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The Association between Outdoor Artificial Light at Night and Breast Cancer Risk in Black and White Women in the Southern Community Cohort Study.

Introduction

Black women in the United States are more likely to develop breast cancer at a younger age and to be diagnosed with more aggressive subtypes and more advanced stage disease, both contributing to higher rates of breast cancer mortality among Black women. (1) Light at night (LAN) has been proposed as a breast cancer risk factor because it inhibits nighttime production of melatonin, a hormone that may modulate biological pathways involved in breast cancer carcinogenesis. (2,3) Several epidemiologic studies have linked higher outdoor LAN estimated from satellite imagery to elevated incidence of breast cancer, including in cohorts predominantly comprised of White women with relatively high socioeconomic status (SES). (4,5,6) However, it remains unclear whether LAN is associated with breast cancer risk among Black women and women of lower SES.

Methods

We examined the relationship between LAN and incident breast cancer in the Southern Community Cohort Study (SCCS). (7,8) The vast majority of participants (86%) were recruited from community health centers in the southeastern United States that primarily served uninsured and underinsured populations, and ~ 2/3 were Black. Our analytic cohort included 30,518 Black and 12,982 White women who were cancer free and reported residential addresses at baseline. LAN exposures were estimated by linking geocoded baseline addresses (2002-2009) with satellite images in 2004 obtained by the U.S. Defense Meteorological Satellite Program's Operational Linescan System, and we used the high-dynamic range data to avoid saturation in high-LAN areas. (9) Incident breast cancer cases were identified via linkage to state cancer registries and vital status was ascertained from the Social Security Administration--both through 31 December 2017. Data on estrogen receptor (ER) status and cancer stage were obtained from cancer registries and supplemented by pathology reports and medical records. Race was self-reported at baseline. Institutional review boards at Vanderbilt University (Nashville, TN) and Meharry Medical College (Nashville, TN) approved the study and participants provided informed consent at the time of enrollment. We used Cox proportional hazards models to estimate hazard ratios (HRs) and 95% confidence intervals (CIs) comparing higher quintiles of LAN (Q2-Q5) with the lowest quintile, as well as for each 10-unit increase in LAN. Models were adjusted for multiple covariates as listed in table footnotes.

Results

Among all women in the cohort, we found a statistically significant increased risk of breast cancer overall in association with increasing levels of LAN [[HR.sub.Q5 vs. Q1] = 1.27 (95% CI: 1.00, 1.60), [p.sub.trend] = 0.05] and for ER+ breast cancer specifically [HRq5 vs. Q1 = 1.37 (95% CI: 1.02, 1.84), [p.sub.trend] = 0.01] (Table 1). For Black women, the highest quintile was associated with a 28% increase in overall and ER+ breast cancer risk [[HR.sub.Q5 vs Q1] = 1.28 (95% CI: 0.98, 1.68), [p.sub.trend] = 0.05 and 33% (1.33 (95% CI: 0.94, 1.88), [p.sub.trend] = 0.02), respectively] with borderline statistical significance. The patterns of association appeared similar in White women, but the effect estimates were relatively less precise owing to smaller sample sizes and the [p.sub.trend] values were not statistically significant. For ER- breast cancer in Black women, breast cancer incidence appeared higher for women in Q2-Q5 of LAN compared to Q1 but did not show a clear exposure-response relationship. Results from the analysis stratified by tumor stage were mixed (Table 2): in Black women, the relationship between LAN and increased breast cancer risk was observed for localized breast cancer only, whereas in White women, the relationship was observed for regional/distant stages.

Discussion

Our findings corroborate the previously reported positive association between LAN and breast cancer risk and extend prior work by characterizing this relationship among both Blacks and Whites in a large cohort of women recruited from disadvantaged communities. Several previous cohort investigations, including in the California Teachers Study, (4) the Nurses' Health Study II, (5) and the National Institutes of Health-AARP Diet and Health Study, (6) reported a modest increase in breast cancer risk associated with higher outdoor LAN levels (10-14%, comparing the highest to the lowest quintile). In our SCCS analysis, the effect sizes appeared larger compared with those in previous cohorts (4,5,6) although the distribution of LAN was similar and the confidence intervals overlap. We speculate that the large proportion of low SES and Black women in the SCCS may have partially contributed to the larger effect sizes. Compared with those in more advantaged populations, low SES individuals are more likely to have sleep disturbances and shorter sleep duration due to poor housing conditions, high stress, and irregular and unpredictable daily schedules, (10) and therefore they may be more likely to engage in nonsleep activities at night that lead to higher exposures to ambient LAN. The strong correlation between LAN and urbanization may also suggest its correlation with cancer screening behaviors, and, subsequently, stage of disease at diagnosis. However, we did not see consistent evidence of a stronger relationship between LAN and stage of disease. We cannot exclude the possibility of residual confounding in our analyses due to factors such as lifestyle, work schedules, and access to health care. Moreover, outdoor LAN estimated from satellite imagery may not accurately reflect LAN exposures at the individual level. Future studies incorporating personal-level measures of light exposure may provide additional support for the association between LAN and breast cancer risk and help disentangle observed differences between groups.

Acknowledgments

This work was supported by the Intramural Research Program of the National Cancer Institute (G.L.G. and R.R.J.) as well as extramural funding (R00 CA201542 from the National Cancer Institute, P.J.; 80NSSC21K0510 from the National Aeronautics and Space Administration Health and Air Quality Applied Science Team, Q.X. and C.B.).

References

(1.) Acheampong T, Kehm RD, Terry MB, Argov EL, Tehranifar P. 2020. Incidence trends of breast cancer molecular subtypes by age and race/ethnicity in the US from 2010 to 2016. JAMA Netw Open 3(8):e2013226, PMID: 32804214, https://doi.org/10.1001/jamanetworkopen.2020.13226.

(2.) Ball LJ, Palesh O, Kriegsfeld LJ. 2016. The pathophysiologic role of disrupted circadian and neuroendocrine rhythms in breast carcinogenesis. Endocr Rev 37(5):450-466, PMID: 27712099, https://doi.org/10.1210/er.2015-1133.

(3.) Hill SM, Belancio VP, Dauchy RT, Xiang S, Brimer S, Mao L, et al. 2015. Melatonin: an inhibitor of breast cancer. Endocr Relat Cancer 22(3):R183-R204, PMID: 25876649, https://doi.org/10.1530/ER-C-15-0030.

(4.) Hurley S, Goldberg D, Nelson D, Hertz A, Horn-Ross PL, Bernstein L, et al. 2014. Light at night and breast cancer risk among California teachers. Epidemiology 25(5):697-706, PMID: 25061924, https://doi.org/10.1097/EDE.0000000000000137.

(5.) James P, Bertrand KA, Hart JE, Schernhammer ES, Tamimi RM, Laden F. 2017. Outdoor light at night and breast cancer incidence in the Nurses' Health Study II. Environ Health Perspect 125(8):087010, PMID: 28886600, https://doi.org/10.1289/EHP935.

(6.) Xiao Q, James P, Breheny P, Jia P, Park Y, Zhang D, et al. 2020. Outdoor light at night and postmenopausal breast cancer risk in the NIH-AARP diet and health study. Int J Cancer 147(9):2363-2372, PMID: 32488897, https://doi.org/10.1002/ijc.33016.

(7.) Signorello LB, Hargreaves MK, Steinwandel MD, Zheng W, Cai Q, Schlundt DG, et al. 2005. Southern Community Cohort Study: establishing a cohort to investigate health disparities. J Natl Med Assoc 97(7):972-979, PMID: 16080667.

(8.) Cohen SS, Sonderman JS, Mumma MT, Signorello LB, Blot WJ. 2011. Individual and neighborhood-level socioeconomic characteristics in relation to smoking prevalence among black and white adults in the southeastern United States: a cross-sectional study. BMC Public Health 11:877, PMID: 22103960, https://doi.org/10.1186/1471-2458-11-877.

(9.) Hsu F-C, Baugh KE, Ghosh T, Zhizhin M, Elvidge CD. 2015. DMSP-OLS radiance calibrated nighttime lights time series with intercalibration. Remote Sens (Basel) 7(2):1855-1876, https://doi.org/10.3390/rs70201855.

(10.) Grandner MA, Patel NP, Gehrman PR, Xie D, Sha D, Weaver T, et al. 2010. Who gets the best sleep? Ethnic and socioeconomic factors related to sleep complaints. Sleep Med 11(5):470-478, PMID: 20388566, https://doi.org/10.1016/j.sleep.2009.10.006.

Qian Xiao, [1] Gretchen L. Gierach, [2] Cici Bauer, [3] William J. Blot, [4] Peter James, [5,6] and Rena R. Jones [7]

[1] Department of Epidemiology, Human Genetics and Environmental Health, School of Public Health, University of Texas Health Science Center at Houston, Houston, Texas, USA

[2] Integrative Tumor Epidemiology Branch, Division of Cancer Epidemiology and Genetics, National Cancer Institute, Rockville, Maryland, USA

[3] Department of Biostatistics and Data Science, University of Texas Health Science Center at Houston, Houston, Texas, USA

[4] Division of Epidemiology, Department of Medicine, Vanderbilt University Medical Center, Nashville, Tennessee, USA

[5] department of Population Medicine, Harvard Medical School and Harvard Pilgrim Health Care Institute, Boston, Massachusetts, USA

[6] Department of Environmental Health, Harvard T.H. Chan School of Public Health, Boston, Massachusetts, USA

[7] Occupational and Environmental Epidemiology Branch, Division of Cancer Epidemiology and Genetics, National CancerInstitute, National Institutes of Health, Rockville, Maryland, USA https://doi.org/10.1289/EHP9381

https://doi.org/10.1289/EHP9381

Address correspondence to Qian Xiao, Department of Epidemiology, Human Genetics and Environmental Sciences, School of Public Health, University of Texas Health Science Center at Houston, Houston, TX 77225 USA. Telephone: (713) 500-9233. Email: qian.xiao@uth.tmc.edu The authors declare they have no actual or potential competing financial interests.

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Table 1. Associations [HR (95% CI)] between LAN and incidence of
overall, [ER.sup.+] and [ER.sup.-] breast cancer in the Southern
Community Cohort Study (2002-2017).
                                            LAN in 2004
                                     Q1                     Q2
LAN, 10nW/[cm.sup.2] per       1.2 (0.8, 1.7)         6.2 (3.8, 9.1)
  steradian [median
  (IQR)]
All women
  Person-years                     97,909                 98,772
Overall breast cancer
  Cases (n)                         233                    230
  Base model                        Ref             1.00 (0.83, 1.20)
  Full model                        Ref             0.98 (0.82, 1.18)
[ER.sup.+] breast cancer
  Cases (n)                         145                    122
  Base model                        Ref             0.85 (0.67, 1.08)
  Full model                        Ref             0.82 (0.64, 1.05)
[ER.sup.-] breast cancer
  Cases (n)                          44                     52
  Base model                        Ref             1.18 (0.79, 1.76)
  Full model                        Ref             1.15 (0.77, 1.72)
Black
  Person-years                     57,224                 61,130
Overall breast cancer
  Cases (n)                         133                    130
  Base model                        Ref             0.92 (0.72, 1.17)
  Full model                        Ref             0.90 (0.71, 1.15)
[ER.sup.+] breast cancer
  Cases (n)                          85                     69
  Base model                        Ref             0.77 (0.56, 1.06)
  Full model                        Ref             0.74 (0.54, 1.02)
[ER.sup.-] breast cancer
  Cases (n)                          26                     38
  Base model                        Ref              1.36(0.82, 2.23)
  Full model                        Ref              1.36(0.82, 2.24)
White
  Person-years                     40,685                 36,641
Overall breast cancer
  Cases (n)                         100                    100
  Base model                        Ref             1.11 (0.84, 1.47)
  Full model                        Ref              1.09 (1.09,0.82)
[ER.sup.+] breast cancer
  Cases (n)                          60                     53
  Base model                        Ref             0.98 (0.68, 1.42)
  Full model                        Ref             0.95 (0.65, 1.39)
[ER.sup.-] breast cancer
  Cases (n)                          18                     14
  Base model                        Ref             0.86 (0.43, 1.74)
  Full model                        Ref             0.84 (0.41, 1.72)
                                            LAN in 2004
                                     Q3                     Q4
LAN, 10nW/[cm.sup.2] per     20.3 (16.3, 24.3)      35.9 (32.3, 39.5)
  steradian [median
  (IQR)]
All women
  Person-years                     96,743                 98,964
Overall breast cancer
  Cases (n)                         258                    229
  Base model                 1.15 (0.96, 1.37)      1.03 (0.86, 1.23)
  Full model                 1.13 (0.93, 1.36)      1.01 (0.82, 1.25)
[ER.sup.+] breast cancer
  Cases (n)                         157                    140
  Base model                 1.13 (0.90, 1.42)      1.02 (0.81, 1.29)
  Full model                  1.10(0.86, 1.40)      1.02 (0.77, 1.34)
[ER.sup.-] breast cancer
  Cases (n)                          58                     59
  Base model                 1.34 (0.91, 1.99)      1.34 (0.91, 1.99)
  Full model                 1.18 (0.78, 1.79)      1.09 (0.70, 1.69)
Black
  Person-years                     69,009                 81,085
Overall breast cancer
  Cases (n)                         195                    188
  Base model                  1.24(1.00, 1.55)       1.04(0.84, 1.30)
  Full model                 1.21 (0.95, 1.53)       1.02 (079, 1.31)
[ER.sup.+] breast cancer
  Cases (n)                         117                    110
  Base model                 1.18 (0.89, 1.56)      0.97 (0.73, 1.29)
  Full model                  1.14(0.85, 1.54)      0.96 (0.70, 1.34)
[ER.sup.-] breast cancer
  Cases (n)                          51                     54
  Base model                 1.64 (1.02, 2.62)       1.49 (0.93,2.37)
  Full model                 1.53 (0.94, 2.50)      1.35 (0.82, 2.25)
White
  Person-years                     27,734                 17,878
Overall breast cancer
  Cases (n)                          63                     41
  Base model                 0.94 (0.68, 1.28)      0.96 (0.67, 1.39)
  Full model                 0.94 (0.67, 1.34)      1.02 (0.66, 1.57)
[ER.sup.+] breast cancer
  Cases (n)                          40                     30
  Base model                 0.99 (0.67, 1.48)      1.18 (0.76, 1.83)
  Full model                 0.94 (0.61, 1.47)      1.06 (0.62, 1.80)
[ER.sup.-] breast cancer
  Cases (n)                          7                      5
  Base model                 0.57 (0.24, 1.37)      0.64 (0.24, 1.72)
  Full model                 0.57 (0.22, 1.49)       0.67 (0.21,2.21)
                                            LAN in 2004
                                     Q5               [p.sub.trend]
LAN, 10nW/[cm.sup.2] per     55.6 (48.9, 68.2)              --
  steradian [median
  (IQR)]
All women
  Person-years                     98,225                   --
Overall breast cancer
  Cases (n)                         274                     --
  Base model                  1.26(1.05, 1.50)             0.01
  Full model                 1.27 (1.00, 1.60)             0.05
[ER.sup.+] breast cancer
  Cases (n)                         175                     --
  Base model                 1.31 (1.05, 1.63)            0.002
  Full model                 1.37 (1.02, 1.84)             0.01
[ER.sup.-] breast cancer
  Cases (n)                          67                     --
  Base model                  1.54(1.05,2.26)              0.03
  Full model                 1.23 (0.77, 1.98)             0.58
Black
  Person-years                     82,379                   --
Overall breast cancer
  Cases (n)                         233                     --
  Base model                 1.29 (1.04, 1.59)             0.01
  Full model                 1.28 (0.98, 1.68)             0.05
[ER.sup.+] breast cancer
  Cases (n)                         146                     --
  Base model                 1.28 (0.98, 1.68)             0.01
  Full model                 1.33 (0.94, 1.88)             0.02
[ER.sup.-] breast cancer
  Cases (n)                          62                     --
  Base model                 1.68 (1.06, 2.67)             0.06
  Full model                  1.52 (0.89,2.61)             0.33
White
  Person-years                     15,846                   --
Overall breast cancer
  Cases (n)                          41                     --
  Base model                  1.12(0.78, 1.62)             0.84
  Full model                  1.31 (0.79,2.18)             0.51
[ER.sup.+] breast cancer
  Cases (n)                          29                     --
  Base model                  1.33 (0.85,2.08)             0.15
  Full model                  1.33 (0.71,2.49)             0.16
[ER.sup.-] breast cancer
  Cases (n)                          5                      --
  Base model                 0.73 (0.27, 1.97)             0.34
  Full model                  0.88 (0.21,3.65)             0.71
                                LAN in 2004
                                 Per 10 nW/
                               [cm.sup.2] per
                             steradian increase
LAN, 10nW/[cm.sup.2] per             --
  steradian [median
  (IQR)]
All women
  Person-years                       --
Overall breast cancer
  Cases (n)                          --
  Base model                 1.03 (1.01, 1.05)
  Full model                 1.03 (1.01, 1.06)
[ER.sup.+] breast cancer
  Cases (n)                          --
  Base model                 1.04 (1.01, 1.07)
  Full model                 1.05 (1.01, 1.08)
[ER.sup.-] breast cancer
  Cases (n)                          --
  Base model                 1.06 (1.01, 1.10)
  Full model                  1.04 (0.98, 109)
Black
  Person-years                       --
Overall breast cancer
  Cases (n)                          --
  Base model                 1.03 (1.01, 1.06)
  Full model                 1.04 (1.00, 1.07)
[ER.sup.+] breast cancer
  Cases (n)                          --
  Base model                 1.04 (1.01, 1.07)
  Full model                 1.05 (1.01, 1.09)
[ER.sup.-] breast cancer
  Cases (n)                          --
  Base model                 1.05 (1.01, 1.10)
  Full model                 1.04 (0.99, 1.10)
White
  Person-years                       --
Overall breast cancer
  Cases (n)                          --
  Base model                 1.00 (0.95, 1.06)
  Full model                 1.03 (0.96, 1.11)
[ER.sup.+] breast cancer
  Cases (n)                          --
  Base model                 1.04 (0.98, 1.11)
  Full model                 1.07 (0.98, 1.16)
[ER.sup.-] breast cancer
  Cases (n)                          --
  Base model                 0.96 (0.83, 1.11)
  Full model                 1.04 (0.84, 1.27)
Note: Base model: adjusted for age (continuous). Full model: adjusted
for age (continuous), education (less than high school, high school or
GED, some college or vocational train-ing, college graduate or
higher), marital status (single, married, separated, divorced or
widowed), income (<$15,000, $15,000-< $25,000, $25,000-< $50,000,
[greater than or equal to] $50,000), health insurance coverage (yes,
no, missing), family history of breast or ovarian cancer among first-
degree female relatives (yes, no), mammogram (never, more than 2 y
ago, within 2 y, missing), smoking status (current, former, never),
pack-years (0, >0-[less than or equal to] 5, >5-[less than or equal
to] 15, >15-[less than or equal to] 30, >30, missing), number of live
births (0, 1, [greater than or equal to]2), age at first birth
(nulliparous, <20, 20-< 30, [greater than or equal to] 30, missing),
age at menarche ([less than or equal to] 12, >12 years of age),
postmenopausal status (yes, no), ever use of menopausal hormone
therapy (yes, no), average number of alcoholic drinks consumed per day
(0, >0-1, >1), and population density and percentage of households
living under the 2000 federal poverty line in the census tract (both
continuous). For variables with >2% missing values (health insurance
coverage, mammogram, pack-years, and age at first birth), participants
with missing values were coded as a separate category. Otherwise,
participants with missing values were grouped with the largest
category (categorical variables) or coded using the median (continuous
variables). --, not applicable; CI, confidence interval; ER, estrogen
receptor; GED, General Educational Development; HR, hazard ratio; IQR,
interquartile range; LAN, light at night; Q, quartile; Ref, reference.
Table 2. Associations (HR (95% CI) between LAN and incidence of breast
cancer according to tumor stage in the Southern Community Cohort Study
(2002-2017).
                            LAN in 2004
                          Q1              Q2
Black
  Localized
    Cases (n)             62              65
    HR (95% CI) (a)       Ref     0.95 (0.67, 1.34)
  Regional/distant
    Cases (n)             65              58
    HR (95% CI) (a)       Ref      083 (0.58, 1.19)
  White
    Localized
      Cases (n)           61              61
      HR (95% CI) (a)     Ref     1.06 (0.73, 1.52)
  Regional/distant
    Cases (n)             37              37
    HR (95% CI) (a)       Ref      1.14(0.71, 1.82)
                                           LAN in 2004
                                  Q3                     Q4
Black
  Localized
    Cases (n)                    105                     99
    HR (95% CI) (a)       1.35 (0.97, 1.89)      1.15 (0.80, 1.65)
  Regional/distant
    Cases (n)                     79                     81
    HR (95% CI) (a)       0.99 (0.69, 1.40)      0.84 (0.58, 1.22)
  White
    Localized
      Cases (n)                   38                     27
      HR (95% CI) (a)     0.85 (0.54, 1.33)      0.95 (0.55, 1.63)
  Regional/distant
    Cases (n)                     23                     13
    HR (95% CI) (a)       1.13 (0.64, 2.01)      1.20 (0.57, 2.53)
                                     LAN in 2004
                                  Q5               [p.sub.trend]
Black
  Localized
    Cases (n)                    119                     --
    HR (95% CI) (a)       1.45 (0.99, 2.14)             0.05
  Regional/distant
    Cases (n)                    103                     --
    HR (95% CI) (a)       1.03 (0.69, 1.53)             0.67
  White
    Localized
      Cases (n)                   22                     --
      HR (95% CI) (a)     0.93 (0.48, 1.81)             0.70
  Regional/distant
    Cases (n)                     17                     --
    HR (95% CI) (a)        2.42(1.07,5.45)              0.08
                            LAN in 2004
                              Per 10nW/
                            [cm.sup.2]per
                          steradian increase
Black
  Localized
    Cases (n)                     --
    HR (95% CI) (a)       1.04 (1.00, 1.08)
  Regional/distant
    Cases (n)                     --
    HR (95% CI) (a)       1.03 (0.98, 1.07)
  White
    Localized
      Cases (n)                   --
      HR (95% CI) (a)     0.99 (0.89, 1.09)
  Regional/distant
    Cases (n)                     --
    HR (95% CI) (a)        1.10(0.99, 1.23)
Note: --, not applicable; CI, confidence intervals; GED, General
Educational Development; HR, hazard ratio; LAN, light at night; Q,
quartile; Ref, reference.
(a) Adjusted for age (continuous), education (less than high school,
high school or GED, some college or vocational training, college
graduate or higher), marital status (single, married, separated,
divorced or widowed), income (<$15,000, $15,000-< $25,000, $25,000-<
$50,000, [greater than or equal to] $50,000), health insurance
coverage (yes, no, missing), family history of breast or ovarian
cancer among first-degree female relatives (yes, no), mammogram
(never, more than 2 y ago, within 2 y, missing), smoking status
(current, former, never), pack-years (0, >0-[less than or equal to]5,
>5-[less than or equal to] 15, >15-[less than or equal to] 30, >30,
missing), number of live births (0, 1, [greater than or equal to]2),
age at first birth (nulliparous, <20, 20-<30, [greater than or equal
to]30, missing), age at menarche ([less than or equal to]12, >12years
of age), postmenopausal status (yes, no), ever use of menopausal
hormone therapy (yes, no), average number of alcoholic drinks consumed
per day (0, >0-1, >1), and population density and percentage of
households living under the 2000 federal poverty line in the census
tract (both continuous). For variables with >2% missing values (health
insurance coverage, mammo-gram, pack-years, and age at first birth),
participants with missing values were coded as a separate category.
Otherwise, participants with missing values were grouped with the
largest category (categorical variables) or coded using the median
(continuous variables). [p.sub.interaction] = 0.28 for Blacks and 0.37
for Whites.
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Title Annotation:Research Letter
Author:Xiao, Qian; Gierach, Gretchen L.; Bauer, Cici; Blot, William J.; James, Peter; Jones, Rena R.
Publication:Environmental Health Perspectives
Article Type:Report
Geographic Code:1USA
Date:Aug 1, 2021
Words:3077
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