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Research
18 October 2023

Association of Redlining and Natural Environment with Depressive Symptoms in Women in the Sister Study

Publication: Environmental Health Perspectives
Volume 131, Issue 10
CID: 107009

Abstract

Background:

Improving mental health is recognized as an important factor for achieving global development goals. Despite strong evidence that neighborhood greenery promotes better mental health, there are environmental justice concerns over the distribution of neighborhood greenery. Underlying these concerns are present-day consequences of historical discriminatory financial investment practices, such as redlining which was established by the U.S. Federal Home Owners’ Loan Corporation (HOLC) in the 1930s. The impacts of redlining on environmental and health disparities have been researched extensively. However, the influences of redlining on the associations between neighborhood environment and health outcomes have not been fully assessed.

Objectives:

The aim of this study was to examine whether associations between residential tree cover and depressive symptoms vary across areas subject to HOLC practices.

Methods:

Depressive symptoms were defined by the 10-item Center for Epidemiologic Studies Depression Scale collected during the period 2008–2012 for 3,555 women in the Sister Study cohort residing in cities subject to HOLC practices across the United States. HOLC rating maps were obtained from the Mapping Inequality Project, University of Richmond, with neighborhoods graded as A (best for financial investment, green), B (still desirable, blue), C (declining, yellow), and D (hazardous, red—known as redlined). Tree cover within 500 m and 2,000 m from residences was estimated using 2011 U.S. Forest Service Percent Tree Canopy Cover. Mixed model using climate zone as the random effect was applied to evaluate the associations with adjustments for potential covariates. Analyses were stratified by HOLC grade.

Results:

Tree cover was significantly higher in neighborhoods with better HOLC grades. A 10% increase in tree cover was associated with reduced odds of depressive symptoms for the full study population, with adjusted odds ratios (AORs) of 0.93 [95% confidence interval (CI): 0.88, 0.99], and 0.91 (0.85, 0.97) for 500 -m and 2,000 -m buffer, respectively. Across HOLC grades, the strongest associations were observed in redlined neighborhoods, with respective AORs of 0.72 (95% CI: 0.52, 0.99) and 0.63 (95% CI: 0.45, 0.90) for 500 -m and 2,000 -m buffer.

Discussion:

Findings support a remediation strategy focused on neighborhood greenery that would address multiple public health priorities, including mental health and environmental justice. https://doi.org/10.1289/EHP12212

Introduction

Mental health disorders are a major contributor to the global burden of disease. In 2019, mental health disorders were the seventh and second leading cause of global disability-adjusted life years and years lived with disability, respectively.1 The prevalence of mental health disorders has steadily increased over the past two decades, with almost a 50% increase from 2009 to 2019.2 Globally, 970  million people, equivalent to 12.6% of the world population, experienced a mental health disorder in 2019.1 Among all the mental health conditions, depression is the most common, with higher prevalence for women than for men in almost all the countries worldwide.1 The impact of mental health conditions on the global economy is substantial, with costs estimated to be around USD  $ 2.5 trillion per year in 2010 and projected to reach USD  $ 6 trillion by 2030.3 Recognizing this issue, the United Nations (UN) 2030 Agenda for Sustainable Development Goals (SDGs) identifies mental health as a key factor for achieving global development goals. Mental health has taken on even greater significance in recent years under the threat and disruption of the COVID-19 pandemic, with a reported 25% increase in anxiety and depression rates worldwide.4 In the United States, the prevalence of depressive symptoms in low-income groups has almost tripled in comparison with the rates in high-income groups during this period.5
Along with the awareness of mental health issues, there has been growing interest in the potentially beneficial effects of the natural environment on human health and well-being. Even small exposures to nature, such as window views,69 may serve as an effective public health strategy for improving human health and well-being, which would go a long way in achieving the UN SDGs.10 The economic value of visiting nature for mental health improvement alone is estimated to be 4 % of the global ecosystem services value (estimated at USD  $ 150 trillion for the year 2018) per year.11 The beneficial effects of natural environment on mental health are derived from myriad ecosystem services,12 including cultural services, such as esthetic enjoyment of landscape,13,14 and regulating services, such as pollutant removal and heat mitigation.1517 Although the definitions of natural environment vary across studies from a single type of vegetation (e.g., trees, grass alone) to a composite index of all natural elements [e.g., Normalized Difference Vegetation Index (NDVI)], studies are consistent in finding that exposure to the natural environment is associated with better mental health.1822 NDVI is calculated as the difference between near-infrared and red reflectance divided by their sum. The values range from 1 to 1, wherein zero and negative values generally indicate barren surfaces (e.g., rock and soil) and nonvegetated land (e.g., water bodies and ice), and greater positive values indicate denser green vegetation.23 Previous research18 using NDVI to estimate overall natural environment reported that a 0.1 increase in NDVI within 500 m of residences was found to be associated with a respective odds ratio (OR) of 0.85 [95% confidence interval (CI): 0.76, 0.95] and 0.81 (95% CI: 0.70, 0.93) of having depression and anxiety in adults. With a focus on women, another study20 reported that participants who lived in a neighborhood with the highest quartile of NDVI within 250 m of their residence had an associated 13% reduction in depression risk in comparison with those living in a neighborhood with the lowest quartile of NDVI. Although natural environment generally benefits mental health, ecosystem services derived from certain types of natural environment may be more relevant to mental health. For instance, many of the psychological benefits from nature are supported by the Attention Restoration Theory24,25 and the Stress Reduction Theory,6,26 which suggest that spending time in or simply looking at nature helps with recovery from mental fatigue, alleviation of anxiety, and stress reduction. These beneficial effects of natural environment may be largely determined by human perception or landscape preference. An experimental study27 reported that people had a preference for higher density of street trees but no preference for herbaceous cover. Other empirical research22 observed a positive association of better mental health with tree cover but not herbaceous cover.
However, exposure to the natural environment is not equitably distributed across the population, with socioeconomic status as a primary basis of inequity and environmental injustice.28,29 Urban greenery is found to be positively associated with income and educational attainment (i.e., undergraduate or graduate degree) and negatively associated with percentage of minoritized racial and ethnic groups and percentage of people living in poverty across neighborhoods in the United States.3032 Likewise, groups experiencing greater disadvantage tend to live in areas with more impervious surfaces and therefore are more susceptible to increased temperature or urban heat island effects.33 Moreover, minoritized and low-income populations tend to live in areas that are subject to more changes in land use/land cover for development and therefore are more susceptible to loss of nature and to deprivation of benefits from ecosystem services.34
The causes of inequitable distribution of access or exposure to natural environment are complex.35,36 Historical housing policies implemented at local, state, and/or federal levels are potential factors driving inequitable access to nature. For instance, the U.S. Federal Home Owners’ Loan Corporation (HOLC) established a policy in the 1930s to identify certain neighborhoods as too risky for mortgage investment. This policy, referred to as redlining, is considered to be a major contributor to persistent racial segregation in the United States.37,38 The HOLC was tasked to create residential security maps to evaluate the risk of housing foreclosures for mortgages in 239 U.S. cities. The HOLC maps were created based on many factors, including housing quality, income, and racial profiles.39,40 Neighborhoods were mapped and assigned a letter grade and a color code: A (best, green), B (still desirable, blue), C (declining, yellow), and D (hazardous, red - thus the term “redlined”). The neighborhoods assigned a grade of D were typically characterized by poor housing quality, predominately non-White and immigrant residents, and/or presence of hazardous environmental exposure sources. Residents who lived in the neighborhoods receiving the worst grade were often declined for loans or favorable mortgage terms,41 resulting in long-term disinvestment in the development and growth of these neighborhoods.42
This historical pattern of racial discrimination driven by redlining has shaped contemporary disparities in environmental exposure,4346 climate adaptation,33,47 and health conditions48 between urban neighborhoods. Nardone et al.44 observed that both present-day (2010) and estimated historical (1930) NDVI values consistently decreased across HOLC Grades A to D. With a specific focus on trees, Locke et al.45 reported that neighborhoods formerly redlined had, on average, 20% less tree cover in comparison with neighborhoods formerly assigned a green or A grade in 37 HOLC cities. A later study46 found similar results when including all cities with digital HOLC data available from the Mapping Inequality Project,41 with 20 % less tree cover in Grade D neighborhoods in comparison with Grade A neighborhoods. In addition, the estimated difference in ecosystem service values derived from tree cover in Grade A vs. D neighborhoods was USD  $ 112  million annually.46
The relative lack of ecosystem services derived from tree cover in redlined neighborhoods may play a role in the disproportionate health burden in these communities. There is a higher prevalence of poor mental health observed in redlined neighborhoods vs. nonredlined neighborhoods.49,50 Although the influence of redlining on the distributions of natural environment4446 and on health conditions has been studied,48,5153 the influence of redlining on the relationships between natural environment and mental health has not been previously investigated. This study attempts to address this research gap by examining associations in the variability of tree cover, depressive symptoms, and HOLC grade using data from a nationwide U.S. cohort of women.

Materials and Methods

Study Population

We included participants from the National Institute of Environmental Health Sciences (NIEHS) Sister Study cohort (henceforth referred to as “Sister Study”) whose residential address at enrollment was located within the historical HOLC graded neighborhoods. The Sister Study is a prospective cohort of 50,884 women 35–74 y of age without a history of breast cancer but with at least one full or half-sister diagnosed with breast cancer at enrollment during the period 2003–2009.54 Data were collected for multiple domains, including biological, sociodemographic, lifestyle, and health-related factors. Participants have been contacted every 2–3 y for detailed follow-ups since 2008. Data used in this analysis were from the Sister Study Data Release 8.1.
All participants in the Sister Study provided written informed consent. The Sister Study is overseen by the institutional review board of the National Institutes of Health (NIH). This analysis was approved by the institutional review board of the University of North Carolina, Chapel Hill (IRB #17-2573), and Human Subject Research Review through the U.S. Environmental Protection Agency (U.S. EPA) (HSR-000941).
We obtained the digital HOLC maps from the Mapping Inequality Project as of March 202141 to assign an historical HOLC grade based on the residential addresses for participants who had not moved since enrollment, because the new residential addresses for those who reported moving were not available at the time for this analysis. A total of 5,089 participants resided in cities subject to HOLC practices. After removing those who reported moving (total number: 680) and those who had missing values for health outcome and/or covariates (total number: 854), a total of 3,555 participants residing within 192 cities (Figure 1) were included for this analysis.
Figure 1. Distribution of the 3,555 Sister Study participants in the 192 cities subject to Home Owners’ Loan Corporation (HOLC) practices in this analysis. This map is created using ArcGIS Pro 3.1.2.

Health Outcome

We used depressive symptoms defined by the 10-item Center for Epidemiologic Studies Depression Scale (CES-D-10) as the health outcome. To match with the time frame of greenery measures, we used the data collected during the first follow-up (2008–2012). The 10-item CES-D is a validated short version of the original 20-item CES-D,55,56 which is one of the most commonly used self-report measures of depressive symptoms.57,58 Eight CES-D-10 statements are worded negatively, and two are worded positively54,59 [please see The Sister Special Survey Stress and Coping (Version 3) questions for CES-D-10 used in the first detailed follow-up in Supplemental Text; full questionnaire can be found on the Sister Study website at The Sister Study: Follow-up Data Collection (nih.gov)]. Each negative statement response is scored from 0 to 3 based on the frequency during the past week, whereas the positive statements are scored inversely from 3 to 0. The responses of frequency are Rarely or none of the time ( < 1 day), Some or a little of the time (1–2 d), Occasionally or a moderate amount of the time (3–4 d), and Most or all of the time (5–7 d). Because a cutoff value of 10 for CES-D-10 scores is found to be effective for classifying subjects with depressive symptoms,59,60 the CES-D scores in this analysis were dichotomized, such that participants with a CES-D score 10 (summing all responses) were considered to have depressive symptoms.

Neighborhood Greenery

Neighborhood greenery was measured using tree cover derived from the U.S. Forest Service (USFS) Tree Canopy Cartographic layer, part of the National Land Cover Database (NLCD) developed by the Multi-Resolution Land Characteristics Consortium (MRLC).61 The MRLC updates NLCD products every 5 y. At the time of the analysis, the USFS Tree Canopy was available for the years 2011 and 2016, and the year 2011 was used to represent the neighborhood tree cover for this analysis. This layer estimates percentage tree canopy in each 30 m × 30 m pixel across the contiguous United States, with values ranging from 0 to 100. Tree canopy exposure was estimated for each participant as the mean values of tree cover within 500 -m and 2,000 -m radial buffers of their primary residence. These two buffers were chosen based on prior research considering green space accessibility and health effects.62 The 500 -m buffer is associated with home environments within a distance corresponding to a walk of 5 to 10 min, whereas the 2,000 -m buffer corresponds to a walk of 20 to 30 min.63,64
Because our tree-cover data were for a single year (2011) and our health outcomes data were from years 2008 to 2012, we wanted to investigate whether the natural environment (tree cover) surrounding each home was consistent over the health outcomes study period. To assess tree cover consistency over time, we obtained NDVI data for the survey period of the health outcome (years 2008–2012). Though NDVI and tree cover are different measures, NDVI can provide information on the overall composition of the natural environment over time and is often used as a proxy of neighborhood greenery because it estimates the density of greenness in an area,65 rather than a specific vegetation type. We obtained the top-of-atmosphere reflectance (TOA) from Landsat 5 Thematic Mapper (TM) (https://landsat.gsfc.nasa.gov/article/landsat-5-2/) for years 2008 to 2011 and Landsat 7 Enhanced Thematic Mapper Plus ( ETM + ) (https://landsat.gsfc.nasa.gov/article/landsat-7-2/) for year 2012. The USFS Tree Canopy layer was developed primarily based on imagery during leaf-on seasons,66,67 and therefore we used the maximum NDVI values in summer as the closest proxy of tree canopy to investigate the temporal patterns of neighborhood greenery over the survey period. The mean values of the maximum NDVI in summer at the largest analysis unit in this study (i.e., 2,000 -m buffer) across the survey period were calculated for each participant. We elected to investigate NDVI for the 2,000 -m buffer only because any change in greenery over time would be more likely to be detected for the larger buffer around the home and any change within the smaller buffer would be captured by the larger buffer. To compare the temporal NDVI values derived from different Landsat satellites, we calibrated the values to the same standard using the equations established by Roy et al.68

Covariates

The covariates used in this analysis were all individual level and collected from the same survey period (i.e., years 2008–2012) as the health outcome, unless otherwise stated (Table 1). We included categorical sociodemographic factors: age ( < 55 y as referent vs. 55–64 y, 65 y), self-reported race and ethnicity (at baseline, non-Hispanic White as referent vs. non-Hispanic Black, Hispanic, and other race and ethnicities, including American Indian or Alaska Native, Asian, and Native Hawaiian or other Pacific Islander), marital status (never as referent vs. married, divorced/separated, and widowed), educational attainment (at baseline, high school or equivalent, or less than high school as referent vs. associate college or some college, bachelor’s degree, and graduate degree), employment status [retired as referent vs. working, homemaker/student, unemployment, and unable to work (i.e., medical leave, disability)], and household income (USD < $ 50,000 as referent vs. $ 50,000 $ 99,999 , and $ 100,000 ). Although antidepressant use may not strictly be considered a confounder, participant responses to the CES-D questions may be affected by medication use,69 and where participants live may affect their access to health care.70 Because many studies reported that neighborhood greenery supports physical activity,7174 which may have a mechanism similar to that of antidepressant medications,75 we ran models with and without self-reported use of medication prescribed for depression treatment. Included medications were identified using the Slone Drug Dictionary76 by their assigned product and class codes.
Table 1 Descriptive statistics of sociodemographic and neighborhood environmental characteristics by depressive symptoms for the Sister Study participants (2008–2012 follow-up) included in this analysis.
Variable Group Depressive symptoms Sample size (n)
Complete cases       3,555
    No Yes Full study population
Mean ± SD or n (%)b Mean ± SD or n (%) Mean ± SD or n (%)
Depressive symptoms Continuous 4.18 ± 2.61 14.53 ± 4.24 6.82 ± 5.48
  Dichotomized measure 2,650 (74.54%) 905 (25.46%) 3,555
Covariatesa
Age (y) Continuous 58.15 ± 8.64 57.31 ± 8.73 57.9 ± 8.67
< 55 883 (33.32%) 343 (37.90%) 1,226 (34.49%)
55–64 1,106 (41.74%) 371 (40.99%) 1,477 (41.55%)
65 661 (24.94%) 191 (21.10%) 852 (23.97%)
Missing 7
Race and ethnicity (baseline, self-reported) Non-Hispanic White 2,068 (78.04%) 698 (77.13%) 2,766 (77.81%)
Non-Hispanic Black 431 (16.26%) 133 (14.70%) 564 (15.86%)
Hispanic 90 (3.40%) 59 (6.52%) 149 (4.19%)
Other race/ethnicity 61 (2.30%) 15 (1.66%) 76 (2.14%)
Marital status Never 280 (10.57%) 135 (14.92%) 415 (11.67%)
Married 1,708 (64.45%) 501 (55.36%) 2,209 (62.14%)
Divorced/separated 508 (19.17%) 204 (22.54%) 712 (20.0%)
Widowed 154 (5.81%) 65 (7.18%) 219 (6.16%)
Missing 43
Education (baseline) High school or less 250 (9.43%) 91 (10.06%) 341 (9.59%)
Associate/college or so 594 (22.42%) 265 (29.28%) 859 (24.16%)
Bachelor 788 (29.74%) 261 (28.84%) 1,049 (29.51%)
Graduate 1,018 (38.42%) 288 (31.82%) 1,306 (36.74%)
Employment status Retired 413 (15.58%) 117 (12.93%) 530 (14.91%)
Homemaker/student 143 (5.40%) 44 (4.86%) 187 (5.26%)
Unable to work 38 (1.43%) 36 (3.98%) 74 (2.08%)
Unemployment 167 (6.30%) 73 (8.07%) 240 (6.75%)
Working 1,889 (71.28%) 635 (70.17%) 2,524 (71.00%)
Missing 63
Household income (USD) < $ 50,000 638 (24.08%) 310 (34.25%) 948 (26.67%)
$ 50,000 $ 99,999 929 (35.06%) 341 (37.68%) 1,270 (35.72%)
$ 100,000 1,083 (40.87%) 254 (28.07%) 1,337 (37.61%)
Missing 192
Use of depression medication No 1,891 (71.36%) 433 (47.85%) 2,324 (65.37%)
Yes 759 (28.64%) 472 (52.15%) 1,231 (34.63%)
Missing 72
Neighborhood greenery Mean ± SD Mean ± SD Mean ± SD
Tree cover at 500 m buffer (%) Continuous 16.96 ± 14.23 14.95 ± 13.44 16.50 ± 14.10
  By HOLC grade
  A 25.70 ± 15.70 23.80 ± 14.80 25.30 ± 15.50
  B 18.40 ± 13.70 17.00 ± 13.40 18.00 ± 13.60
  C 14.00 ± 12.00 13.80 ± 12.40 13.90 ± 12.10
  D 7.90 ± 10.10 5.28 ± 6.74 7.17 ± 9.34
Tree cover at 2,000 m buffer (%) Continuous 16.58 ± 12.54 14.75 ± 11.62 16.10 ± 12.30
  By HOLC grade
  A 22.30 ± 13.30 21.10 ± 12.20 22.10 ± 13.20
  B 17.60 ± 12.30 16.60 ± 11.50 17.4 ± 12.10
  C 15.10 ± 11.60 14.20 ± 11.10 14.90 ± 11.50
  D 8.95 ± 9.24 6.12 ± 6.19 8.16 ± 8.59
Random effect n (%) n (%) n (%)
Climate zone Arid 85 (3.21%) 35 (3.87%) 120 (3.38%)
Continental 1,913 (72.19%) 640 (70.72%) 2,553 (71.81%)
Temperate 652 (24.60%) 230 (25.41%) 882 (24.81%)
Stratification n (%) n (%) n (%)
HOLC grade A 521 (19.66%) 114 (12.60%) 635 (17.86%)
B 881 (33.25%) 310 (34.25%) 1,191 (33.50%)
C 908 (34.26%) 350 (38.67%) 1,258 (35.39%)
D 340 (12.83%) 131 (14.48%) 471 (13.25%)
Sensitivity analysis for census tract–level variables
1940 Census tract-level variables
Residing in a 1940 census tract 2,210
  Mean ± SD or n (%) Mean ± SD or n (%) Mean ± SD or n (%)
Percent non-White (%) Continuous 2.82 ± 9.91 3.02 ± 10.44 2.87 ± 10.05
1st Quartile (0.00–0.12) 402 (24.65%) 151 (26.08%) 553 (25.02%)
2nd Quartile (0.13–0.45) 412 (25.26%) 140 (24.18%) 552 (24.98%)
3rd Quartile (0.46–1.53) 399 (24.46%) 153 (26.42%) 552 (24.98%)
4th Quartile (1.54–99.9) 418 (25.63%) 135 (23.32%) 553 (25.02%)
Percent population with at least high school degree (%) Continuous 37.61 ± 13.34 34.95 ± 13.77 36.92 ± 13.50
1st Quartile (0.00–26.62) 377 (23.11%) 176 (30.40%) 553 (25.02%)
2nd Quartile (26.63–37.51) 400 (24.52%) 153 (26.42%) 553 (25.02%)
3rd Quartile (37.52–47.91) 421 (25.81%) 130 (22.45%) 551 (24.93%)
4th Quartile (47.92–76.64) 433 (26.55%) 120 (20.73%) 553 (25.02%)
Percent population employed (%) Continuous 39.44 ± 5.52 39.15 ± 6.05 39.36 ± 5.66
1st Quartile (0.00–36.34) 393 (24.10%) 160 (27.63%) 553 (25.02%)
2nd Quartile (36.35–39.01) 407 (24.95%) 145 (25.04%) 552 (24.98%)
3rd Quartile (39.02–41.83) 416 (25.51%) 137 (23.66%) 553 (25.02%)
4th Quartile (41.84– 80.00) 415 (25.44%) 137 (23.66%) 552 (24.98%)
2012 census tract–level variables
Residing in a 2012 census tract 3,555
  Mean ± SD or n (%) Mean ± SD or n (%) Mean ± SD or n (%)
Percent non-White (%) Continuous 30.44 ± 27.16 31.69 ± 26.81 30.75 ± 27.09
1st Quartile (0.18–10.85) 692 (26.15%) 199 (22.04%) 891 (25.11%)
2nd Quartile (10.86–20.70) 654 (24.72%) 228 (25.25%) 882 (24.85%)
3rd Quartile (20.71–42.12) 651 (24.60%) 238 (26.36%) 889 (25.05%)
4th Quartile (42.13–100.00) 649 (24.53%) 238 (26.36%) 887 (24.99%)
Percent population with at least high school degree (%) Continuous 90.15 ± 9.45 88.92 ± 9.97 89.82 ± 9.71
1st Quartile (0.00–85.33) 644 (24.34%) 244 (27.02%) 888 (25.02%)
2nd Quartile (85.34–89.82) 640 (24.19%) 249 (27.57%) 889 (25.05%)
3rd Quartile (89.83–96.98) 653 (24.68%) 235 (26.02%) 888 (25.02%)
4th Quartile (96.99–100.00) 709 (26.80%) 175 (19.38%) 884 (24.91%)
Percent population employed (%) Continuous 61.79 ± 9.94 61.53 ± 10.04 61.70 ± 10.01
1st Quartile (0.00–56.41) 649 (24.53%) 238 (26.36%) 887 (24.99%)
2nd Quartile (56.42–61.70) 668 (25.25%) 219 (24.25%) 887 (24.99%)
3rd Quartile (61.71–68.35) 661 (24.98%) 225 (24.92%) 886 (24.96%)
4th Quartile (68.36–86.99) 668 (25.25%) 221 (24.47%) 889 (25.05%)
Median household income (USD) Continuous 69,928.17 ± 36,181.76 63,901.79 ± 32,840.96 68,650.33 ± 36,077.66
< $ 25,000 138 (5.22%) 49 (5.43%) 187 (5.27%)
$ 25,001 $ 49,999 746 (28.19%) 300 (33.22%) 1,046 (29.47%)
$ 50,000 $ 74,999 794 (30.01%) 288 (31.89%) 1,082 (30.49%)
$ 75,000 $ 99,999 471 (17.80%) 151 (16.72%) 622 (17.53%)
$ 100,000 497 (18.78%) 115 (12.74%) 612 (17.24%)
Missing 1
Note: —, no data; HOLC, Home Owners’ Loan Corporation; SD, standard deviation; USD, U.S. dollars.
a
Obtained mostly from the same survey period (2008–2012 follow-up) as the health outcome from the Sister Study, unless otherwise stated as baseline (2003–2008).
b
Total number of missing covariates are reported under each covariate if applicable. Numbers are mean values ± SDs for continuous variables, and total number with percentage in parentheses for categorical variables. Mean and SD values and percentages are calculated based on complete cases (total number: 3,555).
We also considered census tract–level socioeconomic variables at years 1940 and 2012 to represent the neighborhood profile during the time when the HOLC maps were created and at present day, respectively, for sensitivity analysis to evaluate the necessity of incorporating census tract–level covariates. The census tract–level covariates were chosen based on the individual-level covariates and the availability of corresponding variables. The 1940 Census variables were based on the decennial census obtained from the Individual Public Use Microdata Series National Historical Geographic Information Systems database (IPUMS).77 The 1940 Census variables considered in this study included total number of non-White people, people who are employed, and people with a high school degree or higher. All the 1940 Census variables were calculated into percentages using the total population in the tract as the denominator and classified into quartiles for analysis. The 2012 Census variables were based on the American Community Survey 5-y estimates (2008–2012) obtained from the U.S. Census Bureau and included median household income (categorical: < USD  $ 25,000 ) as referent vs. $ 25,000 $ 49,999 , $ 50,000 $ 74,999 , $ 75,000 $ 99,999 , and $ 100,000 , percentage of non-White population in quartiles, percentage of people who are employed in quartiles, and percentage of people with at least high school degree in quartiles. Each participant’s residential location was geolocated to the 1940 and 2012 Census tract polygons obtained from the IPUMS and U.S. Census Bureau, respectively, using Spatial Join (point to polygon) in ArcGIS Pro (version 2.9.2, Environmental Systems Research Institute, ESRI). Census tract boundaries were delineated for only 60 cities in the 1940s,78 which left 2,210 participants who resided in a HOLC neighborhood where information on 1940 Census tract was also available.

Analytical Approach

The analytical approach (Figure 2) included comparison of neighborhood greenery across years 2008–2012, generalized mixed effect modeling to estimate the relationships between depressive symptoms and tree cover, and stratification by HOLC grade to observe the differences in the associations across HOLC grades. We compared the mean differences in tree cover between HOLC groups at both buffer sizes using one-way analysis of variance (ANOVA) and Tukey Honestly Significant Difference (HSD) test for post hoc comparisons. To understand whether the patterns of tree cover across HOLC grades at year 2011 were a one-time phenomenon or consistent across the survey period, we also compared mean differences in NDVI values across years 2008–2012. The mean differences in tree cover and NDVI values between HOLC groups were adjusted for individual-level covariates mentioned above. A generalized linear mixed effect model was used to analyze the associations between neighborhood greenery and depressive symptoms. Because climate plays a critical role in vegetation distribution79,80 and may play a role in human perception of nature,81 we applied a random intercept to account for the dependency between individuals within climate zones (cluster). We divided the contiguous United States into arid, continental, and temperate climate zones defined by the Köppen climate classification.82 The main characteristic of arid climate zone is low precipitation, and continental and temperate climate zones are primarily characterized by temperature—at least 1 month below 3 ° C and at least 1 month above 10°C, and the coldest temperature between 3 ° C and 18°C, respectively.83
Figure 2. Analytical approach to model the associations between neighborhood greenery and depressive symptoms using data from the Sister Study cohort collected from the 2008–2012 follow-up.
Effect modification was examined by incorporating multiplicative interaction terms for all the covariates and greenery measures. Based on the examination of interaction terms, we stratified the analysis to observe the relationships between present-day neighborhood greenery and depressive symptoms for participants residing in the historical HOLC graded A to D neighborhoods separately. Last, we performed sensitivity analysis to include census tract–level covariates in 1940 and 2012 separately to examine whether the relationships are affected by the historical or present-day area-level sociodemographic factors. Results with a p -value < 0.05 were considered to be statistically significant in this analysis. All the statistical analyses were performed using SAS (version 9.4; SAS Institute Inc.).

Additional Analysis

We applied the analytical approach described above to additionally examine the associations between neighborhood greenery and depressive symptoms using different populations in the Sister Study. This analysis included all the participants in the Sister Study cohort and participants who did not reside in areas subject to HOLC practices. We also performed another analysis for season of survey completion (i.e., spring, summer, fall, and winter) to account for seasonal variability.

Results

Participants’ Characteristics

Approximately one quarter of the participants had depressive symptoms as determined from CES-D scores at the first detailed follow-up (Table 1). Mean values of CES-D score were 14.5 [ standard deviation  ( SD ) = 4.2 ] and 4.2 ( SD = 2.6 ) for participants with and without depressive symptoms, respectively. Mean age was 57.9 y, with 25 % of the participants 65 y of age and older. Most of the participants (77.8%) were non-Hispanic White, married (62.1%), and with a bachelor’s (29.5%) or graduate (36.7%) degree. Approximately 70% of the participants were currently working, and 40 % of the participants had an annual household income USD  $ 100,000 . Approximately 35% of the participants reported using antidepressant medication. Most of the participants (71.8%) resided in continental climate, and only 3.4% of the participants resided in an arid climate. Approximately 18% of the participants resided within the historical HOLC grade A area, and 33.5%, 35.4%, and 13.3% of the participants lived in the historical HOLC grades B, C, and D areas, respectively.
Characteristics by HOLC grade (Figure 3 and the numeric values in Supplemental Excel Table S1) showed that 18 % of the participants who resided in Grade A neighborhoods had depressive symptoms, but more than a quarter of the participants in all other HOLC grades had depressive symptoms. The age distribution was similar across HOLC grades, with 25 % of the participants 65 y of age and older. In Grade A neighborhoods, higher percentages of participants were non-Hispanic White (91.0% vs. 82.0%, 73.3%, and 61.6% for Grades B, C, D, respectively), married (74.8% vs. 64.5%, 59.5%, 46.1%), and homemaker or student (7.6% vs. 4.7%, 4.7%, and 5.1%), and had at least a bachelor’s degree (78.7% vs. 71.3%, 58.0%, and 58.6%), a household income USD  $ 100,000 (57.3% vs. 41.1%, 28.3%, and 27.2%), and more use of depression medication (36.2% vs. 35.5%, 34.8%, and 29.7%) in comparison with neighborhoods with other HOLC grades.
Figure 3. Individual-level participants’ characteristics by HOLC grade for the 3,555 Sister Study participants used in this analysis. Study population (N) in each HOLC grade are labeled in the y-axis. Note: HOLC, Home Owners’ Loan Corporation.
The 1940 Census tract–level variables (Table 1) indicated that population demographics for the historical census tracts where the participants resided comprised 2.9% ( SD = 10.1 ) non-White, 36.9% ( SD = 13.5 ) had at least high school degree, and 39.4% ( SD = 5.7 ) were employed. The 2012 Census tract–level variables showed that population demographics for the current census tracts were 30.8% ( SD = 27.1 ) non-White, 89.8% ( SD = 9.7 ) had at least high school degree, 61.7% ( SD = 10.0 ) were employed, and 65.3% had a median household income > USD  $ 50,000 ( mean = $ 68,650 , SD = 36,078 ).

Characteristics of Neighborhood Greenery

Mean values of percentage tree cover within 500 -m and 2,000 -m buffers were both 16 % (Table 1). Participants who did not have depressive symptoms had slightly higher mean values of tree cover at both buffer sizes (17.0% for 500 -m and 16.6% for 2,000 -m buffers) in comparison with those who had depressive symptoms (15.0% for 500 -m and 14.8% for 2,000 -m buffers). Higher mean values of percentage tree cover were also observed for those without depressive symptoms in comparison with those with depressive symptoms across HOLC grades (Neighborhood greenery by HOLC grade in Table 1).
One-way ANOVA showed significant differences in tree cover by HOLC grade at both buffer sizes with adjustment for potential covariates ( F = 136.9 , p < 0.001 for 500 -m buffer and F = 97.6 , p < 0.001 for 2,000 -m buffer). Post hoc comparisons using the Tukey HSD test showed that mean values of tree cover after adjusting for potential covariates were significantly less in each consecutive groups from Grades A to D at both buffer sizes (Figure 4A). Accordingly, the greatest differences in mean values were observed between Grades D and A, with a mean difference of 18.0 % (95% CI: 19.9 % , 16.2 % ) at 500 -m buffer and 13.7 % (95% CI: 15.5 % , 12.0 % ) at 2,000 -m buffer. The smallest differences were between observed Grades C and B at both buffer sizes ( 4.1 % , 95% CI: 5.3 % , 2.9 % at 500 -m buffer and 2.5 % , 95% CI: 3.7 % , 1.4 % ) at 2,000 -m buffer. This pattern was confirmed by the greenness measured by NDVI across years 2008–2012 (Figure 4B). Significant differences in mean NDVI values across HOLC grades were observed (respective F values for years 2008, 2009, 2010, 2011, and 2012 were 147.2, 154.1, 148.8, 147.4, and 123.2; p < 0.001 for all years). Mean NDVI values were also decreased across each consecutive group from HOLC Grades A to D, and the greatest and smallest differences in NDVI values were between Grades D and A and Grades C and B, respectively.
Figure 4. Pairwise comparison of HOLC grades for mean difference with 95% CIs in the brackets of (A) tree cover in the year 2011 at 500 -m and 2,000 -m buffer, and (B) NDVI values in years 2008–2012 at 2,000 -m buffer around 3,555 Sister Study participants’ homes. Study population (N) in each HOLC grade are labeled in the y-axis. Note: CI, confidence interval; HOLC, Home Owners’ Loan Corporation; NDVI, Normalized Difference Vegetation Index.

Relationships between Present-Day Neighborhood Greenery and Depressive Symptoms

Models results based on including vs. excluding use of depression medication were nearly identical, and therefore we present the results with the use of depression medication in the main tables and include the results without depression medication in the Supplemental Table 1.
For the full study population across the 192 historical redlining areas, a 10% increase of tree cover was associated with 0.93 (95% CI: 0.88, 0.99) and 0.91 (95% CI: 0.85, 0.97) reduced odds of having depressive symptoms at 500 -m and 2,000 -m buffers, respectively (Table 2).
Table 2 AOR and 95% CI of having depressive symptoms, given a 10% increase in tree cover at 500 -m and 2,000 -m buffers from home for the full study population and stratification by HOLC grade for the Sister Study participants (2008–2012 follow-up) included in this analysis.
  n Tree covera
500 -m buffer 2,000 -m buffer
AORb (95% CI) AOR (95% CI)
Full study population 3,555 0.93 (0.88, 0.99) 0.91 (0.85, 0.97)
Stratification by HOLC Grade
A 635 0.98 (0.85, 1.14) 0.98 (0.82, 1.16)
B 1,191 0.92 (0.83, 1.02) 0.93 (0.83, 1.04)
C 1,258 1.02 (0.91, 1.14) 0.94 (0.84, 1.06)
D 471 0.72 (0.52, 0.99) 0.63 (0.45, 0.90)
Note:
AOR, adjusted odds ratio; CI, confidence interval; HOLC, Home Owners’ Loan Corporation.
a
Estimated using 2011 U.S. Forest Service Percent Tree Canopy.
b
Estimated using generalized linear mixed effect model with climate zone as the random effect with adjustment for age, self-reported race/ethnicity, marital status, educational attainment, employment status, income, and use of depression medication.
Effect modification examined by incorporating interaction terms between tree cover and each covariate showed that no significant ( p < 0.05 level) interactions were observed (Table 3), but a marginal significance ( p = 0.088 and 0.096 for canopy at 500 m and 2,000 m , respectively) was observed by the interaction between tree cover and HOLC grade.
Table 3 p -Values for interaction terms between tree cover and each covariate.
Potential effect modifier (Covariatea) Groups Exposure (tree coverb)
500 -m buffer 2,000 -m buffer
p -Values for interaction p -Values for interaction
Age (y) < 55 (Ref.), 55–64, 65 0.567 0.309
Race and ethnicity (baseline) Non-Hispanic White (Ref), Non-Hispanic Black, Hispanic, Other race and ethnicity 0.816 0.600
Marital status Never (Ref), Married, Divorced/Separated, Widowed 0.164 0.305
Education (baseline) High school or less (referent), Associate/College or so, Bachelor, Graduate 0.698 0.928
Employment status Retired (Ref), Homemaker/Student, Unable to work, Unemployment, Working 0.133 0.230
Household income (USD) < $ 50,000 (Ref), $ 50,000 $ 99,999 , $ 100,000 0.601 0.259
Use of depression medication No (Ref), Yes 0.521 0.381
HOLC graded A (Ref), B, C, D 0.088 0.096
Note: HOLC, Home Owners’ Loan Corporation; Ref, referent.
a
Obtained mostly from the same survey period (2008–2012 follow-up) as the health outcome from the Sister Study for 3,555 participants used in this analysis, unless otherwise stated as baseline (2003–2008).
b
Estimated using 2011 U.S. Forest Service Percent Tree Canopy.
c
Estimated using generalized linear mixed effect model with climate zone as the random effect with adjustment for age, self-reported race/ethnicity, marital status, educational attainment, employment status, income, and use of depression medication.
d
Used for stratification in this analysis.
Within HOLC grade strata (Table 2), an association between greater tree cover and reduced odds of having depressive symptoms was only apparent among participants living in HOLC Grade D neighborhoods. A 10% increase in tree cover was associated with 0.72 (95% CI: 0.52, 0.99) and 0.63 (95% CI: 0.45, 0.90) reduced odds of having depressive symptoms for 500 -m and 2,000 -m buffers, respectively, for participants who resided in historically redlined neighborhoods.
Sensitivity analysis by incorporating the historical and present-day census tract–level variables showed that the results were similar to those based on models that were adjusted for individual-level variables only (Figure 5). No significant differences were observed between models that included the additional 1940 Census tract–level variables vs. those that did not ( Chi-square = 8.32 , p = 0.5 ; AICC: 2,381 for model with tract-level variables vs. 2,371 for model with only individual-level variables). Similarly, no difference was observed for the 2012 Census tract–level variables ( Chi-square = 9.58 , p = 0.4 ; AICC: 3,817 vs. 3,807 for models with tract-level and only individual-level variables, respectively).
Figure 5. Sensitivity analysis comparing models adjusting for individual-level covariates only (solid line) vs. additionally adjusting for census tract–level covariates (dashed line) for 1940 (left panel) and 2012 (right panel). AOR is estimated using a 10% increase of tree cover. Total number (N) of full study population and within each HOLC grade (A–D) are labeled on the top of the panel. All models were adjusted for individual-level age, self-reported race/ethnicity, marital status, educational attainment, employment status, income, and use of depression medication. Additional census tract–level covariates at year 1940 and year 2012 for sensitivity analysis included percentage non-White, percentage of population with at least high school degree, and percentage of population employed. Census tract–level covariates at year 2012 additionally included median household income. Note: AOR, adjusted odds ratio; HOLC, Home Ownes’ Loan Corporation.
Additional analysis for the comparisons of different study populations based on all the participants in the Sister Study cohort and participants who did not reside in areas subject to HOLC practices (Supplemental Table 2) showed that tree cover was generally associated with lower odds of having depressive symptoms at both buffer sizes. The results based on models with and without survey season as a covariate (Model A and B, respectively, in Supplemental Table 3) showed that the results were identical.

Discussion

We observed a statistically significant association between current neighborhood greenery (tree cover) and women’s depressive symptoms. This association and neighborhood greenery independently varied by HOLC grade. The importance of the natural environment in promoting human health and well-being is well-recognized.84,85 Just as adverse effects of the environment have been shown to disproportionately impact socioeconomically disadvantaged communities,28,29 there is concern that this burden may be compounded by the unequal distribution of benefits derived from the natural environment. To achieve the goals for healthy and sustainable communities, it is critical to understand the disparities in environmental exposure, health, and their relationships across communities. Recognizing the public health importance of mental health with a consideration of historical economic practices of redlining, we examined the present-day associations between neighborhood greenery and depressive symptoms across neighborhoods with historically defined HOLC grades.
Our findings on the depressive symptoms are consistent with previous research reporting that redlined neighborhoods had higher prevalence of poor mental health.50 In this analysis, CES-D scores and rates of having depressive symptoms tended to be higher in neighborhoods with the less-desirable HOLC grades. Consistent with Nardone et al.,44 we observed that exposure to the natural environment as estimated by NDVI is significantly lower in historically redlined neighborhoods in comparison with those that were not. In addition, the observed differences of tree cover in Grade D and A neighborhoods were not only one-time phenomenon but consistent throughout the survey period, with findings similar to those observed in previous studies.45,46 At the address level, neighborhoods formerly assigned as Grade D had on average 20% and 13% less tree cover at the 500 -m and 2,000 -m buffer, respectively, in comparison with neighborhoods formerly assigned as Grade A. The greater difference observed at the smaller buffer size is likely attributable to a smaller classification error because there is greater probability that the larger buffer area will stray into adjacent areas that were assigned other HOLC grades. Because environmental exposures are not restricted by administrative boundaries, further investigation is needed to understand the effects of redlining in differently graded adjacent neighborhoods.
Although the contemporary disparities in the distribution of neighborhood greenery and health conditions are both associated with the historical patterns of racial discrimination, the effects of neighborhood greenery on health outcomes can be complex. Although some studies suggest that there is a minimum threshold of exposure to natural environment for meeting better health outcomes,22,86 small amounts of neighborhood greenery, such as those observed in the redline neighborhoods, may not show evident effects on health outcomes. However, stratified analysis by HOLC grade reveals that more tree cover is associated with reduced odds of having depressive symptoms across all the HOLC grades. The benefits of tree cover on depressive symptoms appear not to be linear across the HOLC grades but rather much more potent in redlined neighborhoods, where a wide range of ecosystem services could be missing because of the scarcity of tree cover.44,46 Disadvantaged groups are likely to suffer precipitous and cumulative impacts associated with poverty and race, including diminished access to health care,8789 air pollution,43,90,91 and noise,92,93 which may lead to a greater gap for improvement in health conditions and environmental exposures (e.g., reduction in air pollution and increase in neighborhood greenery) in comparison with those in nondisadvantaged groups.94 Thus, even with only 13% of the participants residing in redlined neighborhoods, we observed much stronger effects of neighborhood greenery on depressive symptoms.
Our findings suggest increased tree cover as a strategy for addressing environmental justice issues. Regardless of the small amount of tree cover in redlined neighborhoods, an increase of the same percentage of tree cover shows greater effects on improving mental health in redlined neighborhoods in comparison with nonredlined neighborhoods. Given that redlined neighborhoods tend to have greater risks for climate impacts such as heat exposure33 and air pollution,43 which are found to associate negatively with many health outcomes,9599 increasing tree cover not only has the potential to reduce the prevalence of depression but also to enhance overall resilience to climate impacts. In addition, increases in tree cover may bring co-benefits for health promotion and the environment through creating opportunities for physical activity and social interactions and through reducing air pollution. An investment of tree planting in vulnerable communities may offer an effective solution for reducing disparities in both environmental exposures and health conditions. The beneficial effects from tree cover may even be more pronounced during public health emergencies, such as the COVID-19 pandemic, whereby many studies reported that disadvantaged communities have greater risks of adverse health outcomes.100102 Although there are complex social and environmental factors involved, our findings support that contact with natural environment may help alleviate mental health issues, especially during public health crises.9,103,104 However, we caution that efforts are needed to ensure that communities are part of decision-making processes when addressing disparities. Factors such as location and types of trees planted, clear descriptions of benefits conveyed, and potential impacts on housing prices should be carefully considered.
The strengths of this analysis include the availability of individual-level data on health outcome and covariates from a large U.S. national cohort, as well as environmental exposures at multiple buffer sizes. The Sister Study collects a wealth of information on biological, sociodemographic, lifestyle, and health-related factors from participants across the United States54 that allowed us to build a model accounting for multiple potential covariates. The broad geographic distribution of Sister Study participants provided us an opportunity to systematically examine the effects of historical HOLC grades on the associations between neighborhood greenery and depressive symptoms. The greenery measures used in this analysis represent the proportion of tree canopy within each 30 -m pixel, which provide sufficient accuracy for estimating tree canopy across the United States.105 Because the distribution of vegetation is greatly affected by climate, the use of a generalized linear mixed effect model accounts for potential clusters by climate zone.
There are also study limitations to consider in the interpretation of these results. First, study findings are based on associations derived from cross-sectional analysis limiting causal inference. Second, although there are aspects of the Sister Study cohort that are nationally representative,54 the cohort consists only of women and is biased in some important ways, including a bias toward non-Hispanic White, well-educated, women over 55 y of age and with a sister diagnosed with breast cancer. Furthermore, by focusing on HOLC cities that included a greater percentage of participants who were non-White, these findings may not generalize to the entire Sister Study cohort. In addition, by focusing only on cities subject to HOLC practices, we eliminated most of the participants in the cohort and therefore limited the power of our statistical analysis. To address this limitation, we analyzed the Sister Study full cohort and the subset sample of participants who were not residing in areas subject to HOLC practices. The results were consistent with the observation in the main analysis that increases in tree cover were associated with reduced ORs of having depressive symptoms. However, the effects were smaller and less evident.
We were able to account for many individual-level covariates but not all. Although redlined neighborhoods are more subject to gentrification, we do not have data to account for this factor. Previous research found that not everyone prefers to have trees in their neighborhoods.106,107 We do not have information about participants’ preferences for landscaping. Likewise, we do not have information to address potential residential self-selection bias. Another limitation related to model adjustment is that we did not account for potential seasonal effects. Others have shown that season has an influence on depressive symptoms.108110 We examined season of CES-D-10 collection as an additional covariate. However, we did not observe differences in results for the models with vs. without season as a covariate. Because the participants in this analysis are mostly over 55 y of age, these findings are consistent with previous research111 reporting that the effects of seasonal patterns on mental health were reduced for people age 55 y and older.
Harmful environmental factors, such as air pollution, are inversely associated with better mental health112,113 but can be mitigated by tree cover.114 As with tree cover, exposure to air pollution is not equitably distributed, where redlined neighborhoods tend to have higher air pollution levels.43 Although we did not account for harmful environmental factors such as air pollution, future research should consider including both beneficial and detrimental environmental factors to understand the compounded disparities in the effects of environmental exposures on health outcomes.
The distribution of vegetation is greatly affected by climate79,80 and may subsequently influence the relationships between neighborhood greenery and health outcomes. Previous studies115,116 observed stronger associations between neighborhood greenery and health outcomes for people living in arid climates, where the vegetation is scarce, in comparison with continental or temperate climates. People who resided in historically redlined neighborhoods in an arid climate may be even more susceptible to potential risks of climate impacts. Due to our sample size, we were not able to evaluate whether the relationships between neighborhood greenery and depressive symptoms vary across climate zones for people who resided in historically redlined neighborhoods. However, our model approach accounts for the clustering by climate zone so that our results are generalizable across climate zones. We acknowledge that the effects of greenery on depressive symptoms by climate zone is of interest and see an important need to build on this line of research.

Conclusions

Relationships between environments, human health, and socioeconomic factors are complex. There are increasing efforts to address environmental and social justice issues across the United States, including President Biden’s Executive Order 13990, titled “Protecting Public Health and the Environment and Restoring Science to Tackle the Climate Crisis.”117 We build on the existing literature by identifying the effects of neighborhood greenery on depressive symptoms and the contemporary disparities in environmental exposures created by the housing policy developed almost a century ago. We further extend current knowledge to understand the variations in the relationships between neighborhood greenery and depressive symptoms in the historical HOLC cities. Findings from this analysis not only provide additional evidence on the benefits of neighborhood greenery on human health but also identify the communities at risk and suggest a remediation strategy focused on neighborhood greenery for those communities continuing to experience legacy environmental injustice because of the economic policies of the 1930s.

Acknowledgments

The authors would like to thank T. Luben and J. Woo for their time and thoughtfulness in providing valuable feedback. The authors would also like to thank the Sister Study Epidemiology Team for all their support and thank our former U.S. EPA ORISE colleagues, R. Silva and F. Cochran for their efforts in establishing this collaborative effort between the U.S. EPA and the NIEHS. Finally, the authors are indebted to our former EPA colleague, L. Jackson, for her dedication and remarkable contributions in fostering the eco-health research field.
This work was funded, in part by the Intramural Research Program of the NIH, NIEHS (ZO1 ES-044005 to D.P.S.).
This paper has been reviewed by the Center for Public Health and Environmental Assessment in the Office of Research and Development at the U.S. EPA and approved for publication. Approval does not signify that the contents reflect the views and policies of the Agency, nor does the mention of trade names of commercial products constitute endorsement or recommendation for use.

Article Notes

The authors declare they have nothing to disclose. They have no conflict of interest and no actual or potential competing financial interests.

Supplementary Material

File (ehp12212.smcontents.508.pdf)
File (ehp12212.s001.acco.pdf)
File (ehp12212.s002.codeanddata.acco.zip)

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Information & Authors

Information

Published In

Environmental Health Perspectives
Volume 131Issue 10October 2023
PubMed: 37851582

History

Received: 29 September 2022
Revision received: 5 September 2023
Accepted: 20 September 2023
Published online: 18 October 2023

Authors

Affiliations

Office of Research and Development, U.S. Environmental Protection Agency (U.S. EPA), Research Triangle Park, North Carolina, USA
Maliha S. Nash
Office of Research and Development, U.S. EPA, Newport, Oregon, USA
Daniel J. Rosenbaum
Oak Ridge Institute for Science and Education at Office of Research and Development, U.S. EPA, Research Triangle Park, North Carolina, USA
Current address: Daniel J. Rosenbaum, Division of Occupational Science and Occupational Therapy, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA.
Steven E. Prince
Office of Research and Development, U.S. Environmental Protection Agency (U.S. EPA), Research Triangle Park, North Carolina, USA
Aimee A. D’Aloisio
Social & Scientific Systems, DLH Holdings Corporation, Durham, North Carolina
Megan H. Mehaffey
Office of Research and Development, U.S. Environmental Protection Agency (U.S. EPA), Research Triangle Park, North Carolina, USA
Dale P. Sandler
National Institute of Environmental Health Sciences, National Institutes of Health, U.S. Department of Health and Human Services, Research Triangle Park, North Carolina, USA
Timothy J. Buckley
Office of Research and Development, U.S. Environmental Protection Agency (U.S. EPA), Research Triangle Park, North Carolina, USA
Anne C. Neale
Office of Research and Development, U.S. Environmental Protection Agency (U.S. EPA), Research Triangle Park, North Carolina, USA

Notes

Address correspondence to Wei-Lun Tsai. Telephone: (919) 966-0651. Email: [email protected]

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