American Journal of Epidemiology Advance Access originally published online on November 13, 2006
American Journal of Epidemiology 2007 165(2):222-230; doi:10.1093/aje/kwk004
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PRACTICE OF EPIDEMIOLOGY |
Comparison of Self-reported Lifetime Sun Exposure with Two Methods of Cutaneous Microtopography
1 Department of Public Health Sciences, Faculty of Medicine, University of Toronto, Toronto, Ontario, Canada
2 Samuel Lunenfeld Research Institute, Mount Sinai Hospital, Toronto, Ontario, Canada
3 Department of Pathology and Laboratory Medicine, Mount Sinai Hospital, Toronto, Ontario, Canada
4 Department of Laboratory Medicine and Pathobiology, Faculty of Medicine, University of Toronto, Toronto, Ontario, Canada
Correspondence to Dr. Julia Knight, Samuel Lunenfeld Research Institute, Mount Sinai Hospital, 60 Murray Street, Box 18, Toronto, Ontario M5T 3L9, Canada (e-mail: knight{at}mshri.on.ca).
Received for publication January 9, 2006. Accepted for publication June 9, 2006.
| ABSTRACT |
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There is currently no "gold standard" for measuring lifetime sun exposure. Exploration of alternatives to self-reports is important for examining illnesses related to ultraviolet light exposure. Using skin replicas obtained from 184 controls in a breast cancer case-control study (Toronto, Ontario, Canada, 20042005), the authors compared self-reported indicators of lifetime sun exposure with two measures of cutaneous microtopography, the Beagley-Gibson system and skin line counts. With the Beagley-Gibson system, significantly increased odds ratios were found for age (odds ratio (OR) = 1.10, 95% confidence interval (CI): 1.05, 1.16), spending 7 days outside per week during the summer (OR = 3.33, 95% CI: 1.48, 7.50), and lifetime number of sunlamp sessions. Significantly decreased odds ratios were found for having darker skin, ever giving birth, and ever using sunlamps. With the skin line count approach, significant positive associations were found for age (OR = 2.31, 95% CI: 1.23, 4.35), age squared, duration of working in outdoor jobs (OR = 0.88, 95% CI: 0.79, 0.98), and average number of outdoor activities per week at ages 2029 years (OR = 1.05, 95% CI: 1.00, 1.10). While the Beagley-Gibson method was associated with more variables than the skin line count method, both methods require further refinement before graded skin replicas can be recommended as a substitute for self-report measures.
data collection; questionnaires; skin; sunlight; validation studies [publication type]
Abbreviations: CI, confidence interval; ICC, intraclass correlation coefficient; OR, odds ratio
| INTRODUCTION |
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Measurement of lifetime sun exposure is important in studies examining illnesses related (directly or inversely) to ultraviolet light exposure. These studies often rely on self-reports of lifetime sun exposure. Reliable self-reported sun exposure measures are difficult to obtain, as subjects are often hard-pressed to recall detailed information on everyday aspects of their lives (1). Few data exist on the validity or reproducibility of such measures, which are typically used in case-control studies (2). Objective measures of lifetime sun exposure could lead to a reduced dependency on subjective questionnaires (3). Although neither self-reports nor objective measures are considered "gold standard" indicators of lifetime sun exposure, comparisons are important for the validation of both measures.
Cutaneous microtopography is a method used to provide more objective indicators of lifetime sun exposure. This method typically involves grading negative skin texture replicas of the dorsum of the hand. Holman et al. (1) and English et al. (2) compared cutaneous microtopography of the hand with measures of lifetime sun exposure. English et al. found a weak-to-moderate degree of agreement between reported lifetime number of hours spent outdoors and sun-induced damage to the hand (2), while Holman et al. found significant associations between evidence of skin damage and several reported sun exposure variables (1).
When using methods such as cutaneous microtopography to assess lifetime sun exposure, several potential factors associated with skin texture (i.e., number of lines on the skin surface) should be considered. These include age, ethnicity/skin color, lifestyle, and hormonal factors. Among South Korean women, Youn et al. (4) found that facial wrinkle severity significantly increased with increased number of full-term pregnancies and with postmenopausal status. Schnohr et al. (5) found that the prevalence of deep wrinkles (lateral to the canthus of the right eye) increased with increasing age and with decreasing household income but found no significant association with body mass index (weight (kg)/height (m)2). Although these studies focused on facial wrinkles, their results may point to possible factors related to skin lines on other sun-exposed parts of the body.
We compared self-reported indicators of lifetime sun exposure with two different objective skin replica measures in a random subset of controls from a case-control study that examined relations between sun exposure, vitamin D intake, and breast cancer risk.
| MATERIALS AND METHODS |
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Case-control study
A case-control study examining the effects of sun exposure and dietary and supplemental vitamin D on breast cancer risk was conducted in Toronto, Ontario, Canada. Cases were women with invasive breast cancer that had been newly diagnosed between July 2003 and August 2004. Cases were identified through the Ontario Cancer Registry. Population controls who had never been diagnosed with breast cancer were identified using randomly selected residential telephone numbers. Controls were frequency-matched by 5-year age group to the expected distribution of the cases on the basis of information in the Ontario Cancer Registry. The study was approved by the Mount Sinai Hospital Research Ethics Board. Upon receipt of consent (from a physician for cases or over the telephone for controls), a package including a letter explaining the study and a copy of the questionnaire was mailed to each subject. This was followed by completion of a questionnaire via telephone interview.
Validation sample
Between September 2004 and January 2005, we randomly selected 292 controls (approximately 30 percent of the recruited controls at that time) to request their participation in the validation study. Controls were eligible for this study if they had completed an interview in the case-control study and had agreed to being recontacted about giving a blood sample (an additional component of the validation study involved serum measurements).
Measurement of skin replicas
Controls who consented to participation in the validation study received a kit through the mail containing the materials needed to make a skin texture replica. This kit included a vial of Antimicrobial Jeltrate Plus Dustless Alginate Impression Material (DENTSPLY Caulk, Milford, Delaware), a fast-setting liquid impression material designed for making dental impressions, and a resealable plastic bag, a plastic spoon, and instructions. The participants were instructed to make the replica on the dorsum of either hand. This involved first mixing the Jeltrate powder with water and stirring for 3045 seconds. The participant then created the skin replica by spooning the mixture onto the back of one hand (away from the knuckles and thumb) and letting the mixture set for 3 minutes to harden. The replicas were returned to the researchers by courier and scanned next to a ruler (figure 1).
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The replicas were graded using two different methods, with raters being blinded to any information on the participant, including age and sun exposure. All replicas were assessed by one rater (L. W.), and a random subset was also evaluated by a second rater (A. W.). The first grading method was the six-category Beagley-Gibson system for grading skin replicas (3). This system measures alterations in the skin surface characteristics thought to reflect prolonged ultraviolet light exposure (1). The approach involves examining the pattern and depth of primary and secondary skin surface lines. Skin with the highest level of sun exposure typically has few or no secondary lines, with widely spaced primary lines; a Beagley-Gibson score of 1 represents low sun exposure, and a score of 6 represents high exposure (figure 2). For the Beagley-Gibson method, each scanned replica was graded in Adobe Photoshop 7.1 (Adobe Systems, Inc., San Jose, California) at 10x magnification.
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The second grading method involved counting the numbers of primary and secondary lines in 1 square centimeter of each scanned skin replica. Each square centimeter was selected on the basis of clarity and representativeness of the skin replica. Each square was formatted by converting the scanned replica to black and white, increasing the contrast, sharpening the image, and magnifying the image at 6x. Two straight lines (horizontal and vertical) were drawn across the image using Adobe Photoshop 7.1. The number of primary and secondary lines that crossed each drawn line were counted, documented, and averaged. Skin with the highest level of sun exposure typically has fewer lines than skin with the lowest level of sun exposure, and therefore a higher line count is associated with lower sun exposure.
Measurement of lifetime sun exposure and other variables
Lifetime sun exposure data were collected through telephone interviews conducted between September 2003 and January 2005. Lifetime sun exposure variables included residence history (ever having resided at or below 40° latitude and total number of years); job history (ever having held, for 1 month or more, a job that involved working outdoors for at least half an hour between 9 a.m. and 5 p.m. daily, and total number of years the job had been held); outdoor activity history (number of times the participant had been involved in outdoor activities during the summer); number of days per week in which the participant had spent at least half an hour outdoors (7 vs. <7); time spent in a summer climate during the winter (ever going to a summer climate during the winter and total number of years); ever using sunscreen; and sunlamp/sun bed use (ever use and total lifetime number of sessions). Most sun exposure measures (except for residence, holding an outdoor job, and sunlamp/sun bed use) were categorized by age group: 1019 years and 2029 years.
Demographic variables evaluated included age, body mass index (continuous variable), skin color (seven categories collapsed into light vs. medium/dark), and ethnicity (European vs. non-European). Reproductive variables included use of hormone replacement therapy (ever use and total number of years of use), ever having given birth, and menopausal status (premenopausal, postmenopausal, or unknown). For purposes of this study, menopause status was defined as follows. A participant was classified as premenopausal if she had had a menstrual period within the past 12 months, unless she was taking hormone replacement therapy. A participant was classified as postmenopausal if she had not had a period in 12 months, had had both ovaries removed, or was 55 years of age or older. A participant's menopausal status was classified as unknown if she was taking hormone replacement therapy or had undergone a hysterectomy without removal of the ovaries and was less than 55 years of age.
Statistical analysis
For the purpose of this analysis, Beagley-Gibson scores were dichotomized, with scores of 5 and 6 being collapsed to represent a high level of sun exposure and scores of 14 representing low sun exposure (1). The skin line counts were also dichotomized, with a high level of sun exposure being defined as less than or equal to an average of 11.5 lines and low sun exposure being defined as greater than 11.5 lines. The cutpoint for dichotomizing the skin line counts was based on the proportion of Beagley-Gibson scores categorized as high exposure. For both the dichotomized Beagley-Gibson method and the dichotomized skin line counts, odds ratios and 95 percent confidence intervals were estimated by unconditional logistic regression analysis. All Beagley-Gibson odds ratios were adjusted for age; for skin line counts, all odds ratios were adjusted for age and age squared (to allow for the observed curvilinearity of the data). We calculated Spearman correlations to examine any collinearity among independent variables. Each independent variable was initially considered in isolation (adjusted only for age), followed by multivariate models using a backwards stepwise approach. During the backwards stepwise regression, variables were removed on the basis of their relation with the dependent variable; we did this to address the question of which variables remained associated with the outcome when all of them were combined in the same model, as opposed to looking specifically for potential confounders. All analyses were conducted using SAS 9.1 (SAS Institute, Inc., Cary, North Carolina). All p values were two-tailed, and values less than 0.05 were considered significant.
Intra- and interrater reliability for skin replica measurements
Fifty randomly selected skin replicas (27 percent) were assessed for intra- and interrater reliability using both the Beagley-Gibson method and the skin line count method. These skin replicas were from European participants only.
| RESULTS |
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Participation
Of the 292 controls contacted for the validation study, 240 (82 percent) consented, 33 (11 percent) refused consent, seven (2 percent) were considered ineligible, three (1 percent) could not be contacted, and nine (3 percent) had not yet consented at the time of this study. Of the 240 persons who consented, 187 (78 percent of those who consented) returned completed skin replicas. Of the returned replicas, five (3 percent) were of insufficient quality for grading. These five participants were recontacted for updated replicas. Two of these participants returned new replicas, resulting in a final sample of 184 skin replicas (77 percent). Of these 184 replicas, there were 169 for which we had complete information on all variables of interest.
Intra- and interrater reliability
There was high intrarater reliability for both skin grading methods. There was 86 percent agreement for the dichotomized skin line counts and 84 percent agreement for the dichotomized Beagley-Gibson scores. Interrater reliability was slightly lower for both methods, with 74 percent agreement for the skin line counts and 72 percent agreement for the Beagley-Gibson scores. There was 68.5 percent agreement when comparing the high and low classifications of Beagley-Gibson scores and skin line counts for all 184 women.
Descriptive statistics
The mean age of the participants in the validation study was 51.4 years (standard deviation, 8.2; range, 2968 years). Table 1 shows descriptive statistics for the demographic variables according to exposure level for each scoring system. The age difference between high and low exposure was greater for the Beagley-Gibson system than for the skin line counts.
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Comparison of cutaneous measures and self-reported sun exposure
We examined the effects of each independent variable adjusted for age (as well as age squared for skin line counts). The results are presented in table 2. Age was found to be one of the most significant predictors of lifetime sun exposure as measured by the Beagley-Gibson system (odds ratio (OR) = 1.11, 95 percent confidence interval (CI): 1.06, 1.16). Statistically significant increased odds ratios were found for spending 7 days outside per week during the summer at ages 1019 years (OR = 2.76, 95 percent CI: 1.22, 6.27) and ages 2029 years (OR = 2.53, 95 percent CI: 1.26, 5.06) and for an increasing number of sunlamp/sun bed sessions (OR = 1.03, 95 percent CI: 1.01, 1.05). Statistically significant decreased odds ratios were found for having darker skin (OR = 0.46, 95 percent CI: = 0.23, 0.90) and for ever giving birth (OR = 0.23, 95 percent CI: 0.07, 0.73). Marginally significant increased odds ratios were found for engaging in a higher average number of outdoor activities per week (during the summer months) at ages 1019 years (OR = 1.04, 95 percent CI: 1.00, 1.08) and ages 2029 years (OR = 1.05, 95 percent CI: 1.00, 1.10).
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As with the Beagley-Gibson method, age was a strong predictor of lifetime sun exposure on the basis of skin counts (OR = 2.12, 95 percent CI: 1.24, 3.63); the square of age was also significant (OR = 0.99, 95 percent CI: 0.99, 1.00). The only other independent variable that was marginally significant after adjustment for age and age squared was duration of working in outdoor jobs (OR = 0.93, 95 percent CI: 0.86, 1.00).
Table 3 presents results from the final multivariate logistic regression models. Similar to the univariate regression model results, significantly increased odds ratios were found in the Beagley-Gibson multivariate model for age (OR = 1.10, 95 percent CI: 1.05, 1.16), spending 7 days outside per week during the summer at ages 2029 years (OR = 3.33, 95 percent CI: 1.48, 7.50), and number of sunlamp/sun bed sessions (OR = 1.03, 95 percent CI: 1.01, 1.05). Significantly decreased odds ratios were found for having darker skin (OR = 0.33, 95 percent CI: 0.15, 0.74), ever giving birth (OR = 0.20, 95 percent CI: 0.05, 0.77), and ever using sunlamps/sun beds (OR = 0.32, 95 percent CI: 0.11, 0.91). Significant or marginal associations with skin line counts were found for age (OR = 2.31, 95 percent CI: 1.23, 4.35), age squared (OR = 0.99, 95 percent CI: 0.99, 1.00), duration of working in outdoor jobs (OR = 0.88, 95 percent CI: 0.79, 0.98), and average number of outdoor activities engaged in per week (during the summer months) at ages 2029 years (OR = 1.05, 95 percent CI: 1.00, 1.10).
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| DISCUSSION |
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The two methods of cutaneous microtopography evaluation considered in this study were significantly associated with age and a select number of ultraviolet light-related and other variables. For the univariate logistic regression models, use of the Beagley-Gibson method resulted in significant or marginal associations with self-reported number of days spent outside per week (for both age categories), sunlamp use, skin color, ever having given birth, and outdoor activities at ages 2029 years. For the univariate skin line count, a marginally significant effect was found for outdoor job duration only.
Similar to the univariate results, in the multivariate models the Beagley-Gibson method produced a slightly higher number of significant variables. Significant associations were found for age, number of days spent outside per week at ages 2029 years, sunlamp use, skin color, and ever giving birth. The multivariate skin line count model produced significant effects for age, age squared, number of years spent working in an outdoor job, and number of outdoor activities engaged in per week (during the summer months) at ages 2029 years.
Overall, use of the Beagley-Gibson method resulted in a higher number of significant variables. However, in the final multivariate models, both methods produced the same number (two) of significant sun-exposure-related independent variables. This might suggest that the Beagley-Gibson approach captures a wider range of both intrinsic and sun-exposure-related variables and captures this information differently than the skin line count approach, as demonstrated by the different variables found to be significant in the final logistic regression models. It is difficult to conclude that either approach is superior to the other; rather, the two approaches appear to reflect different aspects of sun exposure and other variables.
Results for some variables, such as outdoor job duration and ever use of a sunlamp or sun bed, did not point in the expected direction. This may indicate that there are other important factors related to these variables that were not accounted for in this analysis. Additionally, the results for ever giving birth (in the Beagley-Gibson models) pointed in the opposite direction than that expected. In this study, ever giving birth was associated with decreased odds of high sun exposure or skin aging (according to the Beagley-Gibson score), in comparison with previous research by Youn et al. (4), which found that facial wrinkle severity significantly increased with increasing number of full-term pregnancies. These conflicting results may be due to differences between facial wrinkling and skin lines on the dorsum of the hand.
Few other studies have directly compared self-reported sun exposure variables with objective skin measurements. Holman et al. (1) compared skin replicas with self-reported constitutional and environmental exposure measures. They found significant crude associations between Beagley-Gibson scores and age, having an outdoor occupation, swimming as a preferred outdoor activity, maintenance of a suntan, and use of sunscreen. They also found that controlling for age and sex appeared to reduce the strength of associations of skin damage with Celtic ethnicity, fair/red hair, and blue eyes, while augmenting the apparent association with burn reaction to sunlight. Holman et al. concluded that age was the strongest determinant of actinic skin damage among those identified (1).
English et al. (2) examined intermethod reliability and reproducibility of lifetime sun exposure measures using cutaneous microtopography of the hand and solar elastosis of the back of the neck. They found that self-reported time spent outdoors was positively associated with cutaneous microtopography; the mean exposure in the highest category of sun damage was approximately double that in the lowest category. However, the cutaneous microtopography variable did not explain much of the variance in reported sun exposure (R2 = 0.07).
Although self-reported sun exposure is commonly used in epidemiologic studies, it is not a gold standard measure. Therefore, it is difficult to assess whether the inconclusive results found in the current study reflect issues with the self-report measures or the cutaneous measures. Rosso et al. (6) examined the reproducibility of self-reported sun exposure data collected through a standard questionnaire by reinterviewing participants in a skin cancer case-control study. They found moderate-to-substantial agreement on weighted indices of outdoor work (intraclass correlation coefficient (ICC) = 0.68), exposure during holidays (ICC = 0.79), and outdoor sports (ICC = 0.56).
The current study had some limitations. The relatively small sample size led to small frequencies within subcategories of self-reported exposure, resulting in some variables' being excluded from the analyses. For example, an important variable to measure is skin reaction to sun (e.g., tanning or burning). This variable had to be omitted because of the low frequency in one of the response categories. The current study also had strengths, however, including the number of variables measured. Additionally, the use of two different scoring methods allowed for comparisons to be made between the objective measure of counted skin lines and the Beagley-Gibson method. Another strength of this study was the ability to have subjects create their own skin replicas, which was critical because of the geographic spread of participants across the study area. Relatively few replicas returned were of poor quality.
The Beagley-Gibson method appears to be significantly related to more variables overall in comparison with the skin line count method. However, both the Beagley-Gibson method and the skin line count approach produced an equivalent number of significant variables related specifically to sun exposure. Overall, the results are not yet consistent or strong enough to recommend the use of skin replicas instead of self-reported sun exposure. However, replicas may provide additional useful information and are relatively easy to obtain. Continued efforts should be made to further validate self-reported lifetime sun exposure. Future research should focus on developing new methods and refining existing methods to objectively measure skin replicas, in order to better reflect lifetime sun exposure.
| ACKNOWLEDGMENTS |
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The authors are grateful to the Canadian Breast Cancer Research Alliance for providing funds for the vitamin D and breast cancer case-control study and to the staff of the Samuel Lunenfeld Research Institute for their role in data collection and their assistance.
Conflict of interest: none declared.
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[Abstract/Free Full Text] - English DR, Armstrong BK, Kricker A. (1998) Reproducibility of reported measurements of sun exposure in a case-control study. Cancer Epidemiol Biomarkers Prev 7:85763.[Abstract]
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[Abstract/Free Full Text]
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