Affiliations of authors: P. Autier, Division of Epidemiology and Biostatistics, European Institute of Oncology, Milan, Italy; J.-F. Doré (Institut National de la Santé et de la Recherche Médicale Unit 453), S. Négrier (Department of Medical Oncology), Centre Léon Bérard, Lyon, France; D. Liénard, F. Lejeune (Multidisciplinary Oncology Centre), R. Panizzon, D. Guggisberg (Department of Dermatology), Centre Hospitalier Universitaire Vaudois, Lausanne, Switzerland; A. M. M. Eggermont, Department of Surgical Oncology, Daniel den Hoed Cancer Center, Rotterdam, The Netherlands.
Correspondence to: Philippe Autier, M.D., Division of Epidemiology and Biostatistics, European Institute of Oncology, Via Ripamonti 435, Milan (20141) (e-mail: pautier{at}ieo.it).
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ABSTRACT |
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INTRODUCTION |
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In contrast to the results of experimental studies, observational studies have repeatedly found sunscreen use to be associated with higher risk of cutaneous melanoma and basal cell skin cancer and with higher counts of nevi (8-16). By way of explaining this difference, it has been hypothesized that, because they delay sunburn occurrence, sunscreens could allow prolonged sun exposure, a situation that could lead to increased skin cancer risk (1,9).
If the hypothesis that sunscreen use encourages longer sun exposure is correct, then higher SPF should lead to greater sun-exposure duration (17). We conducted a two-center, double-blind, randomized study to determine whether, in the habitual conditions of sunscreen use by European young adults, the SPF had an influence on duration of sun exposure.
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SUBJECTS AND METHODS |
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Study subjects were healthy, paid volunteers 18-24 years old recruited in universities in Lyon (France) and Lausanne (Switzerland) and from nonmedical disciplines. Participants had to have a positive history of sunburn in the past and to be regular sunscreen users intending to have at least 15 days of holidays in sunny areas during the next 2 months. Volunteers with a current skin disease, even minor, or who had a history of a skin disease that lasted for 1 year or more were not eligible. Pregnant women, subjects with a chronic physical illness, or subjects taking a photosensitizing medication were also ineligible.
Participants were randomly assigned to receive an SPF 10 or an SPF 30 sunscreen. The two sunscreens used in this study were broad spectrum, commercially available, high-quality preparations from the same brand. The two sunscreens were prepared with the same chemical absorbents and mineral-oxide reflectants active in the UV A and B wavelengths, but the SPF 30 sunscreen contained a higher concentration of these substances. Both sunscreens had the same appearance, fragrance, color, and texture. They were bought from a local retailer and repackaged in unidentifiable tubes. Five tubes of 60 mL per participant were prepared by an experienced pharmacist (average, 373-g gross weight).
The study was conducted in accordance with the principles of the Helsinki declaration and was submitted for approval to an Ethical Review Committee of the Centre Léon Bérard (Lyon) and of the Centre Hospitalier Universitaire Vaudois (Lausanne). Each participant signed a written informed consent before randomization.
Study Design
The trial design is shown in Fig. 1. The study end point was the
duration of recreational sun exposure. Recreational sun exposure included sunbathing and other
outdoor activities, such as walking, playing, and enjoying sport (e.g., swimming or boating) in
the sun. To avoid the possibility that knowledge of the actual end point could influence
sun-exposure behavior, the stated study end point for participants and all persons in contact with
them was the influence of different types of sunscreens on pigmented lesions of the skin. Since
nevus counting and the assessment of the freckling index merely served to distract subjects from
the real study objective, data on pigmented skin lesions are not presented.
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A person who had no contact with the participants or the medical personnel involved in the study performed the randomization on an individual basis. By use of a table of random numbers, a five-digit random number was assigned to each set of five sunscreen tubes. Next the sets were ordered by successive random numbers.
Potential participants were invited to attend a medical examination. Following eligibility checking, the freckling index (face, arms, and shoulders) was assessed and the numbers of nevi were counted on both arms and on the back. A photograph of the back was also taken. Randomized sets of five sunscreen tubes were given to participants on a consecutive basis. To keep the trial close to participants' habitual conditions of recreational sun exposure, no recommendation was made either about sun exposure or about sunscreen use. Participants were asked to complete a standard daily diary recording detailed data on their sun exposure: hours and type of sun exposure (e.g., sunbathing, swimming, and boating), amount of clothing (e.g., nude, naked breasts, and one- or two-piece swimming suit), number of sunscreen applications, time of application (i.e., before or after starting sun exposure), and sunburn or skin-reddening experience (sunburn was defined as an episode of painful skin erythema; skin reddening was defined as an episode of painless skin erythema). If another sunscreen was used, the participant was asked to record the day and time of day the other sunscreen was used, the commercial name, the SPF, and the motive for changing to another product.
In September, the participants attended a second medical examination during which all sunscreen tubes were taken back and weighed. The daily diaries were collected and verified for completeness. In case there were missing data, the participants were directly asked to provide the missing information during that second medical examination. Participants also completed a questionnaire on their lifetime sun-exposure habits, sunburn experience, and sunscreen use. Their skin phototype was determined according to their propensity to sunburn or to get a tan when going unprotected in the mid-day sun (19): The skin phototype I subject always burns and never tans, the skin phototype II subject always burns first and tans after, and the skin phototype III subject sometimes burns but always gets a deep tan. In this study, there were no skin type IV subjects, i.e., subjects who never burn and always get a deep tan.
Statistical Analysis
Sun-exposure durations were calculated from the daily record diaries. Missing or imprecise
data on sun-exposure hours remained for 5 (0.4%) of the 1312 days with sun exposure.
Sun exposures during these 5 days could thus not be included in the calculations of sun-exposure
duration. After data entry, the randomization code was broken and the analysis was performed.
Student's t test, the uncorrected 2, and the Wilcoxon rank
sum test were used for testing univariate statistical associations. Least-squares regression
multivariate analysis was used to assess the influence of different factors on study end point. All
statistical tests were two-sided.
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RESULTS |
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There was no major imbalance in the distribution of baseline characteristics between the two
groups (Table 1), who showed similar patterns of skin phototype, skin
complexion, past sun-exposure habits, sunburn experience, and sunscreen use. SPF 10
participants spent their holidays in 139 different areas, of which 47% were countrysides or
lakes, 26% were very sunny areas (e.g., the Mediterranean coast), and 27% were
other places (e.g., swimming pools in cities). SPF 30 participants spent their holidays in 127
different areas, of which 50% were countrysides or lakes, 28% were very sunny
areas, and 22% were other places.
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The mean daily duration of sun exposure, sunbathing, or outdoor activities was calculated by use of the number of days on which these activities occurred. The increase in daily sun exposure associated with the SPF 30 sunscreen was observed mainly for sunbathing activities. The increase in sunbathing duration was retrieved in the three subgroups of skin color at initial medical examination, despite the small numbers of participants in the skin color categories.
The starting hour of sunbathing activities was identical in both groups during the first holiday
day with sunbathing (Fig. 2). As the holidays progressed, however, SPF
30 participants tended to start sunbathing systematically earlier than SPF 10 participants,
resulting in more sun exposure during the middle of the day.
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Because clothes normally cover them during time spent outdoors, women's breasts are
highly sensitive to the sun. Five women in the SPF 10 group and eight in the SPF 30 group
sunbathed with naked breasts (Table 3). All sunbathing sessions with
naked breasts were preceded by sunscreen applications to the trunk. While duration of holidays
and numbers of skin erythemal episodes were identical in the two groups of women, the use of
the SPF 30 sunscreen was associated with five times longer sunbathing with naked breasts. Also,
while women in the SPF 30 group were more inclined to sunbathe with naked breasts in the early
days of their vacation, most women in the SPF 10 sunscreen group waited at least 1 week before
exposing their breasts to the sun.
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Eleven French participants, seven in the SPF 10 group and four in the SPF 30 group, used another sunscreen than that provided. Alternative products were used, for a total of 18 days in the SPF 10 group and 7 days in the SPF 30 group. The SPFs of the alternative sunscreens were 5, 6, 6, 10, 10, 20, and 20 in the SPF 10 group and 8, 30, 30, and 60 in the SPF 30 group (Wilcoxon rank sum test for the difference in SPF: P = .070), suggesting that alternative products used by SPF 30 participants were of higher SPF than alternative products used by SPF 10 participants.
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DISCUSSION |
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Participants in the two study arms were similar in terms of natural susceptibility to sunlight,
history of sun exposure and sunburn, duration of holidays, and the types of places they
vacationed. Furthermore, our data suggest that those participants who used SPF 30 sunscreen
actually increased their sun exposure over the course of the holidays (Fig. 2). Therefore, it is unlikely that the difference in sun-exposure duration stemmed from
differences in baseline characteristics and choice of holiday location; rather, it appears to be
related to protection from burning conferred by the stronger sunscreen.
Data collection was done prospectively by use of standard diaries completed on a daily basis. Therefore, biases in the recording of sun-exposure duration have probably been minimal. If some bias was present, however, it is reasonable to assume that it has been equally distributed among the two study groups. We thus consider that the reported sun-exposure durations in this study are a valid reflection of the true sun exposure of participants during their holidays and that our findings are unlikely to be due to bias.
An adult should use roughly 35 mL of sunscreen per single whole-body application to correspond to the doses used by laboratories for measuring the SPF of a sunscreen (20). In that respect, our study participants should have consumed at least three to four times the quantities actually used, and it is thus probable that, in most participants, the effective SPF of the sunscreens used was about three to four times lower. However, our study shows that an increased ability to delay sun-induced skin erythemal reactions is sufficient to cause longer sun exposure, even when moderate quantities of sunscreen are used.
The increase we observed in sun-exposure duration may explain why sunscreen use has been reported to be a risk factor for melanoma, basal cell cancer, and nevus development. It also demonstrates that the longer sun exposure allowed by sunscreen use is an unconscious phenomenon, which makes individual control difficult, particularly where children are concerned.
Sunburn or skin-reddening experience among participants was independent of the SPF and of the quantity of sunscreen used. This observation suggests that sunscreen use during recreational sun exposure does not imply protection against sunburns. Sunburns are essentially due to the UV B radiation (1). Equivalence of sunburns and skin-reddening experiences in the two groups suggest that doses of UV B radiation received by skin cells were probably similar in the two groups. However, the delivery of these doses to skin cells of SPF 30 participants would have taken a longer time than that to skin cells of SPF 10 participants.
The issue addressed by this study is common to all sunscreens. Because we did not want to single out the products of a specific company, we chose not to disclose the commercial name and the exact composition of the sunscreens used in this trial.
From our results, it is reasonable to infer that equivalent or greater differences in sun-exposure duration would have been observed if one had compared subjects using a sunscreen with subjects not using any sunscreen. One could have considered a placebo-controlled trial using as placebo a lotion without any chemical or physical substance able to block UV radiation. In this study, a placebo group was not possible. First, it was ethically difficult to allow a placebo sunscreen when the sun-protection virtues of sunscreens are widely acknowledged. Second, it was not easy to provide a placebo sunscreen without informing subjects of both study groups that they should be careful in their sun exposure to avoid severe sunburns. Third, many subjects in the placebo group would have rapidly changed to a real sunscreen, which would have endangered the trial.
Experiments that tested the ability of sunscreens to reduce the incidence of UV-induced lesions have not examined the possibility that these products could modify the sun-exposure behaviors of subjects eager to acquire a tan or to stay in the midday sun with large parts of the body uncovered. The two human placebo-controlled trials that showed the ability of sunscreen use to reduce the incidence of actinic keratoses (6,7) enrolled subjects having a mean age of 64 years who had a history of nonmelanoma skin cancer or of other sun-induced skin lesions, who were highly aware of the hazards of sun exposure, who were not keen to acquire a suntan, and who apparently never had sunburn during the trials. Clearly, these trials did not reproduce the normal or reasonably foreseeable conditions of sunscreen use in North America and Europe, where sunscreen use by younger people remains largely driven by the desire to enjoy the sun and to acquire a "safe suntan" (21-24).
The protective effect of sunscreen use against skin cancer, particularly melanoma, has not been demonstrated in the general population, but there are compelling data that show a strong relationship between duration of recreational sun exposure and skin cancer. It is therefore desirable that people should be warned against the danger that using a sunscreen may inadvertently prolong recreational sun exposure.
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NOTES |
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We thank Professor T. Philip, Centre Léon Bérard (Lyon, France), for his supportive interest in this work; M.-J. Blasco, Auchan Hypermarkets (Lyon), and H. K. Marchand for their help in the provision and repackaging of sunscreens; and M. Friedrich (Lyon), Dr. K. Buxtorf, and Dr. M. Derighetti (Lausanne, Switzerland) for their assistance.
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Manuscript received November 17, 1998; revised May 25, 1999; accepted June 7, 1999.
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