Introduction: Melanoma is considered a generally preventable cancer, with excessive ultraviolet radiation (UVR) exposure being a strong causal factor. UVR exposure following a melanoma diagnosis can be modified to reduce risk of second primary melanomas. The goal of this study was to compare measures of UVR exposure and protection behaviors between long-term melanoma survivors and controls.

Methods: Participants from a previously conducted case–control study were recruited for a cross-sectional survey. Melanoma cases were 25 to 59 years old at diagnosis; controls were age and sex matched. Participants were asked about UVR exposure and protection measures used in the past year, and comparisons between melanoma survivors and controls were conducted using logistic regression models, adjusting for potential confounders.

Results: A total of 724 (62.0%) long-term melanoma survivors and 660 (59.9%) controls completed the follow-up survey. Melanoma survivors were significantly less likely to report high sun exposure on a typical weekday [OR, 0.72 (0.55–0.94)], sunburns [OR, 0.40 (0.30–0.53)], or indoor tanning [OR, 0.20 (0.09–0.44)] than controls; however, high sun exposure on a typical weekend day was similar. Report of optimal sun protection behaviors was higher in melanoma survivors compared with controls. However, a few melanoma survivors reported indoor tanning, 10% reported intentionally seeking sun to tan, and 20% reported sunburns.

Conclusions: Although long-term melanoma survivors reported healthier UVR exposure and protection behaviors compared with controls, a sizeable proportion still reported elevated sun exposure, sunburns, and suboptimal UVR protection behaviors.

Impact: Opportunities remain for improving sun protection to reduce future melanoma risk among melanoma survivors. Cancer Epidemiol Biomarkers Prev; 26(4); 607–13. ©2017 AACR.

This article is featured in Highlights of This Issue, p. 441

Melanoma is considered a generally preventable cancer, with excessive ultraviolet radiation (UVR) exposure being one of the strongest risk factors for the disease (1, 2). Additional risk factors include a large number of moles and/or freckles, fair skin, light hair or eye color, family history of melanoma, and immune suppression (3). Patients diagnosed with melanoma experience high rates of recurrence with an approximately 9-fold increased risk of developing another melanoma (4). Excess risk of recurrence remains 20 years after the initial diagnosis (4, 5). For melanomas that develop as a consequence of UVR exposure, the damage done to the skin prior to the first melanoma cannot be ameliorated, and this damage may increase risk of a subsequent melanoma. Importantly, however, UVR exposure following a melanoma diagnosis can be modified to reduce risk of a new melanoma diagnosis (6).

It has been suggested that cancer may be a “teachable moment” for health behavior change (7). Unfortunately, while some cancer survivors initiate positive health behaviors, others do not (8). In the case of melanoma, reduction of sun exposure is paramount. Individuals are advised to limit time in the sun during peak hours, seek shade, wear protective clothing, use sunscreen, and avoid indoor tanning devices (9).

The young age at diagnosis of melanoma for some suggests ample opportunity to engage in improved sun protection behaviors following diagnosis. Little research has documented UVR exposure among melanoma survivors. Results from studies to date on sun protection behaviors among melanoma survivors have been mixed, though most suggest that if an improvement in sun behaviors among melanoma survivors is present, it is moderate (10, 11). Further clarification of these behaviors in long-term melanoma survivors is needed to help devise effective interventions for this group. In particular, data are lacking on sun exposure patterns and specific sun protection behaviors compared with an appropriately matched control group with measured potential confounders. The objective of this study was to compare measures of UVR exposure and protection behaviors between long-term melanoma survivors and controls.

Study design and population

Approval for this study was granted by the University of Minnesota Institutional Review Board and the Minnesota Cancer Surveillance System. We recruited participants from the Skin Health Study, a population-based case–control study conducted from 2004 to 2009 designed to assess indoor tanning use and risk of melanoma. The Skin Health Study is described elsewhere (12). Briefly, cases in the Skin Health Study were ascertained by the Minnesota Cancer Surveillance System, a population-based, statewide cancer registry. Individuals with invasive cutaneous melanoma diagnosed between July 2004 and December 2007, between the ages of 25 and 59, with a state driver's license or state identification card, were eligible to participate. Controls were randomly selected from the Minnesota state driver's license list (which included persons with state identification cards) and frequency-matched to cases in a 1:1 ratio on age (in 5-year age groups) and sex. Eligible cases and controls were required to be English-speaking and to have a telephone number. A total of 1,167 cases (84.6% among eligible) and 1,101 controls (69.2% among eligible) participated in the original study.

Recruitment and data collection

All Skin Health Study participants who were alive at the time of the survey administration were identified for this follow-up study. Deaths among cases and controls were identified using the Minnesota Death Index and the Minnesota Cancer Surveillance System. Cause of death was ascertained whenever possible. The Minnesota Cancer Surveillance System required updated permission from the physician of record in the registry before re-contacting each person with melanoma (case).

Participants were recruited by mail to complete an online or paper survey using methods outlined by Dillman to maximize response (13). We recruited potential participants by sending an initial letter with a link to the online survey, programmed using REDCap (14), along with an incentive (two $2 bills). Three additional reminder letters and a paper copy of the survey were sent to nonresponders.

Survey measures

The primary outcomes for this follow-up study were self-reported sun exposure and protection measures. The validated questionnaire included nine items related to sun exposure and protection practices (15, 16). All items had categorical responses. Two questions asked about number of hours outside per day between 10 am and 4 pm in the summer separately for weekdays and weekend days using the following categories: 0 to 30 minutes, 31 minutes to 1 hour, 2, hours, 3 hours, 4 hours, 5 hours, or 6 hours. Participants were also asked to report the number of red or painful sunburns that lasted a day or more in the past year: 0, 1, 2, 3, 4, or 5 or more. Sun protection methods utilized during the summer on a warm sunny day, including wearing sunscreen, a shirt with sleeves, or a hat with a wide brim, staying in the shade, and spending time in the sun in order to get a tan (intentional tanning), were collected using the following categories: never, rarely, sometimes, often, or always. The final question asked whether the participant had used a tanning bed or booth in the past 12 months (yes, no). For the purposes of this analysis and ease of interpretation, all measures were dichotomized into “optimal” and “suboptimal” categories. The following were considered optimal: weekday sun exposure in the summer of 1 hour or less, weekend day sun exposure in the summer of 1 hour or less, no sunburns in the past year, no indoor tanning in the past year, and reporting often or always using sunscreen, often or always wearing a shirt with sleeves, often or always wearing a hat, often or always staying in the shade, and rarely or never intentionally tanning.

Potential confounders collected at the time of the original study included self-report of skin, hair, and eye color, and presence and pattern of freckles and moles. Indoor tanning and sun exposure, history and number of painful sunburns before and after age 18, and sun protection behaviors, including sunscreen use, were collected during a telephone interview. A phenotypic risk score was calculated based on hair and eye color, and tanning ability using a previously reported measure (17). Potential confounders collected at the time of the follow-up survey included education, income, smoking status, personal history of other skin cancer, and family history of melanoma.

Statistical methods

To assess how death and nonresponse may have biased the results, comparisons were made between those eligible and ineligible for the study and between those who did and did not participate in the follow-up survey using data from the original Skin Health Study.

Demographic, general health characteristics, and prediagnosis sun exposure and protection behaviors were compared between melanoma survivors and population controls that completed the survey using χ2 tests for categorical data and t tests and Wilcoxon Rank Sum tests as appropriate for continuous data.

Primary analyses compared optimal UVR exposure and protection behaviors between melanoma survivors and population controls. Controls who reported a personal history of melanoma at the time of the follow-up study (N = 21) were excluded from the analysis. Initial comparisons between melanoma survivors and population controls for all categories were conducted using χ2 tests. Multivariate logistic regression models, both sex and age-adjusted, and fully-adjusted, were conducted, and ORs and 95% confidence intervals (CI) for each outcome are presented. Confounding variables were defined a priori and included age (continuous), sex, education (high school, vocation/associates, some college, college graduate, graduate/professional degree), income (<$50,000, $50,000–$74,999, $75,000–$149,999, $150,000+, prefer not to say), current smoking status, phenotypic risk score (low, intermediate, high), freckles (none/few/some/many), moles (none/few/some/many), personal history of other skin cancer, family history of melanoma, and sun exposure data reported prior to diagnosis (lifetime sun exposure, outdoor activity sun exposure, mean sunscreen use, and number of sunburns).

To explore whether differences in optimal UVR exposure and sun protection behaviors between melanoma survivors and controls differed according to age or sex, stratified analyses were conducted within age groups (30–49, 50–59, 60–72 years) and by sex. Analyses were fully adjusted for all confounders, as previously described, and an interaction effect was included to examine whether a statistically significant interaction between melanoma status and age or sex was present. P values <0.05 were considered statistically significant.

Among cases and controls from the Skin Health Study, 724 (62.0%) melanoma survivors and 660 (59.9%) controls completed the follow-up survey (Table 1). A total of 80 cases died during the follow-up period; the cause of death was available for 73, and 54 died of melanoma. A total of 15 controls died during the follow-up period; the cause of death was available for 10 and none died of melanoma. Those who completed the survey were generally similar to those who did not respond, though they were older, more likely to have completed college, and less likely to have ever used indoor tanning. When examined separately for melanoma survivors and controls, these differences were similar. Melanoma survivors and controls were not statistically significantly different across the demographic and health characteristics with the exceptions of race and smoking status (Table 2). However, melanoma survivors were more likely than controls to have a high phenotypic risk score (P < 0.0001), some to many freckles (P < 0.0001), some to many moles (P < 0.0001), use indoor tanning before their diagnosis (P < 0.0001), and report more lifetime sunburns prior to their diagnosis (P < 0.0001).

Table 1.

Final study recruitment

Cases (N = 1,167)Controls (N = 1,101)
N (%)N (%)
Not eligible 
 Previous refusal for future contact 0 (0.0) 7 (0.6) 
 Physician refusal 17 (1.5) 0 (0.0) 
 Deceased 80 (6.8) 15 (1.4) 
Eligible 
 Unable to locate 59 (5.1) 87 (7.9) 
 Refusal 8 (0.7) 18 (1.6) 
 Nonresponse 279 (23.9) 314 (28.5) 
 Survey complete 724 (62.0) 660a (59.9) 
Cases (N = 1,167)Controls (N = 1,101)
N (%)N (%)
Not eligible 
 Previous refusal for future contact 0 (0.0) 7 (0.6) 
 Physician refusal 17 (1.5) 0 (0.0) 
 Deceased 80 (6.8) 15 (1.4) 
Eligible 
 Unable to locate 59 (5.1) 87 (7.9) 
 Refusal 8 (0.7) 18 (1.6) 
 Nonresponse 279 (23.9) 314 (28.5) 
 Survey complete 724 (62.0) 660a (59.9) 

a21 controls with personal history of melanoma excluded from analyses.

Table 2.

Demographic and general health characteristics among melanoma survivors and population controls that completed the follow-up survey

Melanoma survivors (N = 724)Population controls (N = 639)
VariableN (%)N (%)P value
Age at survey   0.98 
 30–39 49 (6.8) 46 (7.2)  
 40–49 117 (16.2) 100 (15.7)  
 50–59 263 (36.3) 234 (36.6)  
 60–72 295 (40.8) 259 (40.5)  
Sex   0.91 
 Female 433 (59.8) 384 (60.1)  
 Male 291 (40.2) 255 (39.9)  
Race   0.0001 
 White, non-Hispanic 718 (99.2) 614 (96.1)  
 Other 6 (0.8) 25 (3.9)  
Education   0.34 
 High school 92 (13.2) 78 (12.4)  
 Vocational/associates 127 (18.3) 141 (22.4)  
 Some college 116 (16.7) 90 (14.3)  
 College graduate 215 (30.9) 185 (29.3)  
 Graduate/professional degree 146 (21.0) 137 (21.7)  
Missing 28 8  
Marital status   0.81 
 Never married 38 (5.5) 37 (5.9)  
 Married/partnered 578 (83.4) 516 (81.5)  
 Widowed 15 (2.2) 14 (2.2)  
 Divorced 62 (9.0) 66 (10.4)  
Missing 31 6  
Income   0.34 
 <$50,000 102 (14.7) 104 (16.5)  
 $50,000–$74,999 126 (18.2) 118 (18.7)  
 $75,000–$149,999 278 (40.1) 235 (37.2)  
 $150,000+ 129 (18.6) 104 (16.5)  
 Prefer not to say 59 (8.5) 70 (11.1)  
Missing 30 8  
Body mass index   0.95 
 Underweight (<18.5 kg/m24 (0.6) 3 (0.5)  
 Normal (18.5–24.9 kg/m2267 (36.9) 242 (37.9)  
 Overweight (25.0–29.9 kg/m2244 (33.7) 218 (34.1)  
 Obese (30.0+ kg/m2209 (28.9) 176 (27.5)  
Current smoker   0.04 
 No 680 (94.4) 582 (91.7)  
 Yes 40 (5.6) 53 (8.4)  
Missing 4 4  
Phenotypic risk index   <0.0001 
 Low 196 (27.3) 236 (37.1)  
 Intermediate 308 (42.9) 279 (43.9)  
 High 214 (29.8) 121 (19.0)  
Missing 6 3  
Freckles   <0.0001 
 None 340 (47.2) 363 (57.0)  
 Very few 193 (26.8) 171 (27.3)  
 Few 131 (18.2) 70 (11.0)  
 Some 47 (6.5) 22 (3.5)  
 Many 9 (1.3) 8 (1.3)  
Missing 4 2  
Moles   <0.0001 
 None 107 (14.9) 243 (38.2)  
 Few 405 (56.5) 336 (52.8)  
 Some 157 (21.9) 51 (8.0)  
 Many 48 (6.7) 6 (0.9)  
Missing 7   
Personal history of nonmelanoma skin cancer   0.77 
 No 674 (95.2) 600 (95.5)  
 Yes 34 (4.8) 28 (4.5)  
Missing 16 11  
Family history of melanoma   0.59 
 No 506 (69.9) 438 (68.5)  
 Yes 218 (30.1) 201 (31.5)  
Measures from Original Study 
Indoor tanning use prior to diagnosis/reference   <0.0001 
 No 277 (38.3) 313 (49.0)  
 Yes 447 (61.7) 326 (51.0)  
Sun exposure—before diagnosis, mean ± SD 723 (2,589 ± 1,739) 637 (2,749 ± 1,739) 0.09 
Outdoor activity exposure—before diagnosis, mean ± SD 723 (2,076 ± 2,495) 639 (2,097 ± 1,701) 0.85 
Mean sunscreen use—before diagnosis, mean ± SD 724 (1.37±1.01) 639 (1.32±1.03) 0.30 
Lifetime sunburns—before diagnosis, median (min, max) 722 [9 (0–400)] 637 [6 (0–250)] <0.0001 
Melanoma survivors (N = 724)Population controls (N = 639)
VariableN (%)N (%)P value
Age at survey   0.98 
 30–39 49 (6.8) 46 (7.2)  
 40–49 117 (16.2) 100 (15.7)  
 50–59 263 (36.3) 234 (36.6)  
 60–72 295 (40.8) 259 (40.5)  
Sex   0.91 
 Female 433 (59.8) 384 (60.1)  
 Male 291 (40.2) 255 (39.9)  
Race   0.0001 
 White, non-Hispanic 718 (99.2) 614 (96.1)  
 Other 6 (0.8) 25 (3.9)  
Education   0.34 
 High school 92 (13.2) 78 (12.4)  
 Vocational/associates 127 (18.3) 141 (22.4)  
 Some college 116 (16.7) 90 (14.3)  
 College graduate 215 (30.9) 185 (29.3)  
 Graduate/professional degree 146 (21.0) 137 (21.7)  
Missing 28 8  
Marital status   0.81 
 Never married 38 (5.5) 37 (5.9)  
 Married/partnered 578 (83.4) 516 (81.5)  
 Widowed 15 (2.2) 14 (2.2)  
 Divorced 62 (9.0) 66 (10.4)  
Missing 31 6  
Income   0.34 
 <$50,000 102 (14.7) 104 (16.5)  
 $50,000–$74,999 126 (18.2) 118 (18.7)  
 $75,000–$149,999 278 (40.1) 235 (37.2)  
 $150,000+ 129 (18.6) 104 (16.5)  
 Prefer not to say 59 (8.5) 70 (11.1)  
Missing 30 8  
Body mass index   0.95 
 Underweight (<18.5 kg/m24 (0.6) 3 (0.5)  
 Normal (18.5–24.9 kg/m2267 (36.9) 242 (37.9)  
 Overweight (25.0–29.9 kg/m2244 (33.7) 218 (34.1)  
 Obese (30.0+ kg/m2209 (28.9) 176 (27.5)  
Current smoker   0.04 
 No 680 (94.4) 582 (91.7)  
 Yes 40 (5.6) 53 (8.4)  
Missing 4 4  
Phenotypic risk index   <0.0001 
 Low 196 (27.3) 236 (37.1)  
 Intermediate 308 (42.9) 279 (43.9)  
 High 214 (29.8) 121 (19.0)  
Missing 6 3  
Freckles   <0.0001 
 None 340 (47.2) 363 (57.0)  
 Very few 193 (26.8) 171 (27.3)  
 Few 131 (18.2) 70 (11.0)  
 Some 47 (6.5) 22 (3.5)  
 Many 9 (1.3) 8 (1.3)  
Missing 4 2  
Moles   <0.0001 
 None 107 (14.9) 243 (38.2)  
 Few 405 (56.5) 336 (52.8)  
 Some 157 (21.9) 51 (8.0)  
 Many 48 (6.7) 6 (0.9)  
Missing 7   
Personal history of nonmelanoma skin cancer   0.77 
 No 674 (95.2) 600 (95.5)  
 Yes 34 (4.8) 28 (4.5)  
Missing 16 11  
Family history of melanoma   0.59 
 No 506 (69.9) 438 (68.5)  
 Yes 218 (30.1) 201 (31.5)  
Measures from Original Study 
Indoor tanning use prior to diagnosis/reference   <0.0001 
 No 277 (38.3) 313 (49.0)  
 Yes 447 (61.7) 326 (51.0)  
Sun exposure—before diagnosis, mean ± SD 723 (2,589 ± 1,739) 637 (2,749 ± 1,739) 0.09 
Outdoor activity exposure—before diagnosis, mean ± SD 723 (2,076 ± 2,495) 639 (2,097 ± 1,701) 0.85 
Mean sunscreen use—before diagnosis, mean ± SD 724 (1.37±1.01) 639 (1.32±1.03) 0.30 
Lifetime sunburns—before diagnosis, median (min, max) 722 [9 (0–400)] 637 [6 (0–250)] <0.0001 

Melanoma survivors were diagnosed an average of 9.6 ± 1.0 years prior to completing the survey; the majority (85.6%) had stage I disease, 6.4% had stage II disease, 6.6% had stage III disease, and 1.4% had stage IV disease. The most common site was the trunk (35.0%), followed by legs (26.9%), arms (26.4%), and head/neck (11.7%). Almost all (99.3%) had surgery and about one-third had lymph node dissection (34.8%).

Compared with controls, survivors were statistically significantly more likely to report optimal exposure behaviors with the exception of sun exposure on weekend days in the summer (Table 3). Specifically, survivors were less likely to spend more than 1 hour outside on weekdays during the summer (34.3% vs. 44.4%, P = 0.01), less likely to report a sunburn in the past year (19.5% vs. 36.5%, P < 0.0001), less likely to have indoor tanned in the past year (1.7% vs. 6.8%, P < 0.0001), and less likely to intentionally tan (10.4% vs. 23.2%, P < 0.0001) than controls. Of note, however, the proportion of melanoma survivors who reported spending more than 1 hour in the sun on a typical weekend day in the summer was similar to controls.

Table 3.

Sun exposure compared between melanoma survivors and nonmelanoma controls

Melanoma survivorsNonmelanoma controlsSex- and age-adjustedFully adjusteda
N (%)N (%)OR (95% CI)P valueOR (95% CI)P value
Hours outside in summer on weekdays    <0.0001  0.01 
 1 hour or less 473 (65.7) 350 (55.6) 1.00  1.00  
 2 hours or more 247 (34.3) 280 (44.4) 0.63 (0.51–0.80)  0.72 (0.55–0.94)  
Hours outside in summer on weekend days    0.04  0.37 
 1 hour or less 181 (25.2) 128 (20.3) 1.00  1.00  
 2 hours or more 538 (74.8) 502 (79.7) 0.76 (0.58–0.99)  0.87 (0.65–1.18)  
Number of sunburns in past 12 months    <0.0001  <0.0001 
 None 581 (80.5) 401 (63.6) 1.00  1.00  
 1 or more 141 (19.5) 230 (36.5) 0.40 (0.31–0.52)  0.40 (0.30–0.53)  
Use of tanning bed in past 12 months    <0.0001  <0.0001 
 No 709 (98.3) 593 (93.2) 1.00  1.00  
 Yes 12 (1.7) 43 (6.8) 0.23 (0.12–0.45)  0.20 (0.09–0.44)  
Spend time in the sun to get a tan    <0.0001  <0.0001 
 Sometimes/often/always 75 (10.4) 147 (23.2) 1.00  1.00  
 Rarely/never 645 (89.6) 488 (76.9) 2.81 (2.05–3.86)  2.88 (2.00–4.13)  
Melanoma survivorsNonmelanoma controlsSex- and age-adjustedFully adjusteda
N (%)N (%)OR (95% CI)P valueOR (95% CI)P value
Hours outside in summer on weekdays    <0.0001  0.01 
 1 hour or less 473 (65.7) 350 (55.6) 1.00  1.00  
 2 hours or more 247 (34.3) 280 (44.4) 0.63 (0.51–0.80)  0.72 (0.55–0.94)  
Hours outside in summer on weekend days    0.04  0.37 
 1 hour or less 181 (25.2) 128 (20.3) 1.00  1.00  
 2 hours or more 538 (74.8) 502 (79.7) 0.76 (0.58–0.99)  0.87 (0.65–1.18)  
Number of sunburns in past 12 months    <0.0001  <0.0001 
 None 581 (80.5) 401 (63.6) 1.00  1.00  
 1 or more 141 (19.5) 230 (36.5) 0.40 (0.31–0.52)  0.40 (0.30–0.53)  
Use of tanning bed in past 12 months    <0.0001  <0.0001 
 No 709 (98.3) 593 (93.2) 1.00  1.00  
 Yes 12 (1.7) 43 (6.8) 0.23 (0.12–0.45)  0.20 (0.09–0.44)  
Spend time in the sun to get a tan    <0.0001  <0.0001 
 Sometimes/often/always 75 (10.4) 147 (23.2) 1.00  1.00  
 Rarely/never 645 (89.6) 488 (76.9) 2.81 (2.05–3.86)  2.88 (2.00–4.13)  

aAdjusted for sex, age, education, income, smoking status, phenotypic risk group, freckles, moles, personal history of other skin cancer, family history of melanoma, and lifetime sun exposure, outdoor activities, mean sunscreen, and sunburns reported prior to diagnosis or reference date.

In addition, melanoma survivors compared with controls were more likely to report often or always engaging in sun protection behaviors, including wearing sunscreen (61.9% vs. 38.4%, P < 0.0001), a shirt with sleeves (77.0% vs. 65.9%, P < 0.0001), and a hat (33.2% vs. 22.6%, P = 0.01); survivors were also more likely to stay in the shade in the summer (48.1% vs. 28.7%, P < 0.0001; Table 4). These comparisons were similar when stratified by weekday and weekend sun exposure (data not shown).

Table 4.

Sun protection behaviors compared between melanoma survivors and nonmelanoma controls

Melanoma survivorsNonmelanoma controlsSex- and age-adjustedFully adjusteda
N (%)N (%)OR (95% CI)P valueOR (95% CI)P value
When outside in the summer on a warm sunny day, how often do you… 
Wear sunscreen    <0.0001  <0.0001 
 Never/rarely/sometimes 275 (38.1) 391 (61.6) 1.00  1.00  
 Often/always 446 (61.9) 244 (38.4) 2.89 (2.29–3.65)  3.31 (2.48–4.41)  
Wear a shirt with sleeves    <0.0001  <0.0001 
 Never/rarely/sometimes 165 (23.0) 216 (34.1) 1.00  1.00  
 Often/always 553 (77.0) 418 (65.9) 1.83 (1.41–2.37)  1.87 (1.40–2.51)  
Wear a hat with brim    <0.0001  0.01 
 Never/rarely/sometimes 480 (66.8) 489 (77.4) 1.00  1.00  
 Often/always 239 (33.2) 143 (22.6) 1.72 (1.34–2.21)  1.44 (1.09–1.90)  
Stay in the shade    <0.0001  <0.0001 
 Never/rarely/sometimes 372 (51.9) 453 (71.3) 1.00  1.00  
 Often/always 345 (48.1) 182 (28.7) 2.38 (1.89–3.00)  1.99 (1.54–2.57)  
Melanoma survivorsNonmelanoma controlsSex- and age-adjustedFully adjusteda
N (%)N (%)OR (95% CI)P valueOR (95% CI)P value
When outside in the summer on a warm sunny day, how often do you… 
Wear sunscreen    <0.0001  <0.0001 
 Never/rarely/sometimes 275 (38.1) 391 (61.6) 1.00  1.00  
 Often/always 446 (61.9) 244 (38.4) 2.89 (2.29–3.65)  3.31 (2.48–4.41)  
Wear a shirt with sleeves    <0.0001  <0.0001 
 Never/rarely/sometimes 165 (23.0) 216 (34.1) 1.00  1.00  
 Often/always 553 (77.0) 418 (65.9) 1.83 (1.41–2.37)  1.87 (1.40–2.51)  
Wear a hat with brim    <0.0001  0.01 
 Never/rarely/sometimes 480 (66.8) 489 (77.4) 1.00  1.00  
 Often/always 239 (33.2) 143 (22.6) 1.72 (1.34–2.21)  1.44 (1.09–1.90)  
Stay in the shade    <0.0001  <0.0001 
 Never/rarely/sometimes 372 (51.9) 453 (71.3) 1.00  1.00  
 Often/always 345 (48.1) 182 (28.7) 2.38 (1.89–3.00)  1.99 (1.54–2.57)  

aAdjusted for sex, age, education, income, smoking status, phenotypic risk group, freckles, moles, personal history of other skin cancer, family history of melanoma, and lifetime sun exposure, outdoor activities, mean sunscreen, and sunburns reported prior to diagnosis or reference date.

Results from the comparison of optimal UVR exposure and sun protection behaviors between melanoma survivors and controls by age group were similar to the overall comparison with the exception of hours spent in the sun on weekend days. The oldest melanoma survivors were more likely to avoid sun exposure on weekend days compared with controls, whereas those 30 to 49 and 50 to 59 years old reported similar sun exposure on weekend days compared with controls. While males and females differed in their sun exposure and protection behaviors, the stratified comparisons by sex between melanoma survivors and controls were similar to the overall comparisons in direction and magnitude of the associations.

This follow-up study of participants in a case-control of melanoma is the largest to date to report UVR exposure and protection behaviors of long-term melanoma survivors compared with a control group. Our study provides a more complete picture of the UVR exposure and protection habits of melanoma survivors as compared with a similarly recruited population control group than previous research. Consistent with other health behaviors reported by cancer survivors (18) and a recent meta-analysis of the limited available literature among melanoma survivors (19), our study indicates long-term melanoma survivors report healthier UVR exposure and protection behaviors compared with controls. Despite this, opportunities remain to reduce future melanoma risk among melanoma survivors as a significant proportion still report elevated sun exposure, sunburns, and suboptimal sun protection behaviors.

Exposure to UVR is a significant and modifiable risk factor for melanoma, with intermittent exposure and sunburns identified as the main causes (20). While debate continues about the best sun protection methods for skin cancer prevention (21), UVR avoidance, including from sun and artificial sources, is crucial. Few studies report UVR exposure among melanoma survivors, with most focusing on frequency of sunbathing or indoor tanning as opposed to time spent in the sun. Consistent with our results, a recent qualitative study reported many melanoma survivors are more conscious of sun exposure and protection (22). However, melanoma survivors in our study reported being outside more than 1 hour on weekend days during peak hours in the summer at similar levels as controls. One possible explanation for this is that this study included long-term melanoma survivors. A small prospective study of melanoma survivors and controls found that UVR exposure was initially lower among survivors compared with controls but then converged over the 3-year study (23, 24).

We found that few melanoma survivors and controls reported indoor tanning in the past year. This may be explained by the fact that this study population is now older and therefore less likely to use indoor tanning, and prevalence of indoor tanning has declined over time (25). While long-term melanoma survivors were less likely to report indoor tanning in the past year than controls, a small number of survivors reported still engaging in this behavior. This phenomenon has been reported elsewhere (26, 27) and indicates a small proportion of individuals will continue this high-risk behavior despite a melanoma diagnosis.

Sunburn is a critical measure of excessive sun exposure. A meta-analysis found increased risk of melanoma with increasing sunburns throughout the lifetime, not just sunburns obtained during childhood (28), emphasizing the importance of continued and improved sunburn prevention among melanoma survivors. Few studies have reported sunburn occurrence among melanoma survivors, however. A large international online survey had a subgroup of participants who reported a previous melanoma diagnosis, and 27% of those cases reported at least one severe sunburn in the past year (29); that percentage is similar to our result of 20%. While our study indicates melanoma survivors are about half as likely to report sunburn in the previous year compared with controls, a significant minority engage in behaviors that result in sunburns.

A number of studies have reported sunscreen use among melanoma survivors (10, 11, 27, 30–33); however, a review found that general population estimates of regular sunscreen use vary greatly in the literature (7%–90%; ref. 34); therefore, it is critical to simultaneously collect data on population controls for comparison. Few studies have included a control group (23, 24, 26, 35); the largest to date compared 156 melanoma survivors with 11,408 respondents without cancer who participated in 2005 and 2007 National Cancer Institute Health Information National Trends Surveys (HINTS; 26). Notably, the results were similar to our study, though HINTS respondents reported slightly lower frequencies of sunscreen use.

Wearing UVR protective clothing and staying in the shade during peak hours are recommended as important components of proper sun protection. A few studies have reported increases in sun-protection behaviors among melanoma patients following diagnosis (30, 32, 36). Studies of melanoma survivors alone, one of which included longer-term survivors, found modest sun protection behaviors similar to our results (10, 11). In comparison to non-cancer controls, two studies found that melanoma survivors use sunscreen and seek shade more frequently than controls (26, 29), whereas another study found sun protection behaviors were similar to general population estimates (10). As found previously, these differences were modest, however, with more than half reporting they do not wear a hat or stay in the shade during peak hours.

While this study has many strengths, including the large sample size, population-based sample, and inclusion of a control group with measured confounding factors, we note important limitations. As with other self-reported measures, participants may have over-reported behaviors due to social desirability, particularly among melanoma survivors, resulting in an overestimate of sun protection behaviors leading to potential bias. The self-report measures used have been previously shown to compare well with direct observation measures, however (16). We were unable to make comparisons with the sun exposure and protection data prior to the diagnosis due to differences in measures. Another limitation is that survivors who responded to our survey may be more likely to practice health behaviors, or those who are still alive may be those who frequently use optimal sun protection behaviors. Further, unfortunately, we do not have access to the information on second primary melanomas for all participants and therefore were unable to address that outcome.

Despite limitations, this study contributes to the field as the largest to date to examine the sun exposure and protection behaviors of long-term melanoma survivors as compared with similarly recruited controls. While a melanoma diagnosis may serve as a trigger for behavior change for many, resulting in better sun protection among survivors compared with controls, one-fifth of survivors experienced sunburn in the past year and many reported engaging in suboptimal sun protection behaviors. These data suggest that interventions are needed to further improve sun behaviors and reduce future risk of skin cancer in this population.

No potential conflicts of interest were disclosed.

Conception and design: R.I. Vogel, A.H. Blaes, D. Lazovich

Development of methodology: R.I. Vogel, L.G. Strayer, K.E. Anderson, D. Lazovich

Acquisition of data (provided animals, acquired and managed patients, provided facilities, etc.): R.I. Vogel, L.G. Strayer, L. Engelman, K.E. Anderson, D. Lazovich

Analysis and interpretation of data (e.g., statistical analysis, biostatistics, computational analysis): R.I. Vogel, A.H. Blaes, K.E. Anderson, D. Lazovich

Writing, review, and/or revision of the manuscript: R.I. Vogel, L.G. Strayer, L. Engelman, H.H. Nelson, A.H. Blaes, K.E. Anderson, D. Lazovich

Administrative, technical, or material support (i.e., reporting or organizing data, constructing databases): L.G. Strayer, D. Lazovich

Study supervision: D. Lazovich

This study was funded by a grant from the Masonic Cancer Center of the University of Minnesota's Internal Grants Program to D. Lazovich, National Cancer Institute NIH grant P30 CA77598 (Principal Investigator: D. Yee) utilizing the Biostatistics and Bioinformatics Core shared resource of the Masonic Cancer Center to R.I. Vogel, and University of Minnesota and Award Number UL1TR000114 (Principal Investigator: B. Blazar) from the National Center for Advancing Translational Sciences (NCATS) of the NIH to R.I. Vogel.

The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked advertisement in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

1.
Gilchrest
BA
,
Eller
MS
,
Geller
AC
,
Yaar
M
. 
The pathogenesis of melanoma induced by ultraviolet radiation
.
N Engl J Med
1999
;
340
:
1341
8
.
2.
Narayanan
DL
,
Saladi
RN
,
Fox
JL
. 
Ultraviolet radiation and skin cancer
.
Int J Dermatol
2010
;
49
:
978
86
.
3.
National Cancer Institute (U.S.). What You Need to Know About Melanoma and Other Skin Cancers. Bethesda, MD: U.S. Department of Health and Human Services, National Institutes of Health, National Cancer Institute, 2010
.
Available at
http://www.cancer.gov/cancertopics/wyntk/skin.pdf.
4.
Bradford
PT
,
Freedman
DM
,
Goldstein
AM
,
Tucker
MA
. 
Increased risk of second primary cancers after a diagnosis of melanoma
.
Arch Dermatol
2010
;
146
:
265
72
.
5.
Freedman
M
,
Miller
BA
,
Tucker
MA
. 
New malignancies following melanoma of the skin, eye melanoma, and non-melanoma eye cancer
.
In
:
Curtis
RE
,
Freedman
DM
,
Ron
E
, et al
editors
.
New malignancies among cancer survivors: SEER Cancer Registries, 1973–2000
.
Bethesda, MD:
National Cancer Institute
; 
2006
.
6.
Kricker
A
,
Armstrong
BK
,
Goumas
C
,
Litchfield
M
,
Begg
CB
,
Hummer
AJ
, et al
Ambient UV, personal sun exposure and risk of multiple primary melanomas
.
Cancer Causes Control
2007
;
18
:
295
304
.
7.
Pinto
BM
,
Eakin
E
,
Maruyama
NC
. 
Health behavior changes after a cancer diagnosis: what do we know and where do we go from here?
Ann Behav Med
2000
;
22
:
38
52
.
8.
Demark-Wahnefried
W
,
Aziz
NM
,
Rowland
JH
,
Pinto
BM
. 
Riding the crest of the teachable moment: promoting long-term health after the diagnosis of cancer
.
J Clin Oncol
2005
;
23
:
5814
30
.
9.
American Cancer Society
.
Cancer facts & figures 2012
.
Atlanta, GA:
American Cancer Society
; 
2012
.
10.
Mujumdar
UJ
,
Hay
JL
,
Monroe-Hinds
YC
,
Hummer
AJ
,
Begg
CB
,
Wilcox
HB
,
Oliveria
SA
,
Berwick
M
. 
Sun protection and skin self-examination in melanoma survivors
.
Psychooncology
2009
;
18
:
1106
15
.
11.
Bowen
D
,
Jabson
J
,
Haddock
N
,
Hay
J
,
Edwards
K
. 
Skin care behaviors among melanoma survivors
.
Psycho-Oncology
2012
;
21
:
1285
91
.
12.
Lazovich
D
,
Vogel
RI
,
Berwick
M
,
Weinstock
MA
,
Anderson
KE
,
Warshaw
EM
. 
Indoor tanning and risk of melanoma: a case-control study in a highly exposed population
.
Cancer Epidemiol Biomarkers Prev
2010
;
19
:
1557
68
.
13.
Dillman
D
,
Smith
J
,
Christian
L
.
Internet, phone, mail, mixed-mode surveys: the tailored design method
.
Hoboken, NJ. Wiley
; 
2014
.
14.
Harris
PA
,
Taylor
R
,
Thielke
R
,
Payne
J
,
Gonzalez
N
,
Conde
JG
. 
Research electronic data capture (REDCap) - A metadata-driven methology and workflow process for providing translational research informatics support
.
J Biomed Inform
2009
;
42
:
377
81
.
15.
Glanz
K
,
Yaroch
AL
,
Dancel
M
,
Saraiya
M
,
Crane
LA
,
Buller
DB
, et al
Measures of sun exposure and sun protection practices for behavioral and epidemiologic research
.
Arch Dermatol
2008
;
144
:
217
22
.
16.
Glanz
K
,
McCarty
F
,
Nehl
EJ
,
O'Riordan
DL
,
Gies
P
,
Bundy
L
, et al
Validity of self-reported sunscreen use by parents, children, and lifeguards
.
Am J Prev Med
2009
;
36
:
63
9
.
17.
Thomas
NE
,
Kanetsky
PA
,
Edmiston
SN
,
Alexander
A
,
Begg
CB
,
Groben
PA
, et al
Relationship between germline MC1R variants and BRAF-mutant melanoma in a North Carolina population-based study
.
J Invest Dermatol
2010
;
130
:
1463
5
.
18.
Rock
CL
,
Doyle
C
,
Demark-Wahnefried
W
,
Meyerhardt
J
,
Courneya
KS
,
Schwartz
AL
, et al
Nutrition and physical activity guidelines for cancer survivors
.
CA Cancer J Clin
2012
;
62
:
243
74
.
19.
Nahar
VK
,
Ford
MA
,
Jacks
SK
,
Thielen
SP
,
Johnson
AK
,
Brodell
RT
, et al
Sun-related behaviors among individuals previously diagnosed with non-melanoma skin cancer
.
Indian J Dermatol Venereol Leprol
2015
;
81
:
568
75
.
20.
Gandini
S
,
Sera
F
,
Cattaruzza
MS
,
Pasquini
P
,
Picconi
O
,
Boyle
P
, et al
Meta-analysis of risk factors for cutaneous melanoma: II. Sun exposure
.
Eur J Cancer
2005
;
41
:
45
60
.
21.
Lazovich
D
,
Choi
K
,
Vogel
RI
. 
Time to get serious about skin cancer prevention
.
Cancer Epidemiol Biomarkers Prev
2012
;
21
:
1893
901
.
22.
Oliveria
SA
,
Shuk
E
,
Hay
JL
,
Heneghan
M
,
Goulart
JM
,
Panageas
K
, et al
Melanoma survivors: health behaviors, surveillance, psychosocial factors, and family concerns
.
Psychooncology
2013
;
22
:
106
16
.
23.
Idorn
LW
,
Datta
P
,
Heydenreich
J
,
Philipsen
PA
,
Wulf
HC
. 
A 3-year follow-up of sun behavior in patients with cutaneous malignant melanoma
.
JAMA Dermatol
2014
;
150
:
163
8
.
24.
Idorn
LW
,
Datta
P
,
Heydenreich
J
,
Philipsen
PA
,
Wulf
HC
. 
Sun behaviour after cutaneous malignant melanoma: a study based on ultraviolet radiation measurements and sun diary data
.
Br J Dermatol
2013
;
168
:
367
73
.
25.
Guy
GP
 Jr.
,
Berkowitz
Z
,
Holman
DM
,
Hartman
AM
. 
Recent changes in the prevalence of and factors associated with frequency of indoor tanning among US adults
.
JAMA Dermatol
2015
;
151
:
1256
9
.
26.
Mayer
D
,
Layman
A
,
Carlson
J
. 
Sun-protection behaviors of melanoma survivors
.
J Am Acad Dermatol
2012
;
66
:
e9
10
.
27.
Palesh
O
,
Aldridge-Gerry
A
,
Bugos
K
,
Pickham
D
,
Chen
JJ
,
Greco
R
, et al
Health behaviors and needs of melanoma survivors
.
Support Care Cancer
2014
;
22
:
2973
80
.
28.
Dennis
LK
,
Vanbeek
MJ
,
Beane Freeman
LE
,
Smith
BJ
,
Dawson
DV
,
Coughlin
JA
. 
Sunburns and risk of cutaneous melanoma: does age matter? A comprehensive meta-analysis
.
Ann Epidemiol
2008
;
18
:
614
27
.
29.
Branstrom
R
,
Kasparian
NA
,
Chang
YM
,
Affleck
P
,
Tibben
A
,
Aspinwall
LG
, et al
Predictors of sun protection behaviors and severe sunburn in an international online study
.
Cancer Epidemiol Biomarkers Prev
2010
;
19
:
2199
210
.
30.
Freiman
A
,
Yu
J
,
Loutfi
A
,
Wang
B
. 
Impact of melanoma diagnosis on sun-awareness and protection: efficacy of education campaigns in a high-risk population
.
J Cutaneous Med Surg
2004
;
8
:
303
9
.
31.
Manne
S
,
Lessin
S
. 
Prevalence and correlates of sun protection and skin self-examination practices among cutaneous malignant melanoma survivors
.
J Behav Med
2006
;
29
:
419
34
.
32.
Soto
E
,
Lee
H
,
Saladi
R
,
Gerson
Y
,
Manginani
S
,
Lam
K
, et al
Behavioral factors of patients before and after diagnosis with melanoma: a cohort study - are sun-protection measures being implemented?
.
Melanoma Res
2010
;
20
:
147
52
.
33.
McMeniman
E
,
De'Ambrosis
K
,
De'Ambrosis
B
. 
Risk factors in a cohort of patients with multiple primary melanoma
.
Australas J Dermatol
2010
;
51
:
254
7
.
34.
Kasparian
NA
,
McLoone
JK
,
Butow
PN
. 
Psychological responses and coping strategies among patients with malignant melanoma: a systematic review of the literature
.
Arch Dermatol
2009
;
145
:
1415
27
.
35.
Zivkovic
M
,
Dediol
I
,
Ljubicic
I
,
Situm
M
. 
Sun behaviour patterns and perception of illness among melanoma patients
.
J Eur Acad Dermatol Venereol
2012
;
26
:
724
9
.
36.
Novak
CB
,
Young
DS
,
Lipa
JE
,
Neligan
PC
. 
Evaluation of sun protection behaviour in patients following excision of a skin lesion.
Can J Plast Surg
2007
;
15
:
38
40
.