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Table. 
Characteristics of Organ Transplant Recipientsa
Characteristics of Organ Transplant Recipientsa
1.
Walder  BKRobertson  MRJeremy  D Skin cancer and immunosuppression. Lancet 1971;2 (7737) 1282- 1283
PubMedArticle
2.
Hartevelt  MMBavinck  JNKootte  AMVermeer  BJVandenbroucke  JP Incidence of skin cancer after renal transplantation in the Netherlands. Transplantation 1990;49 (3) 506- 509
PubMedArticle
3.
Bordea  CWojnarowska  FMillard  PRDoll  HWelsh  KMorris  JP Skin cancer in renal-transplant recipients occur more frequently than previously recognized in a temperate climate. Transplantation 2004;77 (4) 574- 579
PubMedArticle
4.
Bavinck  JN BouwesHardie  DRGreen  A  et al.  The risk of skin cancer in renal transplant recipients in Queensland, Australia: a follow-up study. Transplantation 1996;61 (5) 715- 721
PubMedArticle
5.
Ramsay  HMFryer  AAHawley  CMSmith  AGHarden  PN Non-melanoma skin cancer risk in the Queensland renal transplant population. Br J Dermatol 2002;147 (5) 950- 956
PubMedArticle
6.
Fuente  MJSabat  MRoca  JLauzurica  RFernández-Figueras  MTFerrándiz  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;149 (6) 1221- 1226
PubMedArticle
7.
Bavinck  JNDe Boer  AVermeer  BJ  et al.  Sunlight, keratotic skin lesions and skin cancer in renal transplant recipients. Br J Dermatol 1993;129 (3) 242- 249
PubMedArticle
8.
Brown  JHHutchison  TKelly  AMMcGeown  MG Dermatological lesions in a transplant population. Transplantation 1988;46 (4) 530- 532
PubMedArticle
9.
Caforio  ALFortina  ABPiaserico  S  et al.  Skin cancer in heart transplant recipients: risk factor analysis and relevance of immunosuppressive therapy. Circulation 2000;102 (19) ((suppl 3)) III222- III227
PubMedArticle
10.
McLelland  JRees  AWilliams  GChu  T The incidence of immunosuppression-related skin disease in long-term transplant patients. Transplantation 1988;46 (6) 871- 874
PubMedArticle
11.
Euvrard  SKanitakis  JPouteil-Noble  C  et al.  Comparative epidemiologic study of premalignant and malignant epithelial cutaneous lesions developing after kidney and heart transplantation. J Am Acad Dermatol 1995;33 (2, pt 1) 222- 229
PubMedArticle
12.
Glanz  KSchoenfeld  EWeinstock  MALayi  GKidd  JShigaki  DM Development and reliability of a brief skin cancer risk assessment tool. Cancer Detect Prev 2003;27 (4) 311- 315
PubMedArticle
13.
Glanz  KYaroch  ALDancel  M  et al.  Measures of sun exposure and sun protection practices for behavioral and epidemiologic research. Arch Dermatol 2008;144 (2) 217- 222
PubMedArticle
14.
Bavinck  JN BouwesEuvrard  SNaldi  L  et al. EPI-HPV-UV-CA group, Keratotic skin lesions and other risk factors are associated with skin cancer in organ-transplant recipients: a case-control study in The Netherlands, United Kingdom, Germany, France, and Italy. J Invest Dermatol 2007;127 (7) 1647- 1656
PubMed
Research Letter
March 2010

Distribution of Skin Type and Skin Cancer in Organ Transplant Recipients

Author Affiliations

Author Affiliations: Department of Dermatology, Northwestern University Feinberg School of Medicine, Chicago, Illinois (Mss Buoy and Ortiz and Drs Yoo, Alam, West, and Robinson); and Institute for Healthcare Studies, Division of Organ Transplantation, Northwestern University Feinberg School of Medicine, Chicago, Illinois (Dr Gordon).

Arch Dermatol. 2010;146(3):344-346. doi:10.1001/archdermatol.2009.397

The higher risk of skin cancer, especially squamous cell carcinoma (SCC), in the organ transplant recipient (OTR) population compared with the general population is well documented.13 Cumulative incidences have been noted as high as 70% to 82.1% in kidney transplant recipients (KTRs) after 20 years of immunosuppression.4,5 In the OTR population, high sun exposure,6 especially in the first 30 years of life, increased age at the time of the transplant,7 and length of exposure to immunosuppressive therapy3,8 are associated with the development of skin cancer. Bordea et al3 found that exposure to immunosuppression for over 10 years conferred a risk of skin cancer almost 10 times higher than exposure to immunosuppression for less than 5 years.

For SCC, an adjusted odds ratio of 4.3 was found for KTRs with Fitzpatrick skin type 1 or 2 to develop SCC.7 Among KTRs who developed skin cancer, skin type 2 was the most common skin type and was a statistical risk factor with a hazard ratio of 3.4 for KTRs developing any type of skin tumor; however, inclusion of KTRs with all skin types was very limited.911 Our hypothesis is that OTRs with skin types 3 through 6 have less risk of developing skin cancer than those with skin types 1 and 2. Given similar environmental exposure to UV light, we hypothesized that the duration of immunosuppression prior to developing skin cancer would be greater for OTRs with skin types 3 through 6 than for those with skin types 1 and 2. Our study of OTRs with all skin types investigated skin cancer development and age of OTR at time of transplant, skin type, and duration of immunosuppression.

Methods

From 2007 to 2009, we conducted 10-minute telephone interviews of OTRs whose transplants were performed at Northwestern Memorial Hospital in Chicago, Illinois, between November 12, 1977, and January 8, 2009. Skin type, date(s) and type of transplant(s), duration of immunosuppression, and skin cancer history were based on participants' self-reports. Participants were asked to select the response that most closely described their skin tone among the following 6 choices: very fair, fair, olive, light brown, dark brown, and very dark. The skin color scale has good reliability (κ = 0.71) and validity compared with the standard Fitzpatrick phototype scale.12,13 We reviewed the medical record to confirm the date of the transplant(s), and the pathology report, when available, to confirm the type of skin cancer. The research was approved by the institutional review board of Northwestern University.

Cumulative incidences of skin cancer were computed for 2 categories: (1) OTRs with skin type 1 or 2; and (2) OTRs with skin types 3 through 6. The number of person-years of immunosuppression was computed between the date of the transplant (used as the starting date) and either the date of skin cancer diagnosis (considered as the end point) or the end of the study (October 2009). A χ2 test was used to detect differences among groups. In all analyses, a 2-sided α level of .05 was considered statistically significant.

Results

Among the 775 living OTRs with valid telephone numbers, 743 participated, for a 95% response rate, and 32 declined to participate because they were too busy. The participants consisted of 63 liver transplant recipients and 680 KTRs. Development of skin cancer was associated with skin types 1 and 2 and age greater than that of those who did not develop skin cancer (P < .001) (Table). A longer period of immunosuppression was associated with development of skin cancer in all OTRs (P < .001). Five percent of those with skin types 3 through 5 developed skin cancer compared with 19% of those with skin type 1 or 2.

Comment

In this study, skin cancer in OTRs was associated with skin types 1 and 2, older age at the time of the transplant, and longer duration of immunosuppression. Interestingly, 5% of those with skin types 3 through 5 developed skin cancer compared with 19% of those with skin types 1 and 2; therefore, darker skin conferred some protection against developing skin cancer. Other studies of OTRs have not defined the incidence of skin cancer among those with skin types 3 through 5.10 In our study, the mean duration of immunosuppression prior to developing skin cancer was greater in those with darker skin; however, it was within the average time of development of skin cancer previously estimated to range from 4 to 9 years after an organ transplant.14

Limitations of our study included the relatively small number of OTRs with skin types 3 through 5, self-report of skin type, our inability to confirm the cumulative dose of immunosuppression, and in some cases our inability to review the pathology report to confirm the type of skin cancer. Our database did not include assessment of sun damage or precancerous lesions at the time of the transplant or history of sun exposure prior to the transplant.

The limited protective effect of skin pigmentation against carcinogenic UV light was demonstrated in our study of OTRs with all skin types. Organ transplant recipients with skin types 3 through 5 underwent a longer period of immunosuppression than those with skin types 1 or 2 before developing skin cancer. All OTRs must receive sun protection messages, take primary prevention measures to minimize their sun exposure, and undergo regular skin examinations with their dermatologists.

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Article Information

Correspondence: Dr Robinson, 132 E Delaware Pl, No. 5806, Chicago, IL 60611 (june-robinson@northwestern.edu).

Author Contributions:Study concept and design: Yoo and Robinson. Acquisition of data: Buoy, Alam, and Robinson. Analysis and interpretation of data: Buoy, Ortiz, West, Gordon, and Robinson. Drafting of the manuscript: Buoy and Robinson. Critical revision of the manuscript for important intellectual content: Buoy, Yoo, Ortiz, West, and Gordon. Administrative, technical, and material support: Buoy, Yoo, Ortiz, West, and Robinson. Study supervision: West and Robinson.

Financial Disclosure: None reported.

Disclaimer: Dr Robinson is the Editor of the Archives of Dermatology, but she was not involved in any of the decisions regarding review of the manuscript or its acceptance.

Additional Contributions: Rob Turrisi, PhD, provided statistical analysis. The support of the members of the Solid Organ Transplantation Team of Northwestern Memorial Hospital is appreciated, especially Michael I. Abecassis, MD, John J. Friedewald, MD, Josh Levitsky, MD, Xunrong Luo, MD, and Daniel R. Ganger, MD.

References
1.
Walder  BKRobertson  MRJeremy  D Skin cancer and immunosuppression. Lancet 1971;2 (7737) 1282- 1283
PubMedArticle
2.
Hartevelt  MMBavinck  JNKootte  AMVermeer  BJVandenbroucke  JP Incidence of skin cancer after renal transplantation in the Netherlands. Transplantation 1990;49 (3) 506- 509
PubMedArticle
3.
Bordea  CWojnarowska  FMillard  PRDoll  HWelsh  KMorris  JP Skin cancer in renal-transplant recipients occur more frequently than previously recognized in a temperate climate. Transplantation 2004;77 (4) 574- 579
PubMedArticle
4.
Bavinck  JN BouwesHardie  DRGreen  A  et al.  The risk of skin cancer in renal transplant recipients in Queensland, Australia: a follow-up study. Transplantation 1996;61 (5) 715- 721
PubMedArticle
5.
Ramsay  HMFryer  AAHawley  CMSmith  AGHarden  PN Non-melanoma skin cancer risk in the Queensland renal transplant population. Br J Dermatol 2002;147 (5) 950- 956
PubMedArticle
6.
Fuente  MJSabat  MRoca  JLauzurica  RFernández-Figueras  MTFerrándiz  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;149 (6) 1221- 1226
PubMedArticle
7.
Bavinck  JNDe Boer  AVermeer  BJ  et al.  Sunlight, keratotic skin lesions and skin cancer in renal transplant recipients. Br J Dermatol 1993;129 (3) 242- 249
PubMedArticle
8.
Brown  JHHutchison  TKelly  AMMcGeown  MG Dermatological lesions in a transplant population. Transplantation 1988;46 (4) 530- 532
PubMedArticle
9.
Caforio  ALFortina  ABPiaserico  S  et al.  Skin cancer in heart transplant recipients: risk factor analysis and relevance of immunosuppressive therapy. Circulation 2000;102 (19) ((suppl 3)) III222- III227
PubMedArticle
10.
McLelland  JRees  AWilliams  GChu  T The incidence of immunosuppression-related skin disease in long-term transplant patients. Transplantation 1988;46 (6) 871- 874
PubMedArticle
11.
Euvrard  SKanitakis  JPouteil-Noble  C  et al.  Comparative epidemiologic study of premalignant and malignant epithelial cutaneous lesions developing after kidney and heart transplantation. J Am Acad Dermatol 1995;33 (2, pt 1) 222- 229
PubMedArticle
12.
Glanz  KSchoenfeld  EWeinstock  MALayi  GKidd  JShigaki  DM Development and reliability of a brief skin cancer risk assessment tool. Cancer Detect Prev 2003;27 (4) 311- 315
PubMedArticle
13.
Glanz  KYaroch  ALDancel  M  et al.  Measures of sun exposure and sun protection practices for behavioral and epidemiologic research. Arch Dermatol 2008;144 (2) 217- 222
PubMedArticle
14.
Bavinck  JN BouwesEuvrard  SNaldi  L  et al. EPI-HPV-UV-CA group, Keratotic skin lesions and other risk factors are associated with skin cancer in organ-transplant recipients: a case-control study in The Netherlands, United Kingdom, Germany, France, and Italy. J Invest Dermatol 2007;127 (7) 1647- 1656
PubMed
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