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Figure.
Questionnaire. BCC indicates basal cell carcinoma; MM, malignant melanoma; SCC, squamous cell carcinoma.

Questionnaire. BCC indicates basal cell carcinoma; MM, malignant melanoma; SCC, squamous cell carcinoma.

Table 1. 
Correlation Between Tumor Type, Tumor Site, Age at First Tumor, Time From Transplantation to First Tumor, Pretransplantation Sunburn, and Skin Type
Correlation Between Tumor Type, Tumor Site, Age at First Tumor, Time From Transplantation to First Tumor, Pretransplantation Sunburn, and Skin Type
Table 2. 
Characteristics Related to Sunscreen Use in Renal Transplant Recipients Before and After Transplantation*
Characteristics Related to Sunscreen Use in Renal Transplant Recipients Before and After Transplantation*
Table 3. 
Univariate Results of Risk Factors Pertaining to the Development of Skin Cancer
Univariate Results of Risk Factors Pertaining to the Development of Skin Cancer
Table 4. 
Multifactorial Model of Risk Factors Pertaining to the Development of Skin Cancer
Multifactorial Model of Risk Factors Pertaining to the Development of Skin Cancer
1.
Lindelof  BSigurgeirsson  BGabel  HStern  RS Incidence of skin cancer in 5356 patients following organ transplantation Br J Dermatol 2000;143513- 519
PubMed
2.
Jensen  PHansen  SMoller  B  et al.  Skin cancer in kidney and heart transplant recipients and different long-term immunosuppressive therapy regimes J Am Acad Dermatol 1999;40177- 186
PubMedArticle
3.
Hariharan  SJohnson  CPBresnahan  BATaranto  SEMcIntosh  MJStablein  D Improved graft survival after renal transplantation in the United States, 1988 to 1996 N Engl J Med 2000;342605- 612
PubMedArticle
4.
Almarzouqi  E Prevalence of Skin Cancer in Irish Renal Transplant Recipients[master’s thesis]  Dublin, Ireland Royal College of Surgeons May2002;
5.
Ramsay  HMFryer  AAHawley  CMSmith  AGHarden  PN Non-melanoma skin cancer risk in the Queensland renal transplant population Br J Dermatol 2002;147950- 956
PubMedArticle
6.
Seukeran  DCNewstead  CGCunliffe  WJ The compliance of renal transplant recipients with advice about sun protection measures Br J Dermatol 1998;138301- 303
PubMedArticle
7.
Gibson  GECodd  MBMurphy  GM Skin type distribution and skin disease in Ireland Ir J Med Sci 1997;16672- 74
PubMedArticle
8.
Rosso  SZanetti  RMartinez  C  et al.  The multicentre south European study “Helios,” II: different sun exposure patterns in the aetiology of basal cell and squamous cell carcinomas of the skin Br J Cancer 1996;731447- 1454
PubMedArticle
9.
Gupta  AKCardella  CJHaberman  HF Cutaneous malignant neoplasms in patients with renal transplants Arch Dermatol 1986;1221288- 1293
PubMedArticle
10.
Kricker  AArmstrong  BKEnglish  DRHeenan  PJ Does intermittent sun exposure cause basal cell carcinoma? a case-control study in Western Australia Int J Cancer 1995;60489- 494
PubMedArticle
11.
Fuente  MJSabat  MRoca  JLauzurica  RFernandez-Figueras  MTFerrandiz  C A prospective study of the incidence of skin cancer and its risk factors in a Spanish Mediterranean population of kidney transplant recipients Br J Dermatol 2003;1491221- 1226
PubMedArticle
12.
Green  AWilliams  GNeale  R  et al.  Daily sunscreen application and betacarotene supplementation in suppression of basal cell and squamous cell carcinomas of the skin Lancet 1999;354723- 729
PubMedArticle
13.
Kasiske  BLVasquez  MAHarmon  WE  et al.  Recommendations for the outpatient surveillance of renal transplant recipients J Am Soc Nephrol 2000;11S1- S86
PubMed
14.
Kelly  DAYoung  ARMcGregor  JMSeed  PTPotten  CSWalker  SL Sensitivity to sunburn is associated with susceptibility to ultraviolet radiation-induced suppression of cutaneous cell-mediated immunity J Exp Med 2000;191561- 566
PubMedArticle
15.
Branstrom  RBrandberg  YHolm  LSjoberg  LUllen  H Beliefs, knowledge and attitudes as predictors of sunbathing habits and use of sun protection among Swedish adolescents Eur J Cancer Prev 2001;10337- 345
PubMedArticle
16.
Bencini  PLMontagnino  GSala  FDe Vecchi  ACrosti  CTarantino  A Cutaneous lesions in 67 cyclosporin-treated renal transplant recipients Dermatologica 1986;17224- 30
PubMedArticle
17.
Neale  RWilliams  GGreen  A Application patterns among participants randomized to daily sunscreen use in a skin cancer prevention trial Arch Dermatol 2002;1381319- 1325
PubMedArticle
18.
Butt  ARoberts  DL Renal transplant recipients and protection from sun: need for education Lancet 1997;349179- 180
PubMedArticle
19.
Cowen  EWBillingsley  EM Awareness of skin cancer by kidney transplant patients J Am Acad Dermatol 1999;40697- 701
PubMedArticle
Study
August 2005

Sunscreen Use Before and After Transplantation and Assessment of Risk Factors Associated With Skin Cancer Development in Renal Transplant Recipients

Author Affiliations

Author Affiliations: Departments of Dermatology (Drs Moloney, Almarzouqi, and Murphy) and Nephrology (Mr O’Kelly and Dr Conlon), Beaumont Hospital, Dublin, Ireland.

Arch Dermatol. 2005;141(8):978-982. doi:10.1001/archderm.141.8.978
Abstract

Objective  To determine the degree of compliance with sunscreen use among renal transplant recipients before and after transplantation and to determine risk factors associated with skin carcinogenesis.

Design  Single-observer study with structured interview using a standardized questionnaire. Medical records and histology reports were examined for details of prior skin cancer. Cox proportional hazards regression was used for analysis of risk factors for developing skin cancer after transplantation.

Setting  Patients attending Beaumont Hospital, the national renal transplantation center in Dublin, Ireland.

Patients  The study population comprised 270 patients (182 male and 88 female).

Main Outcome Measures  Patients’ use of sunscreens before and after transplantation relative to known skin cancer risk factors and subsequent skin carcinogenesis.

Results  Prior to transplantation, 68.5% of patients never applied sunscreen on a sunny day compared with 25.9% after transplantation. Patients 50 years or younger were more likely to always apply sunscreen both before and after transplantation (P = .01), as were female patients prior to transplantation (P = .02). Those patients who participated in an outdoor recreation were more likely to subsequently develop nonmelanoma skin cancer (P = .04), as were those older than 50 years (P<.001) and those with a history of 2 or more painful sunburns (P = .03).

Conclusions  Transplant recipients are poorly compliant with the use of sunscreens both before and after transplantation. Compliance is poorest in those groups at higher risk of nonmelanoma skin cancer.

Renal transplant recipients develop neoplasms more commonly compared with the general population, especially squamous cell carcinoma (SCC) and basal cell carcinoma (BCC) of the skin.1 The risk of skin cancer increases in proportion to the duration of immunosuppressive drug use.2 The past decade has seen an exponential increase in the numbers of skin cancers, paralleling the noticeable improvement in long-term graft survival.3 Cumulative sun exposure is also a major contributing risk factor. Of Irish renal transplant recipients, 40% will develop skin cancer after 20 years since transplantation.4 In contrast, over a similar period, 82% of transplant patients in Queensland, Australia, have developed a skin cancer.5 Historically, skin cancer prevention had low priority in the pretransplantation and early posttransplantation period. Seukeran et al6 have previously highlighted poor compliance among transplant recipients with advised sun protection measures. The present study aimed to establish patterns of sunscreen use in the pretransplantation and posttransplantation settings, identify factors associated with poor compliance with sun protection measures, and outline a set of guidelines for skin cancer education and prevention in renal transplant recipients.

METHODS

A study of skin cancer prevalence was carried out from 2000 to 2001 in Beaumont Hospital, the national renal transplantation center in Dublin, Ireland. A total of 270 patients (182 male and 88 female) were interviewed in the setting of the renal and dermatology outpatient departments. The patients’ median age was 46.9 years (age range, 13.6-84.2 years), with a median duration since transplantation of 6.8years (range, 0.2-31.2 years). Most patients were receiving standard triple immunosuppressive therapy with cyclosporin, azathioprine, and prednisolone. Through the use of a standardized questionnaire (Figure), data were collected on cumulative occupational and recreational sun exposure, patient skin type according to Fitzpatrick standard criteria, history of 2 or more painful sunburns, sun bed use, personal or family history of skin cancer, and prior attendance at a dermatology clinic. Medical records and histology reports were examined for details of prior skin cancer.

For statistical purposes, patients with skin types I and II were compared with skin types III and IV. There were no patients with skin type V or VI. Outdoor occupation was classified as those patients who worked partially or completely outdoors during daylight hours between May and September for a minimum of 5 years. Outdoor recreation was classified as those patients who had hobbies that exposed them to a minimum of 1 hour per day of weekend sun for longer than 5 years. Patients were asked whether they would apply sunscreen if going out on a sunny day in a pretransplantation and posttransplantation setting. Fisher exact tests were used to compare selected pretransplantation and posttransplantation variables for the 3 categories of sunscreen use (ie, always, sometimes, never).

We also examined risk factors for developing skin cancer after transplantation and included sunscreen use as a predictor of outcome. Cox proportional hazards regression was used for risk analysis, and selected variables were analyzed individually and then as part of a combined model to test for independence of effect. The process of including variables in the multifactorial model follows a standard convention of placing significant (or close to significant) variables from univariate tests into the overall model. P<.05 was deemed statistically significant.

RESULTS

There was no history of malignant melanoma in the 270 patients interviewed. Fifty-six patients developed 100 nonmelanoma skin cancers (76 SCCs and 24 BCCs). Ten patients had both SCC and BCC (Table 1). All nonmelanoma skin cancers occurred predominantly on sun-exposed sites, in particular SCC with 93.5% situated on the arms or head and neck. The median time from transplantation to the development of first BCC (3.5 years) was slightly less than the median time to the development of first SCC (4 years); however, the median age at first tumor was older in the BCC group. There was no significant difference in pattern of sunburn history or skin type between those patients with SCC and those with BCC. There was, however, an overrepresentation of skin type I observed in those transplant recipients with skin cancer; 52.3% of transplant recipients who developed SCC and 54.5% of those who developed BCC had skin type I. The expected prevalence of skin type I in an Irish population is 26%.7

Prior to transplantation, 68.5% of the patients questioned admitted to having never applied sunscreen on a sunny day, with a further 25.9% applying occasionally. Only 5.6% had always applied sunscreen. After transplantation, the percentage that always applied sunscreen had increased to 36.7%; however, more than a quarter (25.9%) conceded that they would still never apply sunscreen on a sunny day.

Prior to transplantation, patients with the following characteristics were less likely to apply sunscreen on a sunny day: older than 50 years, male sex, outdoor occupation, outdoor hobbies, or a subsequent history of skin cancer (Table 2). Prior to transplantation, the median age of those who always applied sunscreen on a sunny day was 31.6 years (age range, 13.6-65.9 years) compared with a median age of 51.3 years (age range 18.4-84.2 years) for those who never applied sunscreen. Female patients were significantly more likely to apply sunscreen on a regular basis before transplantation. Of those transplant recipients who subsequently developed a skin cancer following transplantation, 80% reported taking no precautions for sun exposure, which was statistically significant (P = .03) when compared with those who remained cancer-free. Four transplant recipients had a history of skin cancer prior to transplantation, none of whom used sunscreen prior to the transplantation. Interestingly, the 45.5% of patients who worked outdoors and the 54.2% who enjoyed outdoor hobbies were less likely to apply sunscreen prior to transplantation.

After transplantation, there was again better compliance with sun avoidance measures in the younger age groups. A median age of 45.5 years (age range, 13.6-84.2 years) for those who always applied sunscreen compared with 53.9 years (age range, 18.6-80.6 years) for those who never applied sunscreen. There was no significant difference identified in sun protection habits after transplantation, based on sex, duration since transplant, skin type, family history of skin cancer, or attendance at a dermatology clinic.

Table 2 indicates that pattern of sunscreen use before transplantation is a significant predictor of skin cancer after transplantation. This association was not significant using a univariate Cox regression model (Table 3); however, the hazard ratio (0.61), indicates a decreased risk associated with the pretransplantation use of sunscreen. Variables that predicted skin cancer included older age, history of bad sunburn, and outdoor recreational sun exposure. Male sex, while indicating an influence on outcome, did not achieve significance. When the chosen variables were placed in a multifactorial model to test for independence of effect, only older age group remained significant at the 5% level (Table 4). This variable remained the dominant predictor of skin cancer outcome, with sunscreen use prior to transplantation and participation in an outdoor hobby having a lesser influence.

COMMENT

UV radiation is the major environmental cause for melanoma and nonmelanoma skin cancer. Skin cancer risk is determined by both total amount and patterns of sun exposure. Increased cumulative lifetime sun exposure is associated with increased risk of SCC.8 Transplant recipients are at particularly high risk of SCC, with up to a 100-fold increase in the relative risk compared with the population without transplants.1 After transplantation, skin cancer occurs primarily on sun-exposed sites. Of the SCC in our patient group, 93.5% occurred on the head, neck, dorsa of the hands, and forearms, which are traditionally sun-exposed sites. The relative risk of BCC after transplantation is also increased but to a lesser extent than SCC.9 It is perceived that infrequent intense exposure to UV may have a greater influence on increasing the risk of BCC compared with total cumulative UV exposure.10 This was not reflected in the sunburn histories of our patient group; however, sample size may not have been large enough to detect a difference. The short mean latent period from transplantation to development of first skin cancer in this study supports recent findings of a study in Mediterranean renal transplant recipients.11

Sunscreen use reduces the prevalence of actinic keratosis and recurrent SCCs in a nonimmunosuppressed population.12 For monitoring renal transplant recipients, sun avoidance and sunscreen application techniques are included in guidelines as part of a skin cancer reduction strategy.13 This study illustrated that female renal transplant recipients are much more likely to wear sunscreen than their male counterparts and also encouragingly showed that those transplant recipients who always applied sunscreen prior to transplantation were less likely to subsequently develop a skin cancer. Younger-aged renal transplant recipients were more likely to apply sunscreen both before and after transplantation, perhaps reflecting a poorer understanding in prior generations of the dangers of UV radiation. It is of concern that those with fairer skin types and high cumulative occupational and recreational sun exposure in our transplant population were no more likely to observe sun protective measures than were renal transplant recipients with lower skin cancer risk profiles. Kelly et al14 showed that skin types I and II are photoimmunosuppressed at lower levels of UV radiation exposure. The 2- to 3-fold greater sensitivity of skin types I and II for a given level of sunburn is linked to increased risk of skin cancer in later years. In this study, there was an overrepresentation of skin type I observed in those transplant recipients with skin cancer.14

It is equally concerning that duration since transplantation, attendance at a dermatology clinic, or even a prior skin cancer seem to have little bearing on sunscreen use. Prior studies suggest that knowledge of skin cancer and the damaging effect of sunbathing do not seem to affect sunbathing habits or use of sun protection.15

So why would more than a quarter of transplant recipients not wear sunscreen on a sunny day? The reasons given for not using sunscreens included the cost of sunscreens, lack of knowledge regarding the harmful effects of UV radiation, a belief that “my skin can take the sun,” simply forgetting to apply sunscreen, and finding sunscreens cosmetically unacceptable or impractical in a work environment. Cyclosporin induces sebaceous gland hyperplasia, folliculitis, acne, and hirsutism.16 Steroids also cause acne. Such factors are likely to have a significant effect on the cosmetic acceptability of a given sunscreen to transplant recipients. The physical or inorganic sunscreens, which are contained in most broad spectrum sunscreens recommended to transplant patients are greasy, comedogenic, and more difficult to rub in. Studies suggest that this cosmetic undesirability results in smaller amounts of sunscreen used, providing a sun protection factor of roughly half that achieved with chemical sunscreens.17 Newer sunscreens available in gel formulation are less greasy and likely to be more cosmetically acceptable.

Motivating people toward using immediate measures to prevent long-term problems has always proved a difficult prospect. This is particularly relevant in the transplant population. Previous studies have indicated that the transplant population complies poorly with sun avoidance measures, with only 57% applying a sunscreen and a minority wearing protective clothing when in the sun.5 This reflects sun protection patterns in the general population and points to the importance of public education campaigns about skin cancer protection.18 Other studies indicate that less than half of transplant recipients recalled receiving specific skin cancer education.19

To address the increasing skin cancer incidence and lack of awareness among transplant recipients, we have instituted protocols aimed at targeting those patients with the highest risk and poorest compliance with sun avoidance. Patients are stratified prior to transplantation into low-, intermediate-, and high-risk skin cancer groups based on skin type, hair and eye color, cumulative sun exposure, and history of skin cancer or precancerous lesion. All patients are given a detailed patient information leaflet on skin care after transplantation. The appropriate application of a cream- or gel-based sunscreen that protects across the UV-B and UV-A spectrum is advised. Allowances are made for those who cannot afford to pay for sunscreens to reclaim the expense under the medical card scheme. Low-risk patients, with no risk factors, are seen routinely 1 year after transplantation. Intermediate-risk patients have a full skin examination every 6 months after transplantation, while those that fall into the high-risk category are seen in a dermatology clinic every 3 months after transplantation. Very-high-risk patients may require monthly assessment. Education and reinforcement of written information on skin care received at time of transplantation occurs at each of the follow-up visits.

The improvement in graft survival outcomes has resulted in a significant increase in immunosuppression-related skin cancers. Lack of appropriate sun protection among the past generation of renal transplant recipients has contributed to this increase. Allowing for recall bias when determining cumulative sun exposure, skin type, and sunscreen use, this study illustrates poor compliance with sun protection measures, particularly in the patient groups at the highest risk of skin cancer. Raising patient awareness, regular skin screening after transplantation, and instituting sun protection protocols with hats, clothing, and cosmetically acceptable broad spectrum sunscreens are the cornerstones to tackling the increasing incidence of skin cancer in renal transplant recipients.

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Article Information

Correspondence: Fergal J. Moloney, MD, Education and Research Center, Beaumont Hospital, Dublin 9, Ireland (fergalmoloney@eircom.net).

Accepted for Publication: June 25, 2004.

Financial Disclosure: None.

References
1.
Lindelof  BSigurgeirsson  BGabel  HStern  RS Incidence of skin cancer in 5356 patients following organ transplantation Br J Dermatol 2000;143513- 519
PubMed
2.
Jensen  PHansen  SMoller  B  et al.  Skin cancer in kidney and heart transplant recipients and different long-term immunosuppressive therapy regimes J Am Acad Dermatol 1999;40177- 186
PubMedArticle
3.
Hariharan  SJohnson  CPBresnahan  BATaranto  SEMcIntosh  MJStablein  D Improved graft survival after renal transplantation in the United States, 1988 to 1996 N Engl J Med 2000;342605- 612
PubMedArticle
4.
Almarzouqi  E Prevalence of Skin Cancer in Irish Renal Transplant Recipients[master’s thesis]  Dublin, Ireland Royal College of Surgeons May2002;
5.
Ramsay  HMFryer  AAHawley  CMSmith  AGHarden  PN Non-melanoma skin cancer risk in the Queensland renal transplant population Br J Dermatol 2002;147950- 956
PubMedArticle
6.
Seukeran  DCNewstead  CGCunliffe  WJ The compliance of renal transplant recipients with advice about sun protection measures Br J Dermatol 1998;138301- 303
PubMedArticle
7.
Gibson  GECodd  MBMurphy  GM Skin type distribution and skin disease in Ireland Ir J Med Sci 1997;16672- 74
PubMedArticle
8.
Rosso  SZanetti  RMartinez  C  et al.  The multicentre south European study “Helios,” II: different sun exposure patterns in the aetiology of basal cell and squamous cell carcinomas of the skin Br J Cancer 1996;731447- 1454
PubMedArticle
9.
Gupta  AKCardella  CJHaberman  HF Cutaneous malignant neoplasms in patients with renal transplants Arch Dermatol 1986;1221288- 1293
PubMedArticle
10.
Kricker  AArmstrong  BKEnglish  DRHeenan  PJ Does intermittent sun exposure cause basal cell carcinoma? a case-control study in Western Australia Int J Cancer 1995;60489- 494
PubMedArticle
11.
Fuente  MJSabat  MRoca  JLauzurica  RFernandez-Figueras  MTFerrandiz  C A prospective study of the incidence of skin cancer and its risk factors in a Spanish Mediterranean population of kidney transplant recipients Br J Dermatol 2003;1491221- 1226
PubMedArticle
12.
Green  AWilliams  GNeale  R  et al.  Daily sunscreen application and betacarotene supplementation in suppression of basal cell and squamous cell carcinomas of the skin Lancet 1999;354723- 729
PubMedArticle
13.
Kasiske  BLVasquez  MAHarmon  WE  et al.  Recommendations for the outpatient surveillance of renal transplant recipients J Am Soc Nephrol 2000;11S1- S86
PubMed
14.
Kelly  DAYoung  ARMcGregor  JMSeed  PTPotten  CSWalker  SL Sensitivity to sunburn is associated with susceptibility to ultraviolet radiation-induced suppression of cutaneous cell-mediated immunity J Exp Med 2000;191561- 566
PubMedArticle
15.
Branstrom  RBrandberg  YHolm  LSjoberg  LUllen  H Beliefs, knowledge and attitudes as predictors of sunbathing habits and use of sun protection among Swedish adolescents Eur J Cancer Prev 2001;10337- 345
PubMedArticle
16.
Bencini  PLMontagnino  GSala  FDe Vecchi  ACrosti  CTarantino  A Cutaneous lesions in 67 cyclosporin-treated renal transplant recipients Dermatologica 1986;17224- 30
PubMedArticle
17.
Neale  RWilliams  GGreen  A Application patterns among participants randomized to daily sunscreen use in a skin cancer prevention trial Arch Dermatol 2002;1381319- 1325
PubMedArticle
18.
Butt  ARoberts  DL Renal transplant recipients and protection from sun: need for education Lancet 1997;349179- 180
PubMedArticle
19.
Cowen  EWBillingsley  EM Awareness of skin cancer by kidney transplant patients J Am Acad Dermatol 1999;40697- 701
PubMedArticle
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