italic d begin subscript lowercase italic i j end subscript less than lowercase italic d begin subscript impact end subscript close parenthesis over lowercase italic d begin subscript lowercase italic i j end subscript∑jI(dijUSD $100,000109 (4.9)13 (1.8)Urbanicity [n (%)] Urban382 (17.1)283 (38.2) Suburban893 (39.9)287 (38.6) Rural, small town, other965 (43.1)172 (23.2)Area deprivation index [n (%)] less than 31<311,213 (54.2)242 (32.6) greater than or equal to 31≥311,027 (45.8)500 (67.4)Primary source of water [n (%)] Bottled water335 (15.0)311 (41.9) Community or private well447 (20.0)32 (4.3) City or town water1,458 (65.0)399 (53.8)Note: The IDW score can be interpreted as a weighted number of proximal Superfund sites. IDW, inverse-distance weighted; USD, U.S. dollars.ap-Values from a t-test comparing difference in means by race: arsenic lowercase italic p equals 0.01p=0.01, cadmium lowercase italic p equals 0.003p=0.003, lead lowercase italic p equals 0.002p=0.002, antimony lowercase italic p less than 0.0001p<0.0001.bp-Values from a Mann-Whitney test comparing difference in medians by race: arsenic lowercase italic p less than 0.0001p<0.0001, cadmium lowercase italic p less than 0.0001p<0.0001, lead lowercase italic p equals 0.55p=0.55, antimony lowercase italic p equals 0.001p=0.001.Overall, we observed positive associations between the IDW score for Superfund sites containing antimony (87.4%, 95% CI: 20.5, 191) and lead (155%, 95% CI: 87.8, 245) in relation to respective toenail levels (Table 2). For cadmium, we observed heterogeneity by race; the IDW score was associated with elevated concentrations only in non-Hispanic Black women (337%, 95% CI: 101, 854 vs. negative 22.9 percent−22.9%, 95% CI: negative 51.9−51.9, 23.5; lowercase italic p-heterogeneity equals 0.01p-heterogeneity=0.01).Table 2 Percent difference in toenail metal concentrations (nanograms per gram) for a 1-unit increase in the sum of the IDW metal-specific Superfund site [less than 20 miles<20 mi (32 km)] exposure score with stratification by race.Main analysis: IDW score [20 miles 32 kilometers20 mi (32 km)]Non-Hispanic WhiteNon-Hispanic BlackMetalExposeda,b (n)/Total (n)Fully adjusted percent difference (95% CI; ng/g)cExposeda,b (n)/Total (n)Adjusted percent difference (95% CI; ng/g)Exposeda,b (n)/Total (n)Adjusted percent difference (95% CI; ng/g)p-HeterogeneityfArsenic1,154/2,982−5.58 (−17.9, 8.63)830/2,240−7.73 (−21.6, 8.51)324/74222.8 (−6.45, 61.3)0.2Cadmium779/2,982−10.0 (−40.1, 35.2)549/2,240−22.9 (−51.9, 23.5)230/742337 (101.0, 854.0)0.01Leadd1,032/2,982155 (87.8, 245)722/2,240142 (70.7, 242.0)310/742299 (103.0, 684.0)0.2Antimony735/2,98287.4 (20.5, 191)496/2,240101 (19.2, 240)239/7428.49 (–45.6, 116.0)0.4Negative control: IDW site exposure score [20 miles per 32 kilometers20 mi (32km)] Arsenice41/2,982−48.7 (−68.6, −16.2)38/2,240−48.6 (−70.2, −11.2)3/742—0.6 Cadmium254/2,9824.53 (–11.1, 22.9)209/2,2404.15 (–13.1, 24.8)45/74285.8 (–18.1, 321.0)0.4 Leadd110/2,98245.3 (16.1, 81.9)103/2,24043.4 (12.1, 83.5)7/7421,714 (81.6, 18,012)0.2 Antimony450/2,98211.7 (–6.77, 33.9)311/2,24011.1 (–9.76, 36.7)139/74228.6 (–13.1, 90.2)0.7Note: —, no data; IDW, inverse-distance weighted.aExposed n for the main analysis refers to the number of participants with a nonzero IDW score for sites that reported emissions of the specific metal during study enrollment (2003–2009). These are nonexclusive categories; women may have been exposed to multiple metals.bExposed n for the negative control analysis refers to the number of participants with a nonzero IDW score for sites that have never reported emissions of the specific metal.cAdjusted for age, education, race, smoking status, census income, urbanicity, area deprivation, and primary source of drinking water.dAdditional adjustment for proximity to airport.eEstimate for non-Hispanic Black women not included due to sample size being less than 5<5.fp-Value for heterogeneity was obtained by testing for effect measure modification by race via likelihood ratio tests comparing the base models to models that included an interaction term between exposure measures and race.In our negative control analysis, we observed negligible associations between the IDW scores for non-cadmium and non-antimony containing sites and the respective metals (Table 2) and an inverse association between non-arsenic sites and toenail arsenic (–48.7%, 95% CI: −68.6, −16.2). In contrast, we estimated elevated lead concentrations for the IDW score for non-lead sites (45.3%, 95% CI: 16.1, 81.9). However, we had limited statistical power to detect associations, particularly for arsenic.DiscussionIn this population of women across the United States, we observed that increased density of nearby metal-containing Superfund sites was associated with higher concentrations of toenail metals, particularly in non-Hispanic Black women.Individuals from minoritized racial and ethnic groups often live closer to industrial pollution (e.g., see Mohai et al.2) and are overburdened by higher levels of arsenic and lead contaminated soil.8 Race correlates with other factors, including co-occurring environmental exposures or social stressors at the community and/or individual level due to residential segregation and racism, and may enhance susceptibility to exposure to metals.9 This possible susceptibility is supported by our findings, which suggest that Non-Hispanic Black women may have higher body burdens of lead and cadmium in relation to Superfund site exposure.The main study strengths are the large, diverse sample across the United States, the use of stable biomarkers that reflect long-term metal exposure, confounder adjustment for socioeconomic and residential factors, and the use of a negative control analysis. However, for some metals, very few women were not exposed, which challenges our inference for the negative control analysis. Because we had geocoded measures of both the participant’s residence and Superfund site location, we were able to use an exposure metric that incorporated both proximity to and density of sites. A limitation of this study is the lack of detailed Superfund site characteristics. This was a cross-sectional study; however, because toenail metals reflect exposure within the past year and Superfund sites are stable over time due to limited cleanup activities, this measurement error may be minimal. Despite the advantages of using toenails, some uncertainty remains regarding the exposure period that they reflect and their suitability as biomarkers for metals due to lack of standardization in sample collection and analytical procedures.10Overall, our results suggest that living near a metal-containing Superfund site is positively associated with toenail metal concentrations and that associations for lead and cadmium are strongest for non-Hispanic Black women in comparison with non-Hispanic White women. Our negative control results suggest that Superfund sites that do not contain lead are located proximal to other sources of lead. These findings are important from a public health standpoint because people continue to be exposed to toxic chemicals—released from such sites—that have well-established adverse health effects. It is imperative that these sites, as well as other sources of exposure that may be colocated with Superfund sites, continue to be remediated to reduce exposure to hazardous chemicals such as metals.AcknowledgmentsThis work was funded in part by the intramural program of the National Institute of Environmental Health Sciences, Z1A ES-103332, Z01 ES044005.References1. U.S. EPA (U.S. Environmental Protection Agency). Population Surrounding 1,857 Superfund Remedial Sites. https://www.epa.gov/sites/production/files/2015-09/documents/webpopulationrsuperfundsites9.28.15.pdf [accessed 10 April 2020]. Google Scholar2. Mohai P, Lantz PM, Morenoff J, House JS, Mero RP. 2009. Racial and socioeconomic disparities in residential proximity to polluting industrial facilities: evidence from the Americans’ Changing Lives Study. Am J Public Health 99(suppl 3):S649–S656, PMID: 19890171, 10.2105/AJPH.2007.131383. Crossref, Medline, Google Scholar3. U.S. EPA. What is Superfund? 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Crossref, Medline, Google ScholarThe authors declare they have nothing to disclose.FiguresReferencesRelatedDetails Vol. 131, No. 3 March 2023Metrics About Article Metrics Publication History Manuscript received1 February 2022Manuscript revised6 February 2023Manuscript accepted21 February 2023Originally published14 March 2023 Financial disclosuresPDF download License information EHP is an open-access journal published with support from the National Institute of Environmental Health Sciences, National Institutes of Health. All content is public domain unless otherwise noted. Note to readers with disabilities EHP strives to ensure that all journal content is accessible to all readers. However, some figures and Supplemental Material published in EHP articles may not conform to 508 standards due to the complexity of the information being presented. If you need assistance accessing journal content, please contact [email protected]. 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