Sun exposure and protection habits in transplant athletes: An international survey

Transplant recipients are particularly prone to the development of skin cancer, and overexposure to UV radiation during outdoor activities increases the risk of carcinogenesis.


| INTRODUC TI ON
Transplant recipients are at an increased risk of developing cancer.
Although immunosuppressive therapies are increasingly tailored to individual needs and are less aggressive than they used to be, the risk of melanoma and non-melanoma skin cancer is still much higher in this population than in the general population. In addition, tumors may behave more aggressively. 1 UV radiation from the sun is the main risk factor for skin cancer and exerts its carcinogenic effect at different levels: through the induction of thymine dimers responsible for DNA mutations, the generation of oxidative stress causing damage to cell structures, and the inactivation of tumor suppression genes such as p53. 2 Transplant recipients on immunosuppressive drugs are highly susceptible to the deleterious effects of UV radiation. 3 Specific risk factors that need to be evaluated in this population are time since transplant, duration and intensity of immunosuppressive therapy, history of cancer, history of sun exposure, and number of sunburn episodes since childhood. 4 On the other hand, it has been shown that athletes who perform sports activities outdoors have higher rates of sunburn and a higher risk of long-term skin cancer, as confirmed in recent studies carried out in international sports competitions. 5,6 However, there are no publications on a specific population of transplanted athletes.
This study aims to know the knowledge and behaviors in relation to sun exposure of transplanted sports athletes during an international competition covering athletes from 5 continents. So the information of such a sample of a great geographic variability provides a very valuable information from a target population with a double risk factor for the development of skin cancer due to its immunosuppression and sun exposure derived from regular sports practice.

| MATERIAL S AND ME THODS
The XXI World Transplant Games (WTG) were held in Malaga, Spain, in 2017. This event brings together over 1000 international athletes who have received a solid-organ or bone marrow transplant. We took advantage of this unique opportunity to analyze sun exposure and protection behaviors, attitudes, and knowledge in transplant athletes from different parts of the world on immunosuppressive therapy who engage in outdoor sports. We also sought to assess sunburn frequency and explore differences in behaviors between athletes with and without a history of skin cancer.
We conducted an observational descriptive study using a previously validated questionnaire designed to collect data on sociodemographic characteristics (age, sex, country of origin, level of education, profession, marital status, and number of children); the practice of sport; sunburn episodes during the past year; skin type; and sun exposure and protection behaviors, attitudes, and knowledge. 7

| RE SULTS
We collected 170 questionnaires from athletes from five continents; 166 of the athletes answered the question on sunburn in the past year. The sociodemographic data are summarized in Table 1. Twentyfive athletes (15.5%) had undergone retransplantation, the vast majority (84.5%) had received two transplants, but one (0.6%) had received four. All the athletes were on immunosuppressive therapy. Over 78% of the athletes had been playing sport for 1-5 years, and 68% of them did so on a regular basis (≥3 days a week). The most common sports were track and field events, followed by swimming and cycling.
The athletes' skin types are shown in Table 1. 64 athletes (42.4%) reported that they experienced mild sunburn on the day after unprotected sun exposure but then developed a medium tan over the following week. A large proportion (79%) had few or no nevi (<50).
Of the 135 athletes with nevi, 60.2% stated that that none of them were larger than 1 cm.
Twenty-four athletes (15.9%) had a personal history of skin cancer (melanoma in 2.6% of cases).
The vast majority of athletes did not sunbathe or sunbathed very little: 89.9% sunbathed <30 days a year and 80.3% spent <3 h in the sun. Nonetheless, 50.3% played sport outside on >30 days a year and 46.3% did so for ≥3 hours a day. Forty-eight athletes reported having being sunburnt in the past year; 39 (81.3%) said they had been burnt just once or twice, but two participants reported having being burnt >10 times. The overall prevalence of sunburn in the past year was 28.9% (95% CI: 21.7%-36.1%).
In the bivariate analysis stratified by history of sunburn, athletes aged <50 years were significantly more likely to have been burnt in the past year than those aged ≥50 years (37.2% vs 21.6%, p = .041). Sunburn episodes were also more common in athletes with no schooling or with primary education only than in those with a secondary or third-level education (58.3% vs 26.6%, p = .045) and in athletes not taking cyclosporin (32.6% vs 11.1% for those taking cyclosporin, p = .044). The only sport significantly associated with a history of sunburn was basketball, with 75% of players reporting having been burnt in the past year (p = .009).
The only sun protection measure significantly associated with not Over 50% of the athletes scored at least 7 out of 10 in the sun-related knowledge section of the questionnaire. The topics with the most correct answers were on the associations between sunbed use and melanoma risk and between UV radiation exposure and photoaging and skin cancer. The most common misconceptions were that tanned skin did not need to be protected with sunscreen and that light-colored clothing offered greater protection than dark clothing.
In the bivariate analysis stratified by a personal history of skin cancer, no differences were observed between men and women.
The mean age of the athletes was 59 years. Athletes in the ≥50 age group were significantly more likely to have had skin cancer than those aged <50 years (24.1% vs 6.9%, p = .008). These rates were almost double when we compared athletes aged >65 years and those aged ≤65 years (42.9% vs 11.5%, p = .001) (Figure 1). Having children also increased the likelihood of a history of skin cancer (23% vs 6.3%, p = .011). The percentage of athletes with a history of skin cancer varied according to country of origin ( Table 2) and type of transplant (

| D ISCUSS I ON
We have analyzed sun protection and exposure behaviors, attitudes, and knowledge in an international sample of transplant recipients of the 5 continents and from more than 15 sports modalities who regularly engage in outdoor sport. Our analyses were stratified by sunburn in the previous year and a personal history of skin cancer and highlight a number of risk behaviors in this population who are already more prone to developing skin cancer as they are on life-long immunosuppressive therapy and are exposed to UV radiation during the practice of outdoor sport. 8 The most widely used protection measures were sunscreen and sunglasses. Long-sleeved shirts and long pants were used by a significantly higher proportion of athletes with a history of skin cancer, although the only measure significantly associated with a lower prevalence of sunburn was wearing a hat or cap.
Numerous studies have shown that cancer risk is influenced by the degree and duration of immunosuppressive therapy and that transplant recipients are more likely to develop skin cancer than any other type of cancer. 1,9 Immunosuppressive treatments have changed considerably since the first organ transplants were performed. Regimens are increasingly tailored to individual needs, and protocols also vary depending on the organ. 10 13 The prevalence of sunburn in F I G U R E 1 Relationship between age and history of skin cancer. A significant upward relationship between age and history of skin cancer is observed. (*1) p = .008. (*2) p = .001 the previous year, 28.9%, was also lower than that reported for other populations who engage in outdoor activities, such as skaters 14 (52.1%) and cyclists (45.6%). 15 The group of skaters, however, with a mean age of 14.3, were much younger than the athletes in our series, whose mean age was similar to that of the cyclists. As seen, age is an important factor to evaluate. Higher rates of sunburn in the previous year have also been reported for general populations, such as 34.2% for adults in the United States. 16 Few studies have analyzed history of sunburn in transplant recipients, and it is therefore difficult to draw comparisons. Haney et al, 17 however, reported a rate of just 2.9% for liver transplant recipients in Turkey in 2016, which is almost 10 times lower than the rate detected in our series.
Although having a tan is still widely considered a sign of beauty, <50% of the athletes in our series wanted to have a tan, and in addition, a substantial proportion stated that they did not like sunbathing and did not think that it was healthy. This observation coincides with recent reports for Spanish cyclists. 15 A large percentage of the athletes stated that they always or Another contradictory finding, however, was that over half of them were concerned about photoaging.
Good sun protection behaviors are crucial for anyone doing outdoor exercise. Although 74.8% of the transplant athletes acknowledged that it was easy to protect themselves from the sun using physical measures, just 48.8% used a hat or cap and just 15.6% wore long-sleeved or long-legged garments while exercising. Rates in the literature vary and may be strongly influenced by type of sport. In their study of cyclists, for example, Doncel et al 15 found that 95.2% wore a hat or cap and 92.8% wore sunglasses.
Fernández-Morano et al, 14 in turn, reported that 65.9% of skaters wore long-sleeved shirts or long pants.
Awareness of the importance of sun protection and the association between sun exposure and cancer was relatively high in our series, with the athletes scoring on average 7 out of 10 in the knowledge section of the questionnaire. This is the same score reported for Spanish cyclists. 15

| Summary statement
One of the key aspects of skin cancer prevention in transplant patients is a photoprotective behavior, specially in that recipients who overexpose during outdoor activities. More than 60% of athletes from a set of 170 participants in XXI World Transplant Games make sport over 15 years spending more than 1 hours/day outdoor.
Approximately 30% reported sunburns in previous year with only sunscreen and sunglasses use for photoprotection. More educational efforts in sun protection should be made for this photosensitive population.

FU N D I N G SO U RCE S
This work has been supported by the project no.