Skin cancer prevention education for kidney transplant recipients: a systematic evaluation of Internet sites

ContextRepeated patient education about skin cancer prevention is important to self-care after transplant. ObjectiveExamine educational materials for kidney transplant recipients available on the Internet that address sun protection and skin self-examination for early detection of squamous cell carcinoma. DesignSystematic review of Web sites for kidney transplant recipients endorsed by transplant physicians and dermatologists. ParticipantsAn expert panel of 8 dermatologists providing care for kidney transplant recipients and 1 research medical anthropologist. Main Outcome MeasuresReading grade level, inclusion of people with skin of color, sufficient content to support effective sun protection, and description of 4 sun-protection strategies and skin self-examination. ResultsOf the 40 sites identified, 11 contained information about sun protection or increased risk of any type of cancer. The Web sites had a ninth-grade median reading level (range, seventh grade to college senior). Interrater reliability for the 25-item assessment tool was assessed by Fleiss kappa ( = 0.87). Skin cancer risk was presented as relevant to those with fair skin. Sites recommended regular use of sunscreen with sun-protection factor of 15 or greater (n = 3) to reduce the risk of skin cancer (n = 4). Few sites recommended using protective clothing (n = 5), seeking shade (n = 4), and avoiding deliberate tanning with indoor or outdoor light (n = 1). Five sites recommended skin self-examination ConclusionBecause many patients seek self-management information from the Internet, Web sites must provide more thorough educational information about skin cancer prevention and health promotion at a lower reading grade level. (Progress in Transplantation. 2010;20:344-349)

June K. Robinson, MD, Murad Alam, MD, Neda Ashourian, MD, Misbah Khan, MD, Roopal Kundu, MD, Anne E. Laumann, MD, Bethanee J. Schlosser, MD, Simon Yoo, MD, Elisa J. Gordon, PhD
Northwestern University Feinberg School of Medicine, Chicago, Ilinois
MD,

Corresponding author: June Robinson, 132 E. Delaware Place #5806, Chicago, IL 60611 (e-mail: june-robinson@northwestern.edu) To purchase electronic or print reprints, contact: The InnoVision Group 101 Columbia, Aliso Viejo, CA 92656 Phone (800) 809-2273 (ext 532) or (949) 448-7370 (ext 532) Fax (949) 362-2049 E-mail reprints@aacn.org

quamous cell carcinoma, which develops predominantly in sun-exposed areas of the body, occurs more frequently with longer duration of immunosuppression.1 After 20 years of immunosuppression, cumulative incidences of squamous cell carcinoma as high as 70% to 82.1% have been noted in kidney transplant recipients (KTRs). 2,3 Skin cancer incidence among KTRs is greater in areas with high solar exposure, such as Australia,3,4 than in areas with low solar exposure, such as the Netherlands.5 This geographic difference in skin cancer incidence among KTRs as well as the predilection for squamous cell carcinoma to occur on commonly sun-exposed areas of the body suggests that sun protection after transplantation may reduce the risk of skin cancer developing. In the first year after transplantation, clinicians have the best opportunity to provide counseling. However, delivery of sun-protection education varies widely, with 60% of transplant centers providing a verbal
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warning and 20% written information.6,7 Counseling usually consisted of telling KTRs that they are at risk of squamous cell carcinoma developing and advising them to use sun protection.8 The absence of uniform guidelines as to when transplant centers transfer care of KTRs to community nephrologists may undermine systematic education of patients.9 In 2006, focus groups of KTRs convened by the National Kidney Foundation indicated that clinicians rarely implemented education about the risks and prevention of skin cancer after transplant, or if they did so, the scope was inadequate to affect behavior.10 Although most KTRs did not recall learning that they were at increased risk of skin cancer developing, many used sunscreen in preparation for planned sun exposure.8 KTRs desired primary and secondary skin cancer self-management information, but did not understand the instructions given to them in the immediate postoperative period, and often sought information from the Internet.11

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Methods We used the terms human kidney transplant and human renal transplant in an exhaustive Internet search for Web sites endorsed by health care organizations, transplant physicians, or dermatologists. Each site was reviewed for information about sun protection or any cancer. If such information was found, then the pages were downloaded, de-identified, formatted, and printed in color for evaluation with an assessment tool that contained 22 questions, 3 of which used 5-point Likert scales. The reading grade level of Web sites was assessed by using 3 measures of reading level to capture different facets of readability: (1) Lexile Measure: values translate to corresponding reading grade levels. (2) Flesch-Kincaid Grade Level: provides a reading score that correlates with grade level. (3) Gunning Fog Index: measures the average number of words per sentence, the length and difficulty of words, and correlates with the hypothetical number of years of full-time education needed to comprehend the text. The volunteer experts, consisting of 8 academic dermatologists providing care for KTRs and 1 research medical anthropologist who examines ways to improve care for KTRs, were selected on the basis of their content expertise in sun protection and early detection of squamous cell carcinoma and their familiarity with clinical care of KTRs. A set of celebrity images labeled with the skin tone was distributed to the expert panel with printed copies of Web-based educational materials and an assessment tool for each Web site. Numbers were randomly assigned to the printed copies from the categories of hospital-affiliated sites and KTR support group sites. In our previous research, the celebrity images were selected by focus groups composed of people of color, who agreed upon
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Little is known about the availability and quality of Internet sites in the provision of education about sun protection to KTRs. Studies commonly document the limitations of the Internet because of the variable quality and accuracy of educational information and reading levels.12,13 These factors, compounded by characteristics of the KTR population, may undermine the ability of Internet messages to be effective for educating KTRs. Considering that a third of KTRs have limited health literacy, KTRs may not comprehend written educational messages.14-16 KTRs receptivity to educational messages depends on whether the messages are linguistically and culturally sensitive, which is especially important given that minorities comprise 38% of living KTRs.17 In this study, we evaluated the quality of educational materials about sun protection and skin self-examination for KTRs available on the Internet. Our evaluation included the assessment of reading grade level and cultural sensitivity of the educational materials.

Skin cancer prevention education for kidney transplant recipients images representing the following skin tones: very fair (Marcia Cross), fair (Renee Zellweger, David Beckham), olive (Enrique Iglesias, Sandra Oh, Yao Ming), light brown (Jennifer Lopez, Eva Longoria, Parminder Nagra, Barack Obama), dark brown (Will Smith, Tiger Woods), and very dark (Michael Jordan). 18 Panel members assessed the skin type of people represented visually and verbally in the Web-based materials. The content of the Web-based materials was evaluated in terms of engaging in skin self-examination and 4 sun-protection strategies: (1) regular use of sunscreen with an SPF of 15 or higher; (2) wearing protective clothing consisting of a shirt with sleeves, long pants, and a hat with a specified brim width; (3) seeking shade when outdoors; and (4) not engaging in deliberate tanning with indoor or outdoor light. The panel also assessed whether the material was presented in separate, manageable steps for sunscreen use, wearing protective clothing, and seeking shade. Of the 25 assessment items, 17 items were dichotomous (yes/no), 5 were multiple choice, and 3 used 5point Likert scales (see assessment form in the Figure). For example, if the regular use of sunscreen was recommended, the panel selected the definition of regular use of sunscreen from the following choices: daily use all year long, daily use when a person anticipates being outdoors, daily use on areas not covered by clothing when a person anticipates being outdoors, use in warm weather months, and use when going to the beach or pool. If the regular use of sunscreen was not recommended, then the subsequent items had no response entered. The Web sites were assessed for recommendations to perform skin self-examination, description of how to perform skin self-examination, and presentation of skin self-examination in separate manageable steps with each of the 3 items having yes/no responses. If the Web site recommended performing skin selfexamination, then the panel chose as many benefits as applied, including finding a potentially concerning spot in the early and treatable phase, being able to alert the doctor to take a look at something, being reassured by the lack of change in a spot that was being watched, and feeling like you are doing everything that you can to take care of yourself. If the material described how to perform skin self-examination, then the panel was asked to choose as many ways as applied, for example, check the skin for raised, rough, red areas, check to see if the diameter increases rapidly (in about 2 weeks), check to see if the spot bleeds spontaneously, or invite a partner to check hard-to-see places. The panel assigned a score from 1 (not at all) to 5 (very well) for the explanation of the benefits of performing skin selfexamination and the description of how to perform skin self-examination. The institutional review board of Northwestern University approved the study.

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Robinson et al
1. Does the material describe the importance of USING SUNSCREEN? (Circle one response) No Yes IF THE ANSWER IS NO, THEN GO TO QUESTION 8 2. Does the material describe the importance of REGULARLY USING SUNSCREEN? (Circle one response) No Yes 3. Is the REGULAR USE OF SUNSCREEN defined? (Circle one response) No Yes IF THE ANSWER IS NO, THEN GO TO QUESTION 5. 4. The REGULAR USE OF SUNSCREEN is defined as: (Circle one response) A) Daily use all year long B) Daily use when the person expects to be outdoors C) Daily use on areas not covered by clothing when the person expects to be outdoors D) Use during warm weather months E) Use when the person is going to the beach or pool 5. Does the material recommend an SPF RATING of the sunscreen? (Circle one response) No Yes IF THE ANSWER IS NO, THEN GO TO QUESTION 7. 6. The SPF RATING of the sunscreen recommended is: (Circle one response) A) 15 or greater B) 30 or greater C) 45 or greater D) The highest number that can be found 7. To what extent did the material describe the following BENEFITS that come from using SUNSCREEN. 14. Is the reader presented with the opportunity to make choices among the SUN PROTECTION STRATEGIES in order to adapt the strategies to their lifestyle? For instance, if a person does not chose to use sunscreen because they consider it messy, or too expensive, are they given a choice of using protective clothing? (Circle one response) No Yes 15. Did the material recommend PERFORMING SKIN SELFEXAMINATION for skin cancer? (Circle one response) No Yes IF NO, THEN GO TO QUESTION 19. 16. To what extent did the material describe the BENEFITS of PERFORMING SKIN SELF-EXAMINATION for skin cancer? The potential benefits of skin self-examination are A) Finding a potentially concerning spot in the early and treatable phase B) Being able to alert the doctor to take a look at something, C) Being reassured by the lack of change in a spot that is being watched. D) Feeling like you are doing everything that you can to take care of yourself. (Circle one response in the rating 1-5) Not at all = 1 1 item = 2 2 items = 3 3 items = 4 All 4 items = 5 Very Poorly Somewhat Poorly OK Somewhat Well Very Well 1 2 3 4 5 17. Did the material describe how to PERFORM SKIN SELFEXAMINATION for skin cancer? (Circle one response) No Yes IF NO, THEN GO TO QUESTION 19.

18. To what extent did the material describe how to PERFORM SKIN SELF-EXAMINATION for skin cancer? The potential ways to check the skin are The potential benefits of using sunscreen are A) check the skin for raised, rough, red areas A) Preventing painful sunburns, B) check to see if the diameter increases rapidly (in about 2 B) Reducing premature wrinkles of the skin, weeks) C) Reducing irregular pigment of the skin, C) check to see if the spot bleeds spontaneously D) Reducing the risk of developing skin cancer? D) invite a partner to check hard-to-see places (Circle one response in the rating 1-5) Not at all = 1 1 item = 2 2 items = 3 3 items = 4 All 4 items = 5 (Circle one response in the rating 1-5) Very Poorly Somewhat Poorly OK Somewhat Well Very Well Not at all = 1 1 item = 2 2 items = 3 3 items = 4 All 4 items = 5 1 2 3 4 5 Very Poorly Somewhat Poorly OK Somewhat Well Very Well 1 2 3 4 5 8. Does the material describe the importance of WEARING A SHIRT WITH SLEEVES? (Circle one response) 19. Does the material break down the goal of sun protection into separate, manageable steps for SUNSCREEN USE? No Yes (Circle one response) 9. Does the material describe the importance of WEARING No Yes LONG PANTS? (Circle one response) 20. Does the material break down the goal of sun protection No Yes into manageable steps for WEARING PROTECTIVE CLOTH10. Does the material describe the importance of WEARING A ING (ie, hat with a 4-inch brim, shirt with sleeves, long HAT? (Circle one response) pants)? (Circle one response) No Yes No Yes IF NO, THEN GO TO QUESTION 12. 21. Does the material break down the goal of sun protection 11. Does the material recommend a certain WIDTH OF THE into manageable steps for SEEKING SHADE? BRIM of the hat? (Circle one response) For example: When the sun is high in the sky, seek shade. If No Yes you are outdoors between 10 AM and 4 PM, seek shade whenever possible. Even on an overcast day, it is best to seek shade 12. Does the material describe the importance of SEEKING between the hours of 10AM and 4 PM. (Circle one response) SHADE whenever possible? (Circle one response) No Yes No Yes 13. Does the material recommend NO DELIBERATE TANNING 22. Does the material break down SKIN SELF-EXAMINATION into separate, manageable steps? (Circle one response) WITH INDOOR OR OUTDOOR LIGHT? (Circle one response) No Yes No Yes Figure Assessment form: evaluation of educational materials.

Skin cancer prevention education for kidney transplant recipients Results The Internet search using Google, Yahoo, and Bing search engines for the terms human kidney transplant or human renal transplant yielded 780 sites. When the sites were examined for discussion of risks of kidney transplantation that included skin cancer or the need for primary or secondary prevention measures among KTRs, 40 Web sites professionally endorsed by transplant physicians and dermatologists were identified. Sites 1, 3, 7, and 10 were supported by hospitals with transplant programs, and sites 2, 4, 5, 6, 8, 9, and 11 were supported by KTR support groups. Eleven sites mentioned sun protection or increased risk of cancer of any type. The Web sites had a ninth-grade median reading level (range, sixth grade to graduate school; Table 1). The 9-member panel comprised 2 men and 7 women; 4 were white and 5 were people of color. The 1 Web site that included people of color discussed susceptibility to tumors but did not mention skin cancer or its prevention. The remaining sites presented skin cancer information as being relevant to KTRs with fair skin. The most prevalent (6/11) recommendation was to use sunscreen to reduce the risk of skin cancer developing. Regular use of sunscreen was recommended by a few sites for daily use (n = 4), all year round (n = 3), and when anticipating being outdoors (n = 1). In the 3 instances when an SPF rating was advised, an SPF of 15 or greater was given. Few sites recommended wearing a hat (n = 5), seeking shade (n = 4), or wearing a long sleeved shirt or long pants (n = 2). Only 1 site mentioned avoiding deliberate tanning with indoor or outdoor light (Table 2). Skin self-examination was recommended by 5 sites. Two of the 5 sites provided the warning signs of
Table 1 Reading grade levels of Internet sites about selfmanagement by kidney transplant patientsa Literacy assessments Site No. 1 2 3 4 5 6 7 8 9 10 11 Lexile measure 1185L 1187L 1105L 1375L 1130L 1460L 1200L 1240L 970L 1340L 1190L Flesch-Kincaid Grade Level 9.0 7.9 8.9 10.7 9.0 14.5 9.9 7.5 6.2 11.5 10.0 Gunning Fog Index 12.0 11.7 12.5 13.7 11.6 17.7 12.5 11.9 9.6 14.7 12.7

a Web sites were analyzed by using 3 measures of reading level: Lexile measure, Flesch-Kincaid Grade Level, and Gunning Fog Index. Lexile values translate to corresponding reading grade levels. Flesch-Kincaid Grade Level provides a reading score that correlates with grade level. Gunning Fog Index measures the average number of words per sentence and the length and difficulty of words. It correlates with the hypothetical number of years of full-time education needed to comprehend the text.

skin cancer and described the benefits of early detection, and 1 suggested seeing a dermatologist regularly. Three sites endorsed keeping a watch on the skin but failed to discuss warning signs of skin cancer. The interrater reliability for the 25 items was assessed by Fleiss kappa ( = 0.87).

Table 2 Advice about sun protection on Internet sites for self-management by kidney transplant patients Use sunscreen Site No. 1 2 3 4 5 6 7 8 9 10 11 Important (Yes/No) Yes Yes Yes Yes No No No Yes Yes No No Regular (Yes/No) Yes Yes No Yes No No Yes No No No No SPF (Yes/No) Yes No No Yes No No Yes Yes Yes No No Benefit,a mean (SD) 1.5 (0.5) 1.0 1.5 (0.5) 2.0 1.0 1.0 2.0 2.0 1.3 (0.2) 1.0 1.0 Wear protective clothing Shirt Pants Hat Brim Seek shade No tanning (Yes/No) (Yes/No) (Yes/No) (Yes/No) (Yes/No) (Yes/No) Yes No No Yes No No No No No No No Yes No No Yes No No No No No No No Yes Yes No Yes No No Yes No Yes No No Yes No No Yes No No No No No No No Yes Yes No Yes No No Yes No No No No No No No Yes No No No No No No No

Abbreviation: SPF, sun-protection factor. a Benefit scale from 1 to 5, where 1 = not at all, 2 = 1 item, 3 = 2 items, 4 = 3 items, 5 = all 4 items.

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Robinson et al Discussion Recommendations about primary and secondary skin cancer prevention provided by Internet Web sites for KTRs that are professionally endorsed by transplant physicians or dermatologists are incomplete. A particularly important oversight is the failure to recommend avoiding deliberate tanning with indoor or outdoor light. Furthermore, we found that the Web sites failed to provide manageable steps and explanations of the benefits of the behaviors. The style of the Web sites was to prescribe rather than describe, and the reading level was generally higher than recommended for lay readers. Last, the sun-protection messages targeted people with fair skin and did not include those with skin tones ranging from olive to very dark. As a consequence, people of color may not perceive that skin protection is necessary and therefore may be at increased risk for squamous cell carcinoma. Thus, it is imperative that Internet sites become culturally sensitive by including KTRs with darker skin in the recommendations to use sun protection in the verbal and pictorial messages. Our previous work with organ transplant recipients identified the belief that no authoritative source exists for primary and secondary skin cancer prevention.11 In the immediate postoperative period, transplant recipients were faced with many stressors that affected their adherence to the medical regimen and physicians instructions.19 The organ transplant recipients felt it best to receive sun-protection information about 4 to 6 months after transplantation and skin cancer early detection warnings about 1 year after transplantation. Repetitive patient education needs to be started and continued across a continuum of time during which the KTR may be transferred from the tertiary care center to the community nephrologists. The scope and intensity of education with reminders and repeated education of patients is challenging. Delivery of education on preventing skin cancer may be enhanced by the Internet, which can serve as an educational resource for KTRs; however, specific information must be presented in a way that engages and includes all KTRs. The cautionary warning that the level of sunburn awareness in the general community is not sufficiently explicit for immunosuppressed people is borne out by KTRs sun-protection attitudes and behaviors.10 In 2003, attitudes among KTRs about the appearance of a tan and looking healthier with a tan exceeded those of the general population (79% of 200 KTRs vs 69% of 1000 people randomly selected from the general population valued the appearance of a tan; 81% of KTRs vs 64% of general population think they look healthier with a tan).20 Approximately 23% of Canadian KTRs with fair skin engaged in intentional tanning.21 Intentional tanning by KTRs may be explained
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by the attitude that having a tan appears healthy, thus when KTRs begin to feel better after receiving a kidney transplant, the desire to appear healthy by having a tan leads to intentional tanning. Another possible reason for intentional tanning is that some KTRs experience skin hyperpigmentation associated with endstage renal disease.22 The skin hyperpigmentation, which may be interpreted as a tanned appearance, fades after transplantation. Some KTRs may intentionally tan to regain their customary appearance. Limitations of the study include the evolving nature of health information online; thus, Web sites may have been updated from the time that this study was performed. Despite the existence of search engines designed to retrieve information from Web sites that have been assigned quality labels (such as the one assigned by the Health on the Net Foundation), general search engines such as those used in this search (Google, Bing, and Yahoo) appear to be the most popular starting points for health information. A limitation of general searches is that the first page, which is the one most likely to be read, provided access to sites that have used optimization strategies in order to be placed on the first page. Sun-protection messages need to include KTRs with skin tones in the range of olive to dark brown. Although skin cancer is more prevalent in KTRs with very fair and fair skin, 5% of those with darker skin tones in our population had skin cancer develop in comparison with 19% of those with very fair or fair skin.23 Traditionally, sun protection and skin cancer awareness campaigns have targeted non-Hispanic whites, emphasizing a high-risk group of individuals with a propensity to sunburn rather than tan. Messages with qualifiers, such as light skin who sunburn easily, exclude people with skin tones in the range of olive to dark brown and promote the normative belief that darker pigmentation is completely protective against skin cancer, thus deterring people with skin of color from regularly monitoring the health status of their skin.24 With greater than a 90% survival rate for kidney, liver, and heart, an estimated 223 000 organ transplant recipients are living in the United States, most of whom are KTRs.17 Consistently providing information on preventing skin cancer and repetitive educational and skills building experiences to all members of this at-risk population is critically important. Because many KTRs seek self-management information from the Internet, Web sites need to provide more thorough educational information about skin cancer prevention and health promotion at a lower reading grade level.
Financial Disclosures None reported.

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Skin cancer prevention education for kidney transplant recipients

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