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ARTICLE
Factors Affecting Knowledge Levels and Protective Behaviors to Prevent the Development of Skin Cancer in Organ Transplant Recipients as a High-Risk Group

Abstract

Objectives: Organ transplant recipients are at high risk of skin cancer due to immunosuppressant therapy. This study investigated the factors affecting organ transplant recipients’ knowledge and protective behaviors to prevent the development of skin cancer.
Materials and Methods: This was a cross-sectional descriptive study of kidney (n = 82) and liver (n = 31) transplant recipients seen at our hospitals in Turkey from June 2019 to February 2020. A sociodemographic and clinical characteristics form, the Skin Cancer and Sun Knowledge scale, the Sun Protection Behavior questionnaire, and the General Self-Efficacy scale were used to collect data.
Results: The mean age of organ transplant recipients was 46.63 ± 13.24 years. Self-efficacy and awareness that transplant increases the risk of skin cancer are 2 characteristics that affected the participants’ knowledge level. The type of graft (kidney) affected participants’ behavior in avoiding outdoor exposure between the hours of 10 am and 4 pm. Green/blue eye color and self-efficacy affected the participants’ hat-wearing behavior. These details showed that, as the patients’ sensitivity and self-efficacy increased, their levels of knowledge and sun protection behaviors were positively affected.
Conclusions: The knowledge level of patients was affected by (1) awareness that transplant is associated with an increased risk of skin cancer and (2) high levels of self-efficacy. We observed that (1) organ transplant recipients with high self-efficacy and kidney transplant recipients were more likely to avoid outdoor exposure between 10 am and 4 pm and that (2) organ transplant recipients with green/blue eyes and high levels of self-efficacy were more likely to wear a hat when outdoors. Organ transplant teams should provide education and counseling about skin cancer and sun protection in the follow-up care of transplant recipients.


Key words : Cancer prevention, Sun exposure, Sun protection

Introduction

Today, the incidence of skin cancer is increasing in both healthy individuals1 and organ transplant (OT) recipients, who are among the high-risk groups for skin cancer.2 Lifelong use of immunosuppressive drugs by OT recipients increases their long-term risk of melanoma and nonmelanoma skin cancer (NMSC).3,4 Compared with the general population, the incidence in OT recipients of squamous cell carcinoma is 60 to 250 times higher5 and the risk of NMSC is 100 times higher.2 The risk of squamous cell carcinoma in OT recipients is 65 times higher compared with the risk for immunocompetent individuals.6

The incidence of NMSC varies in different geographic regions. In Mediterranean regions with high sun exposure, the incidence rate is 10.0 cases per 1000 posttransplant person-years.7 In a study conducted in Spain, the rate of NMSC development after kidney transplant (KT) was 25.2%.8 In a study conducted in Turkey, the rate of malignancy after KT was 0.75%. Also, in patients with malignancy, NMSC was more common (40%).9 In a different study, the rate of NMSC development was found to be 2.6% in KT recipients.10 Since Turkey is located in the Mediterranean region and has high sun exposure, it is a risky country in terms of skin cancer development.

The main predisposing factors for skin cancers are male sex,11 Fitzpatrick skin type I and type II,4,11 older age,11-13 human papillomavirus occurrence, the type of immunosuppressive drugs (azathioprine > cyclosporin A > tacrolimus), the type of transplanted organ (heart > lung > kidney > liver), a longer duration of immunosuppression,8,11-13 cigarette smoking, family history of cancer,11 and age at the time of transplant.8 A systematic review has found that the most important risk factors in the development of NMSC after organ transplant in the last 20 years were exposure to ultraviolet radiation (UVR), use of immunosuppressive agents (especially azathioprine), and papillomavirus infections.14

Ultraviolet radiation is a well-established risk factor for skin cancer development, and sun exposure increases the risk of skin cancer in OT recipients8,11,14 Also, UVR exposure is the most important modifiable risk factor for the development of NMSC15; thus, OT recipients need to focus on protecting themselves from sun exposure.12 On this basis, we investigated the sun protection behaviors of patients and the risk factors that negatively affect these behaviors. The sun protection behaviors of most OT recipients are inadequate.15-17 Studies have shown that 35% to 63% of patients are unaware of the relationship between sun exposure and skin cancer.15,18,19 Those who are educated about posttransplant skin cancer and who are aware of the relationship between sun exposure and skin cancer exhibit better sun protection behaviors.18 Therefore, we sought to discover the knowledge level among OT recipients regarding skin cancer and sun exposure, their sun protection behaviors, and the factors that may affect these behaviors, as well as details of OT recipient belief systems that may affect their sun protection behaviors. This information can provide a basis to develop health education programs to encourage preventative behaviors.20 This study investigated the factors affecting OT recipients’ knowledge of various concepts of skin cancer and their protective behaviors for prevention of skin cancer.

Materials and Methods

Study design
The study design was cross-sectional and descriptive.

Participants
The study included KT recipients (n = 82) and liver transplant (LT) recipients (n = 31) who were seen in outpatient clinics at 2 university hospitals in Izmir from June 2019 to February 2020. The inclusion criteria were as follows: over 18 years of age, willingness to participate in the study, and recipient of a KT or LT. The exclusion criteria were multiorgan transplant and hospitalization. The sample size was calculated according to the study data of Haney and colleagues (2019)17 with the G*Power program (version 3.0.10). The sample size was determined to be 77 based on a regression coefficient of 0.25, type I error (α) of .05, and type II error (β) of .20.

Measurement
The questionnaire for sociodemographic and clinical characteristics was developed by the researchers and included 18 questions related to sociodemographic, clinical, and skin cancer characteristics. To assess the participant’s knowledge about transplant and skin cancer, there were 2 questions: “Does transplantation increase the risk of skin cancer?” and “Have you received information about the dangers of sun exposure after transplantation?”

The knowledge among OT recipients about the relationship between skin cancer and sun exposure was assessed with the Skin Cancer and Sun Knowledge (SCSK) scale, developed by Day and colleagues.21 The SCSK scale includes questions related to skin cancer and sun exposure in 5 domains: sun protection, tanning, skin cancer risk factors, the prevalence of skin cancer, and the signs of skin cancer. The scale has a 1-factor structure and contains 15 true/false questions and 10 multiple-choice questions. The possible score ranges from 0 to 25, and higher scores indicate a higher level of knowledge. The content validity index, internal consistency reliability index (Kuder-Richardson formula 20), and test-retest reliability coefficient (n = 34) values of the Turkish version of the SCSK scale were 93.71%, 0.51%, and 0.52%, respectively (p < .001).22

The Sun Protection Behavior questionnaire was developed by the researchers. The questionnaire included 13 items to determine the participants’ frequency to exhibit sun protection behaviors on sunny days (eg, wearing a hat, using an umbrella, staying in the shade when outdoors). Participants rated their sun protection behavior on a 5-point Likert-type scale ranging from 1 to 5 (1 = never, 2 = rarely, 3 = sometimes, 4 = often, and 5 = always). The total possible score ranges from 0 to 65, and higher scores indicate more positive behaviors.

The self-efficacy of the OT recipients was evaluated with the General Self-Efficacy scale, as developed by Sherer and Adams in 1982.23 The General Self-Efficacy scale has a 2-factor structure: general self-efficacy (explained variance 26.5%, Cronbach α = 0.86) and social self-efficacy (explained variance 8.5%, Cronbach α = 0.71). The general self-efficacy factor does not define a specific behavioral domain. The social self-efficacy factor defines efficacy expectations in various social situations. The questionnaire relies on a 5-point Likert scale, with the range of total scores from 17 to 85; higher scores indicate a higher level of belief in personal self-efficacy. The load factor of each item on the questionnaire was 0.43 to 0.70. The correlation coefficient between the General Self-Efficacy scale and the other scales was statistically significant (r = 0.30-0.49). The Cronbach α coefficient and the test-retest reliability were found to be 0.80 and 0.69, respectively.24

Ethical considerations
Written consent was obtained from all participants prior to data collection. Participants were informed that all information provided in the study would remain confidential. Permission for this study was obtained from Dokuz Eylül University Hospital and Ege University Hospital. The study protocol was approved by the Dokuz Eylül University Non-Invasive Research Ethics Committee (decision No. 2019/15-15; date 19.06.2019).

Statistical analyses
We used the SPSS software (version 24.0) for statistical analysis. Descriptive statistics were used. To create the multivariate linear regression analysis model, we first analyzed all affecting variables via 1-way analyses (Pearson correlation, t test, Mann-Whitney U test, Kruskal-Wallis test, 1-way analysis of variance, and the chi-square test). As a result of these analyses, we included the following variables in the model: SCSK scores and sun protection behaviors. Multivariate linear regression analysis was performed to determine the factors for these 2 variables.

Results

The mean age of the patients was 46.63 ± 13.24 years. The incidence of living donors was 59.29%, all of whom were related donors, and 26.86% (n = 18) were mothers of OT recipients. Of the 113 total OT recipients, 72.6% (n = 82) were patients who were aware that transplant increases the risk of skin cancer, 59.3% (n = 67) were male, 46.0% (n = 52) were primary school graduates, and 72.6% (n = 82) were married. Only 1 patient (0.9%) had been previously diagnosed with skin cancer. Of total OT recipients, 2.7% (n = 3) had a family history of skin cancer, 72.6% (n = 82) were KT recipients, 59.3% (n = 67) did not undergo regular skin examinations, 75.2% (n = 85) did not consult a dermatologist at least once a year, and 52.2% (n = 59) had not received information about the dangers of posttransplant sun exposure. The participants’ mean score (±SD, min-max range) on the General Self-Efficacy scale was 61.47 ± 9.17 (min-max, 39-85); the mean score for KT recipients was 63.16 ± 9.66 (min-max, 39-85), and the mean score for LT recipients was 56.98 ± 5.78 (min-max, 45-70) (Table 1).

Skin cancer and sun-related knowledge
The mean score of the OT recipients on the SCSK scale was 12.17 ± 2.84. The item for which OT recipients showed the highest level of knowledge was, “Skin cancer is not seen in people with dark skin” (item 15). No participants gave the correct answer to 2 items on the questionnaire: “What types of clothing block UV rays (from the sun)?” (item 20) and “What is the most common type of skin cancer?” (item 24).

According to the results of the multiple regression analysis shown in Table 2, the relationship between the independent variables and the participants’ knowledge of the relationship between skin cancer and sun exposure was significant among the OT recipients (R = 0.544, R2 = 0.295, F = 3.30; p < .05). The independent variables accounted for 29% of the participants’ knowledge of skin cancer and sun exposure; the significant variables affecting the scores for skin cancer and sun knowledge were (1) awareness that transplant increases the risk of skin cancer and (2) and self-efficacy.

Sun protective behaviors
The mean score for OT recipient responses on the Sun Protection Behavior questionnaire was 37.20 ± 10.97. The most common behavior reported by the patients was, “Using sunscreen with high protection (SPF of 15 or more) at least 15 minutes before going out” (item 7). The least common behavior reported was, “Not being outside between 10 am and 16 pm” (item 1).

The affecting factors were analyzed (independent variables) according to the total mean of sun-protective behaviors. The regression model was not found to be significant (R = 0.319, R2 = 0.102, F = 1.361, p = .22). Therefore, each item (behavior) was analyzed, and only the items with affecting factors are provided in Table 3. “Not being outside between the hours of 10 am and 16 pm” (R = 0.416, R2 = 0.173, F = 2.54, p < .05) and “Wearing a hat” (R = 0.410, R2 = 0.168, F = 2.45, p < .05) were found to be significant in the regression model. The type of graft (kidney) and self-efficacy were the significant variables affecting the behavior described as, “Not being outside between the hours of 10 am and 16 pm.” Eye color (blue/green) and self-efficacy were the significant variables affecting the item, “Wearing a hat.”

Discussion

In this study, the mean score of OT recipients on the SCSK scale was 12.17 ± 2.84; 65.5% of the OT recipients did not know that organ transplant increased the risk of skin cancer, and 52.2% had not received any information about sun damage. Organ transplant recipients who knew that an organ transplant increases the risk of skin cancer had a better SCSK score. In terms of behavioral change, it is important for patients after organ transplant to be educated about the risk of skin cancer, to know that organ transplant increases the risk of skin cancer, and to be aware that they are in a high-risk group. A multicenter study in the United Kingdom reported that 24% of the centers did not provide skin cancer education after transplant.25 Several studies have found that 22% to 37% of OT recipients did not receive any education on skin cancer and sun protection, and another study stated that only 11% of patients received complete information.12,15,19,26 In 2 studies conducted in Turkey, 33% of OT recipients and 65% of LT recipients did not receive education on skin cancer and sun protection, and 19% of LT recipients did not know that organ transplant increases the risk of skin cancer.17,18 Another study reported that 49% of KT recipients did not consider themselves to be in a risk group for skin cancer,15 and yet another study found that 60% of OT recipients did not know that sun exposure is a risk for skin cancer development and that the patients who were not aware of this had worse sun-protective behaviors.18 Only 2 studies have previously examined the factors affecting patients’ level of knowledge about skin cancer risk after transplant. One study has reported that high education levels in LT recipients and awareness that sun exposure increases the risk of skin cancer were 2 factors that affected patients’ SCSK scores.17 Another study found that men showed a greater lack of knowledge about sun protection versus women.27 All of these studies show that OT recipients lack education about skin cancer and sun protection behaviors. Both patients and health care professionals need to be educated about sun-protective behaviors, and skin cancer care and education should be integrated into follow-up care after transplant.4 In addition, the factors that affect the SCSK score warrant further investigation.

Primary and secondary prevention methods should be applied to reduce the risk of skin cancer with a multidisciplinary approach.13 In our study, the most frequently exhibited behavior related to sun protection was, “Using high-protection sunscreen (SPF factor 15 or higher) at least 15 minutes before going out,” and the most infrequently reported behavior was, “Not being outside between the hours of 10 am and 16 pm.” In a previous study, the participants reported that, after transplant, they avoided sun exposure more than they had previously and their sun exposure had decreased by 1 hour.12 In another study, participants reported increased use of sunscreen after transplant,28 and the rate of sunscreen use in KT recipients was 58%.26

Similar to our study, 2 studies have found little evidence that either LT recipients or KT recipients avoided going outside at peak UVR hours,15,26 whereas another study has shown that the majority of KT recipients were not exposed to sunlight during peak UVR hours.12 In other studies, 19% of OT recipients and 7% of KT recipients did not show any sun protection behavior when they went outdoors,3,12 whereas KT recipients stayed in the shade more frequently after transplant.12 In other studies, LT recipients showed a high rate of sun protection behaviors (eg, hat, sunscreen, sunglasses, clothing)26,27 and 31% of OT recipients wore a hat, 17% used sunscreen, and 11% wore clothing with long sleeves.3 A different study reported the following rates for KT recipients: seeking shade 86%, wearing sunglasses 38%, wearing a hat 45%, using sunscreen 42%, and wearing long-sleeved clothing 35%.12 Tuncer Vural and colleagues, in a study from 2018, stated that only 14% of OT recipients used sunscreen on a daily basis, 14% regularly visited a dermatologist (once or twice a year), and 21% wore a hat.18 Another study found that 51% of OT recipients performed regular skin self-examination,27 and a further study reported that 54% of KT recipients did not use any type of sunscreen and that most patients demonstrated inadequate sun protection behavior.15 Although no standard training material exists on sun protection for transplant recipients, many studies of various types of training have observed an increase in the sun protection behaviors of OT recipients.4,29,30 A study conducted in Canada found that, although there an assigned person to provide pretransplant education to patients on skin cancer, patients received most education from their doctors.27 Nurses should educate patients about sun-protective behavior both before and after transplant. Therefore, there is a need for future interventional studies on OT recipients to discover factors to improve sun-protective behaviors.

There are limited studies in the literature on factors affecting the sun protection behaviors of patients. In addition, there is no consensus on the variables addressed in these studies or on the research results. These studies have shown that male patients showed a tendency to sunburn after sun exposure and that patients with lighter skin showed more consistent use of multiple protective measures.3 Some examples are younger age recipients demonstrated better sunscreen use,27 female recipients were less likely to go outdoors at peak UVR hours and their sunscreen use was better,3,26,27 recipients with lighter skin who received pretransplant advice on sunscreen from a health care provider demonstrated better sunscreen use,28 and highly educated recipients demonstrated better sunscreen use.11,27 Our study found that KT recipients were more likely to avoid being outdoors and avoid sunbathing during peak UVR hours compared with LT recipients. A study has reported KT recipients with a 4.1-fold higher risk of developing nonmelanoma cancer compared with LT recipients.11 Kidney transplant patients are also at risk of developing cancer due to pretransplant kidney diseases. For this reason, it is expected that KT recipients have better sun protection behaviors. There is a need to evaluate the sun protection behaviors of OT recipients using a standard measurement tool and to determine the factors that affect sun protection behaviors of OT recipients.

Self-efficacy is defined as the belief in the personal ability to exhibit a behavior.31 Studies show that self-efficacy level is an important factor to improve health behaviors.32,33 Self-efficacy was stated to be an important factor in skin cancer prevention for self-assessment to monitor signs of skin cancer.20 A study has determined that the level of self-efficacy affected self-care behavior in KT recipients.32 Therefore, a high sense of self-efficacy is important in terms of understanding of skin cancer as preventable and detectable through personal responsibility for sun protection behaviors.

The development of malignancy, especially skin cancer due to the long-term use of posttransplant immunosuppressants, is an important problem. Nurses have important roles in skin assessment and education of patients on skin cancer risk factors and preventive measures. Our study has shown that, as the patients’ sensitivity and efficacy increased, their knowledge levels and behaviors were positively affected. Organ transplant teams should provide education and counseling about skin cancer and sun protection in the follow-up care of transplant recipients.4 Cancer screening and surveillance should be standard practice in every transplant center. There is a need to examine the factors that affect patients’ knowledge levels and to identify risk groups by evaluating sun protection behaviors with a standard measurement tool. It is recommended to design interventional studies that improve patients’ sun-protective behaviors and to adapt interventions with proven effectiveness to clinical care.

Limitations
This study has several limitations. First, a self-reported survey method was used to assess sun protection behaviors, which may have created a self-reporting bias. Second, no valid and reliable instrument exists to assess the sun protection behaviors of OT recipients; therefore, we developed a standardized questionnaire to assess participants’ sun protection behaviors. Third, although the participating KT and LT recipients had different backgrounds, the results cannot be generalized to all KT and LT recipients in Turkey.

Conclusions

This study determined that OT recipients received insufficient information after transplant about the need for sun protection behaviors and that their knowledge level about the increased risk of skin cancer after transplant was low. The study found that awareness that transplant increases the risk of skin cancer and a high level of self-efficacy increased the SCSK scores. Only 2 factors were found to positively impact sun protection behaviors: (1) OT recipients with high self-efficacy and KT recipients were more likely to remain indoors (ie, avoid going outdoors) between 10 am and 16 pm; and (2) OT recipients with green/blue eyes and high levels of self-efficacy were more likely to wear a hat when outdoors.


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DOI : 10.6002/ect.2021.0304


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From tthe 1Department of Surgical Nursing, Dokuz Eylül University Nursing Faculty, Izmir; the 2Department of Surgical Nursing, Ege University Nursing Faculty, Izmir; and the 3Department of Anesthesia, Denizli Healthcare Vocational School, Pamukkale University, Denizli, Turkey
Acknowledgements: The authors have not received any funding or grants in support of the presented research or for the preparation of this work and have no declarations of potential conflicts of interest.
Corresponding author: Eda Ayten Kankaya, Department of Surgical Nursing, Dokuz Eylül University Nursing Faculty, 35340 Balçova- İzmir, Turkey
E-mail: edayten@gmail.com