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Night Shift Work Increases the Risks of Multiple Primary Cancers in Women: A Systematic Review and Meta-analysis of 61 Articles

Xia Yuan, Chenjing Zhu, Manni Wang, Fei Mo, Wei Du and Xuelei Ma
Xia Yuan
State Key Laboratory of Biotherapy and Cancer Center, West China Hospital, West China Medical School, Sichuan University, Chengdu, P.R. China.
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Chenjing Zhu
State Key Laboratory of Biotherapy and Cancer Center, West China Hospital, West China Medical School, Sichuan University, Chengdu, P.R. China.
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Manni Wang
State Key Laboratory of Biotherapy and Cancer Center, West China Hospital, West China Medical School, Sichuan University, Chengdu, P.R. China.
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Fei Mo
State Key Laboratory of Biotherapy and Cancer Center, West China Hospital, West China Medical School, Sichuan University, Chengdu, P.R. China.
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Wei Du
State Key Laboratory of Biotherapy and Cancer Center, West China Hospital, West China Medical School, Sichuan University, Chengdu, P.R. China.
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Xuelei Ma
State Key Laboratory of Biotherapy and Cancer Center, West China Hospital, West China Medical School, Sichuan University, Chengdu, P.R. China.
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  • For correspondence: drmaxuelei@gmail.com
DOI: 10.1158/1055-9965.EPI-17-0221 Published January 2018
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This article has been retracted. Please see:

  • Retraction: Night Shift Work Increases the Risks of Multiple Primary Cancers in Women: A Systematic Review and Meta-analysis of 61 Articles - February 4, 2019

Abstract

A growing number of studies have examined associations between night shift work and the risks of common cancers among women, with varying conclusions. We did a meta-analysis to identify whether long-term night shift work increased the risks of common cancers in women. We enrolled 61 articles involving 114,628 cases and 3,909,152 participants from Europe, North America, Asia, and Australia. Risk estimates were performed with a random-effect model or a fixed-effect model. Subgroup analyses and meta-regression analyses about breast cancer were conducted to explore possible sources of heterogeneity. In addition, we carried out a dose–response analysis to quantitatively estimate the accumulative effect of night shift work on the risk of breast cancer. A positive relationship was revealed between long-term night shift work and the risks of breast [OR = 1.316; 95% confidence interval (CI), 1.196–1.448], digestive system (OR = 1.177; 95% CI, 1.065–1.301), and skin cancer (OR = 1.408; 95% CI, 1.024–1.934). For every 5 years of night shift work, the risk of breast cancer in women was increased by 3.3% (OR = 1.033; 95% CI, 1.012–1.056). Concerning the group of nurses, long-term night shift work presented potential carcinogenic effect in breast cancer (OR = 1.577; 95% CI, 1.235–2.014), digestive system cancer (OR = 1.350; 95% CI, 1.030–1.770), and lung cancer (OR = 1.280; 95% CI, 1.070–1.531). This systematic review confirmed the positive association between night shift work and the risks of several common cancers in women. We identified that cancer risk of women increased with accumulating years of night shift work, which might help establish and implement effective measures to protect female night shifters. Cancer Epidemiol Biomarkers Prev; 27(1); 25–40. ©2018 AACR.

This article is featured in Highlights of This Issue, p. 1

Introduction

In modern society, the fast-growing productivity demands for working across time zones and night shift work is increasingly prevalent in different industries such as food production, entertainment, health care, and transportation (1). Circadian disruption from electric lighting poses huge challenges on public health, including cardiovascular diseases, neuropsychiatric and endocrine system disorders, and even cancers, in particular breast cancer (2–4). Cancer incidence in industrialized regions is noticeably higher than that in developing countries, suggesting that environmental factors of modern society play an role in cancer etiology. In 2007, the International Agency for Research on Cancer (IARC) has identified “shift work that involves circadian disruption” to be probably carcinogenic (Group 2A), based on “limited evidence in humans for the carcinogenicity of shift work that involves night work,” and “sufficient evidence in experimental animals for the carcinogenicity of light during the daily dark period (biological night)” (5). Among night shift workers, female employees account for a large proportion, and the number of women in nursing is always overwhelming more than male. During 2004–2005, night shift workers accounted for 12.4% of the female working population and 17.4% for European countries (6). Long-term night shift work serves as a potential risk factor for the common cancers in female population.

Much of the research has examined that nocturnal melatonin suppression and circadian rhythm disruption caused by night shift work function as carcinogens that increase tumor incidence (5). Melatonin, primarily produced by pineal gland, was reported to play an important role in inhibiting tumor growth through antioxidation, antiangiogenesis, and regulation of immunity (7). Unnatural light at night reduced melatonin release, which contributed to tumor development. However, melatonin suppression had a negative feedback effect on hypothalamic-pituitary-gonadal axis, promoting gonadotropins secretion (8). Previous studies stated that night shift work increased the risk of hormone-dependent cancers including prostate cancer in men, breast cancer and ovarian cancer in women (9). In addition, another mechanism was related to clock genes expression which played an important role in several cellular processes such as DNA repair and cell apoptosis. Circadian rhythm disturbance among shift workers resulted in changes of clock genes expression, ultimately increased cancer susceptibility (10, 11).

Animal models focused on light at night to study the effect of circadian disruption on cancer incidence (12), whereas epidemiological evidence is limited with differing results. A growing number of females are being exposed to night shift work and employments in different working fields vary in exposure status such as frequency and period time. Nursing group are generally exposed to long-term and high-intensity night shift work. The association between night shift work and cancer risk of female nurses was not covered by published reviews. Breast cancer is the most common cancer in women worldwide. Most of previous meta-analyses emphasized, in particular, the association between night shift work and breast cancer and had controversial conclusions (13–17). Some of them concluded that night shift work was significantly associated with higher risk of breast cancer (13, 14, 17) whereas another study provided limited evidence (16) and also one study reported a small nonsignificant effect of long-term night shift work (15). Thus it still remains unknown whether night shift work elevates the risk of common cancers such as breast cancer, ovarian cancer and lung cancer. Here we performed a meta-analysis to demonstrate the effect of night shift work on the risk of common cancers among women. Meanwhile, the group of female nurses was evaluated for the separate risk estimation of multiple common cancers. By systematically integrating a multitude of previous data, we expected to arrive at a convincing conclusion which would help propose health protection programs for long-term female night shift workers.

Materials and Methods

Literature search

We conducted the meta-analysis following the quality standards of a meta-analysis. An extensive systematic literature search updated to October, 2016 was performed. We searched the keywords “night shift” “shift work” “shift-work” “cancer risk” “cancer mortality” in PubMed, Embase, Medline, and Web of Science databases. Only English articles were enrolled, and no other limitations were restricted. Also, we manually searched citing and reference lists to identify other relevant studies.

Inclusion and exclusion criteria

Studies were identified according to inclusion and exclusion criteria. Studies were included if they met the following criteria: (i) cohort study, case–control study, or nested case–control study within cohort study; (ii) study evaluating cancer risk among women that were ≥18 years old and were exposed to night shift work; (iii) study involving OR, RR, HR, or standardized incidence ratio (SIR) with 95% confidence intervals (CIs) or providing sufficient data to calculate the above parameters. Studies were excluded if they met the following criteria: (i) study involving female cancer risks that could not be separated from that of male; (ii) study providing overlapping or insufficient data; (iii) study involving recurrent cancer.

Data extraction

Extracted information from enrolled studies included first author, published year, number of cases and subjects, OR and corresponding 95% CI, study design, quality score, region, type of cancer, range of night shift work, occupation, variables of adjustment, and exposure assessment. We adopted the shortest and longest exposure time for preceding analysis. Data extraction was performed independently by two investigators and a third author resolved the differences by face-to-face discussion.

Quality evaluation

We used the Newcastle-Ottawa Quality Assessment Scale (NOS; ref. 18) for quality evaluation of eligible studies. NOS adopted the star system with a maximum of nine stars scoring from 0 to 9, which was divided into four parts: participant selection, comparability of study group, exposure assessment, outcome evaluation, and scoring <7 indicated a low quality. NOS quality evaluation was conducted by two investigators independently and a third author settled all disagreements.

Statistical analysis

We evaluated the association between night shift work and female cancer risk using statistical software STATA Version 11.0 (StataCorp). ORs with their corresponding 95% CIs were used as effect measure. Statistical heterogeneity was evaluated by Q and I2 statistics. P < 0.10 and I2 > 50% indicated an existence of statistical heterogeneity and a random-effect model was then carried out, otherwise a fixed-effect model was used (19). To explore the possible sources of heterogeneity regarding breast cancer, meta-regression analyses were performed. Moreover, we conducted subgroup analyses stratified by region, study design, occupation, exposure assessment, number of variables, and quality score.

For dose–response meta-analysis, we retrieved studies which involved at least three levels of exposure categories and information of cases, number of total subjects, person-year, years of exposure in each category were extracted. The midpoint of lower and high boundary was used as average time of night shift exposure. The range of highest category was supposed to be the same as the adjacent category if the upper boundary was not provided (20). Two-stage random-effect model was adopted to estimate the overall dose–response trend.

Begg funnel plot was performed to evaluate the publication bias of enrolled studies and P < 0.05 suggested the evidence of publication bias (15). In the Begg funnel plot, the standard error of logarithm (Log) for OR was plotted against its OR, and Log OR was plotted versus standard error of Log OR for each enrolled study (21).

Results

Literature search and selection of studies

The initial search yielded 368 articles, and 98 articles were retrieved after checking titles and abstracts. Then, we reviewed full texts of these articles and 56 were included according to eligibility criteria. Also, 5 relevant studies were identified by manually searching citing and reference lists. Finally, 61 articles (22–82) were eligible for a comprehensive analysis. The selection flowchart is shown in Fig. 1.

Figure 1.
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Figure 1.

Flow chart of eligible studies selection process. An extensive systematic literature search updated to October, 2016 was performed in PubMed, Embase, Medline, and Web of Science databases, yielding 368 articles, and finally 61 articles were included according to eligibility criteria.

Study characteristics

Sixty-one articles were enrolled in the meta-analysis including 26 cohort studies, 24 case–control studies, and 11 nested case–control studies. Several articles investigated whether the carcinogenic effect of night shift was related to breast cancer estrogen-receptor status (ER+ and ER− breast cancer; ref. 38) or menopausal status (premenopausal and postmenopausal; ref. 46) or different years in employment (60). In addition, several articles reported the risks for a number of cancers including breast cancer, cervical cancer, and colon cancer, and so on (57, 61, 62, 71, 77). One study (82) evaluated associations between night shift work and the risk of breast cancer in two cohorts, respectively [Nurses' Health Study (NHS) and Nurses' Health Study II (NHS2)]. Thus, 67 studies from 61 articles comprising 114,628 cases and 3,909,152 participants were analyzed for the association between night shift work and common cancers at 11 sites of women including breast cancer, digestive system cancer, skin cancer, reproductive system cancer, hematologic system cancer, endocrine system cancer, nervous system cancer, urinary system cancer, lung cancer, bone and soft tissue cancer. Most studies reached a standard of high follow-up rate or favorable response rate. Seventeen out of 67 studies were conducted among nurses, and 49 out of 67 studies evaluated the association between night shift work and the risk of breast cancer. Questionnaire, interview, and databases were adopted for exposure assessment, and we extracted the shortest versus longest history of night shift work as exposure indicator. Forty-nine studies were adjusted for >3 confounders and 18 studies for ≤3 confounders. The main characteristics of the included studies were summarized in Table 1.

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Table 1.

Main characteristics of included studies on the relationship between night shift work and the risks of common cancers in female populations

Risk assessment and heterogeneity

We integrated multivariable-adjusted ORs of longest versus shortest exposure duration to identify the correlation between night shift work and the risk of common cancers. Long-term night shift work increased the risk of female cancer (OR = 1.190; 1.122–1.262) and OR forest plots (with 95% CIs) of cancer for long-term night shift female workers were shown in Supplementary Fig. S1. A positive association was observed regarding breast cancer (OR = 1.316; 95% CI, 1.196–1.448), digestive system cancer (OR = 1.177; 95% CI, 1.065–1.301) and skin cancer (OR = 1.408; 95% CI, 1.024–1.934). OR forest plots (with 95% CIs) of breast cancer, reproductive system cancers, digestive system cancers, lung cancer, and skin cancer were shown in Fig. 2. ORs of association between night shift work and the risk of common cancers in women were summarized in Supplementary Table S1. With regard to nurses, the risk of six common cancers were estimated and as a result night shift work was associated with increased risk of breast cancer (OR = 1.577; 95% CI, 1.235–2.014), digestive system cancer (OR = 1.350; 95% CI, 1.030–1.770), and lung cancer (OR = 1.280; 95% CI, 1.070–1.531). ORs of the common cancers in nurses were shown in Supplementary Table S2.

Figure 2.
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Figure 2.

Forest plots of the association between night shift work and the risks of common cancers. I2, measure to quantify the degree of heterogeneity in meta-analyses. The squares and horizontal lines correspond to the study-specific OR and 95% CI. The area of the squares reflects the study-specific weight. The diamond represents the pooled OR and 95% CI.

Significant heterogeneity was observed in the groups of breast cancer (P = 0.000, I2 = 80.4%), skin cancer (P = 0.009, I2 = 64.7%), and uterine cancer (P = 0.042, I2 = 59.6%), and risk estimates were conducted with a random-effect model. No evidence of heterogeneity existed among the other groups.

Subgroup analysis and meta-regression analysis

Subgroup analyses about breast cancer were conducted stratified by geographic location, study design, number of variables, study quality, exposure assessment, and occupation. When stratified by geographical location, Europe (OR = 1.416; 95% CI, 1.246–1.610) and North America (OR = 1.236; 95% CI, 1.048–1.459) shared higher OR estimates, whereas positive correlation did not exist in Asia (OR = 1.236; 95% CI, 0.865–1.767) and Australia (OR = 1.040; 95% CI, 0.852–1.271). When stratified by design, the highest pooled OR estimate was obtained among nested case–control studies (OR = 1.555; 95% CI, 1.115–2.169) and the lowest was among cohort studies (OR = 1.193; 95% CI, 1.030–1.382). In terms of occupation, it was revealed that the strongest OR existed in the nursing group (OR = 1.577; 1.235–2.014). In the analysis stratified by quality score, both groups of high score (OR = 1.273; 95% CI, 1.152–1.407) and low score (OR = 1.434; 95% CI, 1.133–1.814) presented a positive association but the latter tended to have significant heterogeneity (P = 0.000, I2 = 89.7%). As for the number of adjusted confounders, both groups indicated that night shift work was associated with increased risk of breast cancer and significant heterogeneity (P = 0.000, I2 = 89.1%) existed in the group adjusted for ≤3 confounders. When stratified by exposure assessment method, the questionnaire group presented a stronger correlation and lower heterogeneity compared with interview and database group, whereas negative association was observed among studies adopting other assessment methods (OR = 0.906; 95% CI, 0.596–1.378).

Furthermore, meta-regression analysis was carried out to explore the possible heterogeneity sources among stratified factors and none of the variables was considered as a potential source of heterogeneity. The results of subgroup analyses and meta-regression were summarized in Table 2.

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Table 2.

Results of subgroup analyses and meta-regression analyses on the correlation between night shift work and the risk of breast cancer in women

Dose–response meta-analysis

Dose–response meta-analysis was performed among studies that involved at least 3 levels of exposure categories. The number of studies on breast cancer accounted for an overwhelming proportion and sixteen studies were included to quantitatively assess the cumulative effect of exposure to night shift work on breast cancer incidence. As for other types of cancers, the number of relevant literature was not enough for dose–response meta-analysis. For every 5 years of night shift work, the risk of breast cancer in women increased by 3.3% (OR = 1.033; 95% CI, 1.012–1.056) as shown in Fig. 3.

Figure 3.
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Figure 3.

OR of breast cancer in women by years of night shift work based on dose-response meta-analysis. Solid line represents the estimated OR and the dotted lines represent the low limit and upper limit of 95% CIs.

Study quality

The NOS was employed for quality evaluation of eligible studies. Their scores ranged from 5 to 8 and the mean value was 7.1, indicating a favorable overall quality. Among the included studies, 43 articles were considered to be of high quality with scores ≥7 and 8 studies got 5 scores because of lack of complete research records and variables of adjustment.

Publication bias

We performed Begg funnel plot to assess the publication bias of included studies. Potential publication bias was identified (P = 0.006) among all retrieved studies probably due to the variety of involved cancers, whereas no publication bias was observed among studies on breast cancer (P = 0.208; Supplementary Fig. S2).

Discussion

Some people in contemporary society work in a 24-hour mode, disrupting the 8-hour day routine (83). With the productive and economic development, night shift work is strongly required in the fields of industry, commerce, and entertainment. Shift workers suffer from disturbance of circadian rhythm and suppression of nocturnal melatonin. Short-term effects of night shift work were summarized as “jet-lag” syndrome, including sleep disorders, digestive troubles, fatigue, emotional fluctuation, and reduced physical activity. Long-term night shift work was reported to be associated with increased risks of cardiovascular disease, neuropsychiatric disorder, endocrine system disorders, and cancer (84–87). Data from the third EU Survey (2000) showed that 76% employee worked beyond normal working time (88). Up to 21.9% of men and 10.7% of women were exposed to shift work, with 7% population working permanently at night (89). Large numbers of people are being exposed to night shift work, which brings huge detrimental impact on health; it is therefore of much significance to conduct the study to illustrate the relationship between night shift work and the risks of frequently-occurred cancers in women.

Sixty-one studies were enrolled in the meta-analysis including 26 cohort studies, 24 case–control studies, and 11 nested case–control studies with 114,628 cases and 3,909,152 participants from Europe, North America, Asia, and Australia. A positive dose–response relationship was present between night shift work and the risks of breast cancer (OR = 1.316; 95% CI, 1.196–1.448), digestive system cancer (OR = 1.177; 95% CI, 1.065–1.301), and skin cancer (OR = 1.408; 95% CI, 1.024–1.934). Among the group of nurses, long-term night shift work increased the risks of breast cancer (OR = 1.577; 95% CI, 1.235–2.014), digestive system cancer (OR = 1.350; 95% CI, 1.030–1.770), and lung cancer (OR = 1.280; 95% CI, 1.070–1.531). A nonsignificant effect was observed for ovarian cancer (OR = 1.135; 0.970–1.328) and no effect was seen for cervical cancer (OR = 0.980; 95% CI, 0.787–1.221). Night shift work elevated the risk of breast cancer in a dose–response way which was consistent with previous studies (6, 20, 90). For every 5 years of night shift work, the risk of breast cancer in women increased by 3.3% (OR = 1.033; 95% CI, 1.012–1.056).

Night shift work causes an increase in sex hormones, which is speculated to be relevant for hormone-dependent cancers (91). Strong epidemiologic evidence supports the association between night shift work and increased risk of breast cancer, and also there is limited evidence on prostate cancer (92, 93) and endometrial cancer (25). In our analysis, the risks of hormone-sensitive cancers including breast cancer, ovarian cancer, and uterine cancer among night shift workers were shown in Table 2. Night shift work was strongly associated with higher risk of breast cancer in females whereas no effect was observed for ovarian cancer and uterine cancer.

The underlying biological mechanisms of the association between night shift work and increased cancer risks are complex. One of the possible hypotheses is that exposure to light at night accompanying night shift work results in the disruption of circadian rhythm and the reduction of melatonin production (5). Melatonin is characterized with oncostatic effect which works through antioxidation, antiangiogenesis, regulation of immunity, and metabolism (7). Melatonin reduction stimulates the production of pituitary gonadotropins by negative feedback, hence increasing the risk of sensitive cancers such as breast cancer, ovarian cancer, and endometrial cancer (8). Animal experiments have demonstrated that long-term oral melatonin supplement offered a protective effect against breast cancer (94). Several in vitro researches showed that melatonin administration of even biological dose had a significant growth inhibition effect on breast cancer cells (95–98) and other tumor cells (99–103). Sun exposure is sharply decreased among night shift workers, leading to reduced vitamin D level. Some experimental and epidemiological researches supported the inverse correlation between circulating vitamin D and the risk of breast cancer (104, 105) or colorectal cancer (106, 107). However, night shift work was often accompanied with irregular eating habits, which somewhat contributed to digestive system tumors. Results in our study were inconsistent with the above theories that night shift work increased the risk of hormone-sensitive cancers and digestive system cancers.

Q and I2 statistics were used to evaluate heterogeneity. As a result, significant heterogeneity was observed in the groups of breast cancer (P = 0.000, I2 = 80.4%), skin cancer (P = 0.009, I2 = 64.7%), and uterine cancer (P = 0.042, I2 = 59.6%). Random-effect model was adopted in an attempt to eliminate all sources of heterogeneity. Furthermore, subgroup analyses about breast cancer were conducted and less heterogeneity existed among cohort studies, high-score studies and studies adjusted for >3 confounders, suggesting that these studies would provide more reliable evidence. Moreover, we carried out meta-regression analysis and no explanation was found for possible heterogeneity sources from variables due to low statistical power, therefore the results of risk estimates should be interpreted with caution. When stratified by region, positive correlation existed in Europe and North America, but not in Asia and Australia. One possible reason might be that Asian population was less sensitive to nightshift exposure. Another was partly attributed to the difference of sleeping habits, economic development, and medical service across different geographical areas. Short sleep duration, light at night, and airline cabin crew servings involved potential circadian rhythm disturbances just like nightshift; therefore, relevant articles were included in this meta-analysis to reduce selection bias. Flight attendants were simultaneously exposed to cosmic radiation which was a potential cancer-related unmeasurable factor, thus the odds risk might be overestimated. Among nurses, remarkable elevation of cancer risk was observed regarding breast cancer (OR = 1.577; 95% CI, 1.235–2.014), digestive system cancer (OR = 1.350; 95% CI, 1.030–1.770), and lung cancer (OR = 1.280; 95% CI, 1.070–1.531). In the future, large-sample and multiregion researches are needed to update and confirm the association.

The present meta-analysis involved 3,909,152 participants and 114,628 female patients with cancers at 11 sites. To the best of our knowledge, this is the first meta-analysis to comprehensively assess the association between night shift work and the risk of common cancers among female population. Compared with previous meta-analyses, the study has the following merits. First, in the methodological aspect we systematically conducted risk estimates, subgroup analyses, meta-regression analysis, and dose–response meta-analysis. Random effect model was used to eliminate the source of heterogeneity to some extent. In addition, subgroup analyses and meta-regression were performed to explore potential sources of heterogeneity from confounding factors. Second, according to inclusion and exclusion criteria, 61 studies were enrolled in the meta-analysis and the accumulated evidence with enlarged sample size enhanced statistical power to derive a more precise and reliable risk estimation. Beyond that, longest versus shortest duration was taken as exposure indicator and each individual article was involved in the pooled risk estimate, increasing the generalizability of results. Third, the majority of included studies (40 out of 67) were carried out among general population, therefore the estimation of association between night shift work and cancer risk of women could be extended, not limited to some particular working groups. A certain amount of studies (17 out of 67) were based on nursing group which was an important part of female shift workers and a stratified analysis revealed that night shift work increased the risk of breast cancer, lung cancer and digestive system cancer in female nurses. Fourth, cohort study is less susceptible to confounding factors and less affected by recall bias, thus result from cohort study is considered more credible and valuable compared with case–control study. In this meta-analysis, 26 cohort studies with enough follow-up period were included and a positive relationship was found in the cohort group.

Nevertheless, some shortcomings in the study have to be mentioned. First, the period time of night shift across all enrolled studies was not defined uniformly, for example one definition was “working at least three nights per month” (29) and another was “working during the night (23:00–06:00 h)” (28). Included studies used very different definitions of period time regarding night shift and the lack of consistent definition might result in a certain degree of misclassification, consequently leading to a dilution of pooled estimates when doing data synthesis. Second, a significant between-study heterogeneity and publication bias was observed. Significant variability existed in different individual studies regarding study population, geographical location, adjustment confounders, study design and exposure definition, and each of these factors may contribute to heterogeneity. Disappointingly, we failed to find out the possible sources of heterogeneity from a meta-regression due to the low statistical power. Given substantial heterogeneity observed among included studies, the evidence supporting the association might be weakened and additional well-designed researches are needed. Third, case–control study are vulnerable to varying levels of bias, and in general patients in case group tend to recall past exposure history of night shift. Twenty-four case–control studies were included in our analysis which could probably bring about selection and recall bias. Also, unstandardized questionnaires might produce information bias and inadequate control of adjustment factors could lead to either underestimation or exaggeration of the pooled risk. Finally, only a small number of enrolled studies were involved in dose-response meta-analysis, hence limiting the reliability of the result.

In conclusion, this meta-analysis updated previous studies and identified that cancer risk in female population was increased with accumulating years of night shift work. Given the expanding prevalence of shift work worldwide and heavy public burden of cancers, further researches, particularly large-size, high-score cohort studies are of great necessity to confirm the relationship between night shift work and cancer risk. Also, in-depth biological researches should be done to explore the mechanisms by which night shift work affects cancer risk. Knowing how night shift work serves as a risk factor for cancers might help establish and implement effective measures to protect female night shifters. Moreover, it is important that long-term night shift workers accept regular physical examination and cancer screening for potential malignancies, particularly breast cancer.

Disclosure of Potential Conflicts of Interest

No potential conflicts of interest were disclosed.

Footnotes

  • Note: Supplementary data for this article are available at Cancer Epidemiology, Biomarkers & Prevention Online (http://cebp.aacrjournals.org/).

  • Received March 22, 2017.
  • Revision received July 27, 2017.
  • Accepted October 11, 2017.
  • Published first January 8, 2018.
  • Corrected online February 4, 2019.
  • ©2018 American Association for Cancer Research.

References

  1. 1.↵
    1. Matheson A,
    2. O'Brien L,
    3. Reid JA
    . The impact of shiftwork on health: a literature review. J Clin Nurs 2014;23:3309–20.
    OpenUrl
  2. 2.↵
    1. Liu R,
    2. Jacobs DI,
    3. Hansen J,
    4. Fu A,
    5. Stevens RG,
    6. Zhu Y
    . Aberrant methylation of miR - 34b is associated with long-term shiftwork: a potential mechanism for increased breast cancer susceptibility. Cancer Causes Control 2015;26:171–8.
    OpenUrl
  3. 3.↵
    1. Stevens RG,
    2. Zhu Y
    . Electric light, particularly at night, disrupts human circadian rhythmicity: is that a problem? Philos Trans R Soc Lond 2015;370:1667.
    OpenUrl
  4. 4.↵
    1. Stevens RG,
    2. Brainard GC,
    3. Blask DE,
    4. Lockley SW,
    5. Motta ME
    . Breast cancer and circadian disruption from electric lighting in the modern world. CA Cancer J Clin 2014;64:207.
    OpenUrlCrossRefPubMed
  5. 5.↵
    1. Straif K,
    2. Baan R,
    3. Grosse Y,
    4. Secretan B,
    5. Ghissassi FE,
    6. Bouvard V,
    7. et al.
    Carcinogenicity of shift-work, painting, and fire-fighting. Lancet Oncol 2007;8:1065–6.
    OpenUrlCrossRefPubMed
  6. 6.↵
    1. Wang X,
    2. Ji A,
    3. Zhu Y,
    4. Liang Z,
    5. Wu J,
    6. Li S,
    7. et al.
    A meta-analysis including dose-response relationship between night shift work and the risk of colorectal cancer. Oncotarget 2015;6:25046–60.
    OpenUrlCrossRefPubMed
  7. 7.↵
    1. Viswanathan AN,
    2. Schernhammer ES
    . Circulating melatonin and the risk of breast and endometrial cancer in women. Cancer Lett 2009;281:1–7.
    OpenUrlCrossRefPubMed
  8. 8.↵
    1. Davis S,
    2. Mirick DK
    . Circadian disruption, shift work and the risk of cancer: a summary of the evidence and studies in Seattle. Cancer Causes Control 2006;17:539–45.
    OpenUrlCrossRefPubMed
  9. 9.↵
    1. Rao D,
    2. Yu H,
    3. Bai Y,
    4. Zheng X,
    5. Xie L
    . Does night-shift work increase the risk of prostate cancer? A systematic review and meta-analysis. Onco Targets Ther 2015;8:2817–26.
    OpenUrlPubMed
  10. 10.↵
    1. Monsees GM,
    2. Kraft P,
    3. Hankinson SE,
    4. Hunter DJ,
    5. Schernhammer ES
    . Circadian genes and breast cancer susceptibility in rotating shift workers. Int J Cancer 2012;131:2547–52.
    OpenUrlCrossRefPubMed
  11. 11.↵
    1. Zienolddiny S,
    2. Haugen A,
    3. Lie JA,
    4. Kjuus H,
    5. Anmarkrud KH,
    6. Kjaerheim K
    . Analysis of polymorphisms in the circadian-related genes and breast cancer risk in Norwegian nurses working night shifts. Breast Cancer Res 2013;15:R53.
    OpenUrlCrossRefPubMed
  12. 12.↵
    1. Van Dycke KC,
    2. Rodenburg W,
    3. van Oostrom CT,
    4. van Kerkhof LW,
    5. Pennings JL,
    6. Roenneberg T,
    7. et al.
    Chronically alternating light cycles increase breast cancer risk in mice. Curr Biol 2015;25:1932–7.
    OpenUrlPubMed
  13. 13.↵
    1. Jia Y,
    2. Lu Y,
    3. Wu K,
    4. Lin Q,
    5. Shen W,
    6. Zhu M,
    7. et al.
    Does night work increase the risk of breast cancer? A systematic review and meta-analysis of epidemiological studies. Cancer Epidemiol 2013;37:197–206.
    OpenUrl
  14. 14.↵
    1. Ijaz S,
    2. Verbeek J,
    3. Seidler A,
    4. Lindbohm ML,
    5. Ojajärvi A,
    6. Orsini N,
    7. et al.
    Night-shift work and breast cancer—a systematic review and meta-analysis. Scand J Work Environ Health 2013;39:431–47.
    OpenUrlCrossRefPubMed
  15. 15.↵
    1. Kamdar BB,
    2. Tergas AI,
    3. Mateen FJ,
    4. Bhayani NH,
    5. Oh J
    . Night-shift work and risk of breast cancer: a systematic review and meta-analysis. Breast Cancer Res Treat 2013;138:291–301.
    OpenUrlCrossRefPubMed
  16. 16.↵
    1. Kolstad HA
    . Nightshift work and risk of breast cancer and other cancers–a critical review of the epidemiologic evidence. Scand J Work Environ Health 2008;34:5.
    OpenUrlCrossRefPubMed
  17. 17.↵
    1. Megdal SP,
    2. Kroenke CH,
    3. Laden F,
    4. Pukkala E,
    5. Schernhammer ES
    . Night work and breast cancer risk: a systematic review and meta-analysis. Eur J Cancer 2005;41:2023–32.
    OpenUrlCrossRefPubMed
  18. 18.↵
    1. Sun ML,
    2. Shin ES,
    3. Sun HL,
    4. Seo KH,
    5. Yu MJ,
    6. Ji EJ
    . Tools for assessing quality and risk of bias by levels of evidence. J Korean Med Assoc 2011;54:419.
    OpenUrl
  19. 19.↵
    1. Lin X,
    2. Chen W,
    3. Wei F,
    4. Ying M,
    5. Wei W,
    6. Xie X
    . Night-shift work increases morbidity of breast cancer and all-cause mortality: a meta-analysis of 16 prospective cohort studies. Sleep Med 2015;16:1381–7.
    OpenUrlCrossRefPubMed
  20. 20.↵
    1. He C,
    2. Anand ST,
    3. Ebell MH,
    4. Vena JE,
    5. Robb SW
    . Circadian disrupting exposures and breast cancer risk: a meta-analysis. Int Arch Occup Environ Health 2015;88:533–47.
    OpenUrlCrossRefPubMed
  21. 21.↵
    1. Begg CB,
    2. Mazumdar M
    . Operating characteristics of a rank correlation test for publication bias. Biometrics 1994;50:1088.
    OpenUrlCrossRefPubMed
  22. 22.↵
    1. Knutsson A,
    2. Alfredsson L,
    3. Karlsson B,
    4. Akerstedt T,
    5. Fransson EI,
    6. Westerholm P,
    7. et al.
    Breast cancer among shift workers: results of the WOLF longitudinal cohort study. Scand J Work Environ Health 2013;39:170–7.
    OpenUrlCrossRefPubMed
  23. 23.↵
    1. Carter BD,
    2. Diver WR,
    3. Hildebrand JS,
    4. Patel AV,
    5. Gapstur SM
    . Circadian disruption and fatal ovarian cancer. Am J Prev Med 2014;46(3 Suppl 1):S34–41.
    OpenUrlCrossRefPubMed
  24. 24.↵
    1. Poole EM,
    2. Schernhammer ES,
    3. Tworoger SS
    . Rotating night shift work and risk of ovarian cancer. Cancer Epidemiol Biomarkers Prev 2011;20:934–8.
    OpenUrlAbstract/FREE Full Text
  25. 25.↵
    1. Viswanathan AN,
    2. Hankinson SE,
    3. Schernhammer ES
    . Night shift work and the risk of endometrial cancer. Cancer Res 2007;67:10618.
    OpenUrlAbstract/FREE Full Text
  26. 26.↵
    1. Åkerstedt T,
    2. Knutsson A,
    3. Narusyte J,
    4. Svedberg P,
    5. Kecklund G,
    6. Alexanderson K
    . Night work and breast cancer in women: a Swedish cohort study. BMJ Open 2015;5:4.
    OpenUrl
  27. 27.↵
    1. Koppes LLJ,
    2. Geuskens GA,
    3. Pronk A,
    4. Vermeulen RCH,
    5. Vroome EMMD
    . Night work and breast cancer risk in a general population prospective cohort study in The Netherlands. Eur J Epidemiol 2014;29:577–84.
    OpenUrlCrossRefPubMed
  28. 28.↵
    1. Nätti J,
    2. Anttila T,
    3. Oinas T,
    4. Mustosmäki A
    . Night work and mortality: prospective study among Finnish employees over the time span 1984 to 2008. Chronobiol Int 2012;29:601–9.
    OpenUrlPubMed
  29. 29.↵
    1. Schernhammer ES,
    2. Kroenke CH,
    3. Laden F,
    4. Hankinson SE
    . Night work and risk of breast cancer. Epidemiology 2006;17:108–11.
    OpenUrlCrossRefPubMed
  30. 30.↵
    1. Pronk A,
    2. Ji BT,
    3. Shu XO,
    4. Xue S,
    5. Yang G,
    6. Li HL,
    7. et al.
    Night-shift work and breast cancer risk in a cohort of Chinese women. Am J Epidemiol 2010;172:953–9.
    OpenUrl
  31. 31.↵
    1. Schernhammer ES,
    2. Laden F,
    3. Speizer FE,
    4. Willett WC,
    5. Hunter DJ,
    6. Kawachi I,
    7. et al.
    Night-shift work and risk of colorectal cancer in the nurses' health study. Journal of the National Cancer Institute 2003;95:825–8.
    OpenUrl
  32. 32.↵
    1. Tilma VH,
    2. Helene GA,
    3. Marie HA,
    4. Hansen J,
    5. Christiansen P,
    6. Kolstad H
    . Night work and breast cancer risk among women in the public Danish health care sector: a short-term follow up of a large scale population. Occup Environ Med 2014;71(suppl 1):A30–A.
    OpenUrlAbstract/FREE Full Text
  33. 33.↵
    1. Schernhammer ES,
    2. Feskanich D,
    3. Liang G,
    4. Han J
    . Rotating night-shift work and lung cancer risk among female nurses in the United States. Am J Epidemiol 2013;178:1434–41.
    OpenUrlCrossRefPubMed
  34. 34.↵
    1. Gu F,
    2. Han J,
    3. Laden F,
    4. Pan A,
    5. Caporaso NE,
    6. Stampfer MJ,
    7. et al.
    Total and cause-specific mortality of U.S. nurses working rotating night shifts. Am J Prev Med 2015;48:241–52.
    OpenUrlCrossRefPubMed
  35. 35.↵
    1. Ren Z
    . Association of sleep duration, daytime napping, and night shift work with breast cancer risk. Cancer Res 2014;74(19 Suppl):2181.
    OpenUrl
  36. 36.↵
    1. Santi SA,
    2. Meigs ML,
    3. Zhao Y,
    4. Bewick MA,
    5. Lafrenie RM,
    6. Conlon MS
    . A case–control study of breast cancer risk in nurses from Northeastern Ontario, Canada. Cancer Causes Control 2015;26:1421–8.
    OpenUrl
  37. 37.↵
    1. Datta K,
    2. Roy A,
    3. Nanda D,
    4. Das I,
    5. Guha S,
    6. Ghosh D,
    7. et al.
    Association of breast cancer with sleep pattern—a pilot case control study in a Regional Cancer Centre in South Asia. Asian Pac J Cancer Prev 2014;15:8641–5.
    OpenUrl
  38. 38.↵
    1. Lie JAS,
    2. Kjuus H,
    3. Shan Z,
    4. Haugen A,
    5. Kjærheim K
    . Breast cancer among nurses: is the intensity of night work related to hormone receptor status? Am J Epidemiol 2013;178:110–7.
    OpenUrlCrossRefPubMed
  39. 39.↵
    1. Lie JA,
    2. Roessink J,
    3. Kjaerheim K
    . Breast cancer and night work among Norwegian Nurses. Cancer Causes Control 2006;17:39–44.
    OpenUrlCrossRefPubMed
  40. 40.↵
    1. Papantoniou K,
    2. Castaño-Vinyals G,
    3. Espinosa A,
    4. Aragonés N,
    5. Pérez-Gómez B,
    6. Ardanaz E,
    7. et al.
    Breast cancer risk and night shift work in a case–control study in a Spanish population. Eur J Epidemiol 2015;31:1–12.
    OpenUrl
  41. 41.↵
    1. Truong T,
    2. Liquet B,
    3. Menegaux F,
    4. Plancoulaine S,
    5. Laurent-Puig P,
    6. Mulot C,
    7. et al.
    Breast cancer risk, nightwork, and circadian clock gene polymorphisms. Endocr Relat Cancer 2014;21:629–38.
    OpenUrlAbstract/FREE Full Text
  42. 42.↵
    1. Hansen J,
    2. Stevens RG
    . Case–control study of shift-work and breast cancer risk in Danish nurses: impact of shift systems. Eur J Cancer 2012;48:1722–9.
    OpenUrlCrossRefPubMed
  43. 43.↵
    1. Kloog I,
    2. Portnov BA,
    3. Rennert HS,
    4. Haim A
    . Does the modern urbanized sleeping habitat pose a breast cancer risk? Chronobiol Int 2011;28:76–80.
    OpenUrlCrossRefPubMed
  44. 44.↵
    1. Hansen J
    . Increased breast cancer risk among women who work predominantly at night. Epidemiology 2001;12:74–7.
    OpenUrlCrossRefPubMed
  45. 45.↵
    1. Grundy A,
    2. Richardson H,
    3. Burstyn I,
    4. Lohrisch C,
    5. SenGupta SK,
    6. Lai AS,
    7. et al.
    Increased risk of breast cancer associated with long-term shift work in Canada. Occup Environ Med 2013;70:831–8.
    OpenUrlAbstract/FREE Full Text
  46. 46.↵
    1. Li Q,
    2. Zheng T,
    3. Holford TR,
    4. Boyle P,
    5. Zhang Y,
    6. Dai M
    . Light at night and breast cancer risk: results from a population-based case–control study in Connecticut, USA. Cancer Causes Control 2010;21:2281–5.
    OpenUrlCrossRefPubMed
  47. 47.↵
    1. Hansen J,
    2. Lassen CF
    . Nested case-control study of night shift work and breast cancer risk among women in the Danish military. Occup Environ Med 2012;69:551–6.
    OpenUrlAbstract/FREE Full Text
  48. 48.↵
    1. Kwon P,
    2. Lundin J,
    3. Li W,
    4. Ray R,
    5. Littell C,
    6. Li GD
    . Night shift work and lung cancer risk among female textile workers in Shanghai, China. J Occup Environ Hygiene 2015;12.
  49. 49.↵
    1. Davis S,
    2. Mirick DK,
    3. Stevens RG
    . Night shift work, light at night, and risk of breast cancer. J Natl Cancer Inst 2002;94:533–4.
    OpenUrlCrossRef
  50. 50.↵
    1. Rabstein S,
    2. Harth V,
    3. Pesch B,
    4. Pallapies D,
    5. Lotz A,
    6. Justenhoven C,
    7. et al.
    Night work and breast cancer estrogen receptor status–results from the German GENICA study. Scand J Work Environ Health 2013;39:448–55.
    OpenUrl
  51. 51.↵
    1. Menegaux F,
    2. Truong T,
    3. Anger A,
    4. Cordina-Duverger E,
    5. Lamkarkach F,
    6. Arveux P,
    7. et al.
    Night work and breast cancer: a population-based case–control study in France (the CECILE study). Int J Cancer 2013;132:924–31.
    OpenUrlCrossRefPubMed
  52. 52.↵
    1. Bhatti P,
    2. Cushinghaugen KL,
    3. Wicklund KG,
    4. Doherty JA,
    5. Rossing MA
    . Nightshift work and risk of ovarian cancer. Occup Environ Med 2013;70:231–7.
    OpenUrlAbstract/FREE Full Text
  53. 53.↵
    1. Wang P,
    2. Ren FM,
    3. Lin Y,
    4. Su FX,
    5. Jia WH,
    6. Su XF,
    7. et al.
    Night-shift work, sleep duration, daytime napping, and breast cancer risk. Sleep Med 2015;16:462–8.
    OpenUrl
  54. 54.↵
    1. Li W,
    2. Ray RM,
    3. Thomas DB,
    4. Davis S,
    5. Yost M,
    6. Breslow N,
    7. et al.
    Shift work and breast cancer among women textile workers in Shanghai, China. Cancer Causes Control 2014;26:143–50.
    OpenUrl
  55. 55.↵
    1. O'Leary ES,
    2. Schoenfeld ER,
    3. Stevens RG,
    4. Kabat GC,
    5. Henderson K,
    6. Grimson R,
    7. et al.
    Shift work, light at night, and breast cancer on Long Island, New York. Am J Epidemiol 2006;164:358–66.
    OpenUrlCrossRefPubMed
  56. 56.↵
    1. Fritschi L,
    2. Erren TC,
    3. Glass DC,
    4. Girschik J,
    5. Thomson AK,
    6. Saunders C,
    7. et al.
    The association between different night shiftwork factors and breast cancer: a case–control study. Br J Cancer 2013;109:2472–80.
    OpenUrlCrossRefPubMed
  57. 57.↵
    1. Schwartzbaum J,
    2. Ahlbom A,
    3. Feychting M
    . Cohort study of cancer risk among male and female shift workers. Scand J Work Environ Health 2007;33:336–43.
    OpenUrlCrossRefPubMed
  58. 58.↵
    1. Bauer SE,
    2. Wagner SE,
    3. Burch J,
    4. Bayakly R,
    5. Vena JE
    . A case-referent study: light at night and breast cancer risk in Georgia. Int J Health Geographics 2013;12:12–23.
    OpenUrl
  59. 59.↵
    1. Kojo K,
    2. Pukkala E,
    3. Auvinen A
    . Breast cancer risk among Finnish cabin attendants: a nested case-control study. Occup Environ Med 2005;62:488–93.
    OpenUrlAbstract/FREE Full Text
  60. 60.↵
    1. Rafnsson V,
    2. Sulem P,
    3. Tulinius H,
    4. Hrafnkelsson J
    . Breast cancer risk in airline cabin attendants: a nested case-control study in Iceland. Occup Environ Med 2003;60:807–9.
    OpenUrlAbstract/FREE Full Text
  61. 61.↵
    1. Pukkala E,
    2. Helminen M,
    3. Haldorsen T,
    4. Hammar N,
    5. Kojo K,
    6. Linnersjö A,
    7. et al.
    Cancer incidence among Nordic airline cabin crew. Int J Cancer 2012;131:2886–97.
    OpenUrlCrossRefPubMed
  62. 62.↵
    1. Linnersjö A,
    2. Hammar N,
    3. Dammström BG,
    4. Johansson M,
    5. Eliasch H
    . Cancer incidence in airline cabin crew: experience from Sweden. Occup Environ Med 2003;60:810–4.
    OpenUrlAbstract/FREE Full Text
  63. 63.↵
    1. Reynolds P,
    2. Cone J,
    3. Layefsky M,
    4. Goldberg DE,
    5. Hurley S
    . Cancer incidence in California flight attendants (United States). Cancer Causes Control 2002;13:317–24.
    OpenUrlCrossRefPubMed
  64. 64.↵
    1. Mcelroy JA,
    2. Newcomb PA,
    3. Titus-Ernstoff L,
    4. Trentham-Dietz A,
    5. Hampton JM,
    6. Egan KM
    . Duration of sleep and breast cancer risk in a large population-based case–control study. J Sleep Res 2006;15:241–9.
    OpenUrlCrossRefPubMed
  65. 65.↵
    1. Schernhammer E
    . Nighshift work and breast cancer risk: good news, bad news? Occup Environ Med 2014;71Suppl 1:A121–A.
    OpenUrlAbstract/FREE Full Text
  66. 66.↵
    1. Marino JL,
    2. Cushing-Haugen KL,
    3. Wicklund KG,
    4. Rossing MA
    . Night shift work and risk of epithelial ovarian cancer. Am J Epidemiol 2008;167:S9–S.
    OpenUrl
  67. 67.↵
    1. Lie JA,
    2. Kjuus H,
    3. Zienolddiny S,
    4. Haugen A,
    5. Stevens RG,
    6. Kjærheim K
    . Night work and breast cancer risk among Norwegian nurses: assessment by different exposure metrics. Am J Epidemiol 2011;173:1272–9.
    OpenUrlCrossRefPubMed
  68. 68.↵
    1. Lie S,
    2. Kjuus HK,
    3. Zienolddiny S,
    4. Haugen AH,
    5. Kjærheim KK
    . Night work and risk of hormone receptor-defined breast cancer. Cancer 2013;119:285–92.
    OpenUrlCrossRefPubMed
  69. 69.↵
    1. Lahti TA,
    2. Partonen T,
    3. Kyyrönen P,
    4. Kauppinen T,
    5. Pukkala E
    . Night-time work predisposes to non-Hodgkin lymphoma. Int J Cancer 2008;123:2148–51.
    OpenUrlCrossRefPubMed
  70. 70.↵
    1. Girschik J,
    2. Heyworth J,
    3. Fritschi L
    . Self-reported sleep duration, sleep quality, and breast cancer risk in a population-based case-control study. Am J Epidemiol 2013;177:316–27.
    OpenUrlCrossRefPubMed
  71. 71.↵
    1. Tsai RJ,
    2. Luckhaupt SE,
    3. Sweeney MH,
    4. Calvert GM
    . Shift work and cancer screening: Do females who work alternative shifts undergo recommended cancer screening? Am J Ind Med 2014;57:265–75.
    OpenUrl
  72. 72.↵
    1. Chu CH,
    2. Chen CJ,
    3. Hsu GC,
    4. Liu IL,
    5. Christiani DC,
    6. Ku CH
    . 510 Shift work is risk factor for breast cancer among Taiwanese women. EJC Supplements 2010;8:209.
    OpenUrl
  73. 73.↵
    1. Juhua L,
    2. Megan S,
    3. Jean WW,
    4. Yiqing S,
    5. Margolis KL
    . Sleep disturbance and incidence of thyroid cancer in postmenopausal women the Women's Health Initiative. Am J Epidemiol 2013;177:42–9.
    OpenUrlCrossRefPubMed
  74. 74.↵
    1. Verkasalo PK,
    2. Lillberg K,
    3. Stevens RG,
    4. Hublin C,
    5. Partinen M,
    6. Koskenvuo M,
    7. et al.
    Sleep duration and breast cancer: a prospective cohort study. Cancer Res 2005;65:9595–600.
    OpenUrlAbstract/FREE Full Text
  75. 75.↵
    1. Jiao L,
    2. Duan Z,
    3. Sangihaghpeykar H,
    4. Hale L,
    5. White DL,
    6. Elserag HB
    . Sleep duration and incidence of colorectal cancer in postmenopausal women. Br J Cancer 2013;108:213–21.
    OpenUrlCrossRefPubMed
  76. 76.↵
    1. Kakizaki M,
    2. Inoue K,
    3. Kuriyama S,
    4. Sone T,
    5. Matsuda-Ohmori K,
    6. Nakaya N,
    7. et al.
    Sleep duration and the risk of prostate cancer: the Ohsaki Cohort Study. Br J Cancer 2008;99:1502–5.
    OpenUrlCrossRefPubMed
  77. 77.↵
    1. Tynes T,
    2. Hannevik M,
    3. Andersen A,
    4. Vistnes AI,
    5. Haldorsen T
    . Incidence of breast cancer in Norwegian female radio and telegraph operators. Cancer Causes Control 1996;7:197–204.
    OpenUrlCrossRefPubMed
  78. 78.↵
    1. Pesch B,
    2. Brüning T
    . Night work and breast cancer - results from the German GENICA study. Scand J Work Environ Health 2010;36:134–41.
    OpenUrlPubMed
  79. 79.↵
    1. Bai Y,
    2. Li X,
    3. Wang K,
    4. Chen S,
    5. Wang S,
    6. Chen Z,
    7. et al.
    Association of shift-work, daytime napping, and nighttime sleep with cancer incidence and cancer-caused mortality in Dongfeng-tongji cohort study. Ann Med 2016;48:641–51.
    OpenUrl
  80. 80.↵
    1. Cohen JM,
    2. Li YT,
    3. Wu S,
    4. Han J,
    5. Qureshi AA,
    6. Cho E
    . Sleep duration and sleep-disordered breathing and the risk of melanoma among US women and men. Int J Dermatol 2015;54:e492–e5.
    OpenUrlCrossRefPubMed
  81. 81.↵
    1. Travis RC,
    2. Balkwill A,
    3. Fensom GK,
    4. Appleby PN,
    5. Reeves GK,
    6. Wang XS,
    7. et al.
    Night shift work and breast cancer incidence: three prospective studies and meta-analysis of published studies. J Natl Cancer Inst 2016;108:12.
    OpenUrl
  82. 82.↵
    1. Wegrzyn LR,
    2. Tamimi RM,
    3. Rosner BA,
    4. Brown SB,
    5. Stevens RG,
    6. Eliassen AH,
    7. et al.
    O14–3 Rotating night shift work and risk of breast cancer in the nurses' health studies: 24 years of follow-up. Am J Epidemiol 2017;73(Suppl 1):A27.1–A.
    OpenUrl
  83. 83.↵
    1. Costa G,
    2. Haus E,
    3. Stevens R
    . Shift work and cancer - considerations on rationale, mechanisms, and epidemiology. Scand J Work Environ Health 2010;36:163–79.
    OpenUrlCrossRefPubMed
  84. 84.↵
    1. Costa G
    . The problem: shiftwork. Chronobiol Int 1997;14:89–98.
    OpenUrlCrossRefPubMed
  85. 85.↵
    1. Nurminen T
    . Shift work and reproductive health. Scand J Work Environ Health 1998;24Suppl 3:28–34.
    OpenUrlPubMed
  86. 86.↵
    1. Akerstedt T
    . Shift work and disturbed sleep/wakefulness. Sleep Med Rev 2003;53:117–28.
    OpenUrl
  87. 87.↵
    1. Knutsson A
    . Health disorders of shift workers. Occup Med 2003;53:103–8.
    OpenUrlCrossRefPubMed
  88. 88.↵
    1. Costa G,
    2. Akerstedt T,
    3. Nachreiner F,
    4. Baltieri F,
    5. Carvalhais J,
    6. Folkard S,
    7. et al.
    Flexible working hours, health, and well-being in Europe: some considerations from a SALTSA project. Chronobiol Int 2004;21:831–44.
    OpenUrlCrossRefPubMed
  89. 89.↵
    1. Conditions LW
    . Fourth European working conditions survey: European Foundation for the Improvement of Living and Working Conditions; 2007.
  90. 90.↵
    1. Wang F,
    2. Yeung KL,
    3. Chan WC,
    4. Kwok CC,
    5. Leung SL,
    6. Wu C,
    7. et al.
    A meta-analysis on dose-response relationship between night shift work and the risk of breast cancer. Ann Oncol 2013;24:2724–32.
    OpenUrlCrossRefPubMed
  91. 91.↵
    1. Schernhammer ES,
    2. Rosner B,
    3. Willett WC,
    4. Laden F,
    5. Colditz GA,
    6. Hankinson SE
    . Epidemiology of urinary melatonin in women and its relation to other hormones and night work. Cancer Epidemiol Biomarkers Prev 2004;13:936–43.
    OpenUrlAbstract/FREE Full Text
  92. 92.↵
    1. Sigurdardottir LG,
    2. Valdimarsdottir UA,
    3. Fall K,
    4. Rider JR,
    5. Lockley SW,
    6. Schernhammer E,
    7. et al.
    Circadian disruption, sleep loss and prostate cancer risk: a systematic review of epidemiological studies. Cancer Epidemiol Biomarkers Prev 2012;21:1002–11.
    OpenUrlAbstract/FREE Full Text
  93. 93.↵
    1. Papantoniou K,
    2. Castaño-Vinyals G,
    3. Espinosa A,
    4. Aragonés N,
    5. Pérez-Gómez B,
    6. Burgos J,
    7. et al.
    Night shift work, chronotype and prostate cancer risk in the MCC-Spain case-control study. Int J Cancer 2015;137:1147–57.
    OpenUrlCrossRefPubMed
  94. 94.↵
    1. El-Aziz MAA,
    2. Hassan HA,
    3. Mohamed MH,
    4. Meki ARMA,
    5. Abdel-Ghaffar SKH,
    6. Hussein MR
    . The biochemical and morphological alterations following administration of melatonin, retinoic acid and Nigella sativa in mammary carcinoma: an animal model. Int J Exp Pathol 2005;86:383–96.
    OpenUrlCrossRefPubMed
  95. 95.↵
    1. Hill SM,
    2. Blask DE
    . Effects of the pineal hormone melatonin on the proliferation and morphological characteristics of human breast cancer cells (MCF-7) in culture. Cancer Res 1988;48:6121–6.
    OpenUrlAbstract/FREE Full Text
  96. 96.↵
    1. Cos S,
    2. Fernández F,
    3. Sánchez-Barceló EJ
    . Melatonin inhibits dna synthesis in mcf-7 human breast cancer cells in vitro. Life Sci 1996;58:2447–53.
    OpenUrlCrossRefPubMed
  97. 97.↵
    1. Mediavilla MD,
    2. Cos S,
    3. Sánchez-Barceló EJ
    . Melatonin increases p53 and p21WAFl expression in MCF-7 human breast cancer cells in vitro. Life Sci 1999;65:415–20.
    OpenUrlCrossRefPubMed
  98. 98.↵
    1. Cos S,
    2. Mediavilla MD,
    3. Fernández R,
    4. González-Lamuño D,
    5. Sánchez-Barceló EJ
    . Does melatonin induce apoptosis in MCF-7 human breast cancer cells in vitro? J Pineal Res 2002;32:90–6.
    OpenUrlCrossRefPubMed
  99. 99.↵
    1. Ying SW,
    2. Niles LP,
    3. Crocker C
    . Human malignant melanoma cells express high-affinity receptors for melatonin: antiproliferative effects of melatonin and 6-chloromelatonin. Eur J Pharmacol 1993;246:89–96.
    OpenUrlCrossRefPubMed
  100. 100.↵
    1. Sze SF,
    2. Ng TB,
    3. Liu WK
    . Antiproliferative effect of pineal indoles on cultured tumor cell lines. J Pineal Res 1993;14:27–33.
    OpenUrlPubMed
  101. 101.↵
    1. Shiu SYW,
    2. Li L,
    3. Xu JN,
    4. Pang CS,
    5. Wong JTY,
    6. Pang SF
    . Melatonin-induced inhibition of proliferation and G 1/S cell cycle transition delay of human choriocarcinoma JAr cells: possible involvement of MT 2 (MEL(1B)) receptor. J Pineal Res 1999;27:183–92.
    OpenUrlCrossRefPubMed
  102. 102.↵
    1. Petranka J,
    2. Baldwin W,
    3. Biermann J,
    4. Jayadev S,
    5. Barrett JC,
    6. Murphy E
    . The oncostatic action of melatonin in an ovarian carcinoma cell line. J Pineal Res 1999;26:129–36.
    OpenUrlPubMed
  103. 103.↵
    1. Kanishi Y,
    2. Kobayashi Y,
    3. Noda S,
    4. Ishizuka B,
    5. Saito K
    . Differential growth inhibitory effect of melatonin on two endometrial cancer cell lines. J Pineal Res 2000;28:227–33.
    OpenUrlCrossRefPubMed
  104. 104.↵
    1. Welsh J
    . Vitamin D and breast cancer: insights from animal models. Am J Clin Nutr 2004;80(6 Suppl):1721S–4S.
    OpenUrlAbstract/FREE Full Text
  105. 105.↵
    1. Bauer SR,
    2. Hankinson SE,
    3. Bertonejohnson ER,
    4. Ding EL
    . Plasma vitamin D levels, menopause, and risk of breast cancer: dose-response meta-analysis of prospective studies. Medicine 2013;92:123–31.
    OpenUrlCrossRefPubMed
  106. 106.↵
    1. Chandler PD,
    2. Buring JE,
    3. Manson JE,
    4. Giovannucci EL,
    5. Moorthy MV,
    6. Zhang S,
    7. et al.
    Circulating vitamin D levels and risk of colorectal cancer in women. Cancer Prev Res 2015;8:675–82.
    OpenUrl
  107. 107.↵
    1. Ward M,
    2. Berry DJ,
    3. Power C,
    4. Hyppönen E
    . Working patterns and vitamin D status in mid-life: a cross-sectional study of the 1958 British birth cohort. Occup Environ Med 2011;68:902–7.
    OpenUrlAbstract/FREE Full Text
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Cancer Epidemiology Biomarkers & Prevention: 27 (1)
January 2018
Volume 27, Issue 1
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Night Shift Work Increases the Risks of Multiple Primary Cancers in Women: A Systematic Review and Meta-analysis of 61 Articles
Xia Yuan, Chenjing Zhu, Manni Wang, Fei Mo, Wei Du and Xuelei Ma
Cancer Epidemiol Biomarkers Prev January 1 2018 (27) (1) 25-40; DOI: 10.1158/1055-9965.EPI-17-0221

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Night Shift Work Increases the Risks of Multiple Primary Cancers in Women: A Systematic Review and Meta-analysis of 61 Articles
Xia Yuan, Chenjing Zhu, Manni Wang, Fei Mo, Wei Du and Xuelei Ma
Cancer Epidemiol Biomarkers Prev January 1 2018 (27) (1) 25-40; DOI: 10.1158/1055-9965.EPI-17-0221
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