Abstract
Breast cancer is the most common cancer and the second-leading cause of cancer-related death among women. Inconsistent findings for the relationship between melatonin levels, sleep duration, and breast cancer have been reported. We investigated the association of sleep duration at cohort entry and its interaction with body mass index (BMI) with risk of developing breast cancer in the large population-based Multiethnic Cohort study. Among the 74,481 at-risk participants, 5,790 breast cancer cases were identified during the study period. Although we detected no significant association between sleep duration and breast cancer risk, higher risk estimates for short (HR=1.03; 95%CI: 0.97–1.09) and long sleep (HR=1.05; 95%CI: 0.95–1.15) compared to normal sleep (7–8 hours) were found. The patterns for models stratified by age, BMI, ethnicity, and hormone receptor status were similar but did not indicate significant interaction effects. When examining the combined sleep duration and BMI interaction effect, in comparison to the normal BMI-normal sleep group, risk estimates for underweight, overweight, and obesity were similar across categories of sleep duration (≤6, 7–8, ≥9 hours). The underweight-normal sleep group had lower breast cancer incidence (HR=0.66, 95%CI: 0.50–0.86), whereas the overweight-short sleep, overweight-normal sleep group and all obese women experienced elevated breast cancer incidence. The respective HRs for short, normal, and long sleep among obese women were 1.35 (95%CI: 1.20–1.53), 1.27 (95%CI: 1.15–1.42), and 1.46 (95%CI: 1.21–1.76). Future perspectives need to examine the possibility that sleep quality, variations in circadian rhythm, and melatonin are involved in breast cancer etiology.
Keywords: Breast cancer, incidence, sleep, cohort, ethnicity
INTRODUCTION
Breast cancer is the most commonly diagnosed cancer among women in the United States [1]. Estimates from the 2018 NCI’s Surveillance, Epidemiology, and End Results (SEER) predicted that 30% of all new cancer diagnoses and 14% of all cancer deaths in women will be from breast cancer [1]. A previous analysis in the Multiethnic Cohort (MEC) found that compared to whites and Japanese Americans, Native Hawaiians were at higher risk for breast cancer (RR=1.31), while African Americans and Latinas (both United States-born and foreign born) were at lower risk (RR=0.80, 0.74, 0.51) [2]. The National Sleep Foundation recommends 7–9 hours of sleep for adults aged 26 to 64 years and 7–8 hours for adults over 65 years [3]. In agreement with other studies among minority populations [4, 5], a report from the MEC found that Native Hawaiians and African Americans had shorter sleep duration than whites and Japanese Americans [6]. The same study also described a U-shaped relation of sleep duration with all-cause and cardiovascular disease mortality [6]. In women, all-cause mortality was 14% higher and 22% higher among those who reported 5 hours of sleep or less and 9 hours of sleep or more, respectively, compared to those who reported 6–8 hours of sleep [6].
A relation between melatonin levels and sleep behavior with breast cancer risk has been hypothesized, but the findings have been inconsistent [7–12]. Several studies found an association between night-shiftwork and a higher breast cancer risk [13–17]. Current evidence for an association of sleep duration and breast cancer risk is also conflicting. Several studies found an association between sleep duration and breast cancer [18, 19], while others did not [20–24]. A 2014 meta-analysis showed no association between sleep duration and breast cancer [25]. Previous research also suggests that the estrogen (ER) and progesterone (PR) receptor status of tumors may affect this association [24, 26]. A previous analysis within the MEC reported the risk of breast cancer was increased by 11% (HR=1.11; 95% CI: 1.07–1.15) for each 5 kg/m2 increase, which suggests BMI may affect the association between sleep duration and breast cancer [27]. A meta-analysis on prospective studies found that in females, short sleep duration was significantly associated with obesity (OR=1.25; 95% CI: 1.06–1.47), and a non-significant association between long sleep duration and obesity (OR=1.11; 95% CI: 0.87–1.42) [28]. The objective of this study is to examine the relation between self-reported sleep duration and breast cancer incidence, as well as a possible interaction with obesity in a large, ethnically diverse cohort. The underlying hypothesis is that inadequate sleep duration, i.e., more or less than 7–8 hours, is associated with a higher breast cancer risk.
MATERIALS AND METHODS
Study Population
Participants in the Multiethnic Cohort (MEC) include whites, Native Hawaiians, and Japanese Americans recruited in Hawaii and African Americans and Latinos recruited in California, primarily Los Angeles [29]. Details of the recruitment methodology have been previously described [29]. In short, driver’s licenses were used to identify ethnic-specific surnames and first names [29, 30]. The initial survey (offered in English and Spanish) consisted of a self-administered 26-page questionnaire on various demographic, anthropometric, and lifestyle factors including hours of sleep per day [29]. A validated food frequency questionnaire included dietary options that were commonly consumed by the five ethnic groups [31]. In addition to demographic characteristics, height, weight, age, education, smoking status, alcohol, physical activity, smoking, medications, medical conditions, family history, and reproductive history were included. Physical activity was summarized as daily metabolic equivalent tasks (METs), which was computed from the number of hours spent doing sedentary, strenuous, vigorous, and moderate activities.
Baseline data were gathered in 1993–1996 from 215,831 participants who were 45–75 years old. After excluding participants who did not belong to one of the five major ethnic groups, had a previous breast cancer diagnosis, and/or were missing essential covariates, a total of 74,481 female participants were included in the current analysis (Figure 1). The study was approved by the Institutional Review Boards of the University of Hawaii and the University of Southern California.
Figure 1.
Inclusion criteria utilized for final study population to analyze the relationship between sleep duration and breast cancer in the MEC.
Exposure Data
Sleep data at cohort entry were obtained from the question, “On the average, during the last year, how many hours in a day did you sleep (include naps)?” Participants were given response options of: ≤5 hours, 6 hours, 7 hours, 8 hours, 9 hours, or ≥10 hours. For the current analysis, sleep duration was categorized into three categories (≤6, 7–8, and ≥9 hours).
Outcomes
Incident breast cancer cases were identified by the Hawaii Tumor Registry in Hawaii [29], the Los Angeles County Cancer Surveillance Program, and the State of California Cancer Registry in California [29]. All registries are part of the National Cancer Center’s Surveillance, Epidemiology, and End Results (SEER) program. Deaths were verified using regular linkages with vital records in Hawaii and California as well as the National Death Index [29].
Statistical Analysis
Frequency measures and proportions for several baseline characteristics including total follow-up time, ethnic group, education, BMI based on self-reported weight and height were computed by sleep duration. Sample means with standard deviations were estimated for age at breast cancer diagnosis, physical activity, and caffeine intake. T-tests and chi-square tests were used to compare differences across the three sleep duration categories.
Cox proportional hazards regression, with age as the time metric, was applied to calculate hazard ratios [32] and 95% confidence intervals (CI) to examine the association between breast cancer incidence and sleep duration, with 7–8 hours as the reference group. Date of diagnosis was taken as the event time for breast cancer cases. Follow-up time for non-cases ended on the earlier of the date of death or December 31, 2013. The following covariates were included in the models based on their known association with breast cancer risk [2, 27]: BMI, ethnicity, age at cohort entry, education, smoking status, alcohol intake, age at menarche, age at birth of first child, number of children, menopause type, family history of breast cancer, caffeine intake, and total energy intake.
Effect modification was evaluated by assessing the Wald statistic for cross-product interaction terms and by performing analyses stratified by ethnicity, age, BMI, education, and combined ER/PR status [21]. To evaluate the interaction between sleep and BMI, a method suggested by Knol and VanderWeele was used [33]. Combined categories for sleep (≤6, 7–8, and ≥9 hours) and four BMI categories were created and evaluated in Cox regression models women with 7–8 hours of sleep and normal BMI as reference group.
In a sensitivity analysis, we repeated the analyses excluding cases diagnosed in the first two years after cohort entry. HRs with 95% CIs were calculated for each sleep group.
Analyses were also conducted separately for each ethnic group. All analyses were performed using SAS 9.4 (SAS Inc., Cary, NC, USA), and p<0.05 was considered statistically significant.
RESULTS
During a total of 1,304,338 person-years of follow-up, 5,790 (7.8%) incident breast cancer cases were identified in this study population. The mean age at breast cancer diagnosis was 68.4±9.3 years. The ethnic distribution was 26.5% white, 17.7% African American, 7.7% Native Hawaiian, 29.2% Japanese American, and 18.9% Latina. The mean BMI was 26.4±5.8 kg/m2. The proportions of women reporting ≤5, 6, 7, 8, 9, and ≥10 hours of sleep were 9.7%, 24.7%, 32.2%, 24.8, 6.6%, and 2.0%, respectively. More than half of the participants reported 7–8 hours of sleep (57%), while less than 10% were in the long sleep duration group (Table 1). Whites and Latinas were less likely to report short sleep duration while Japanese Americans were less likely to report long sleep hours. Individuals with short sleep were more likely to be highly educated, report higher physical activity, be current smokers, have a family history of breast cancer, and report higher caffeine intake, while women with long sleep duration were more likely to report higher alcohol consumption and higher BMI.
Table 1:
Demographic and breast cancer-related characteristics by sleep duration, MEC, 1993–2013
| Characteristic | All (N) | Hours of Sleep | p1 | ||
|---|---|---|---|---|---|
| ≤6 | 7–8 | ≥9 | |||
| Number of participants | 74481 | 25648 (34.4%) | 42432 (57.0%) | 6401 (8.6%) | |
| Total follow-up time (person-years) | 1304338 | 448283 | 749389 | 106666 | |
| Breast cancer cases | 5790 | 2002 | 3301 | 487 | |
| Breast cancer stage2,3 | |||||
| In Situ | 1166 | 402 (34.5%) | 668 (57.3%) | 96 (8.2%) | |
| Local | 3284 | 1103 (33.6%) | 1922 (58.5%) | 259 (7.9%) | |
| Regional | 1163 | 427 (36.7%) | 619 (53.2%) | 117 (10.1%) | |
| Distant | 128 | 49 (38.3%) | 66 (51.6%) | 13 (10.2%) | |
| Ethnicity2 | <0.0001 | ||||
| White | 19749 | 4652 (23.6%) | 13113 (66.4%) | 1984 (10.1%) | |
| African American | 13188 | 5447 (41.3%) | 6361 (48.2%) | 1380 (10.5%) | |
| Native Hawaiian | 5698 | 2382 (41.8%) | 2782 (48.7%) | 534 (9.4%) | |
| Japanese American | 21766 | 8498 (39.0%) | 12312 (56.6%) | 956 (4.4%) | |
| Latina | 14080 | 4669 (33.2%) | 7863 (55.9%) | 11547 (1.0%) | |
| Education2 | 0.74 | ||||
| <12 years | 31019 | 11190 (36.1%) | 16727 (53.9%) | 3102 (10.0%) | |
| 13–15 years | 23458 | 8020 (23.2%) | 13467 (57.4%) | 1971 (8.4%) | |
| ≥16 years | 20004 | 6438 (32.2%) | 12238 (61.2%) | 1328 (6.6%) | |
| BMI2 | 0.08 | ||||
| Overall4 | 74481 | 26.7 ± 6.0 | 26.0 ± 5.5 | 27.5 ± 6.3 | |
| Underweight | 2077 | 753 (36.2%) | 1170 (56.3%) | 155 (7.5%) | |
| Normal | 33347 | 10905 (32.7%) | 20079 (60.2%) | 2362 (7.1%) | |
| Overweight | 22986 | 8033 (35.0%) | 12872 (56.0%) | 2081 (9.1%) | |
| Obese | 16071 | 5958 (37.1%) | 8311 (51.7%) | 1802 (1.2%) | |
| Alcohol consumption2 | <0.0001 | ||||
| <1/month | 48306 | 17643 (36.5%) | 26601 (55.1%) | 4062 (8.4%) | |
| ≥1/month to <1/day | 19168 | 6171 (32.2%) | 11455 (59.8%) | 1542 (8.0%) | |
| ≥1/day | 7007 | 1834 (26.2%) | 4376 (62.5%) | 797 (11.4%) | |
| Smoking status2 | <0.0001 | ||||
| Never | 41003 | 14409 (33.1%) | 23452 (57.2%) | 3142 (7.7%) | |
| Past | 22609 | 7338 (32.5%) | 13095 (57.9%) | 2176 (9.6%) | |
| Current | 10869 | 3901 (35.9%) | 5885 (54.1%) | 1083 (10.0%) | |
| Family history of breast cancer2 | 8228 | 2842 (34.4%) | 4668 (56.7%) | 718 (8.7%) | 0.76 |
| Age at breast cancer diagnosis (years)4 | 68.4 ± 9.3 | 68.1 ± 9.3 | 68.5 ± 9.2 | 68.4 ± 9.4 | 0.30 |
| Physical activity (METS per day)4 | 1.6 ± 0.3 | 1.7 ± 0.3 | 1.6 ± 0.3 | 1.5 ± 0.3 | <0.0001 |
| Caffeine (mg/day)4 | 171 ± 153 | 169 ± 158 | 172 ± 150 | 168 ± 153 | 0.05 |
p values calculated by analysis of variance and χ2 test
n (%)
49 (0.9%) were missing breast cancer stage data
mean ± SD
The adjusted HRs did not indicate a higher risk of breast cancer in women who reported short (HR=1.03; 95% CI: 0.97–1.09) or long (HR=1.05; 95% CI: 0.95–1.15) sleep duration as compared to 7–8 hours (Table 2) although the latter suggested a borderline elevated risk. When using 7 hours as the reference category, similar associations were found for short HR=1.04; 95% CI: 0.98–1.11) and long (HR=1.06; 95% CI: 0.96–1.17) sleep duration (data not shown). In a minimally-adjusted model (covariates: ethnicity and BMI) with minimal exclusions (n=99597), risk estimates changed by less than 3% for short (HR=0.96; 95% CI: 0.91–1.00) and long (HR=0.99; 95% CI: 0.91–1.07) sleep duration.
Table 2:
Risk of breast cancer associated with self-reported sleep duration, MEC 1993–2013
| Sleep Duration | ||||
|---|---|---|---|---|
| Group | ≤6 hr | 7–8 hr | ≥9 hr | p-interaction2 |
| HR (95%CI)1 | HR (95%CI) | HR (95%CI)1 | ||
| Overall3 | 1.03 (0.97–1.09) | 1.00 | 1.05 (0.95–1.15) | 0.45 |
| Ethnicity3 | 0.61 | |||
| White | 1.04 (0.92–1.18) | 1.00 | 0.93 (0.79–1.23) | |
| African American | 0.95 (0.83–1.09) | 1.00 | 0.99 (0.78–1.22) | |
| Native Hawaiian | 1.03 (0.87–1.23) | 1.00 | 1.01 (0.76–1.36) | |
| Japanese American | 1.04 (0.94–1.14) | 1.00 | 1.16 (0.93–1.43) | |
| Latina | 1.08 (0.93–1.26) | 1.00 | 1.20 (0.97–1.50) | |
| Age (%)3 | 0.64 | |||
| <55 years | 1.08 (0.99–1.19) | 1.00 | 1.10 (0.93–1.29) | |
| 55–64 years | 1.10 (1.00–1.21) | 1.00 | 1.07 (0.91–1.26) | |
| 65+ years | 0.88 (0.79–0.99) | 1.00 | 0.95 (0.80–1.14) | |
| BMI (kg/m2)3 | 0.45 | |||
| Underweight | 1.25 (0.83–1.90) | 1.00 | 1.48 (0.74–2.98) | |
| Normal | 1.06 (0.97–1.15) | 1.00 | 1.06 (0.91–1.24) | |
| Overweight | 1.00 (0.91–1.10) | 1.00 | 0.96 (0.81–1.13) | |
| Obese | 1.04 (0.92–1.17) | 1.00 | 1.15 (0.96–1.38) | |
| ER and PR status4 | 0.23 | |||
| ER+PR+5 | 1.07 (0.99–1.16) | 1.00 | 1.04 (0.91–1.19) | |
| ER−PR−6 | 1.06 (0.90–1.24) | 1.00 | 0.93 (0.70–1.22) | |
| Discordant7 | 1.03 (0.86–1.22) | 1.00 | 1.29 (0.98–1.70) | |
HRs (Hazard Ratios) obtained from Cox regression adjusted for BMI, ethnicity, age, education, family history of breast cancer, smoking status, alcohol use, physical activity, age at menarche, age at first live birth, number of children, hormone treatment, menopausal status, caffeine intake, and total energy intake
p-interaction is based on Wald statistic for cross-product interaction terms
Corresponding number of participants per group are found in Table 1
4426 breast cancer cases who had a specific ER and PR type
Positive ER (estrogen receptor) and PR (progesterone receptor) breast cancer status; based on 3056 participants (≤6 hr=1075; 7–8hr=1734; ≥9hr=247)
Negative ER and PR breast cancer status; based on 738 participants (≤6 hr=262; 7–8hr=419; ≥9hr=75)
Positive ER and negative PR, or negative ER and positive PR breast cancer status; based on 632 participants (≤6 hr=216; 7–8hr=355; ≥9hr=61)
None of the interaction terms with various stratification variables, i.e., ER/PR status, age, or BMI, were statistically significant, but small differences appeared in stratified models. Ethnic-specific analyses indicated that Japanese Americans and Latinas followed a similar pattern of association as the entire population. The same pattern was seen in participants within the underweight, normal, and obese BMI categories and those with ER+/PR+ and discordant ER/PR status. Only among women ≥65 years, those with short sleep duration had a lower breast cancer risk (HR=0.88, 95% CI: 0.79–0.99).
Within women sleeping 7–8 hours, the adjusted HRs for the combination of sleep duration and BMI (Figure 2) for underweight, overweight, and obese women had HRs of 0.66 (95% CI: 0.50–0.86), 1.22 (95% CI: 1.12–1.33), and 1.27 (95% CI: 1.15–1.42) respectively. Compared to women sleeping 7–8 hours with a normal BMI, short sleepers who were overweight had a 21% higher risk of breast cancer (HR=1.21, 95% CI: 1.10–1.34) and those who were obese had a 35% higher risk of breast cancer (HR=1.35, 95% CI: 1.20–1.53). Among long sleepers, those in the obese group had almost 50% higher risk of breast cancer (HR=1.46, 95% CI: 1.21–1.76) compared to normal BMI and normal sleep. The patterns within each sleep category are similar and indicate that BMI is a stronger predictor for breast cancer risk than sleep duration. The comparison across ethnic groups demonstrated a stronger influence of BMI status in Japanese Americans than among whites and weaker associations within the other three ethnic groups. Notably, BMI status predicted breast cancer incidence in Latinas and to a very small degree in African Americans.
Figure 2.
Association of sleep duration and BMI on the risk of breast cancer, by race/ethnicity. Note: HRs were adjusted for ethnicity, age, education, family history of breast cancer, smoking status, alcohol use, physical activity, age at menarche, age at first live birth, number of children, hormone treatment, menopausal status, caffeine intake and total energy intake.
The sensitivity analysis excluded cases diagnosed in the first two years. The HRs for short (HR=1.03, 95% CI: 0.97–1.09) and long (HR=1.04, 95% CI: 0.94–1.15) sleep did not change the results.
DISCUSSION
In this large ethnically diverse population-based cohort study, sleep duration was not significantly associated with breast cancer incidence. None of the stratified analyses detected associations between sleep duration and breast cancer incidence, although the HRs for long sleep were elevated without reaching significance. This pattern was also seen in the underweight, normal, and obese BMI strata, as well as some ER/PR strata. Although ethnic differences were not significant, Japanese Americans and Latinas had a higher risk of breast cancer in the long sleep group. In the combined BMI-sleep analyses, participants with overweight or obesity had a higher risk of breast cancer across all sleep categories.
In other large population-based, predominantly white, prospective cohort studies, similar null results indicating no association between sleep duration and breast cancer were found [20–24, 26, 34]. However, a report from the Ohsaki Cohort in Japan described a higher risk of breast cancer (HR=1.62, 95% CI: 1.05–2.50) [19], which differs from our risk estimate of 1.04 (95% CI=0.94 to 1.14) for Japanese Americans with short sleep duration. The primarily white NIH-AARP Diet and Health Study described a lower risk of breast cancer among short sleepers (HR=0.84, 95% CI: 0.71–0.98), which differed from our risk estimate of 1.04 (95% CI: 0.92–1.18) [35]. A case-control study with Chinese women described higher odds of breast cancer for women with short (OR=1.53, 95% CI: 1.10–2.12) and long sleep (OR=1.59, 95% CI: 1.17–2.17) [18], but the retrospective design may account for the difference in findings. Also, in contrast to our findings, previous studies reported that women with ER+/PR+ tumors had a significantly lower risk of breast cancer when comparing short to normal sleep duration [24].
The current study was based on a large population-based cohort made up of five different ethnic groups with a long follow-up time and sufficient sample sizes for stratified analyses. Breast cancer diagnoses were obtained from high quality cancer registries, which makes misclassification bias very unlikely. As a previous MEC study reported that 88% of females reported having at least one mammography in the past, this cohort has good access to healthcare [36]. Another strength is the collection of sleep duration information prior to breast cancer diagnosis, thereby limiting recall bias. The availability of a wide range of covariates allowed the adjustment for many known risk factors associated with breast cancer. The combined analysis with BMI made it possible to separate possible interactions between sleep duration and obesity, one of the strongest predictors of postmenopausal breast cancer incidence [27, 37].
A limitation to our study is that sleep duration, as well as most other covariates, was self-reported at one point in time, which may not be an accurate reflection of sleep duration over the long follow-up time. A tendency to overestimate sleep onset latency [38] and evidence that sleep duration is a poor estimation for sleep efficiency, sleep latency, slow wave sleep, and time spent in rapid eye movement (REM) sleep [39, 40] are also of concern. Previous research suggests that self-reported sleep duration may be over-reported by 16 to 43 minutes when compared to polysomnography [32, 38–41], one of the available methods to measure sleep duration more objectively in future investigations. We also did not have quantifiable information about other aspects of sleep, such as quality, naps, nightshift work in earlier years before retirement, and melatonin levels [7–17]. Our study was also limited because we did not have information on medications such as sleeping pills and corticosteroids that could have affected the ability to sleep. The number of study subjects in the long sleep category was also quite small, leading to unstable estimates.
Despite the inconsistent reports relating nightshift work and melatonin to breast cancer [8–12], there is increasing evidence that circadian rhythm is related to breast cancer [13–17]. In 2013, a global study on cancer found that breast cancer incidence was lower in developing countries (40 per 100,000) than in industrialized countries (75 per 100,000) [42]. The authors suggested that these findings might be due to circadian disruption from electrical lighting [43].
Our findings provide little support for a role of sleep duration as reported in middle age in breast cancer development after considering BMI and other important predictors of breast cancer incidence. This does not exclude the possibility that sleep quality, variations in circadian rhythm, and melatonin are involved in breast cancer etiology.
ACKNOWLEDGEMENTS
The work within the Multiethnic Cohort was supported by the following grants from the National Institutes of Health: R37CA54281 (L.N. Kolonel), U01CA164973 (L. Le Marchand, L.R. Wilkens, C.A. Haiman). The tumor registries were supported by NCI contracts N01 PC 35137 and N01 PC 35139.
Footnotes
Conflicts of Interest: None
Novelty: This study was conducted on the Multiethnic Cohort (MEC), which is one of the largest ethnically diverse population-based cohort studies, and provides the first results on sleep duration and breast cancer among individuals of white, African American, Japanese American, Native Hawaiian, and Latino origin. Although sleep duration was not significantly associated with breast cancer incidence, we used a novel approach to examine the interaction effect of BMI and sleep duration on breast cancer risk.
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