IJC International Journal of Cancer

Night shift work, chronotype and prostate cancer risk in the MCC-Spain case-control study ~o-Vinyals1,2,3,4, Ana Espinosa1,2,3,4, Nuria Aragone s4,5,6, Kyriaki Papantoniou1,2,3,4, Gemma Castan 4,5,6 4,7,8,9 4,10,11 4,10,11 rez-Go mez s G o mez-Acebo 4,12, Beatriz Pe , Javier Burgos , Ine , Javier Llorca , Rosana Peiro 4,13 4,14,15 4,16 4,5,6 n , Francisco Arredondo n , Marina Pollan Jose Juan Jimenez-Moleo , Adonina Tardo and Manolis Kogevinas1,2,3,4,17 1

Centre for Research in Environmental Epidemiology (CREAL), Barcelona, Spain Bioanalysis Research Group, IMIM (Hospital Del Mar Medical Research Institute), Barcelona, Spain 3 Universitat Pompeu Fabra (UPF), Barcelona, Spain 4 blica (CIBERESP), Madrid, Spain CIBER Epidemiologıa Y Salud Pu 5 Environmental and Cancer Epidemiology Area, National Center of Epidemiology, Carlos III Health Institute, Madrid, Spain 6 Cancer Epidemiology Research Group, Oncology and Hematology Area, IIS Puerta De Hierro, Madrid, Spain 7 n Y Cajal, Madrid, Spain Servicio De Urologıa, Hospital Ramo 8 n Y Cajal De Investigacio n Sanitaria (IRYCIS), Madrid, Spain Instituto Ramo 9 Universidad De Alcala De Henares, Madrid, Spain 10 University of Cantabria, Santander, Spain 11 IDIVAL, Santander, Spain 12 n Para El Fomento De La Investigacio n Sanitaria Y Biomedica De La Comunidad Valenciana (FISABIO), Valencia, Spain Fundacio 13 n Biosanitaria Ibs.GRANADA, Hospitales Universitarios De Granada/UniverDepartment of Preventive Medicine and Public Health, Instituto De Investigacio sidad De Granada, Granada, Spain 14 Hospital Infanta Elena, Huelva, Spain 15 n En Salud Y Medio Ambiente (CYSMA), Universidad De Huelva, Spain Centro De Investigacio 16 IUOPA, Universidad De Oviedo, Asturias, Spain 17 National School of Public Health, Athens, Greece

Night shift work has been classified as a probable human carcinogen based on experimental studies and limited human evidence on breast cancer. Evidence on other common cancers, such as prostate cancer, is scarce. Chronotype is an individual characteristic that may relate to night work adaptation. We evaluated night shift work with relation to prostate cancer, taking into account chronotype and disease severity in a population based case-control study in Spain. We included 1,095 prostate cancer cases and 1,388 randomly selected population controls. We collected detailed information on shift schedules (permanent vs. rotating, time schedules, duration, frequency), using lifetime occupational history. Sociodemographic and lifestyle factors were assessed by face-to-face interviews and chronotype through a validated questionnaire. We used unconditional logistic regression analysis adjusting for potential confounders. Subjects who had worked at least for one year in night shift work had a slightly higher prostate cancer risk [Odds Ratio (OR) 1.14; 95%CI 0.94, 1.37] compared with never night workers; this risk increased with longer duration of exposure (28 years: OR 1.37; 95%CI 1.05, 1.81; p-trend 5 0.047). Risks were more pronounced for high risk tumors [D’Amico classification, Relative Risk Ratio (RRR) 1.40; 95%CI 1.05, 1.86], particularly among subjects with longer duration of exposure (28 years: RRR 1.63; 95%CI 1.08, 2.45; p-trend 5 0.027). Overall risk was higher among subjects with an evening chronotype, but also increased in morning chronotypes after long-term night work. In this large population based study, we found an association between night shift work and prostate cancer particularly for tumors with worse prognosis.

Key words: night shift work, chronotype, prostate cancer, prognosis, survival Additional Supporting Information may be found in the online version of this article. Grant sponsor: “Accion Transversal del Cancer,” Spanish Ministry Council; Grant sponsor: Instituto de Salud Carlos III-FEDER; Grant numbers: PI08/1770, PS09/00773, PS09/01286, PS09/01903, PS09/02078, PS09/01662, AP_061/10, PI11/01889 and PI12/01270; Grant sponsor: predoctoral grant PFIS; Grant number: FI09/00385 DOI: 10.1002/ijc.29400 History: Received 8 Aug 2014; Accepted 2 Dec 2014; Online 20 Dec 2014 Correspondence to: Manolis Kogevinas, Centre for Research in Environmental Epidemiology (CREAL), Barcelona, Doctor Aiguader, 88 08003 Barcelona, Spain, E-mail: [email protected]

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Epidemiology

What’s new? Up to 20% of workers do night-shift work, which may increase the risk of some cancers. In this study, the authors found that long-term night-shift work was associated with an increased risk of prostate cancer and decreased survival. Overall risk was higher among workers with an evening chronotype (i.e., a preference for working in the evening vs. in the morning), but risk also increased for morning chronotypes if the duration of night-shift work increased. These results may improve our understanding of prostate cancer etiology and potential prevention strategies.

Prostate cancer is the most common cancer in males with an increasing incidence worldwide.1,2 The etiology of this tumor remains largely unknown and the only well-known risk factors include age, race and family history of prostate cancer.3 Hereditary factors are important and numerous genes associated with prostate cancer have been identified.4 Physical inactivity, smoking, sleep deprivation, vitamin D deficiency due to low sun exposure and diet related factors, such as high meat and alcohol and low vegetable consumption are possible risk factors for prostate cancer, for which evidence is still inconclusive.3 Androgens also play a key role in the prostate cell’s growth, function and proliferation. Lifetime exposure to increased androgen levels may increase risk for prostate cancer and antiandrogenic therapies are commonly used against prostate cancer.5 A potential effect of circadian disruption on prostate cancer incidence has been recently suggested (evidence reviewed in Sigurdardottir et al. 2012).6 Night shift work, the main cause of circadian disruption, is one of the most widespread occupational exposures in the industrialized part of the world, with about 15–20% of total active population working partly or entirely during the night. Night shift work has been classified by the International Agency for Research on Cancer (IARC) as a probable carcinogen (group 2A) for humans.7 Most epidemiological studies have focused on female breast cancer8 and evidence on other tumor sites is scarce. An increased prostate cancer risk has been observed among night workers in a few studies, however some reports were based on small number of cases or limited information on shift work.9–12 A consensus report stressed the need for a more refined exposure assessment to capture aspects of shift work schedules (permanent vs. rotating shifts, number of night shifts, years of night work) that might be more relevant for cancer risk and preventive actions.13 Night shift work and subsequent exposure to light at night disrupts human biologic rhythms resulting in circadian disruption, melatonin suppression, sleep deprivation and circadian gene deregulation, possibly involved in prostate cancer related pathways.14,15 A small number of circadian genes are responsible for maintaining the 24-hr circadian rhythms but also control about 10% of the whole genome.16 Chronic disruption of the circadian genes may lead to cell cycle deregulation and could increase DNA damage replication errors and resulting mutations, thus lead to tumor initiation.17 Furthermore some experimental evidence suggests that circadian disruption may as well accelerate tumor development and

growth.18,19 A recent study showed an association between shift work and elevated prostate-specific antigen (PSA) levels,20 a marker of higher prostate cancer risk, but also worse disease prognosis and increased mortality.21 Therefore it is hypothesized that shift work that involves circadian disruption may be associated not only with increased cancer risk but also with decreased survival.22 Chronotype is an individual characteristic that describes the circadian phase and correlates with diurnal preference, the individual preference for morning or evening activity.23,24 It has been suggested that chronotype may modify the risk for cancer since it has been associated to the capacity of night workers to adapt to nonday work schedules.25 A few recent studies have evaluated chronotype in conjunction with night shift work and breast cancer risk,26–28 and no previous study has evaluated this hypothesis for prostate cancer. We examined the association between night shift work and prostate cancer among males enrolled in the MCC-Spain study, a population based case-control study. We assessed circadian disruption in shift workers using detailed exposure metrics taking into account individual chronotype and severity of prostate cancer.

Methods Study population

The MCC-Spain study is a population based multicasecontrol study on frequent tumors in Spain that includes 23 hospitals in 12 regions and assesses 5 types of cancer (breast, colorectal, prostate, stomach and chronic lymphocytic leukemia) using the same series of population controls for all cases. The main aim of this study is to investigate environmental and genetic factors related to the above cancer types in Spain (www.mccspain.org). The MCC-Spain study began in the year 2008 and the recruitment of incident cancer cases and population controls took place until the end of 2013. Prostate cancer cases, aged 27–85, were recruited in 11 hospitals in 7 Spanish regions (Barcelona, Madrid, Cantabria, Valencia, Granada, Huelva and Asturias). All cases had a new histologically confirmed diagnosis of prostate cancer from September 2008 through December 2012 and lived in the catchment area of each hospital for at least 6 months prior to diagnosis. Control subjects were men free of prostate cancer history, living in the same catchment area as cases. Controls were selected randomly from the rosters of General Practitioners at the primary health centers (PHC) involved in the study and were frequency matched to cases by age in 5C 2014 UICC Int. J. Cancer: 00, 00–00 (2015) V

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Data collection

Information was obtained through face-to-face interviews performed by trained personnel. Lifetime occupational history was assessed for all jobs held for more than a year. Detailed questions were used to ascertain information on shift work for each job, including shift work type (permanent vs. rotating), beginning and ending year, time schedules, hours worked per day, job title and workers activity. Information was also collected on other potential risk factors such as age, educational level, family socioeconomic level, race, body mass index (BMI), family history of prostate cancer, smoking status and leisure time physical activity. Food consumption was reported for all cases and controls through a self-administered diet questionnaire, completed by 85% of participants. Participants were contacted again and a phone interview was performed to collect missing information on jobs with rotating night shift work (exact time schedules for each shift, nights performed per month) and assess individual chronotype with the use of the Munich Chronotype Questionnaire (MCTQ).29 In total, 2,104 subjects (1,208 controls and 896 cases) agreed to participate in this follow-up and completed the chronotype questionnaire. Clinical information was collected for most cases (n 5 1,068) from medical records including anatomopathological and clinical stage, PSA levels and Gleason score. We used the D’Amico classification of prostate cancer that classifies patients in groups of low (cT1-cT2a, Gleason score < 7 and PSA < = 10 ng/ml), medium (cT2b, Gleason score 5 7 or PSA > 10 and PSA < = 20 ng/ml) and high (cT2c or PSA > 20 ng/ml or Gleason > 7) risk. We also used Gleason score at diagnosis alone (Gleason score < 7, Gleason score 5 7 and Gleason score > 7) to classify prostate cancer patients. The MCC-Spain Study followed the national and international directives on ethics and data protection [declaration of Helsinki and Spanish law on confidentiality of data (Ley Organica 15/1999 de 13 Diciembre de Proteccion de Datos de caracter personalLOPD)]. All subjects that agreed to participate and fulfilled the eligibility criteria signed an informed consent form. Night shift work assessment

Night shift work was defined as a working schedule that involved working partly or entirely between 00:00 and 06:00 C 2014 UICC Int. J. Cancer: 00, 00–00 (2015) V

hr, at least three times per month. This definition included late evening shifts, overnight shifts and early morning shifts. Information on the type of night shift work was collected and permanent vs. rotating schedules were compared. The rotating shift without nights was a shift schedule that included rotation between the morning and afternoon shifts. The reference group consisted of men who were ever employed but had never performed night shift work for more than a year. Rotating shift workers with no night shifts (55 controls and 35 cases) were included in the reference group. Cumulative duration of night shift work was calculated as the P total number of years worked at night [ jobs(years night work/job)] and cumulative frequency was the total number P of nights worked [ jobs(night shifts/month/job * months worked/job)] over working life. Cumulative duration and frequency of night shift work was assessed using tertiles of exposure among controls that had ever performed night shift work and the same cut-offs were applied in the analysis of permanent and rotating night shift work. Chronotype and other risk factors

Chronotype (MSFcorr) was estimated as the mid-sleep time on free days [MSF 5 (sleep onset on free day 1 sleep duration on free day)/2)], corrected for oversleep on free days compared to working days [MSFcorr 5 MSF – (sleep duration on free day-sleep duration on a working day)/2]. For example, if an individual slept at 00:00 hr and woke up at 08:00 hr both on free and working days, his chronotype (MSFcorr) score would be at 04:00 hr [MSFcorr 5 MSF 5 00:00 1 (8/2 hrs) 5 00:00 14 hrs 5 04:00 hr]. We assessed chronotype using the continuous MSF score expressed in local time, but also categorical variables with seven, five and three categories (morning type: MSF < 04:00 hr, neither type: MSF 5 04:01– 05:00 hr, evening type: MSF > 05:00 hr). Actual sleep duration was assessed and the answers included only integers. Sleep problems (waking up during the night, problems falling asleep, use of sleep medication) were assessed over lifetime for problems that persisted for at least 1 year. Educational status, a proxy for socioeconomic status, reflects the highest grade completed. Daily consumption of meat, vegetable, fruit and total energy intake were calculated in g/day based on the different food items and using food composition tables. Alcohol intake (g ethanol/day) was calculated for both present and past (at 30–40 years of age) consumption. Leisure time physical activity information (type of activity, frequency: days per week and hours per day, duration: age beginning and age ending) was available for all activities held over lifetime. Total and average annual estimations (METS-hr) were performed over lifetime, adulthood and the last 10 years of life. The annual mean of physical activity (METS-hr/week) over the last 10 years was finally used in the models categorizing subjects as inactive: 0 METS-hr/week, slightly active: from 0.0001 to 8 METS-hr/week, moderately active: 8.0001 to 16 METS-hr/week and very active: greater than 16 METS-hr/ week. Family history of prostate cancer was available for all

Epidemiology

year age groups and study area. They were contacted on behalf of their doctor and invited to participate to the study. Subjects incapable to participate in the interview due to communication difficulties or excess impairment of physical ability were excluded. In total, 1,115 cases and 1,562 male controls recruited were eligible for participation and completed the interview. In this analysis, we included 1,095 prostate cancer cases and 1,388 population controls, with shift work information. Response rates varied between centers and were on average 74% among cases (range 47–94%) and 54% (range 30–94%) among controls with valid telephone numbers in the PHC rosters.

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Table 1. Potential prostate cancer risk factors among participants in the MCC-Spain study (numbers may differ due to missing values; SD: standard deviation) Controls (N 5 1388)

Cases (N 5 1095)

Factor

N (%)

N (%)

p values

Age; mean (SD)

66 (0.2)

66 (0.2)

0.492

Barcelona

478 (34.4)

396 (36.2)

Night shift work, chronotype and prostate cancer risk in the MCC-Spain case-control study.

Night shift work has been classified as a probable human carcinogen based on experimental studies and limited human evidence on breast cancer. Evidenc...
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