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Original article
Night shift work and stomach cancer risk in the MCC-Spain study
  1. Georgina Gyarmati1,
  2. Michelle C Turner1,2,3,4,
  3. Gemma Castaño-Vinyals1,2,3,5,
  4. Ana Espinosa1,2,3,5,
  5. Kyriaki Papantoniou1,2,3,5,6,
  6. Juan Alguacil3,7,
  7. Laura Costas8,9,
  8. Beatriz Pérez-Gómez3,10,11,
  9. Vicente Martin Sanchez3,12,
  10. Eva Ardanaz3,13,14,
  11. Victor Moreno3,15,16,
  12. Inés Gómez-Acebo3,17,
  13. Guillermo Fernández-Tardon3,18,
  14. Vicent Villanueva Ballester19,
  15. Rocio Capelo7,
  16. Maria-Dolores Chirlaque3,20,
  17. Miguel Santibáñez17,
  18. Marina Pollán3,10,11,
  19. Nuria Aragonés3,10,11,
  20. Manolis Kogevinas1,2,3,5
  1. 1ISGlobal, Centre for Research in Environmental Epidemiology (CREAL), Barcelona, Spain
  2. 2Universitat Pompeu Fabra (UPF), Barcelona, Spain
  3. 3CIBER Epidemiología y Salud Pública (CIBERESP), Madrid, Spain
  4. 4McLaughlin Centre for Population Health Risk Assessment, University of Ottawa, Ottawa, Canada
  5. 5IMIM (Hospital del Mar Medical Research Institute), Barcelona, Spain
  6. 6Department of Epidemiology, Medical University of Vienna, Vienna, Austria
  7. 7Centro de Investigación en Salud y Medio Ambiente (CYSMA), Universidad de Huelva, Huelva, Spain
  8. 8Unit of Infections and Cancer, Cancer Epidemiology Research Programme, IDIBELL, Catalan Institute of Oncology, Barcelona, Spain
  9. 9Department of Medicine, University of Barcelona, Barcelona, Spain
  10. 10Environmental and Cancer Epidemiology Area, National Center of Epidemiology, Carlos III Health Institute, Madrid, Spain
  11. 11Cancer Epidemiology Research Group, Oncology and Hematology Area, IIS Puerta de Hierro, Madrid, Spain
  12. 12Grupo de Investigación en Interacciones Gen-Ambiente y Salud, Universidad de León, León, Spain
  13. 13Navarra Public Health Institute, Pamplona, Spain
  14. 14IdiSNA, Navarra Institute for Health Research, Pamplona, Spain
  15. 15Unit of Biomarkers and Susceptibility, Cancer Prevention and Control Program, IDIBELL, Catalan Institute of Oncology, Barcelona, Spain
  16. 16Department of Clinical Sciences, Faculty of Medicine, University of Barcelona, Barcelona, Spain
  17. 17University of Cantabria—IDIVAL, Santander, Spain
  18. 18IUOPA, Universidad de Oviedo, Asturias, Spain
  19. 19Fundación para el Fomento de la Investigación Sanitaria y Biomédica de la Comunidad Valenciana (FISABIO), Valencia, Spain
  20. 20Department of Epidemiology, Murcia Health Council, IMIB-Arrixaca, Murcia University, Murcia, Spain
  1. Correspondence to Dr Michelle C Turner, Centre for Research in Environmental Epidemiology (CREAL), Parc de Recerca Biomèdica de Barcelona, Doctor Aiguader, 88 Barcelona 08003 Spain; mturner{at}creal.cat

Abstract

Objectives Night shift work has been classified as a probable human carcinogen by the International Agency for Research on Cancer, based on experimental studies and limited evidence on human breast cancer risk. Evidence at other cancer sites is scarce. We evaluated the association between night shift work and stomach cancer risk in a population-based case–control study.

Methods A total of 374 incident stomach adenocarcinoma cases and 2481 population controls were included from the MCC-Spain study. Detailed data on lifetime night shift work were collected including permanent and rotating shifts, and their cumulative duration (years). Adjusted unconditional logistic regression models were used in analysis.

Results A total of 25.7% of cases and 22.5% of controls reported ever being a night shift worker. There was a weak positive, non-significant association between ever having had worked for at least 1 year in permanent night shifts and stomach cancer risk compared to never having worked night shifts (OR=1.2, 95% CI 0.9 to 1.8). However, there was an inverse ‘U’ shaped relationship with cumulative duration of permanent night shifts, with the highest risk observed in the intermediate duration category (OR 10–20 years=2.0, 95% CI 1.1 to 3.6) (p for trend=0.19). There was no association with ever having had worked in rotating night shifts (OR=0.9, 95% CI 0.6 to 1.2) and no trend according to cumulative duration (p for trend=0.68).

Conclusion We found no clear evidence concerning an association between night shift work and stomach cancer risk.

  • Night shift work
  • stomach cancer
  • case-control study
  • Spain

https://doi.org/10.1136/oemed-2016-103597

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    What this paper adds

    • Night shift work has been classified as a probable human carcinogen by the International Agency for Research on Cancer, based on experimental studies and limited evidence on human breast cancer risk; however, evidence at other cancer sites is scarce.

    • We evaluated the association between lifetime history of night shift work and stomach cancer risk in a population-based case–control study.

    • There was a weak positive, non-significant association with having worked for at least one year in permanent night shifts compared to never having worked night shifts, although there was no clear trend with number of years of permanent night shift work.

    • We found no clear evidence concerning an association between night shift work and stomach cancer risk.

    Introduction

    Shift work affects a large proportion, approximately 20%, of the labour force worldwide.1 ,2 Shift work, especially night shift work, requires workers to adapt their daily activity-rest cycle and can result in sleepiness, impaired safety and reduced productivity and quality of life.3 ,4 Increasing evidence suggests that shift work may also lead to a variety of chronic diseases, including high blood pressure, cardiovascular disease and an increased risk of cancer.5 ,6 In 2007, the International Agency for Research on Cancer (IARC) classified shift work with circadian disruption as a probable human carcinogen (group 2A), based on sufficient evidence in experimental animal studies on the carcinogenicity of light at night, with limited evidence in humans.1 ,7 Although epidemiological studies have typically focused on risk of breast cancer among women8–12 and prostate cancer among men,13 night shift work may also be associated with cancer at other sites; however, the literature is scarce.14–17

    One of the main hypotheses for an increased cancer risk associated with night shift work is the ‘melatonin hypothesis’, which highlights the link between light at night exposure and subsequent decreased melatonin secretion.18 ,19 Experimental studies reported that melatonin, the main hormone of the pineal gland, has direct and indirect anticancer effects including proapoptotic, antiproliferative, and antioxidative effects, and regulates the immune system.18 However, there may also be other potentially overlapping mechanisms including phase shift or desynchronisation, sleep deprivation impaired immune function, lifestyle disturbances and unhealthy behaviour, as well as lower levels of vitamin D in night shift workers.19

    Stomach cancer currently represents the fifth most commonly diagnosed cancer and third leading cause of cancer death worldwide, with an estimated 951 000 new cases and 700 000 deaths in 2012.20 In Spain, it was estimated that there were 7800 new stomach cancer cases and 5400 deaths in the same year.21 Although stomach cancer has been associated with a variety of environmental and behavioural risk factors, including Helicobacter pylori colonisation, cigarette smoking, consumption of nitrates and salted foods, as well as genetic and epigenetic factors,22 other environmental factors, including occupational exposures, may also play an important role in gastric carcinogenesis.

    Previous studies of night shift work and stomach cancer risk reported no clear association. Parent et al15 examined risk for 10 cancer sites in a population-based case–control study in Montreal, Canada, including 228 incident male stomach cancer cases. There was a weak non-significant association observed for stomach cancer risk among night shift workers (OR=1.3, 95% CI 0.9 to 2.1). A cohort study of German male chemical workers reported no association between rotating shift work and stomach cancer incidence (HR=1.2, 95% CI 0.5 to 2.7).23 A Swedish study evaluated shift work by classifying jobs according to the percentage of shift workers and reported a SIR of 1.2 (95% CI 0.6 to 2.3) for stomach cancer in women and 1.1 (95% CI 1.0 to 1.2) in men.16

    We evaluated the association between night shift work and stomach cancer risk in a large population-based case–control study, MCC-Spain, which included detailed data on lifetime night shift work history as well as a variety of potential confounding factors. The MCC-Spain study has previously been used to examine associations between night shift work and both, breast and prostate cancer risk, and presents a unique opportunity to examine associations at other cancer sites.24 ,25

    Methods

    Study population

    The MCC-Spain study is a multicentre, population-based, case–control study designed to examine potential associations between various environmental and genetic factors, and risk of five common cancers (breast, chronic lymphocytic leukaemia, colorectal, prostate and stomach cancer). Detailed data on the study are provided elsewhere.26 In brief, the study included 12 provinces and 23 public hospitals across Spain. Recruitment of incident cancer cases took place between the years 2008 and 2013, and used the same set of controls for all cancer cases. The MCC-Spain study was reviewed and approved by the ethics committees of the participating institutions. All participants provided informed consent prior to enrolment into the study.

    Newly diagnosed stomach cancer cases were recruited in 10 Spanish centres (Asturias, Barcelona, Cantabria, Granada, Huelva, Leon, Madrid, Murcia, Navarra and Valencia). Cases were defined by the following International Classification of Disease 10 (ICD-10) codes: C16 and D00.2 representing stomach cancer cases, and C15.5 representing cancer cases of the lower third of the oesophagus. Cases were aged 20–85 years, confirmed histologically and lived in the study area for at least 6 months before diagnosis. Exclusion criteria included having communication difficulties or a physical condition prohibiting participation. A total of 459 stomach cancer cases were recruited, with a response rate of 55%. Clinical data were obtained from medical records including tumour histological type, localisation, Lauren classification, the 2010 classification of the WHO and degree of differentiation.27 ,28 Data on H. pylori status were available in 279 cases, with 93% positive. In the remaining cases, H. pylori status was unknown.

    Controls aged 20–85 years were selected randomly from the rosters of general practitioners at the primary health centres involved in the study, lived in the same catchment area as cases, and were frequency-matched to all cancer cases by sex and age in 5-year groups. Since the same set of controls was used for all cancer cases in MCC-Spain, there were no initial exclusion criteria related to personal cancer history as part of the recruitment process. A total of 3440 eligible controls were recruited with a response rate of 51%.

    Data collection and night shift work definition

    Detailed data on a range of sociodemographic, lifestyle and clinical factors were collected in face-to-face interviews by trained personnel. Occupational history data were obtained for all jobs held for more than 1 year, including job title, tasks, start and stop dates, and shift work information (time schedules, hours worked per day, percentage worked in the morning, evening and night). Ever night shift work was defined as working partly or entirely between 24:00 and 6:00. Permanent night shifts consisted of working constantly, partly or entirely, between 24:00 and 6:00. Rotating night shifts consisted of working at least three night shifts per month, or 10% of working time. Cumulative duration of night shifts, permanent night shifts and rotating night shifts, was calculated as the total number of years worked at night.

    Statistical analysis

    We analysed the association between night shift work and stomach cancer risk, using unconditional logistic regression models. We calculated adjusted ORs and 95% CIs for stomach cancer in relation to ever performing night shift work, permanent night shift work, or rotating night shift work, as well as categories of cumulative duration (years). Models were adjusted a priori for age, sex, centre and level of education. The reference group included participants who were ever employed but had never performed night shifts.

    We examined the impact of further adjustment for body mass index (BMI), cigarette smoking status, family history of stomach cancer, physical activity level during adulthood (from age 16 years, excluding the past 2 years prior to diagnosis or interview (metabolic equivalents hour/week)), current sleep duration (≤6, 7–8, ≥9 hours/day) and ever sleep problems (for at least 1 year). Further, in a subset of all participants (75% of cases and 86% of controls), additional data on usual dietary intake during the previous year were collected using a self-administered modified version of a semiquantitative Food Frequency Questionnaire (FFQ), designed to include regional food products. Adjustment for total energy consumption, and consumption of red meat, processed-meat, cured-meat, fresh fruit and vegetables, and alcohol, was also examined among this participant subset.

    Stratified analyses were conducted by categories of age (<65 vs ≥65 years), sex, education (primary or less vs high school/university), family history of stomach cancer (none vs any), cigarette smoking status (non-smoker, former smoker, current smoker), BMI (18–25 vs >25 kg/m2), physical activity level (inactive/slightly active vs moderately/very active), sleep duration (≤ 6, 7–8, ≥9 hour/day) and sleep problems (never vs ever). Potential effect modification was assessed by entering product terms into unconditional logistic regression models and assessing their significance according to the likelihood ratio test. To evaluate the association between night shift work, and severity and clinical presentation of the disease, we used multinomial logistic regression to analyse associations according to Lauren classification (intestinal vs diffuse) and tumour localisation (cardia tumours, including the oesophageal junction and lower third of the oesophagus, vs non-cardia tumours).

    Analyses were conducted using Stata 14 (StataCorp, Stata Statistical Software: Release 14, College Station, TX: StataCorp LP 2015).

    Results

    A total of 374 stomach cancer cases and 2481 controls were included in the main analysis, following the exclusion of participants with no or missing occupational history data (66 cases, 516 controls), participants from study centres with few (<5) cases (Granada and Murcia) (5 cases, 118 controls), controls with a personal history of any cancer (n=204) and participants with missing data on key covariates of interest (14 cases, 121 controls).

    There were proportionally more included male cases than controls (table 1). Cases also tended to be older, have a lower educational level and to report stomach cancer more frequently in their family history. Cases also reported exercising less during adulthood, having a lower BMI, sleeping more, having greater total energy and red meat consumption, and lower alcohol consumption than controls.

    View this table:
    Table 1

    Distribution of participant characteristics, stomach cancer cases and controls, MCC-Spain, 2008–2013

    Excluded participants tended to be somewhat older (mean (SD) age excluded cases=73.0 (9.3) years, controls=68.2 (10.5) years), more likely female (62.4% cases, 49.3% controls) and to have a lower level of educational attainment (89.4% cases, 65.9% controls) compared to that of included participants (p<0.01).

    Table 2 summarises the characteristics of permanent night shift, rotating night shift, and day workers among controls. There were proportionally more male participants among night shift workers. Night shift workers also tended to have achieved lower educational levels, and were more likely to report being a current or former smoker and to have a higher BMI, longer sleep duration, and higher total energy and red meat consumption, compared to those who had never worked night shifts. Table 3 provides a listing of the main occupations contributing to permanent or rotating night shift work. These include housekeeping and restaurant services workers (9.6%); motor-vehicle drivers (8.1%); personal care and related workers (6.7%); and domestic and related helpers, cleaners and launderers (4.5%).

    View this table:
    Table 2

    Distribution of participant characteristics by night shift history, controls, MCC-Spain, 2008–2013

    View this table:
    Table 3

    Main occupations contributing to night shift work (including permanent or rotating night shifts), MCC-Spain, 2008–2013

    The association between ever working night shifts, permanent night shifts and rotating night shifts, and stomach cancer risk, is presented in table 4. A total of 25.7% of cases and 22.5% of controls reported ever working night shifts. Among night shift workers, there were more who had worked in a rotating night shift schedule (13.6% cases, 13.6% controls) than in permanent night shifts (12.0% cases, 8.8% controls). There was no association between ever working night shifts and stomach cancer risk (OR=1.0, 95% CI 0.8 to 1.3). There was a weak positive, non-significant association with having had worked for at least 1 year in permanent night shifts compared to never having worked night shifts (OR=1.2, 95% CI 0.9 to 1.8). There was no association with rotating night shifts (OR=0.9, 95% CI 0.6 to 1.2).

    View this table:
    Table 4

    Association between night shift work and stomach cancer risk, MCC-Spain, 2008–2011

    The exposure–response relationship between cumulative duration of night shifts and stomach cancer risk showed an inverse ‘U’ shape (table 4). The highest risk for permanent night shift workers was observed in the intermediate duration category (OR 10–20 years=2.0, 95% CI 1.1 to 3.6) (p trend=0.19). Analysis according to quartiles of cumulative duration did not result in any meaningful change in the relationship (results not shown). There was also no clear trend according to categories of lifetime cumulative frequency of night shifts with ORs of 1.5 (95% CI 0.8 to 2.8) and 1.6 (95% CI 0.9 to 2.8) (p=0.07) observed for categories of <1800 and ≥1800 nights worked, respectively, among the 56.8% of permanent night shift workers with data on frequency of night shifts.

    The association between ever, permanent and rotating night shift work, and stomach cancer risk, was similar after further adjusting for BMI, cigarette smoking status, family history and physical activity level (table 4). Further adjustment for either sleep duration or sleep problems also resulted in virtually identical ORs (results not shown). Additionally, the association between night shift work and stomach cancer risk did not change on evaluation of participants with either a reliable or high-quality interview, as reported by the interviewer (86.1% of participants) (results not shown).

    In the analysis of associations among the subset of participants who completed the FFQ (279 cases and 2157 controls), results were somewhat stronger but showed the same general pattern. In the fully-adjusted model, the OR (95% CI) for permanent night shift work was 1.5 (95% CI 1.0 to 2.4), adjusting for detailed dietary and alcohol consumption data (table 5). Results according to cumulative duration also revealed a stronger association for participants who worked from 10 to 20 years in permanent night shifts (OR=3.4, 95% CI 1.7 to 6.7) and no evidence for a trend (p=0.12).

    View this table:
    Table 5

    Association between night shift work and stomach cancer risk, dietary questionnaire participants, MCC-Spain, 2008–2011

    There was no evidence for effect modification of associations between permanent night shift work and stomach cancer risk according to various demographic and lifestyle factors examined (p>0.05) (results not shown). Associations with permanent night shift work were also similar according to categories of Lauren classification (relative risk ratio (RRR) intestinal=1.8, 95% CI 1.0 to 3.2, n=128 cases; RRR diffuse=1.4, 95% CI 0.7 to 2.8, n=86 cases) and tumour localisation (RRR cardia=1.3, 95% CI 0.7 to 2.4, n=98 cases; RRR non-cardia=1.3, 95% CI 0.9 to 2.0, n=267 cases), where data were available.

    Discussion

    Overall, we found equivocal evidence concerning an association between night shift work and stomach cancer risk. Although there was a weak positive, non-significant association with having worked for at least 1 year in permanent night shifts compared to never having worked night shifts, there was no clear trend with number of years of permanent night shift work, with the highest risk observed in the intermediate duration category of 10–20 years. There was no association with rotating night shifts.

    The reason for the observed inverse ‘U’ shape relationship with cumulative duration of night shifts is unclear. Possible explanations may include random variation or a type of healthy worker effect, including adaptation to night shift work in long-term or permanent night shift workers,29 though this is unlikely as symptoms of stomach cancer are apparent close to its detection. Further, results did not change when stratifying by tumour grade.

    The main results of the study are in concordance with the limited amount of previous data related to the association of night shift work and stomach cancer risk. Though one study reported a weak positive, non-significant association similar to that reported here,15 another study based on personnel records reported no association between rotating shift work and stomach cancer incidence in men.22 One study that did not evaluate individual information on shift work also reported no clear association.16

    In previous analyses in MCC-Spain, there was a weak positive association between being a night shift worker and breast cancer risk, particularly among premenopausal women, and for tumours with positive hormonal receptors.24 Risk was also higher for women with an evening or morning chronotype (an individual characteristic that describes the circadian phase and correlates with diurnal preference, the individual preference for morning or evening activity) compared to the neither type. Night shift workers, particularly those of long duration and evening chronotype, were also at higher prostate cancer risk.25 There was no chronotype information available in MCC-Spain for stomach cancer cases.

    The melatonin hypothesis is one of the most widely accepted pathological pathways related to increased cancer risk among night shift workers; though it remains controversial, its relevance for stomach cancer is unclear.18 Recently, an inverse association between urinary melatonin levels and prostate cancer was observed among elderly men.30 Some studies showed decreased blood or urine melatonin levels among night shift workers, though others showed interpersonal variability suggesting that some people may be better able to adapt to night shifts than others.31 ,32

    The current study has several strengths including that it is a population-based multicentre study with a considerable number of cases and controls. We obtained detailed data on night shift work including type of night shifts, and their cumulative duration and frequency. The prevalence of night shift work in this study—22.5% of controls reporting ever night shift work—is similar to other European estimates of night workers (19% of workers in the EU27 overall increasing to 23% among men).2 A recent Spanish survey observed that 13% of workers reported night shift work in the past year, which may be lower than our estimate based on lifetime history among controls in larger population centres.33 Although we defined night shift work as working partly or entirely between 24:00 and 6:00, as in previous work in MCC-Spain,24 ,25 it is possible that this definition may have limited our ability to detect an association if work during a particular portion of the night may be more disruptive than another, such as in the early morning period, for example, or among workers with greater proportions of the shift at night. However, little is known regarding the importance of particular timing or patterns of night shift work.

    Although residual confounding cannot be ruled out, there was information available for many recognised risk factors for stomach cancer, though dietary variables were only available in a subsample of the total study population and reflected intake during the previous year, which may be affected by the developing cancer. BMI also reflects current BMI at the study interview. Though reported total energy and red meat consumption was slightly greater among ever versus never night shift workers, there may also be other differences in dietary patterns, including eating patterns, cooking method and eating-out, for example, that were not captured in the study questionnaire here and that may be relevant.34 ,35 Results were largely unchanged, with the adjustment for such detailed demographic and lifestyle data here.

    Although some data were available on self-reports of sleep duration and history of sleep problems, such data likely reflect more recent sleep habits and do not necessarily relate to sleeping problems because of shift work. There were also few differences between day, permanent night and rotating night workers, in terms of sleep duration and problems. Confounding by other occupational exposures is unlikely as few occupational exposures have been related to stomach cancer.36 ,37 Night shift work is also not relevant for some of the occupations that have been previously linked to stomach cancer (such as coal mining, metal processing and rubber manufacturing, for example) (table 3).38 Although information was available for H. Pylori infection, the high proportion of positive cases did not allow further evaluation of this factor.

    Other potential limitations include the moderate response rate of 55% in cases and 51% in controls. A low response rate among cases is common in studies on stomach cancer because of the poor prognosis of the disease. Proxy respondents were not permitted as part of MCC-Spain. Population-based studies are also known to have lower response rates for controls than are hospital-based studies. The reasons for the low response rate could have differed between cases and controls, and could lead to selection bias. For example, people with a higher educational level tended to participate more in MCC-Spain,26 were less likely to have worked night shifts and experienced a lower risk of stomach cancer than those with low educational attainment.39 Also relevant to the current work, there may be selection bias by occupational status with controls currently working night shifts possibly less prone to participate due to their work schedules, which could lead to some spurious association. However, telephone contact was attempted during recruitment a minimum of five different times in the day. There were also no clear differences in findings according to age group, where potential selection bias by occupational status may be minimised in the older age group, or by education, though statistical power was limited. Finally, recruitment was based in the public health system, which would not capture government employees, particularly controls, with private insurance.

    In conclusion, our study found no clear evidence concerning an association between night shift work and stomach cancer risk. Further analysis including data on chronotype may contribute to better understanding of the relationship between night shift work and stomach cancer risk.

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    Footnotes

    • Contributors GG, MCT, KP and MK were involved in the study conception and design. GC-V, JA, LC, BP-G, VMS, EA, VM, IG-A, GF-T, VVB, RC, M-DC, MS, MP, NA and MK were involved in the participant data collection. GG and AE were involved in the statistical analysis. GG and MCT were involved in the drafting of the manuscript. All the authors participated in the interpretation of data and revision and approval of the manuscript.

    • Funding The study was partially funded by the ‘Accion Transversal del Cancer’, approved by the Spanish Ministry Council on 11 October 2007, by the Instituto de Salud Carlos III-FEDER (PI08/1770, PI08/1359, PI09/00773, PI09/01286, PI09/01903, PI09/02078, PI09/01662, PI11/01403, PI11/01889, PI12/00265), the Fundación Marqués de Valdecilla (API 10/09), the Junta de Castilla y León (LE22A10–2), the Consejería de Salud of the Junta de Andalucía (2009-S0143), the Conselleria de Sanitat of the Generalitat Valenciana (AP_061/10), the Recercaixa (2010ACUP 00310), the Regional Government of the Basque Country, the Consejería de Sanidad de la Región de Murcia, the European Commission grants FOOD-CT-2006–036224-HIWATE, the Spanish Association Against Cancer (AECC) Scientific Foundation, the Catalan Government DURSI grant 2014SGR647, the Fundación Caja de Ahorros de Asturias and by the University of Oviedo. MCT was funded by a Canadian Institutes of Health Research Fellowship.

    • Competing interests None declared.

    • Patient consent Obtained.

    • Ethics approval Ethics committees of the participating institutions.

    • Provenance and peer review Not commissioned; externally peer reviewed.