Personal UVR exposure of farming families in four European countries

Journal of Photochemistry & Photobiology, B: Biology 153 (2015) 267–275

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Personal UVR exposure of farming families in four European countries M. Bodekær a,⁎, G.I. Harrison b, P. Philipsen a, B. Petersen a, M. Triguero-Mas c,d,e, A.W. Schmalwieser f, M. Rogowski-Tylman g, P. Dadvand c,d,e, A. Lesiak g, J. Narbutt g, P. Eriksen h, J. Heydenreich a, M. Nieuwenhuijsen c,d,e, E. Thieden a, A.R. Young b, H.C. Wulf a a

Department of Dermatology, Bispebjerg Hospital, Copenhagen, Denmark King's College London, London, United Kingdom Centre for Research in Environmental Epidemiology (CREAL), Barcelona, Spain d Universitat Pompeu Fabra (UPF), Barcelona, Spain e CIBER Epidemiología y Salud Pública (CIBERESP), Barcelona, Spain f University of Veterinary Medicine, Vienna, Austria g Medical University of Lodz, Lodz, Poland h Danish Meteorological Institute, Copenhagen, Denmark b c

a r t i c l e

i n f o

Article history: Received 13 July 2015 Received in revised form 8 September 2015 Accepted 5 October 2015 Available online 9 October 2015 Keywords: UVR exposure UVR dosimetry Sun behaviour Europe Outdoor workers Farming Children

a b s t r a c t Background: The main risk factor for skin cancer is ultraviolet radiation (UVR). Farming families living in rural areas with easy outdoor access may experience excessive UVR exposure. Differences between countries in latitude, altitude and sun behaviour could result in different personal UVR exposures. However, no studies have examined this until now. Objectives: To determine personal UVR exposure in work and leisure situations among farming families in Europe. Methods: Prospective cohort study of farmers, their partners (spouses) and children in Denmark (DK), Poland (PL), Austria (AT), and Spain (ES) from 2009 to 2011. Personal UVR exposure and sun behaviour were recorded by dosimetry and diaries. Results: Farmers' average daily UVR exposure on working days ranged from 1.4 SED (DK, AT) to 2.7 SED (ES). Corresponding figures for partners were: 0.6 SED (DK) to 1.9 SED (PL), and for children (day-care/school days): 0.7 SED (ES) to 1.3 SED (PL). Discussion and Conclusions: Farmers' UVR exposure was comparable to that of outdoor workers in previous studies and exceeded the recommended UVR exposure limits on 36% (DK, AT), 29% (PL) and 56% (ES) of their working days. Attention to sun protection for outdoor workers across Europe in preventing UVR-induced skin cancer is still needed. © 2015 Elsevier B.V. All rights reserved.

1. Introduction The main risk factor for skin cancer is ultraviolet radiation (UVR), which may be experienced in work or leisure situations. Skin and eye UVR exposure limits have been recommended for working situations [1]. These limits (≤1.3 SED/8 h working day) are often exceeded, especially among outdoor workers [2–10], who have also been found to have an increased risk of basal cell carcinoma (BCC) and squamous cell carcinoma (SCC) [11–13]. Several studies throughout the world have tried to map people's UVR exposure. In Europe, studies on personal UVR exposure using dosimetry have been conducted targeting different populations, e.g., children, indoor ⁎ Corresponding author at: Department of Dermatology, D-92, Bispebjerg Hospital, Bispebjerg Bakke 23, 2400 Copenhagen, Denmark. Tel.: +45 35 316188; fax: +45 35 316010. E-mail address: [email protected] (M. Bodekær).

http://dx.doi.org/10.1016/j.jphotobiol.2015.10.002 1011-1344/© 2015 Elsevier B.V. All rights reserved.

workers, and outdoor workers [2–10,14–19], but only two European studies have directly compared personal UVR exposure between countries [20,21]. These studies targeted sun worshippers and urban gardeners. In the present study, we therefore aimed to compare the personal UVR exposure of a broad range of adults (outdoor and indoor workers) and children in four countries in northern, central and southern Europe over a summer period. Since farming is an occupation carried out in most European countries and involves working outdoors for a considerable amount of time, we chose to focus on farmers and their families in the present study. We chose farmers, as they may represent the general outdoor rural worker, the farmers' partners, as they represent both indoor and outdoor workers, and the farmers' and partners' children, as they represent a broad age range of rural children attending both day-care and school. We expected to find differences between countries in personal UVR exposure owing to differences in e.g., latitude and altitude [22–25], differences in type of farming (production) and access to farm technology [7], and differences in cultural and leisure factors [25].

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2. Materials and Methods 2.1. Study Design and Setting Four prospective cohorts were studied: from Denmark (DK), Poland (PL), Austria (AT) and Spain (ES). The countries were chosen to represent northern, central and southern latitudes across Europe. Identical protocols were followed for all study participants who were recruited in DK (54°44′N–55°55′N), PL (52°00′N), AT (46°90′N–48°90′N), and Catalonia in ES (41°49′ N), approximate altitudes: 5 m, 100 m, 350 m, and 280 m above sea level, respectively. The study was conducted during the summers of 2009 (DK), 2010 (PL and ES) and 2011 (AT). Minimum solar zenith angles for the period (April/October–July) were 60°–33° (DK), 55°–28° (PL), 52°–25° (AT), and 45°–19° (ES). Ethical approval was obtained from the research ethics committees of the respective countries (DK: no. H-D-2009-034, PL: no. RNN/192/08/KE, AT: no. EK 978/2011, ES: no. 2009/3692/I). Informed written consent was obtained from the adult participants, also on behalf of their children. The study was conducted in accordance with the Declaration of Helsinki [26]. 2.2. Study Population Farming families engaged in outdoor crop farming typical for the country concerned were recruited (DK: 152 participants, PL: 102 participants, AT: 87 participants, ES: 56 participants). We aimed at recruiting families consisting of an adult farmer working for a minimum of 6 h outdoors per day (including time driving machinery), their partner (spouse) working at or away from the farm (adults between 20 and 70 years of age), and a minimum of one child from 5 to 19 years of age. Farming families were recruited through advertisements in agricultural magazines and by personal contact to agricultural advisors. Potential participants were interviewed on telephone to determine whether they could be included in the study. Participants needed to have typical and similar ethnicity for each country, have skin types I–IV and be able to read and understand the language of the country. Exclusion criteria were: persons with skin cancer, psoriasis, atopic dermatitis, polymorphic light eruption and persons taking sun-sensitizing medication, disabled persons and organ transplant recipients.

consists of a silicone carbide photodiode with a spectral response that mimics the International Commission of Illumination (CIE) erythema action spectrum [30] and measures time-stamped UVR exposure in standard erythema doses (SEDs) [31]. Each dosimeter was calibrated with the sun as UVR source, under clear sky conditions at La Reunion (France, February), using a spectroradiometer as a reference. The spectroradiometer comprises a Bentham DMc-150f double-grating monochromator, a photomultiplier tube (Bentham Instruments, Reading, UK), and an optical fibre with a cosine angular response. The spectroradiometer has a calibration traceable to the UK National Physical Laboratory [32]. Participants were instructed to wear the SunSaver uncovered on their wrist every day from at least 7 am to 7 pm. Ambient UVR data for Denmark were available from the Danish Meteorological Institute (DMI) from a Brewer spectrophotometer located in Copenhagen, within a distance of 150 km from the farms. Ambient UVR data for Poland and Spain were available from SunSaver groundstations [22,29,32] which were located within the area of the farms and were calibrated along with the dosimeters. For days when ambient UVR data were missing from the groundstations in Poland, data were available from a SolarLight Biometer located in Belsk, approximately 50 km from the farms, and operated by the Institute of Geophysics at the Polish Academy of Sciences. For days when ambient UVR data were missing from the groundstations in Spain, data were available from Yankee Environments YES-UVB instruments located in Barcelona, approximately 50 km from the farms, and operated by the State Meteorological Agency (AEMET). For Austria, ambient UVR data were available from a SolarLight Biometer located in Vienna, approximately 150 km from the farms, and operated by the Austrian UV monitoring network [33]. For days when ambient UVR data were missing from the Biometer in Vienna, global radiation calculations were performed by the DMI with global radiation data available from the Austrian Meteorological Service (Zentralanstalt für Meteorologie und Geodynamik, ZAMG). All instruments measured erythema weighted UVR irradiance in accordance with the CIE [30]. Fig. 2 shows the daily ambient UVR expressed as SED during the study period for each country.

2.3. Personal UVR Dosimeter and Ambient UVR Measurements Personal UVR exposure was measured by an electronic dosimeter (SunSaver), including a watch (Fig. 1), which has been previously described in detail [9,20,21,27–29]. Briefly, the electronic UVR dosimeter

Fig. 1. The UVR dosimeter. The personal, electronic dosimeter (SunSaver) is worn like a regular wrist-watch. The dosimeter is fitted inside a housing with the UVR sensor penetrating a round opening. Inside the housing a separate watch is placed.

Fig. 2. Ambient UVR. A scatterplot shows the daily ambient UVR dose in SED during the entire study period (May–September) of each country. The central marking on the xaxis of each country represents July 1. The ranges of dates for each country are: DK: May 8–September 30, 2009; PL: May 1–September 30, 2010; AT: May 1–September 30, 2011; and ES: May 1–September 30, 2010.

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2.4. Diary

2.7. Statistical Analysis

The participants were instructed to fill in a personal sun behaviour diary each day at the end of the day [28], recording: (i) if it had been either a working day, a day off, or a holiday day away from the farm, (ii) if they had been intentionally sunbathing, (iii) if they had exposed their shoulders or upper body to the sun, other than sunbathing, (iv) if they had used sunscreen, (v) if they had visited the beach, and (vi) if they had sunburned. Participants were instructed that children's “working days” were days when they were in school or day-care, and that “sunburn” was any degree of self-perceived skin redness acquired from UVR exposure. To analyse the diary data we defined “risk days” as days with “risk behaviour”, which were days when participants removed clothes and exposed a major part of the body (here shoulders/upper body) to the sun in sunbathing, work or leisure situations.

The variables examined are presented in Tables 1–4 and Figs. 3–5. Each participant's mean value during the study period was used, thus weighting each person equally in the analysis, eliminating factors like unequal number of days between persons (Table 1). As most variables were normally distributed, parametric tests were used for analysis, and results are given in terms of the variables' mean and standard deviations (SD). The independent samples t-test was used to examine differences between countries for the groups of farmers, partners and children. Fisher's exact test [35] was used to examine skin type differences between countries for the groups of farmers, partners and children. Since multiple comparisons (6 for each group) were performed, the results were corrected using the Bonferroni method (multiplying the p-value with a factor of 6) [35]. The significance level was set at p b 0.05. SPSS Statistics 19.0 (IBM, Armonk, New York, USA) was used for analysis.

2.5. UVR and Diary Days Used for the Analysis

3. Results

Data from May 1 to September 30 were included, but only complete days on which participants had both worn the SunSaver and filled in the diary were included in the analysis. No assumptions were made when data were missing. Participants were excluded from the analysis if they did not have daily data for a minimum of 31 days during the whole study period (from May 1 to September 30) and a minimum of 21 days during UVR peak months from June to August (Table 1).

3.1. Study Population We enrolled 397 participants in the study, 353 of whom (89%), with 39,598 measuring days, were included in the analysis (Table 1). All families contained a farmer, but not all farmers had a partner or a child. One Austrian farmer had two grandchildren below 20 years of age living at the farm, who were included as children. Another Austrian farmer, aged 72, was included in the analysis, since he was still actively working. Danish farmers had significantly more study days (122 days) than Austrian farmers (105 days), likewise, Danish and Polish children had significantly more study days (107 days, and 113 days, respectively) than Austrian children (84 days) (p ≤ 0.039). Danish farmers had significantly more holiday days (4 days) than both Polish (1 day) and Spanish

2.6. Skin Type Skin type was defined according to Fitzpatrick's classification system [34] by participants' self assessment.

Table 1 Description of the sample.

Participants Included in the study (n) Included in analysis (n), with complete daysa and fulfilling criteriab Number of days Participant groupc (n) Mean age (years) Males (%) Females (%) Skin type (%)d I II III IV Mean number of: Study days Holiday days Risk days Sunscreen days No sunscreen days (% participants) Beach days Sunburn days

Denmark

Poland

Austria

Spain

Total

152 150

102 84

87 72

56 47

397 353

17,374 F 44 45 100 0

P 44 42 0 100

C 62 11 50 50

9629 F 21 43 62 38

P 16 41 19 81

C 47 14 45 55

7372 F 31 51 48 52

P 25 51 48 52

C 16 13 50 50

5223 F 17 43 100 0

P 16 43 0 100

C 14 11 21 79

39,598 F 113 46 79 21

P 101 44 15 85

C 139 12 45 55

7 64 27 2

14 57 23 7

8 50 27 15

5 24 57 14

0 56 38 6

2 47 47 4

3 39 55 3

8 44 40 8

6 25 50 19

12 24 41 24

0 69 6 25

0 14 29 57

6 43 43 8

8 55 27 10

5 42 37 16

122 4 9 1 52 5 1

121 4 22 7 23 7 2

107 6 16 6 18 9 2

115 1 15 1 81 1 3

119 0 23 1 81 1 4

113 14 16 2 75 1 4

105 2 16 3 71 2 2

111 1 12 4 52 1 3

84 5 11 7 25 8 2

114 1 9 6 41 3 1

119 4 27 26 13 5 2

98 7 16 11 21 4 0

115 2 12 2 61 3 2

118 3 20 8 38 4 3

106 9 16 5 38 6 2

The number of participants (n) included in the study and in the final analysis are given in total and for each country. The number of days in the final analysis is also given in total and for each country. Participants are further registered by group (F: farmer, P: partner, C: child). Number (n), mean age (years), gender (%), Fitzpatrick skin type (%), mean number of study days and mean number of days with sun-related activities are provided for these groups. Bolds indicate totals. a Complete days: the participant has filled in the diary, has worn the dosimeter as registered in the diary and the dosimeter shows daily UVR measurements of ≥0 SED. b Participation criteria: minimum 31 days during the study period (May 1–Sept 30) and 21 days in June/July/August. c Participant group: F: farmers. P: partners. C: children. d Skin type distribution significantly different between: DK farmers and PL farmers, DK farmers and ES farmers, AT partners and ES partners, DK children and ES children, PL children and ES children (p b 0.05).

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Table 2 Farmers' UVR exposure.

Time spent outdoors (hours) on a daily basis and UVR exposure in SED and % of ambient UVR in different situations are given for farmers, split according to country. Values are given in mean, standard deviation (SD) and number of participants (n). Differences between countries are visualised in the last column, where (NS) represents non-significance. Highest values are shaded dark grey, lowest values are shaded light grey.

farmers (1 day), and Danish partners had significantly more holiday days (4 days) than Polish (0 days) and Austrian partners (1 days) (p ≤ 0.011). No significant differences in number of risk days or number of sunscreen days were found among the groups. Danish farmers had significantly more beach days (5 days) than Polish farmers (1 day), and Danish partners had significantly more beach days (7 days) than both Polish and Austrian partners (1 day for each), while Danish, Austrian and Spanish children had significantly more beach days (9 days, 8 days, and 4 days, respectively) than Polish children (1 day), and

Table 3 Partners' UVR exposure.

Table 4 Children's UVR exposure.

Time spent outdoors (hours) on a daily basis and UVR exposure in SED and % of ambient UVR in different situations are given for children, split according to country. Values are given in mean, standard deviation (SD) and number of participants (n). Differences between countries are visualised in the last column, where (NS) represents non-significance. Highest values are shaded dark grey, lowest values are shaded light grey.

Danish children had also significantly more beach days than Spanish children (p ≤ 0.013.). Danish and Polish children had significantly more sunburn days (2 and 4 days, respectively) than Spanish children (0 days) (p ≤ 0.028) (Table 1). 3.2. UVR Exposure 3.3. Farmers 3.3.1. Danish Farmers. Danish farmers spent more time outdoors in the sun (5.0 h, not including time driving machinery) than Austrian (4.5 h) and Polish farmers (3.6 h) (DK farmers vs PL farmers: p = 9.1 ∗ 10−4), but their daily UVR exposure (1.5 SED) and their UVR exposure on working days (1.4 SED) were among the lowest of all farmers (Table 2, Fig. 3). On holidays, risk days, sunscreen days, beach days and sunburn days, Danish farmers had the highest UVR exposure, also in percentage of ambient UVR (Table 2). On days off, Danish farmers had a significantly higher UVR exposure (1.7 SED), also in percentage of ambient UVR (7.8%), than Austrian farmers (1.1 SED, 3.9%) (dose: p = 0.023, and % amb.: p = 8.2 ∗ 10−5) (Fig. 4). 3.3.2. Polish Farmers. Polish farmers spent less time outdoors in the sun than the other farmers (significance mentioned above) (Table 2), but received the highest percentage of ambient UVR on working days and days off (8.0% for both) of all farmers (not statistically significant) (Figs. 3–4). 3.3.3. Austrian Farmers. Austrian farmers received the lowest UVR doses and percentages of ambient UVR of all the farmers on a daily basis (1.4 SED, 5.4%), on working days (1.4 SED, 5.4%), days off (1.1 SED, 3.9%), risk days (2.1 SED, 7.5%), and beach days (1.2 SED, 3.9%) (Table 2, Figs. 3–4).

Time spent outdoors (hours) on a daily basis and UVR exposure in SED and % of ambient UVR in different situations are given for partners, split according to country. Values are given in mean, standard deviation (SD) and number of participants (n). Differences between countries are visualised in the last column, where (NS) represents non-significance. Highest values are shaded dark grey, lowest values are shaded light grey.

3.3.4. Spanish Farmers. Spanish farmers spent more time outdoors in the sun (5.6 h, not including time driving machinery) than the other farmers (ES farmers vs PL farmers (3.6 h): p = 5.0 ∗ 10− 4), and received a higher daily UVR dose (2.6 SED), also on working days (2.7 SED) than both Danish (1.5 SED, 1.4 SED) and Austrian farmers

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Fig. 3. Personal UVR exposure on working days. The mean UVR exposure on working days (school days or day-care days for children) is given in SED and percentage of ambient UVR for the farmers, partners and children, split according to country.

(1.4 SED for both) (ES vs DK farmers: p = 0.003 and p = 0.001) (ES vs AT farmers: p = 1.3 ∗ 10−4 and p = 0.002) (Table 2, Fig. 3). On days off, the Spanish farmers' UVR exposure was among the highest (2.0 SED), though this was not statistically significant (Fig. 4). Spanish farmers received the highest total UVR exposure during the study period (305 SED), significantly higher than that of Danish (180 SED) and Austrian farmers (152 SED) (ES vs DK farmers: p = 0.03) (ES vs AT farmers: p = 0.0095) (Fig. 5). 3.4. Partners 3.4.1. Danish Partners. Danish partners received one of the lowest daily UVR exposures (1.1 SED), also on working days, likewise, the lowest

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Fig. 4. Personal UVR exposure on days off. The mean UVR exposure on days off is given in SED and percentage of ambient UVR for the farmers, partners and children, split according to country.

percentage of ambient UVR on working days (DK partners (0.6 SED, 2.9%) vs AT partners (1.6 SED, 5.8%) on working days: dose: p = 0.002, % amb.: p = 0.0014). On sunscreen days and sunburn days, Danish partners received the highest UVR exposure (4.5 SED, 5.1 SED) of all groups of partners and they likewise received the highest percentage of ambient UVR on days off (6.7%), holidays (9.2%), sunscreen days (14.8%) and sunburn days (17.0%) (Table 3, Figs. 3–4). 3.4.2. Polish Partners. On average the Polish partners spent less time outdoors than the other partners (PL partners (2.9 h) vs AT partners (4.3 h): p = 0.035), but received the highest UVR exposure on a daily basis (1.8 SED), on working days (1.9 SED), days off (1.8 SED) and risk days (4.3 SED). Likewise, the Polish partners received the highest percentage of ambient UVR on a daily basis (7.1%), and on (working days

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statistically significant. On sunscreen days, the Danish children received the highest UVR exposure and the highest percentage of ambient UVR (DK children (5.1 SED, 16.8%) vs AT children (2.0 SED, 6.2%): p = 0.016, and p = 0.0030) (Table 4, Fig. 3). 3.5.2. Polish Children. Polish children received the highest daily UVR exposure (1.8 SED), and together with the Danish children the highest percentage of ambient UVR (PL children (6.4%) vs AT children (3.0%): p = 0.042, and PL children vs ES children (3.1%): p = 0.048). The Polish children had the highest UVR exposure on working days (school days or day-care days) (1.3 SED), on days off (1.7 SED), and on risk days (3.7 SED), although this was not statistically significant. Polish children also received the highest percentage of ambient UVR on days off, on risk days, and on beach days (PL children (12.3%) vs AT children (5.7%) on risk days: p = 0.049) (Table 4, Figs. 3–4). Polish and Danish children received the highest total UVR exposures during the study period (180 SED and 144 SED, respectively), significantly higher than that of the Austrian children (72 SED) (p = 0.003 and p = 0.002, respectively), but not the Spanish children (129 SED) (Fig. 5).

Fig. 5. Total UVR exposure. The mean total UVR exposure for the study period is given in SED for the farmers, partners and children, split according to country.

7.4%). On sunscreen days (2.5 SED) and beach days (2.9 SED), Polish partners received the lowest UVR exposure. None of these differences, however, reached statistical significance (Table 3, Figs. 3–4). 3.4.3. Austrian Partners Austrian partners spent more time outdoors (4.3 h) than the other partners (significance mentioned above), but received neither the highest daily UVR exposure (1.6 SED), nor the highest percentage of ambient UVR (5.9%). On holidays, the Austrian partners received the lowest UVR exposure and the lowest percentage of ambient UVR (AT (0.7 SED, 2.1%) vs DK partners (2.3 SED, 9.2%): dose: p = 0.015, % amb.: p = 8.7 ∗ 10−4). On risk days and beach days, the Austrian partners received the highest UVR exposure (beach days) and the highest percentages of ambient UVR (risk days, beach days), although this did not reach statistical significance (Table 3).

3.5.3. Austrian Children. Austrian children spent less time outdoors than the other children (significance stated above), and received the lowest UVR exposure on a daily basis (0.9 SED), on days off (1.1 SED), on holidays (1.6 SED), on risk days (1.9 SED), on sunscreen days (2.0 SED), on beach days (1.5 SED) and on sunburn days (2.0 SED). They also received the lowest percentages of ambient UVR on a daily basis, on risk days, on sunscreen days, on beach days, and on sunburn days (Table 4, Fig. 4). 3.5.4. Spanish Children. Spanish children spent less time outdoors than the other children (ES children (2.1 h) vs DK children (3.3 h): p = 0.0059), and received the lowest UVR exposure and percentage of ambient UVR of all children on working days (school days or day-care days) (ES children (2.0%) vs DK children (5.4%): % amb.: p = 1.6 ∗ 10− 4). On days off, the Spanish children received the lowest percentage of ambient UVR (3.7%), although this was not statistically significant. On holidays, they received one of the highest UVR exposures (2.4 SED), on a level with that of Danish children (2.4 SED), although while Danish children received the highest percentage of ambient UVR (9.3%), Spanish children received the lowest (5.2%). This difference was, however, not statistically significant. On beach days, Spanish children received the highest UVR exposure (ES children (4.4 SED) vs AT children (1.5 SED): p = 0.020) (Table 4, Figs. 3–4). 4. Discussion

3.4.4. Spanish Partners. Spanish partners received one of the lowest daily UVR exposures (1.1 SED) of the partners, also on days off (1.3 SED), on risk days (2.6 SED) and on sunburn days (2.4 SED). They also received the lowest percentage of ambient UVR on a daily basis (2.9%), on working days (2.9%), on days off (3.3%), on risk days (6.1%), on sunscreen days (7.3%), on beach days (7.8%), and on sunburn days (5.4%). Spanish partners received a significantly lower UVR exposure in percentage of ambient UVR than Danish partners on a daily basis (DK: 4.7%, p = 0.030), on days off (DK: 6.7%, p = 0.0084), on sunscreen days (DK: 14.8%, p = 0.010) and on sunburn days (DK: 17.0%, p = 2.0 ∗ 10−4) (Table 3, Fig. 3–4).

The aim of the present study was to compare the UVR exposure of farming families in four European countries during a summer season. This has never previously been examined. Since personal UVR exposure is determined by several factors: occupation, outdoor activities, orientation of the body to the sun, cultural and social behaviour, type of clothing, use of sunscreen and ambient UVR level, which in turn is determined by season, time of day, latitude, altitude, cloud cover, surface reflection and air pollution [25], we expected to find differences in personal UVR exposure between participants from different countries.

3.5. Children

4.1. Farmers

3.5.1. Danish Children. Danish children spent more time outdoors (3.3 h) than all other children (ES: 2.1 h, p = 0.0059, PL: 2.5 h, p = 0.013, AT: 2.1 h, p = 8.4 ∗ 10−4), and on working days (school days or day-care days), they received the highest percentage of ambient UVR (DK children (5.4%) vs AT children (2.8%): p = 0.0064, and DK children vs ES children (2.0%): p = 1.6 ∗ 10−4). On holidays and sunburn days, they received the highest UVR exposure (2.4 SED, 5.8 SED) and the highest percentages of ambient UVR (9.3%, 20.7%), although this was not

Spanish farmers received the highest daily UVR exposure among the farmers, which can be explained by a combination of more time spent outdoors and a higher ambient UVR level in Spain, but in terms of exposure in percentage of ambient UVR, Spanish farmers actually received an exposure that was similar to that of the other groups of farmers. To make comparisons between countries independently of geographical factors, we used the received percentage of ambient UVR. When using this measure, differences in UVR exposure can be attributable to

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behavioural factors. Spanish farmers may therefore actually have a less sun-seeking attitude than farmers at higher latitudes and plan outdoor work in shaded areas, instead of in direct sunlight, or during hours of the day when UVR levels are relatively lower [20], and many Spanish farmers may take the traditional Mediterranean siesta around noon, which a recent study showed to apply to 60% of a Spanish cohort [36]. Our results also indicate that Spanish farmers spent less time outdoors on work days between 12 and 15 (Table 2). Nevertheless, Spanish farmers accumulated the highest UVR exposure over the study period, highlighting the impact of ambient UVR level on personal UVR exposure. The farmers exceeded the UVR exposure limits for the skin set by the ICNIRP (N1.3 SED) [1] for working days on 36% (DK, AT), 29% (PL) and 56% (ES) of their working days. In the present study, however, leisure time exposure was included on working days, which may overestimate the actual working time exposure. Since we measured UVR doses to the wrist, the corresponding doses to the vertex (top of head) will be twice as high [37], when the body is upright. The exposure of the Danish farmers was similar to that found in a previous study of Danish gardeners [20], while the exposure of the Austrian farmers was similar to that found in a previous study of Austrian farmers [7]. Correspondingly, our finding on the exposure of the Spanish farmers was similar to findings in previous studies of Spanish environmental agents [3] and gardeners [10] (Table 5). UVR exposure to the skin depends on clothing or sunscreen coverage, and the effect of exposure on the skin again depends on individual factors, such as constitutive and facultative skin protection ability [38]. In the present study, most farmers had skin types II–III, although a considerable part of the Spanish farmers had skin type IV (ES farmers' skin type significantly higher than DK farmers', p = 0.007). At the vertex, Spanish farmers would receive an estimated UVR exposure of 5.4 SED on working days, which would be enough to produce erythema in unprotected skin in most skin types I–III and even in skin type IV [31,39]. Spanish farmers must, however, be expected to build up a considerable amount of skin pigmentation (sunadapted skin) during the summer season, owing to the high chronic UVR exposure on working days, which actually helps prevent sunburn [38]. Also, farmers in general would be expected to cover their body with clothes during work, e.g., during harvesting, and, accordingly, we found that farmers had few days during the study period when they exposed a major part of the body to the sun (risk behaviour) (Table 1, mean number of risk days: 9–16, p N 0.05). Data on sunscreen use showed infrequent use of sunscreen during the summer period, but sunburn was not frequently reported by the farmers either, which may be explained by the factors mentioned above. Although sunburn was infrequent among the farmers, their high level of chronic UVR

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exposure on working days puts them at risk of skin cancer, and studies in Germany and Italy have also shown an increased risk of BCC and SCC for outdoor workers, including farmers [11,40]. Among Nordic farmers, however, a decreased risk of SCC has been found, while an increased risk of lip cancer has been found for male farmers [41]. The lowest daily UVR exposure was received by the Austrian farmers, despite the central European location (mid-latitude), and generally higher altitude. This shows that other factors can counterbalance the expected altitude effect on personal UVR exposure [22,24,25], for example individual factors, like posture and orientation, which have also previously been shown to account more than altitude on the variance of effective daily UVR exposure [8]. On days with risk behaviour, sunscreen use and beach visits, Danish farmers received the highest UVR exposure, also highest in percentage of ambient UVR, perhaps indicating a more sun-seeking attitude in northern Europe, where sunshine is relatively limited for a major part of the year. 4.2. Partners Spanish and Danish partners received the lowest daily UVR exposure, also on working days, which may be partly explained by type of occupation, since most had indoor occupations, e.g., teaching and nursing, while most Polish and Austrian partners were housewives or helpers at the farm, increasing the likelihood of outdoor activities. On days with risk behaviour, sunscreen use, beach visit, sunburns, partners at higher latitudes received a higher percentage of ambient UVR than the Spanish partners, which indicates a more sun-seeking behaviour for the northern partners. Although differences were found in specific situations, all partners accumulated similar UVR doses over the study period. 4.3. Children Contrary to what might be expected, the children of the most southern European countries (AT and ES) generally received the lowest UVR exposure and percentages of ambient UVR on a daily basis and on working days (school/day-care days), while the children of the most northern countries (PL and DK) received the highest. For Danish children, this is partly explained by more time spent outdoors, also during UVR peak hours (Table 4). On days with risk behaviour, sunscreen use, beach visit, and sunburns, Danish and Polish children also received a higher percentage of ambient UVR than the Austrian and Spanish children, again perhaps indicating a more sun-seeking behaviour for the northern children, who were also more frequently sunburned.

Table 5 UVR exposure of different outdoor workers in Europe. Occupation

Country

Time of year

Dosimeter

Selected body location

Daily SED

Strawberry production workers Environmental agents Construction workers Professional mountain guides Vineyard workers

Italy Spain Spain Germany/Alps Italy

Jan–Sept 2012 Jun–Aug 2012 Jul 2010 Jul 1999–Jun 2000 Apr 2005 Jul 2005 Oct 2005

Electronic Spore film Spore film Spore film Polysulphone

Farmers Building workers at various altitudes

Austria Switzerland

Apr–Oct 2006 Jul–Sept 2005

Electronic Spore film

0.48–1.24 (different activities) 2.6 7.41 6.6 10.3 14.5 5.9 10.0 2.0 3.0 2.99 11.9–28.6

Gardeners and lifeguards

Spain

Jun–Jul 2008

Spore film

Gardeners

Ireland Denmark

May–Aug 2001

Electronic

Forearm Wrist Shoulder Lateral side of head Left arm Back of neck Left arm Back of neck Left arm Back of neck Forehead Mean of forehead, neck, left and right shoulder Top of shoulder (gardeners) Wrist (lifeguards) Wrist

4.13 (gardeners) 11.43 (lifeguards) 0.97 (Irish) 1.6 (Danish)

Ref. 2 3 4 5 6

7 8 10 20

The daily UVR exposures of different outdoor workers are given in SEDs as reported in the respective studies. These studies have all used erythemally weighted personal dosimetry and report on the UVR exposure during working days.

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4.4. Limitations The Danish and Spanish farmers were all males, while many Polish and Austrian farmers were females. However, as we did not find a strong gender effect on farmers' UVR exposure after performing a subanalysis of Polish and Austrian farmers (data not shown here), we believe that the different family structures do not influence our results. Because of the complexity connected with participation in the study, recruiting participants was not easy, and differences in numbers of participants between countries (Table 1) may have introduced some uncertainty to our results. 4.5. Strengths The use of objective, personal, time-stamped UVR dosimetry for an entire summer period in combination with diary information to obtain data on personal UVR exposure provides much more detail and lower risk of recall bias than the use of retrospective questionnaires, the method most often used for assessment of personal UVR exposure [42]. We were able to conduct the study with identical protocols in four European countries covering different latitudes and altitudes, which gives important information about differences in personal UVR exposure between countries, factors that have not previously been examined. In conclusion, our results show that on 29% to 56% of their working days all farmers, irrespective of country, exceeded the UVR exposure limits set by the ICNIRP (N 1.3 SED) [1] (including leisure time exposure), which calls for attention to the issue of sun protection for outdoor workers across Europe in order to prevent UVR-induced skin cancer. Although ambient UVR has an impact on personal UVR exposure, our results indicate that behavioural factors also play an important role. Our results indicate a stronger sun-seeking attitude among farmers, partners and children at higher latitudes, which in combination with their lower level of sun sensitivity could put them at an increased risk of developing skin cancer. Future preventive campaigns could benefit from this information. Conflicts of Interest None declared. Acknowledgments The authors wish to thank all the study participants. Further thanks to: the companies Segura Viudas and Freixenet for their help with data collection in the Spanish study; Prof. Janusz W. Krzyscin from the Institute of Geophysics at the Polish Academy of Sciences for his help in providing Polish ambient UVR data; the Danish Meteorological Institute (DMI) and the Spanish Meteorological Agency (AEMET) for their help providing Danish and Spanish ambient UVR data; the Austrian UV monitoring network for help collecting Austrian ambient UVR data and the Austrian Meteorological Service (Zentralanstalt für Meteorologie und Geodynamik, ZAMG) for providing global radiation data. This study has received funding from the European Community's Seventh Framework Programme under grant agreement no.: 227020, under the project: The impact of climatic and environmental factors on personal ultraviolet radiation exposure and human health (ICEPURE). None of the funders were involved in the design, analysis or interpretation of this study. The research was also supported by the National Institute for Health Research (NIHR) BioResource at Guy's & St Thomas' NHS Foundation Trust and NIHR Biomedical Research Centre based at Guy's and St Thomas' NHS Foundation Trust and King's College London. The views expressed are those of the authors and not necessarily those of the NHS, the NIHR or the Department of Health. The research was also

supported by The Ministry of Science and Higher Education, Poland (grant agreement no. 1238/7.PR UE/2009/7). Payam Dadvand is funded by a Ramón y Cajal fellowship (RYC2012-10995) awarded by the Spanish Ministry of Economy and Competitiveness.

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