- Email: [email protected]
Evaluating Retention of Skin Cancer Education in Kidney Transplant Recipients Reveals a Window of Opportunity for Re-education
Evaluating Retention of Skin Cancer Education in Kidney Transplant Recipients Reveals a Window of Opportunity for Re-education P.H. Patela,*, K. Bibeeb, G. Limb, S.M. Malikc, C. Wuc, and M. Pugliano-Maurob a University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA; bDepartment of Dermatology, University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania, USA; and cDepartment of Medicine, University of Pittsburgh Medical Center, Thomas E. Starzl Transplantation Institute, Pittsburgh, Pennsylvania, USA
ABSTRACT Background. Skin cancer is the most common malignancy after solid organ transplant and can lead to significant morbidity. The likelihood of developing squamous cell carcinomas and melanomas is 100 and 2.4 times more likely, respectively, in kidney transplant recipients when compared with the general population. There are few data regarding the assessment and influence of solid organ transplant recipient (SOTR) knowledge of skin cancer and its effect on short- and long-term awareness and behavior. Methods. The purpose of this study was to assess the baseline knowledge of SOTR immediately after transplantation, and then to reassess their knowledge following a 5minute educational video. We also wanted to determine whether lifestyle modifications had been implemented 4 to 8 months after the intervention. Results. Forty patients were enrolled within 2 months of transplantation. Eighty-seven percent of patients were renal transplant recipients, and 75% of patients were available for long-term follow-up. There was a significant increase in knowledge in the immediate postintervention period, which was sustained at 4- to 8-month follow-up, as assessed by patient questionnaire. Patients appeared to be applying this knowledge by participating in lifestyle risk modification and positive sun-protective behavior. Conclusions. Our study suggests that incorporating additional skin cancer education into the early transplant timeline (perhaps in the first one or two outpatient follow-up visits) with an easy to administer educational video and question and answer form increases patient knowledge and influences positive sun-protective behavior.
HE NUMBER of patients living with a solid organ transplant (SOT) in the United States is increasing each year [1]. Of all organ transplants performed in 2014, 58% were kidney transplants, with a total of 17,107 patients receiving kidneys during this time [2,3]. Because of both direct and indirect consequences of the immunosuppression regimens and underlying disease, the likelihood of developing malignancies and infections is much higher in transplant patients than in the general population. Skin cancer is the most common type of malignancy encountered post SOT, with 95% of skin cancers being nonmelanoma skin cancers [1]. The likelihood of developing squamous cell carcinomas and melanomas is 100 and 2.4 times more likely, respectively, in kidney transplant patients when compared with the general population [4]. An Australian study found
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that the incidence of skin cancer in kidney transplant recipients increased by 5% annually starting 1-year posttransplantation, rising to a cumulative 44% after 9 years [5]. Other types of skin tumors, such as viral warts, are also more prevalent in this population [6]. Given the high incidence of skin cancer in solid organ transplant recipients (SOTRs), it is imperative to educate these patients on their risk. Previous studies have investigated the impact of various educational interventions on patient knowledge after transplant [7e11]. To the best of our knowledge, there are few data regarding SOTR knowledge of skin cancer risk and *Address correspondence to Parth Patel, BS, 3550 Terrace St, M240 Scaife Hall, Pittsburgh, PA 15261. Tel: þ1 (412)-648-8714. E-mail: [email protected] ª 2017 Elsevier Inc. All rights reserved. 230 Park Avenue, New York, NY 10169
Transplantation Proceedings, 49, 1318e1324 (2017)
SKIN CANCER EDUCATION IN KIDNEY RECIPIENTS
education regarding preventative measures immediately after transplant. Assessing patient knowledge during this early post-transplant period would allow us to redirect educational efforts to the most receptive time. The purpose of the current study was to assess the baseline knowledge of kidney transplant recipients immediately after SOT, via a questionnaire, and then to reassess their knowledge following a 5-minute educational video emphasizing skin cancer prevalence, risk, and prevention. We also wanted to determine whether lifestyle modifications had been implemented 4 to 8 months after the intervention. METHODS Participants and Setting Approval for this interventional study was issued by the University of Pittsburgh Institutional Review Board (PRO15110066). Patients were recruited from the University of Pittsburgh Medical Starzl Transplantation Institute from January 2016 to June 2016. Informed consent was obtained from all participants. Patients were eligible to participate if they were 18 years of age or older at time of transplant, able to speak and comprehend English, and within 2 months from date of transplantation. We did not exclude patients based on type of organ received. Patients were excluded if they had a history of prior transplant, did not have mental capacity to consent, or did not meet any of the inclusion criteria. Of note, patients received the standard immunosuppression protocol of thymoglobulin induction with tacrolimus and mycophenolate mofetil maintenance.
Data Collection We developed a 13-item questionnaire (pretest) to administer to patients after obtaining consent. This was developed with review of the literature. This questionnaire consisted of 6 background questions, assessing the patient’s educational level, family and or personal history of skin cancer, pretransplant education, and general knowledge of increased risk of skin cancer; the remaining 7 questions were knowledge-based questions, assessing the patient’s knowledge regarding skin cancer risk and prevention (Supplementary Questionnaire 1). Once patients had completed this questionnaire, they were shown a 5-minute educational video regarding skin cancer risk in SOTRs and steps toward prevention. The educational video consisted of a PowerPoint (Microsoft, Redmond, Wash, United States) presentation with voiceover and was shown on an iPad (Apple, Cupertino, Calif, United States). Immediately after the educational intervention, patients were given a post-test, which was the same questionnaire as the pretest, excluding the first 6 background questions. The entire process, including the pretest, video, and post-test, took approximately 15 minutes to complete. The questionnaire and viewing of the video took place at a mean of 16.7 (range 3e54) days post-transplantation. To assess how much knowledge our patients had retained and applied, we did a follow-up evaluation at 4 to 8 months from the initial intervention. Patients were contacted via phone and were asked the questions listed on the original post-test. In addition, they were asked 3 yes-or-no questions (regarding use of sunscreen, avoidance of midday sun, and follow-up with dermatology) to assess how many skin cancer prevention techniques they had applied to their lives (Supplementary Questionnaire 2).
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Data Analysis
Sample Size. The sample size in our study was 40 patients. This number was chosen to allow us to detect a significant improvement from pretest to post-test, with conservative estimates of standard deviation. Primary and Secondary Outcomes. The primary outcome measure of this study was participants’ knowledge of skin cancer before and after our educational intervention as measured by average pretest and post-test score differences. The long-term retention of knowledge (measured by pretest and follow-up score differences) and application of knowledge were our secondary outcomes. For knowledge questions (7e13), respondents were assigned a score from 0 to 7 total questions correct, with 1 point assigned for each fully correct answer (partial credit was assigned for a “check all that apply” question, with ¼ awarded for each correct choice and another ¼ point awarded for not selecting the incorrect choice). Preintervention scores, postintervention scores, and long-term follow-up scores were summarized with means and standard deviations. Within-respondent comparisons between preintervention and postintervention scores, as well as between preintervention and long-term follow-up scores, were examined via paired t test analysis. Other background and follow-up questions were summarized with frequencies and percentages. Two-sided P values < .05 were determined to be statistically significant. All analysis was conducted in IBM SPSS version 24 (IBM Corp, Armonk, NY, United States). RESULTS
Patient background information, as assessed by questions 1 to 6a in the pretest, is detailed in Table 1. In our cohort of patients, the preintervention knowledge score mean was 2.475 with a standard deviation of 1.288 (Fig 1). After watching the educational video, the mean score improved to 5.831 with a standard deviation of 1.287 (Fig 2). In comparing patient performance on the postintervention test versus the preintervention test, the mean difference was 3.356, with P < .001, showing a statistically significant increase in knowledge score (Fig 3). With regard to long-term follow-up (4e8 months from intervention), 30 out of the original 40 respondents participated (75% follow-up rate). The mean follow-up score was 4.275, with standard deviation of 1.099 (Fig 4). The mean preintervention score was 2.533 among the 30 patients who also had a valid follow-up response. This is an average improvement of 1.742, with P < .001, showing a statistically significant increase between the preintervention and followup scores (Fig 5). Finally, we also investigated the patient’s actions based on their sustained knowledge. Regarding the use of sunscreen, 18 patients (60%) reported using sunscreen during the summer between the intervention and the follow-up. Of the 18 patients who reported using sunscreen, 17 (94.4%) said they had been using sunscreen more consistently after watching the educational video compared with their use prior to the intervention. With respect to avoiding midday sun, 27 (90%) said they had implemented this lifestyle change, and 3 (10%) said they had not. In terms of followup with dermatology, 14 (46.7%) said they had either seen a
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PATEL, BIBEE, LIM ET AL Table 1. Patient Background Information Characteristics
Type of organ (1 patient received a simultaneous liver-kidney transplant) Kidney Liver Intestine Highest degree of education completed Did not complete high school High school degree Undergraduate degree Graduate degree Frequency of use of medical websites for information Never Once a week Once in the last month Once in the last year Number of skin cancers prior to transplant 0 1 2 Family history of skin cancer Yes No Given educational information about skin cancer during pretransplant evaluation? Yes No Before transplant, were you aware of higher risk of skin cancer post-transplant? Yes No If aware of higher risk, how concerned?
Very concerned Moderately concerned Somewhat concerned A little bit concerned Not concerned
n (%)
35 (87.5) 4 (10) 1 (2.5) 4 14 17 5
(10) (35) (42.5) (12.5)
15 12 11 2
(37.5) (30) (27.5) (5)
38 (95) 1 (2.5) 1 (2.5) 3 (7.5) 37 (92.5)
11 (27.5) 29 (72.5)
23 (57.5) 17 (42.5) Valid percent reported (n ¼ 19, 4 patients erroneously omitted question) 0 (0) 8 (42.1) 3 (7.5) 6 (15) 2 (5)
Fig 1. Distribution of pretest scores (maximum possible score of 7). Abbreviation: Std. Dev., standard deviation.
18.23e46.10]) [14,15]. In our study, we found that over half (57.5%) of patients were aware that they would be at an increased risk for skin cancer post-transplant. However, despite this knowledge, none of the patients expressed being “very concerned” about this risk. Patients underestimate the risk and complications of skin cancer in comparison with other post-transplant complications. Previous studies have affirmed that patients are not effectively given adequate information regarding skin cancer [16,17]. In our study, only 27.5% of patients reported receiving educational information on skin cancer risk while being evaluated for their transplant, despite this education
dermatologist or were scheduled to see one, and the remaining 16 (53.3%) had done neither.
DISCUSSION
The top 3 causes of death in kidney transplant patients are cardiovascular disease, malignancies, and infections [12,13]. The likelihood of dying from skin cancer in SOTRs is significantly increased when compared with the general population, with skin cancer having the highest incremental risk of death for SOTRs, including all cancer deaths (standardized mortality ratio, 29.82 [95% confidence interval,
Fig 2. Distribution of post-test scores (maximum possible score of 7). Abbreviation: Std. Dev., standard deviation.
SKIN CANCER EDUCATION IN KIDNEY RECIPIENTS
Fig 3. Distribution of post-test minus pretest scores (positive values indicate improvement). Abbreviation: Std. Dev., standard deviation.
being a standard element of pretransplant evaluation at our institution. Therefore, even when information is given during the initial evaluation, it is often not retained by the patients. This lack of retention may be due to the long interval from evaluation to transplant due to long wait-list times. General nephrologists and dialysis unit staff who have more frequent and regular contact with patients prior to transplant may be able to improve patient awareness pretransplant. During the peritransplant time period, recipients focus more on their immediate health concerns as opposed to long-term complications such as skin cancer [8,18e20].
Fig 4. Distribution of follow-up scores (maximum possible score of 7). Abbreviation: Std. Dev., standard deviation.
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Fig 5. Distribution of follow-up scores minus pretest scores (positive values indicate improvement). Abbreviation: Std. Dev., standard deviation.
Williams et al demonstrated that kidney transplant recipients prioritized current health issues, such as graft survival, existing comorbid illnesses, and medication side effects in the immediate post-transplant period and had limited capacity to absorb information about long-term risks [18]. Based on these findings, patients should be re-educated during the post-transplant period, after the stress of the acute phase, to reiterate the increased risk and promote risk reduction measures. Studies have repeatedly shown the benefit of educating SOTRs regarding their increased risk of skin cancer posttransplant and the resulting positive impact on patient behavior [7e11]. Other studies have assessed the effectiveness of various modes of education (ie, brochures vs videos) [8,21,22]. In accordance with these prior studies, the current study showed an increased knowledge of skin cancer and prevention in patients immediately after intervention and at a follow-up period, suggesting that a video intervention is an effective way to increase patient knowledge in both the short-term and long-term periods. This study adds to existing literature, in particular, through its focus on intervention in the early post-transplant period and assessment of patient knowledge and behavior at a follow-up period. The study shows that patients are applying this knowledge in their everyday lives, as noted by the affirmative responses to sunscreen use and avoidance of midday sun. Furthermore, 50% had either seen a dermatologist or were scheduled to see one by our follow-up period. Our data demonstrate that the majority of our patients are engaging in sun-protective behaviors during long-term follow-up, suggesting they understood and responded to our skin cancer education given in the postoperative period. Given the longitudinal relationships that nephrologists develop with their transplant patients, we believe that they
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have a unique opportunity to educate patients regarding skin cancer risk and positively influence their behavior using this educational video during post-transplant visits. Our video intervention is unique in its ease of implementation, requires no specific training for the administrator and a minimal time commitment for both the patient and the administrator, and can be routinely offered to patients during outpatient follow-up visits, for example, when patients are waiting to be seen. We believe that integrating this education during early post-transplant visits would provide patients with a level of baseline knowledge they can begin to apply even before they see a dermatologist. Our study has several limitations. First, our study included a small percentage of nonrenal transplant recipients (12.5%). Consequently, a difference in perceived skin cancer risk in recipients of nonrenal organs compared with risk perceived by kidney transplant recipients may have introduced bias. Additionally, our study involved a small cohort of patients from a single center, mostly Caucasian, and our data may not be generalizable to the renal transplant population nationwide. In addition, our study may have been subject to selection bias, because 10 eligible individuals refused to participatedpatients who chose to enroll in the study may have been more interested in learning about their risk of skin cancer and implementing behavioral changes. Furthermore, 10 patients (25%) were lost to follow-up, primarily due to voluntary refusal. Finally, with regard to our 3 follow-up questions, it is possible that these questions were susceptible to response bias. Questions from a physician about health behaviors may tend to elicit overly positive responses to avoid guilt or blame [23]. In summary, our study suggests that incorporating additional skin cancer education into the transplant timeline (perhaps in the first 1 or 2 outpatient follow-up visits) with an easy-to-administer educational video and questionand-answer form increases patient knowledge and influences positive sun-protective behavior. By reiterating this risk in the post-transplant period, our hope is that patients will be more proactive in taking preventative measures as well as seeking appropriate dermatologic care after transplantation. ACKNOWLEDGMENTS We thank the staff at the Clinical Translational Science Institute at the University of Pittsburgh for their help in formulating the questionnaire and performing data analysis.
REFERENCES [1] O’Reilly Zwald F, Brown M. Skin cancer in solid organ transplant recipients: advances in therapy and management: Part I. Epidemiology of skin cancer in solid organ transplant recipients. J Am Acad Dermatol 2011;65:253e61. [2] United Network for Organ Sharing. Providing More Opportunity for Transplant Candidates: 2015 in Review. https://www. unos.org/about/annual-report/ [accessed 20.11.16].
PATEL, BIBEE, LIM ET AL [3] The National Kidney Foundation. Organ donation and transplantation statistics, https://www.kidney.org/news/newsroom/ factsheets/Organ-Donation-and-Transplantation-Stats [accessed 07.01.17]. [4] Euvrard S, Kanitakis J, Claudy A. Skin cancers after organ transplantation. N Engl J Med 2003;348:1681e91. [5] Hardie IR, Strong RW, Hartley LC, et al. Skin cancer in Caucasian renal allograft recipients living in a subtropical climate. Surgery 1980;87:177e83. [6] Kwak EJ, Julian K. Human papillomavirus infection in solid organ transplant recipients. Am J Transplant 2009;9:151e60. [7] Feuerstein I, Geller AC. Skin cancer education in transplant recipients. Prog Transplant 2008;18:232e41. [8] Trinh N, Novice K, Lekakh O, Means A, Tung R. Use of a brief educational video administered by a portable video device to improve skin cancer knowledge in the outpatient transplant population. Dermatol Surg 2014;40:1233e9. [9] Robinson JK, Turrisi R, Mallett KA, et al. Efficacy of an educational intervention with kidney transplant recipients to promote skin self-examination for squamous cell carcinoma detection. Arch Dermatol 2011;147:689. [10] Clowers-Webb HE, Christenson LJ, Phillips PK, et al. Educational outcomes regarding skin cancer in organ transplant recipients. Arch Dermatol 2006;142(6):712e8. [11] Robinson JK, Guevara Y, Gaber R, et al. Efficacy of a sun protection workbook for kidney transplant recipients: a randomized controlled trial of a culturally sensitive educational intervention. Am J Transplant 2014;14:2821e9. [12] Matas AJ, Smith JM, Skeans MA, et al. OPTN/SRTR 2013 annual data report: kidney. Am J Transplant 2015;15(Suppl 2): 1e34. [13] Briggs JD. Causes of death after renal transplantation. Nephrol Dial Transplant 2001;16:1545e9. [14] Lott DG, Manz R, Koch C, Lorenz RR. Aggressive behavior of nonmelanotic skin cancers in solid organ transplant recipients. Transplantation 2010;90:683e7. [15] Acuna SA, Fernandes KA, Daly C, et al. Cancer mortality among recipients of solid-organ transplantation in Ontario, Canada. JAMA Oncol 2016;2:463. [16] Cramer E, Rasmussen K, Jemec GBE. Patients’ knowledge of the risk of skin cancer following kidney transplantation. Ugeskr Laeger 2009;171:3341e5. [17] National Kidney Foundation. Cancer risk after transplantation: a report to transplant professionals on recipients’ knowledge, awareness of risk, and preventive actions related to malignancy, http://nephrologyassociatesyakima.com/kidneyhealth/ TransMaligReport.pdf; 2006 [accessed 20.11.16]. [18] Williams NC, Tong A, Howard K, Chapman JR, Craig JC, Wong G. Knowledge, beliefs and attitudes of kidney transplant recipients regarding their risk of cancer. Nephrology 2012;17:300e6. [19] Cowen EW, Billingsley EM. Awareness of skin cancer by kidney transplant patients. J Am Acad Dermatol 1999;40(5 Pt 1): 697e701. [20] Muehrer RJ, Becker BN. Psychosocial factors in patients with chronic kidney disease: life after transplantation: new transitions in quality of life and psychological distress. Semin Dial 2005;18(2):124e31. [21] Idriss NZ, Alikhan A, Baba K, Armstrong AW. Online, video-based patient education improves melanoma awareness: a randomized controlled trial. Telemed J E Health 2009;15: 992e7. [22] Robinson JK, Friedewald JJ, Desai A, Gordon EJ. A randomized controlled trial of a mobile medical app for kidney transplant recipients. Transplant Direct 2016;2:e51. [23] Short ME, Goetzel RZ, Pei X, et al. How accurate are selfreports? Analysis of self-reported health care utilization and absence when compared with administrative data. J Occup Environ Med 2009;51:786e96.
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SUPPLEMENTARY QUESTIONNAIRE 1: PRETEST QUESTIONNAIRE (WITH ANSWERS IN BOLD) SOT Patient Knowledge of Skin Cancer Survey
9. How frequently should sunscreen be re-applied, regardless of sun protection factor (SPF)? A. Every hour B. Every 2 hours C. Every 4 hours D. Sunscreen does not need to be re-applied E. I don’t know 10. What is the minimum SPF to provide adequate protection of your skin from ultraviolet radiation, for everyday use? A. 4 B. 8 C. 15 D. 30 E. 80 F. I don’t know 11. How much sunscreen should be applied to exposed areas of the body (ie, face, arms, hands, ears, etc)? A. The equivalent of a “shot glass” (ie, about 2 tablespoons or 1 ounce) B. A “quarter-sized” amount C. Half of a cup (4 ounces) D. I don’t know 12. Which of the following will help to decrease your risk of skin cancer (choose all that apply)? A. Avoidance of midday sun (10 AM to 4 PM) B. Use of sun protective clothing C. Daily use of sunscreen of adequate SPF D. Using a tanning bed to get a “base tan” prior to sun exposure 13. How often should post-transplant patients see a dermatologist at the very minimum? A. Once a year B. Once every 2 years C. Once every 6 months (2 times a year) D. Once every 3 months (4 times a year) E. I don’t know
Choose the one, best answer for each question unless indicated otherwise. 1. What is your highest degree or level of education completed? A. Did not complete high school B. High school degree C. Undergraduate degree D. Graduate degree 2. In general, how often do you visit medical-related websites for information? A. Never B. Once a week C. Once in the last month D. Once in the last year 3. Did you have any skin cancers before your transplant surgery? A. Yes (list the approximate number in the blank) ______________ B. No 4. Do you have a family history of skin cancer? A. Yes B. No 5. Were you given any educational information regarding skin cancer while being evaluated for your organ transplant? A. Yes B. No 6. Before you received a transplant, were you aware that you would be at a higher risk for skin cancer posttransplant? A. Yes B. No 6a. If you answered yes to question 5, how concerned were you about your increased risk of skin cancer? A. Very concerned B. Moderately concerned C. Somewhat concerned D. A little bit concerned E. Not concerned 7. What is the most common type of skin cancer in transplant recipients? A. Melanoma B. Squamous cell carcinomas C. Basal cell carcinomas D. Merkel cell carcinomas E. I don’t know 8. How does appropriate use of sunscreen change the likelihood of getting skin cancer, including melanoma? A. Decreases the risk by 20% B. Decreases the risk by 50% C. Decreases the risk by 90% D. Does not change the risk E. I don’t know
SUPPLEMENTARY QUESTIONNAIRE 2: FOLLOW-UP QUESTIONNAIRE (WITH ANSWERS IN BOLD)
1. What is the most common type of skin cancer in transplant recipients? A. Melanoma B. Squamous cell carcinomas C. Basal cell carcinomas D. Merkel cell carcinomas E. I don’t know 2. How does appropriate use of sunscreen change the likelihood of getting skin cancer, including melanoma? A. Decreases the risk by 20% B. Decreases the risk by 50% C. Decreases the risk by 90% D. Does not change the risk E. I don’t know
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3. How frequently should sunscreen be reapplied, regardless of sun protection factor (SPF)? A. Every hour B. Every 2 hours C. Every 4 hours D. Sunscreen does not need to be reapplied E. I don’t know 4. What is the minimum SPF to provide adequate protection of your skin from ultraviolet radiation, for everyday use? A. 4 B. 8 C. 15 D. 30 E. 80 F. I don’t know 5. How much sunscreen should be applied to exposed areas of the body (ie, face, arms, hands, ears, etc)? A. The equivalent of a “shot glass” (ie, about 2 tablespoons or 1 ounce) B. A “quarter-sized” amount C. Half of a cup (4 ounces) D. I don’t know
PATEL, BIBEE, LIM ET AL
6. Which of the following will help to decrease your risk of skin cancer (choose all that apply)? A. Avoidance of midday sun (10 AM to 4 PM) B. Use of sun protective clothing C. Daily use of sunscreen of adequate SPF D. Using a tanning bed to get a “base tan” prior to sun exposure 7. How often should post-transplant patients see a dermatologist at the very minimum? A. Once a year B. Once every two years C. Once every 6 months (2 times a year) D. Once every 3 months (4 times a year) E. I don’t know Follow-up Questions
1. Did you use sunscreen this summer? A. If yes, have you been using sunscreen more consistently in comparison to before our intervention? 2. Are you avoiding midday sun? 3. Have you seen a dermatologist or are you scheduled to see one?
ABSTRACT Background. Skin cancer is the most common malignancy after solid organ transplant and can lead to significant morbidity. The likelihood of developing squamous cell carcinomas and melanomas is 100 and 2.4 times more likely, respectively, in kidney transplant recipients when compared with the general population. There are few data regarding the assessment and influence of solid organ transplant recipient (SOTR) knowledge of skin cancer and its effect on short- and long-term awareness and behavior. Methods. The purpose of this study was to assess the baseline knowledge of SOTR immediately after transplantation, and then to reassess their knowledge following a 5minute educational video. We also wanted to determine whether lifestyle modifications had been implemented 4 to 8 months after the intervention. Results. Forty patients were enrolled within 2 months of transplantation. Eighty-seven percent of patients were renal transplant recipients, and 75% of patients were available for long-term follow-up. There was a significant increase in knowledge in the immediate postintervention period, which was sustained at 4- to 8-month follow-up, as assessed by patient questionnaire. Patients appeared to be applying this knowledge by participating in lifestyle risk modification and positive sun-protective behavior. Conclusions. Our study suggests that incorporating additional skin cancer education into the early transplant timeline (perhaps in the first one or two outpatient follow-up visits) with an easy to administer educational video and question and answer form increases patient knowledge and influences positive sun-protective behavior.
HE NUMBER of patients living with a solid organ transplant (SOT) in the United States is increasing each year [1]. Of all organ transplants performed in 2014, 58% were kidney transplants, with a total of 17,107 patients receiving kidneys during this time [2,3]. Because of both direct and indirect consequences of the immunosuppression regimens and underlying disease, the likelihood of developing malignancies and infections is much higher in transplant patients than in the general population. Skin cancer is the most common type of malignancy encountered post SOT, with 95% of skin cancers being nonmelanoma skin cancers [1]. The likelihood of developing squamous cell carcinomas and melanomas is 100 and 2.4 times more likely, respectively, in kidney transplant patients when compared with the general population [4]. An Australian study found
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that the incidence of skin cancer in kidney transplant recipients increased by 5% annually starting 1-year posttransplantation, rising to a cumulative 44% after 9 years [5]. Other types of skin tumors, such as viral warts, are also more prevalent in this population [6]. Given the high incidence of skin cancer in solid organ transplant recipients (SOTRs), it is imperative to educate these patients on their risk. Previous studies have investigated the impact of various educational interventions on patient knowledge after transplant [7e11]. To the best of our knowledge, there are few data regarding SOTR knowledge of skin cancer risk and *Address correspondence to Parth Patel, BS, 3550 Terrace St, M240 Scaife Hall, Pittsburgh, PA 15261. Tel: þ1 (412)-648-8714. E-mail: [email protected] ª 2017 Elsevier Inc. All rights reserved. 230 Park Avenue, New York, NY 10169
Transplantation Proceedings, 49, 1318e1324 (2017)
SKIN CANCER EDUCATION IN KIDNEY RECIPIENTS
education regarding preventative measures immediately after transplant. Assessing patient knowledge during this early post-transplant period would allow us to redirect educational efforts to the most receptive time. The purpose of the current study was to assess the baseline knowledge of kidney transplant recipients immediately after SOT, via a questionnaire, and then to reassess their knowledge following a 5-minute educational video emphasizing skin cancer prevalence, risk, and prevention. We also wanted to determine whether lifestyle modifications had been implemented 4 to 8 months after the intervention. METHODS Participants and Setting Approval for this interventional study was issued by the University of Pittsburgh Institutional Review Board (PRO15110066). Patients were recruited from the University of Pittsburgh Medical Starzl Transplantation Institute from January 2016 to June 2016. Informed consent was obtained from all participants. Patients were eligible to participate if they were 18 years of age or older at time of transplant, able to speak and comprehend English, and within 2 months from date of transplantation. We did not exclude patients based on type of organ received. Patients were excluded if they had a history of prior transplant, did not have mental capacity to consent, or did not meet any of the inclusion criteria. Of note, patients received the standard immunosuppression protocol of thymoglobulin induction with tacrolimus and mycophenolate mofetil maintenance.
Data Collection We developed a 13-item questionnaire (pretest) to administer to patients after obtaining consent. This was developed with review of the literature. This questionnaire consisted of 6 background questions, assessing the patient’s educational level, family and or personal history of skin cancer, pretransplant education, and general knowledge of increased risk of skin cancer; the remaining 7 questions were knowledge-based questions, assessing the patient’s knowledge regarding skin cancer risk and prevention (Supplementary Questionnaire 1). Once patients had completed this questionnaire, they were shown a 5-minute educational video regarding skin cancer risk in SOTRs and steps toward prevention. The educational video consisted of a PowerPoint (Microsoft, Redmond, Wash, United States) presentation with voiceover and was shown on an iPad (Apple, Cupertino, Calif, United States). Immediately after the educational intervention, patients were given a post-test, which was the same questionnaire as the pretest, excluding the first 6 background questions. The entire process, including the pretest, video, and post-test, took approximately 15 minutes to complete. The questionnaire and viewing of the video took place at a mean of 16.7 (range 3e54) days post-transplantation. To assess how much knowledge our patients had retained and applied, we did a follow-up evaluation at 4 to 8 months from the initial intervention. Patients were contacted via phone and were asked the questions listed on the original post-test. In addition, they were asked 3 yes-or-no questions (regarding use of sunscreen, avoidance of midday sun, and follow-up with dermatology) to assess how many skin cancer prevention techniques they had applied to their lives (Supplementary Questionnaire 2).
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Data Analysis
Sample Size. The sample size in our study was 40 patients. This number was chosen to allow us to detect a significant improvement from pretest to post-test, with conservative estimates of standard deviation. Primary and Secondary Outcomes. The primary outcome measure of this study was participants’ knowledge of skin cancer before and after our educational intervention as measured by average pretest and post-test score differences. The long-term retention of knowledge (measured by pretest and follow-up score differences) and application of knowledge were our secondary outcomes. For knowledge questions (7e13), respondents were assigned a score from 0 to 7 total questions correct, with 1 point assigned for each fully correct answer (partial credit was assigned for a “check all that apply” question, with ¼ awarded for each correct choice and another ¼ point awarded for not selecting the incorrect choice). Preintervention scores, postintervention scores, and long-term follow-up scores were summarized with means and standard deviations. Within-respondent comparisons between preintervention and postintervention scores, as well as between preintervention and long-term follow-up scores, were examined via paired t test analysis. Other background and follow-up questions were summarized with frequencies and percentages. Two-sided P values < .05 were determined to be statistically significant. All analysis was conducted in IBM SPSS version 24 (IBM Corp, Armonk, NY, United States). RESULTS
Patient background information, as assessed by questions 1 to 6a in the pretest, is detailed in Table 1. In our cohort of patients, the preintervention knowledge score mean was 2.475 with a standard deviation of 1.288 (Fig 1). After watching the educational video, the mean score improved to 5.831 with a standard deviation of 1.287 (Fig 2). In comparing patient performance on the postintervention test versus the preintervention test, the mean difference was 3.356, with P < .001, showing a statistically significant increase in knowledge score (Fig 3). With regard to long-term follow-up (4e8 months from intervention), 30 out of the original 40 respondents participated (75% follow-up rate). The mean follow-up score was 4.275, with standard deviation of 1.099 (Fig 4). The mean preintervention score was 2.533 among the 30 patients who also had a valid follow-up response. This is an average improvement of 1.742, with P < .001, showing a statistically significant increase between the preintervention and followup scores (Fig 5). Finally, we also investigated the patient’s actions based on their sustained knowledge. Regarding the use of sunscreen, 18 patients (60%) reported using sunscreen during the summer between the intervention and the follow-up. Of the 18 patients who reported using sunscreen, 17 (94.4%) said they had been using sunscreen more consistently after watching the educational video compared with their use prior to the intervention. With respect to avoiding midday sun, 27 (90%) said they had implemented this lifestyle change, and 3 (10%) said they had not. In terms of followup with dermatology, 14 (46.7%) said they had either seen a
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PATEL, BIBEE, LIM ET AL Table 1. Patient Background Information Characteristics
Type of organ (1 patient received a simultaneous liver-kidney transplant) Kidney Liver Intestine Highest degree of education completed Did not complete high school High school degree Undergraduate degree Graduate degree Frequency of use of medical websites for information Never Once a week Once in the last month Once in the last year Number of skin cancers prior to transplant 0 1 2 Family history of skin cancer Yes No Given educational information about skin cancer during pretransplant evaluation? Yes No Before transplant, were you aware of higher risk of skin cancer post-transplant? Yes No If aware of higher risk, how concerned?
Very concerned Moderately concerned Somewhat concerned A little bit concerned Not concerned
n (%)
35 (87.5) 4 (10) 1 (2.5) 4 14 17 5
(10) (35) (42.5) (12.5)
15 12 11 2
(37.5) (30) (27.5) (5)
38 (95) 1 (2.5) 1 (2.5) 3 (7.5) 37 (92.5)
11 (27.5) 29 (72.5)
23 (57.5) 17 (42.5) Valid percent reported (n ¼ 19, 4 patients erroneously omitted question) 0 (0) 8 (42.1) 3 (7.5) 6 (15) 2 (5)
Fig 1. Distribution of pretest scores (maximum possible score of 7). Abbreviation: Std. Dev., standard deviation.
18.23e46.10]) [14,15]. In our study, we found that over half (57.5%) of patients were aware that they would be at an increased risk for skin cancer post-transplant. However, despite this knowledge, none of the patients expressed being “very concerned” about this risk. Patients underestimate the risk and complications of skin cancer in comparison with other post-transplant complications. Previous studies have affirmed that patients are not effectively given adequate information regarding skin cancer [16,17]. In our study, only 27.5% of patients reported receiving educational information on skin cancer risk while being evaluated for their transplant, despite this education
dermatologist or were scheduled to see one, and the remaining 16 (53.3%) had done neither.
DISCUSSION
The top 3 causes of death in kidney transplant patients are cardiovascular disease, malignancies, and infections [12,13]. The likelihood of dying from skin cancer in SOTRs is significantly increased when compared with the general population, with skin cancer having the highest incremental risk of death for SOTRs, including all cancer deaths (standardized mortality ratio, 29.82 [95% confidence interval,
Fig 2. Distribution of post-test scores (maximum possible score of 7). Abbreviation: Std. Dev., standard deviation.
SKIN CANCER EDUCATION IN KIDNEY RECIPIENTS
Fig 3. Distribution of post-test minus pretest scores (positive values indicate improvement). Abbreviation: Std. Dev., standard deviation.
being a standard element of pretransplant evaluation at our institution. Therefore, even when information is given during the initial evaluation, it is often not retained by the patients. This lack of retention may be due to the long interval from evaluation to transplant due to long wait-list times. General nephrologists and dialysis unit staff who have more frequent and regular contact with patients prior to transplant may be able to improve patient awareness pretransplant. During the peritransplant time period, recipients focus more on their immediate health concerns as opposed to long-term complications such as skin cancer [8,18e20].
Fig 4. Distribution of follow-up scores (maximum possible score of 7). Abbreviation: Std. Dev., standard deviation.
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Fig 5. Distribution of follow-up scores minus pretest scores (positive values indicate improvement). Abbreviation: Std. Dev., standard deviation.
Williams et al demonstrated that kidney transplant recipients prioritized current health issues, such as graft survival, existing comorbid illnesses, and medication side effects in the immediate post-transplant period and had limited capacity to absorb information about long-term risks [18]. Based on these findings, patients should be re-educated during the post-transplant period, after the stress of the acute phase, to reiterate the increased risk and promote risk reduction measures. Studies have repeatedly shown the benefit of educating SOTRs regarding their increased risk of skin cancer posttransplant and the resulting positive impact on patient behavior [7e11]. Other studies have assessed the effectiveness of various modes of education (ie, brochures vs videos) [8,21,22]. In accordance with these prior studies, the current study showed an increased knowledge of skin cancer and prevention in patients immediately after intervention and at a follow-up period, suggesting that a video intervention is an effective way to increase patient knowledge in both the short-term and long-term periods. This study adds to existing literature, in particular, through its focus on intervention in the early post-transplant period and assessment of patient knowledge and behavior at a follow-up period. The study shows that patients are applying this knowledge in their everyday lives, as noted by the affirmative responses to sunscreen use and avoidance of midday sun. Furthermore, 50% had either seen a dermatologist or were scheduled to see one by our follow-up period. Our data demonstrate that the majority of our patients are engaging in sun-protective behaviors during long-term follow-up, suggesting they understood and responded to our skin cancer education given in the postoperative period. Given the longitudinal relationships that nephrologists develop with their transplant patients, we believe that they
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have a unique opportunity to educate patients regarding skin cancer risk and positively influence their behavior using this educational video during post-transplant visits. Our video intervention is unique in its ease of implementation, requires no specific training for the administrator and a minimal time commitment for both the patient and the administrator, and can be routinely offered to patients during outpatient follow-up visits, for example, when patients are waiting to be seen. We believe that integrating this education during early post-transplant visits would provide patients with a level of baseline knowledge they can begin to apply even before they see a dermatologist. Our study has several limitations. First, our study included a small percentage of nonrenal transplant recipients (12.5%). Consequently, a difference in perceived skin cancer risk in recipients of nonrenal organs compared with risk perceived by kidney transplant recipients may have introduced bias. Additionally, our study involved a small cohort of patients from a single center, mostly Caucasian, and our data may not be generalizable to the renal transplant population nationwide. In addition, our study may have been subject to selection bias, because 10 eligible individuals refused to participatedpatients who chose to enroll in the study may have been more interested in learning about their risk of skin cancer and implementing behavioral changes. Furthermore, 10 patients (25%) were lost to follow-up, primarily due to voluntary refusal. Finally, with regard to our 3 follow-up questions, it is possible that these questions were susceptible to response bias. Questions from a physician about health behaviors may tend to elicit overly positive responses to avoid guilt or blame [23]. In summary, our study suggests that incorporating additional skin cancer education into the transplant timeline (perhaps in the first 1 or 2 outpatient follow-up visits) with an easy-to-administer educational video and questionand-answer form increases patient knowledge and influences positive sun-protective behavior. By reiterating this risk in the post-transplant period, our hope is that patients will be more proactive in taking preventative measures as well as seeking appropriate dermatologic care after transplantation. ACKNOWLEDGMENTS We thank the staff at the Clinical Translational Science Institute at the University of Pittsburgh for their help in formulating the questionnaire and performing data analysis.
REFERENCES [1] O’Reilly Zwald F, Brown M. Skin cancer in solid organ transplant recipients: advances in therapy and management: Part I. Epidemiology of skin cancer in solid organ transplant recipients. J Am Acad Dermatol 2011;65:253e61. [2] United Network for Organ Sharing. Providing More Opportunity for Transplant Candidates: 2015 in Review. https://www. unos.org/about/annual-report/ [accessed 20.11.16].
PATEL, BIBEE, LIM ET AL [3] The National Kidney Foundation. Organ donation and transplantation statistics, https://www.kidney.org/news/newsroom/ factsheets/Organ-Donation-and-Transplantation-Stats [accessed 07.01.17]. [4] Euvrard S, Kanitakis J, Claudy A. Skin cancers after organ transplantation. N Engl J Med 2003;348:1681e91. [5] Hardie IR, Strong RW, Hartley LC, et al. Skin cancer in Caucasian renal allograft recipients living in a subtropical climate. Surgery 1980;87:177e83. [6] Kwak EJ, Julian K. Human papillomavirus infection in solid organ transplant recipients. Am J Transplant 2009;9:151e60. [7] Feuerstein I, Geller AC. Skin cancer education in transplant recipients. Prog Transplant 2008;18:232e41. [8] Trinh N, Novice K, Lekakh O, Means A, Tung R. Use of a brief educational video administered by a portable video device to improve skin cancer knowledge in the outpatient transplant population. Dermatol Surg 2014;40:1233e9. [9] Robinson JK, Turrisi R, Mallett KA, et al. Efficacy of an educational intervention with kidney transplant recipients to promote skin self-examination for squamous cell carcinoma detection. Arch Dermatol 2011;147:689. [10] Clowers-Webb HE, Christenson LJ, Phillips PK, et al. Educational outcomes regarding skin cancer in organ transplant recipients. Arch Dermatol 2006;142(6):712e8. [11] Robinson JK, Guevara Y, Gaber R, et al. Efficacy of a sun protection workbook for kidney transplant recipients: a randomized controlled trial of a culturally sensitive educational intervention. Am J Transplant 2014;14:2821e9. [12] Matas AJ, Smith JM, Skeans MA, et al. OPTN/SRTR 2013 annual data report: kidney. Am J Transplant 2015;15(Suppl 2): 1e34. [13] Briggs JD. Causes of death after renal transplantation. Nephrol Dial Transplant 2001;16:1545e9. [14] Lott DG, Manz R, Koch C, Lorenz RR. Aggressive behavior of nonmelanotic skin cancers in solid organ transplant recipients. Transplantation 2010;90:683e7. [15] Acuna SA, Fernandes KA, Daly C, et al. Cancer mortality among recipients of solid-organ transplantation in Ontario, Canada. JAMA Oncol 2016;2:463. [16] Cramer E, Rasmussen K, Jemec GBE. Patients’ knowledge of the risk of skin cancer following kidney transplantation. Ugeskr Laeger 2009;171:3341e5. [17] National Kidney Foundation. Cancer risk after transplantation: a report to transplant professionals on recipients’ knowledge, awareness of risk, and preventive actions related to malignancy, http://nephrologyassociatesyakima.com/kidneyhealth/ TransMaligReport.pdf; 2006 [accessed 20.11.16]. [18] Williams NC, Tong A, Howard K, Chapman JR, Craig JC, Wong G. Knowledge, beliefs and attitudes of kidney transplant recipients regarding their risk of cancer. Nephrology 2012;17:300e6. [19] Cowen EW, Billingsley EM. Awareness of skin cancer by kidney transplant patients. J Am Acad Dermatol 1999;40(5 Pt 1): 697e701. [20] Muehrer RJ, Becker BN. Psychosocial factors in patients with chronic kidney disease: life after transplantation: new transitions in quality of life and psychological distress. Semin Dial 2005;18(2):124e31. [21] Idriss NZ, Alikhan A, Baba K, Armstrong AW. Online, video-based patient education improves melanoma awareness: a randomized controlled trial. Telemed J E Health 2009;15: 992e7. [22] Robinson JK, Friedewald JJ, Desai A, Gordon EJ. A randomized controlled trial of a mobile medical app for kidney transplant recipients. Transplant Direct 2016;2:e51. [23] Short ME, Goetzel RZ, Pei X, et al. How accurate are selfreports? Analysis of self-reported health care utilization and absence when compared with administrative data. J Occup Environ Med 2009;51:786e96.
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SUPPLEMENTARY QUESTIONNAIRE 1: PRETEST QUESTIONNAIRE (WITH ANSWERS IN BOLD) SOT Patient Knowledge of Skin Cancer Survey
9. How frequently should sunscreen be re-applied, regardless of sun protection factor (SPF)? A. Every hour B. Every 2 hours C. Every 4 hours D. Sunscreen does not need to be re-applied E. I don’t know 10. What is the minimum SPF to provide adequate protection of your skin from ultraviolet radiation, for everyday use? A. 4 B. 8 C. 15 D. 30 E. 80 F. I don’t know 11. How much sunscreen should be applied to exposed areas of the body (ie, face, arms, hands, ears, etc)? A. The equivalent of a “shot glass” (ie, about 2 tablespoons or 1 ounce) B. A “quarter-sized” amount C. Half of a cup (4 ounces) D. I don’t know 12. Which of the following will help to decrease your risk of skin cancer (choose all that apply)? A. Avoidance of midday sun (10 AM to 4 PM) B. Use of sun protective clothing C. Daily use of sunscreen of adequate SPF D. Using a tanning bed to get a “base tan” prior to sun exposure 13. How often should post-transplant patients see a dermatologist at the very minimum? A. Once a year B. Once every 2 years C. Once every 6 months (2 times a year) D. Once every 3 months (4 times a year) E. I don’t know
Choose the one, best answer for each question unless indicated otherwise. 1. What is your highest degree or level of education completed? A. Did not complete high school B. High school degree C. Undergraduate degree D. Graduate degree 2. In general, how often do you visit medical-related websites for information? A. Never B. Once a week C. Once in the last month D. Once in the last year 3. Did you have any skin cancers before your transplant surgery? A. Yes (list the approximate number in the blank) ______________ B. No 4. Do you have a family history of skin cancer? A. Yes B. No 5. Were you given any educational information regarding skin cancer while being evaluated for your organ transplant? A. Yes B. No 6. Before you received a transplant, were you aware that you would be at a higher risk for skin cancer posttransplant? A. Yes B. No 6a. If you answered yes to question 5, how concerned were you about your increased risk of skin cancer? A. Very concerned B. Moderately concerned C. Somewhat concerned D. A little bit concerned E. Not concerned 7. What is the most common type of skin cancer in transplant recipients? A. Melanoma B. Squamous cell carcinomas C. Basal cell carcinomas D. Merkel cell carcinomas E. I don’t know 8. How does appropriate use of sunscreen change the likelihood of getting skin cancer, including melanoma? A. Decreases the risk by 20% B. Decreases the risk by 50% C. Decreases the risk by 90% D. Does not change the risk E. I don’t know
SUPPLEMENTARY QUESTIONNAIRE 2: FOLLOW-UP QUESTIONNAIRE (WITH ANSWERS IN BOLD)
1. What is the most common type of skin cancer in transplant recipients? A. Melanoma B. Squamous cell carcinomas C. Basal cell carcinomas D. Merkel cell carcinomas E. I don’t know 2. How does appropriate use of sunscreen change the likelihood of getting skin cancer, including melanoma? A. Decreases the risk by 20% B. Decreases the risk by 50% C. Decreases the risk by 90% D. Does not change the risk E. I don’t know
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3. How frequently should sunscreen be reapplied, regardless of sun protection factor (SPF)? A. Every hour B. Every 2 hours C. Every 4 hours D. Sunscreen does not need to be reapplied E. I don’t know 4. What is the minimum SPF to provide adequate protection of your skin from ultraviolet radiation, for everyday use? A. 4 B. 8 C. 15 D. 30 E. 80 F. I don’t know 5. How much sunscreen should be applied to exposed areas of the body (ie, face, arms, hands, ears, etc)? A. The equivalent of a “shot glass” (ie, about 2 tablespoons or 1 ounce) B. A “quarter-sized” amount C. Half of a cup (4 ounces) D. I don’t know
PATEL, BIBEE, LIM ET AL
6. Which of the following will help to decrease your risk of skin cancer (choose all that apply)? A. Avoidance of midday sun (10 AM to 4 PM) B. Use of sun protective clothing C. Daily use of sunscreen of adequate SPF D. Using a tanning bed to get a “base tan” prior to sun exposure 7. How often should post-transplant patients see a dermatologist at the very minimum? A. Once a year B. Once every two years C. Once every 6 months (2 times a year) D. Once every 3 months (4 times a year) E. I don’t know Follow-up Questions
1. Did you use sunscreen this summer? A. If yes, have you been using sunscreen more consistently in comparison to before our intervention? 2. Are you avoiding midday sun? 3. Have you seen a dermatologist or are you scheduled to see one?