Ultraviolet radiation and skin cancer risk in offshore workers

Abstract

Background

Excess skin cancer mortality and incidence have been reported among both land-based and offshore petroleum workers. The association between skin cancer and ultraviolet radiation (UVR) exposure has not been examined in these workers, although they have long off-duty periods and high average income that may allow travelling to sunny destinations. In addition, they have access to solariums free of charge on many accommodation platforms.

Aims

To prospectively examine risk of incident cutaneous melanoma (CM) and non-melanoma skin cancer (NMSC), according to sun-tanning habits with adjustment for aromatic hydrocarbon exposure.

Methods

A cohort of men employed offshore from 1965 to 1999 was linked through the Cancer Registry of Norway 1999–2012. Cox regression adapted to a stratified case-cohort design was used to estimate hazard ratios with 95% confidence intervals.

Results

The cohort included 24917 men. During 13.5 years of follow-up, 112 CMs and 70 NMSCs occurred. A positive dose–response relationship was seen between sunburn frequency and risk of CM (P_trend < 0.05) and NMSC (P_trend < 0.01). Solarium use both before and after age 20 was related to increased risk of NMSC. Sunscreen use was associated with increased risk of NMSC (P_trend < 0.001).

Conclusions

UVR exposure seems to be a significant contributor to the elevated risk of skin cancer observed in North Sea offshore workers. The positive association between solarium use and NMSC risk adds to the growing body of literature on artificial UV devices as carcinogenic.

Introduction

Excess skin cancer mortality and incidence have been reported among petroleum workers from the UK, Australia, Canada and Norway [1–4]. However, the role of individual ultraviolet radiation (UVR) exposure in these skin cancer excesses has not been examined. Except from the face, offshore workers generally have all body parts covered due to strict regulations on use of personal protective equipment. However, long off-duty periods (e.g. 3–4 weeks after 2-week work periods) and high average income allow ample leisure-time outdoor activities and travels to sunny destinations. In addition, free access to solariums has been provided on many accommodation platforms [5]. Offshore workers may also be exposed to occupational skin carcinogens during handling of the petroleum stream as well as to mineral oils used for lubrication in drilling and maintenance operations [6].

The aim of the present study was to prospectively examine skin cancer risk according to individual UVR exposure, with adjustment for occupational exposure to aromatic hydrocarbons.

Methods

In 1998, the Cancer Registry of Norway conducted a questionnaire-based survey on work history and lifestyle among active and former offshore workers, thereby establishing a cohort of 27987 individuals who confirmed working on the Norwegian continental shelf for at least 20 days between 1 January 1965 and 31 December 1998 (inclusion criterion). The male members of the cohort were linked to the Cancer Registry of Norway and to the Norwegian National Population Register and were followed prospectively from 1999 to 2012 until a skin cancer diagnosis, death, emigration or end of follow-up. Individuals with skin cancer prior to start of follow-up were excluded.

Complete work history data were extracted manually for each worker, to obtain estimates of occupational hydrocarbon exposure. For cost reasons, this was done for a random subsample of the cohort and for all skin cancer cases (Figure S1, available as Supplementary data at Occupational Medicine Online), following a stratified case-cohort design.

In 1998 (prior to skin cancer diagnosis), the participants reported on sunburn frequency (never, 1–3/year, ≥4/year), sunbathing (never, 1–3 weeks/year, 4–5 weeks/year, ≥6 weeks/year) and frequency of solarium use (never, 1–2/month, ≥3/month) before and after the age of 20, as well as present sunscreen use (never/rarely, often or almost always) (see Supplemental Material) and education (compulsory, vocational training, upper secondary, university/college). Data on benzene exposure, an aromatic hydrocarbon, were individually assigned according to work duration and divided into tertiles (unexposed ‘0 year’, tertile 1 ‘>0–5 years’, tertile 2 ‘>5–13 years’, tertile 3 ‘>13–34 years’). Exposure to benzene was used as a proxy for aromatic hydrocarbon exposure occurring in the petroleum stream.

Cox regression, adapted to a stratified case-cohort design, was used to estimate hazard ratios (HRs) of skin cancer with corresponding 95% confidence intervals (CIs) (see Supplemental Material), using Stata version 14.1 (StataCorp, College Station, TX, USA).

Necessary legal and ethical approvals were obtained from the Norwegian Data Inspectorate, the Regional Committee for Medical Research Ethics, and the Norwegian Directorate of Health.

Results

There were 24917 males available for the study. Individuals with skin cancer prior to start of follow-up were excluded (n = 19). Complete work history data were available for a random subsample (n = 1643) and for all skin cancer cases (n = 182).

During 13.5 years of follow-up, 112 cutaneous melanoma (CM) and 70 non-melanoma skin cancer (NMSC) were diagnosed (Table 1). Table 2 shows risk of CM and NMSC according to UVR exposure (before or after age 20), and sunscreen use at start of follow-up.

For exposures before age 20, sunburn frequency showed dose-related patterns for both CM (P_trend < 0.05) and NMSC (P_trend < 0.001). Solarium sessions (1–2 per month) showed an HR of 4.16 (95% CI 1.89, 9.17) for NMSC. For exposures after age 20, there were dose-related patterns for sunburn frequency and risk of CM (P_trend < 0.05) and NMSC (P_trend < 0.01). No clear pattern was seen for sunbathing, while three to five solarium sessions per month showed an HR for NMSC of 4.02 (95% CI 1.14, 14). The NMSC risk increased with increasing frequency of sunscreen use (P_trend < 0.001), but no association was seen for CM risk. In supplemental analyses (Table S1, available as Supplementary data at Occupational Medicine Online), where CM and NMSC were combined and analysed by anatomical site, both solarium use (before age 20) and sunburns (after age 20) were linked to head, neck and trunk cancers.

Discussion

Our data confirmed significant dose–response relationships between sunburn frequency and risk of both CM and NMSC. Solarium and sunscreen use were related to increased risk of NMSCs.

Strengths of the present study include the prospective case-cohort design, data from a population-based cancer registry and individual UVR data by age of exposure. Limitations include the potential for misclassification bias in the reporting of UVR exposure and the low case numbers in some exposure categories, yielding wide CIs. NMSCs have a stronger age-specific risk gradient than CMs, which is seen in the age distribution between CM and NMSC in this cohort (Table 1) and in the national incidence rates (Figure S2, available as Supplementary data at Occupational Medicine Online). We cannot rule out the possibility that this age difference may explain why measures of UVR seemed more closely related to NMSC than CM. Although UVR exposure is a recognized risk factor for both CM and NMSC, results from analyses combining them should be interpreted cautiously, as they may have different pathways related to UVR exposure [7].

Our findings suggest that individual UVR exposure and sunbathing habits can explain some of the previously reported excesses in skin cancer incidence and mortality in petroleum workers from UK, Australia, Canada and Norway [1–4]. The marked increase in CM and NMSC risk by sunburn frequency is in agreement with the patterns reported by others [8]. Although we had few exposed cases, we found an association between solarium use and NMSC risk. These findings accord with those of Zhang et al. [9] where risks related to solarium use appeared stronger for basal cell carcinoma and squamous cell carcinoma than risk of CM, and with a recent meta-analysis concluding that indoor tanning is associated with a significantly increased risk of NMSC [10].

In conclusion, our analysis shows strong associations between UVR exposure and skin cancer among offshore petroleum workers. The association between solarium use and skin cancer seen in our data adds to existing evidence that artificial UVR tanning devices are carcinogenic.

Funding

This work was funded by the Research Council of Norway’s PETROMAKS Program (grant no. 220782), a grant from the Statoil Fund for Research in Occupational Medicine, the Cancer Registry of Norway Research Fund and the Norwegian Cancer Society (grant no. 5829980).

Conflicts of interest

None declared.

Acknowledgements

We wish to thank our former Department Head Aage Andersen and Researcher Leif-Åge Strand for conducting the offshore survey and launching the studies of offshore workers; Advisor Tone Eggen and Data Manager Ronnie Babigumira for data cleaning of the work histories and for help with preparing and linking exposure ratings to the cohort; and Industrial Hygienist Bjørg Eli Hollund (Department of Occupational Medicine, Haukeland University Hospital, Norway) and Research Director John Cherrie (Institute of Occupational Medicine, Edinburgh, UK) for assisting with development of the benzene exposure estimates.

References