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Table 1.  
Demographics and Clinical Characteristics of 259 Organ Transplant Recipients
Demographics and Clinical Characteristics of 259 Organ Transplant Recipients
Table 2.  
Skin Cancer by Organ Transplant Type
Skin Cancer by Organ Transplant Type
Table 3.  
Demographic and Clinical Factors Among Skin of Color Organ Transplant Recipients With Skin Cancer
Demographic and Clinical Factors Among Skin of Color Organ Transplant Recipients With Skin Cancer
Table 4.  
Skin Cancer Type and Location by Race
Skin Cancer Type and Location by Race
1.
United Network for Organ Sharing. https://optn.transplant.hrsa.gov/data/view-data-reports/national-data/#. Accessed May 9, 2016.
2.
Berg  D, Otley  CC.  Skin cancer in organ transplant recipients: Epidemiology, pathogenesis, and management.  J Am Acad Dermatol. 2002;47(1):1-17.PubMedGoogle ScholarCrossref
3.
Euvrard  S, Kanitakis  J, Claudy  A.  Skin cancers after organ transplantation.  N Engl J Med. 2003;348(17):1681-1691.PubMedGoogle ScholarCrossref
4.
Zwald  FO, 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(2):253-261.PubMedGoogle ScholarCrossref
5.
Gogia  R, Binstock  M, Hirose  R, Boscardin  WJ, Chren  MM, Arron  ST.  Fitzpatrick skin phototype is an independent predictor of squamous cell carcinoma risk after solid organ transplantation.  J Am Acad Dermatol. 2013;68(4):585-591.PubMedGoogle ScholarCrossref
6.
Buoy  AG, Yoo  S, Alam  M,  et al.  Distribution of skin type and skin cancer in organ transplant recipients.  Arch Dermatol. 2010;146(3):344-346.PubMedGoogle ScholarCrossref
7.
Agbai  ON, Buster  K, Sanchez  M,  et al.  Skin cancer and photoprotection in people of color: a review and recommendations for physicians and the public.  J Am Acad Dermatol. 2014;70(4):748-762.PubMedGoogle ScholarCrossref
8.
Kailas  A, Solomon  JA, Mostow  EN, Rigel  DS, Kittles  R, Taylor  SC.  Gaps in the understanding and treatment of skin cancer in people of color.  J Am Acad Dermatol. 2016;74(5):1020-1021.PubMedGoogle ScholarCrossref
9.
Battie  C, Gohara  M, Verschoore  M, Roberts  W.  Skin cancer in skin of color: an update on current facts, trends, and misconceptions.  J Drugs Dermatol. 2013;12(2):194-198.PubMedGoogle Scholar
10.
Gloster  HM  Jr, Neal  K.  Skin cancer in skin of color.  J Am Acad Dermatol. 2006;55(5):741-760.PubMedGoogle ScholarCrossref
11.
US Census Bureau. 2010 Census data. http://www.census.gov/2010census/data/. Accessed April 14, 2016.
12.
Karagas  MR, Nelson  HH, Sehr  P,  et al.  Human papillomavirus infection and incidence of squamous cell and basal cell carcinomas of the skin.  J Natl Cancer Inst. 2006;98(6):389-395.PubMedGoogle ScholarCrossref
13.
Arron  ST, Jennings  L, Nindl  I,  et al; Viral Working Group of the International Transplant Skin Cancer Collaborative (ITSCC) & Skin Care in Organ Transplant Patients, Europe (SCOPE).  Viral oncogenesis and its role in nonmelanoma skin cancer.  Br J Dermatol. 2011;164(6):1201-1213.PubMedGoogle ScholarCrossref
14.
Schmidt  SA, Hamilton-Dutoit  SJ, Farkas  DK, Steiniche  T, Sørensen  HT.  Human papillomavirus and the incidence of nonmelanoma and melanoma skin cancer using cervical conization as a surrogate marker: a nationwide population-based Danish cohort study.  Ann Epidemiol. 2015;25(4):293-296.e2.PubMedGoogle ScholarCrossref
15.
Connolly  K, Manders  P, Earls  P, Epstein  RJ.  Papillomavirus-associated squamous skin cancers following transplant immunosuppression: one Notch closer to control.  Cancer Treat Rev. 2014;40(2):205-214.PubMedGoogle ScholarCrossref
16.
Iftner  A, Klug  SJ, Garbe  C,  et al.  The prevalence of human papillomavirus genotypes in nonmelanoma skin cancers of nonimmunosuppressed individuals identifies high-risk genital types as possible risk factors.  Cancer Res. 2003;63(21):7515-7519.PubMedGoogle Scholar
17.
Wright  TC  Jr.  Cervical cancer screening in the 21st century: is it time to retire the PAP smear?  Clin Obstet Gynecol. 2007;50(2):313-323.PubMedGoogle ScholarCrossref
18.
Koh  D, Wang  H, Lee  J, Chia  KS, Lee  HP, Goh  CL.  Basal cell carcinoma, squamous cell carcinoma and melanoma of the skin: analysis of the Singapore Cancer Registry data 1968-97.  Br J Dermatol. 2003;148(6):1161-1166.PubMedGoogle ScholarCrossref
19.
Chuang  TY, Reizner  GT, Elpern  DJ, Stone  JL, Farmer  ER.  Nonmelanoma skin cancer in Japanese ethnic Hawaiians in Kauai, Hawaii: an incidence report.  J Am Acad Dermatol. 1995;33(3):422-426.PubMedGoogle ScholarCrossref
Original Investigation
December 2016

Nonmelanoma Skin Cancer in Nonwhite Organ Transplant Recipients

Author Affiliations
  • 1Department of Dermatology, Henry Ford Hospital, Detroit, Michigan
  • 2Department of Internal Medicine, Drexel University, Philadelphia, Pennsylvania
  • 3Department of Dermatology, Drexel University, Philadelphia, Pennsylvania
  • 4Department of Surgery, Drexel University, Philadelphia, Pennsylvania
JAMA Dermatol. 2016;152(12):1348-1353. doi:10.1001/jamadermatol.2016.3328
Key Points

Question  Should all organ transplant recipients, regardless of race, be evaluated for skin cancer?

Findings  A total of 413 transplant patients were evaluated. Most were nonwhite (62.7%), male (57.9%), and had had a kidney transplant (83.0%). Nineteen lesions were identified in 15 patients (5.8%) representing all 3 racial groups: black (6 [3.2%]), Asian (5 [14.3%]), and Hispanic (4 [12.1%]).

Meaning  This study underscores the importance of follow-up in a transplant dermatology center, a baseline total-body skin examination that includes a thorough inspection of the groin and genitalia and counseling regarding risk factors, and photoprotection for all organ transplant recipients.

Abstract

Importance  Organ transplant recipients have a higher incidence of skin cancer. This risk is magnified over time and with continued exposure to immunosuppression. Skin cancer in nonwhite patients is associated with greater morbidity and mortality owing to diagnosis at a more advanced stage, which suggests that nonwhite organ transplant recipients are at even higher risk.

Objective  To describe demographic and clinical factors and the incidence of skin cancer in nonwhite organ transplant recipients.

Design, Setting, and Participants  We performed a retrospective medical record review of patients who were organ transplant recipients (154 were white and 259 nonwhite [black, Asian, Hispanic, Pacific Islander]) seen from November 1, 2011, to April 18, 2016 at an academic referral center.

Main Outcomes and Measures  Variables were analyzed and compared between racial groups, including sex, age, race/ethnicity, Fitzpatrick type, type and location of skin cancer, type of organ transplanted, time to diagnosis of skin cancer after transplantation, and history of condyloma acuminata and/or verruca vulgaris.

Results  Most of the 413 patients (62.7%) evaluated were nonwhite organ transplant recipients; 264 were men, and 149 were women. Their mean (SD) age was 60.09 (13.59) years. Nineteen skin cancers were identified in 15 patients (5.8%) representing 3 racial/ethnic groups: black (6 patients), Asian (5), and Hispanic (4). All squamous cell carcinomas in blacks were diagnosed in the in situ stage, located on sun-protected sites, and occurred in patients whose lesions tested positive for human papilloma virus (HPV) and/or who endorsed a history of condyloma acuminata or verruca vulgaris. Most skin cancers in Asians were located on sun-exposed areas and occurred in individuals who emigrated from equatorial locations.

Conclusions and Relevance  Nonwhite organ transplant recipients are at risk for developing skin cancer posttransplantation. Follow-up in a specialized transplant dermatology center and baseline total-body skin examination should be part of posttransplantation care in all organ transplant recipients, including nonwhite patients. A thorough inspection of the groin and genitalia is imperative in black organ transplant recipients. History of HPV infection, particularly in black organ transplant recipients, and sun exposure/emigration history in Asian organ transplant recipients should be documented. Vigilant photoprotection may be of lesser importance in the prevention of skin cancer in black organ transplant recipients. Risk factors for nonwhite organ transplant recipients differ between races/ethnicities and warrant further study in efforts to better counsel and prevent skin cancer in these patients.

Introduction

The population of immunosuppressed patients with organ transplants is growing every year in the United States, with more than 13 000 nonwhite (black, Asian, Hispanic, Pacific Islander) individuals receiving organ transplants in 2015.1 Transplant recipients have a markedly higher incidence of new skin cancers, and this risk magnifies over time with continued exposure to immunosuppression.2-4 Squamous cell carcinoma (SCC) is increased 65-fold, basal cell carcinoma (BCC) 10-fold, and melanoma 3-fold in this particular patient cohort.4 The increased risk of skin cancer is attributable to various factors that include duration and intensity of immunosuppression, the type of organ transplanted, and Fitzpatrick skin type, among others.4-6

Although there are data detailing the incidence of skin cancer in patients with darker skin types, these data are limited and more sparse among nonwhite organ transplant recipients (OTRs). When compared with their white counterparts, the overall incidence of skin cancer among all diagnosed malignant lesions in nonimmunosuppressed nonwhite patients remains significantly lower because it represents 5% of all neoplasms seen in Hispanics, 4% in Asians, and 2% in blacks vs 40% in the white population.7 It is also well documented that, despite the lower overall incidence, skin cancer in nonwhite individuals is often diagnosed at a more advanced stage and associated with worse outcomes.7-10 Thus, not only is it likely that trends regarding type, location, morbidity, and mortality differ among races/ethnicities in the immunosuppressed transplant population, it is also plausible that nonwhite OTRs are at greater risk for developing cutaneous malignant neoplasms that are associated with even higher rates of morbidity and mortality than their immunocompetent nonwhite counterparts.

According to the 2014 US Census projections,11 50.3% of Americans will be comprised of nonwhite minorities by the year 2044. Of the more than 120 000 patients on the waiting list for organs, 58% are nonwhite. These changing demographics, worse skin cancer outcomes in nonwhite patients, and limited studies on skin cancer in nonwhite OTRs warrant a better understanding of the epidemiology of skin cancer in this underrepresented patient population. The objective of this study was to describe demographic and clinical factors and the incidence of histologically confirmed skin cancer in a diverse cohort of nonwhite OTRs through a retrospective medical record review.

Methods

The Drexel Dermatology Center for Transplant Patients at Drexel University College of Medicine is a multidisciplinary medical-surgical dermatology center. The Drexel University abdominal transplant program refers all patients who have undergone solid organ transplantation to the Dermatology of Dermatology Center for Transplant Patients for a comprehensive total-body skin examination, which includes evaluation of all cutaneous lesions on the head, neck, chest, back, abdomen, all extremities, and buttocks, including perianal area, groin, and genitalia. All suspicious lesions are biopsied, with particular attention to high-risk sites, including the perianal and genital areas in nonwhite patients. Those with histologic findings suggestive of viral change are sent for human papilloma virus (HPV) typing. All patients are counseled on self–skin examination and photoprotection and receive introductory educational packets containing written materials regarding skin cancer in transplant patients. After the initial referral, all patients are scheduled at least yearly for a total-body skin examination.

An institutional review board–approved retrospective medical record review of 413 OTRs referred to the transplant center from November 1, 2011, to April 18, 2016, was performed using the electronic medical record. Of the 413 patients, 264 were men, and 149 were women. Their mean (SD) age was 60.09 (13.59) years. Patients were stratified by race/ethnicity and included 154 white patients and 259 nonwhite patients (black, Asian, Hispanic, Pacific Islander). According to the US Census Bureau, people who identify as Hispanic, Latino, or Spanish may be of any race. All Hispanic patients were grouped together, irrespective of race, with most patients endorsing a Fitzpatrick score of III or IV.

Among nonwhite patients, only those with a histologically-confirmed cutaneous malignant neoplasm that was diagnosed after the date of transplantation were included in the final analysis. Demographic and clinical variables were analyzed and compared between the groups and included sex, age, race/ethnicity, Fitzpatrick skin type, type and location of skin cancer, type of organ transplanted, date of transplant, time to diagnosis of a skin cancer posttransplant, and history of clinically evident condyloma acuminata or verruca vulgaris (CA-VV). Fitzpatrick skin type was a self-reported measure determined by asking patients how their skin responded to sun exposure without sunscreen.

Results

A total of 413 OTRs were evaluated during the study period (Table 1). Most patients (259 [62.7%]) were nonwhite. Among those, there were 190 blacks (73.4%), 35 Asians (13.5%), 33 Hispanics (12.7%), and 1 Pacific Islander (0.4%). Most patients (57.9%) were men, and most (83.0%) had received a kidney transplant. Skin cancers were diagnosed across all transplant types (Table 2).

Fifteen nonwhite patients (5.8%) had a total of 19 histologically confirmed skin cancers (Table 3). There were 6 black patients, 5 Asian patients, and 4 Hispanic patients. The 19 lesions represented 13 squamous carcinomas in situ (SCCISs), 1 SCC, 4 BCCs, and 1 sebaceous carcinoma. The mean time to diagnosis after transplantation was 7.8 years, and the mean duration of follow-up after diagnosis was 2.1 years.

Results by Race
Black Patients

There were 6 black patients with 9 biopsy-confirmed skin cancers and a median time of immunosuppression of 8 years (interquartile range [IQR], 6.0-16.5 years). These lesions represented 7 SCCISs and 2 BCCs with a median time to diagnosis of 8 years (IQR, 4.0-13.0 years) and 15.5 years (IQR, 12.8-18.8 years), respectively. All SCCISs were found on non–sun-exposed sites including 1 on the fingertip and 6 in the groin-genital area (Table 4). All patients with groin-genital SCCIS endorsed a history of CA-VV. Two of the 3 groin-genital lesions that were sent for HPV typing tested positive for high-risk HPV types 16 or 18. One of the 2 BCC occurred in a patient with a concomitant diagnosis of porphyria cutanea tarda.

Asian Patients

There were 5 Asian patients with 6 biopsy-confirmed skin cancers and a median time of 4 years (IQR, 2.5-5.5 years) of immunosuppression. Two patients were East Asian, and 3 were Southeast Asian. The skin cancers comprised 1 SCC, 3 SCCISs, 1 BCCs, and 1 sebaceous carcinoma with a median time to diagnosis of 4 years (IQR, 3.0-4.0 years) for SCCIS. Five lesions were found on sun-exposed areas. One SCCIS was located in the groin of a patient with a history of VV.

Hispanic Patients

There were 4 Hispanic patients with 4 biopsy-confirmed skin cancers and median time of 9 years (IQR, 2.8-16.0 years) of immunosuppression. There were 3 SCCISs and 1 BCCs. Three of 4 lesions were located on the lower extremity. Two patients with SCCIS reported a history of CA-VV.

Discussion

This study population is unique in that most of the patients evaluated (62.7%) were nonwhite OTRs. Skin cancer developed in patients of 3 racial/ethnic groups: black (6 patients [3.2%]), Asian (5 [14.3%]), and Hispanic (4 [12.1%]). While the cohort is small, several interesting trends can be gleaned from these data.

All skin cancers in black patients were diagnosed at an early stage. This finding was unexpected because skin cancer in immunocompetent nonwhite patients is typically diagnosed at more advanced stages and is associated with increased morbidity and mortality. Squamous cell carcinoma is the most common type of skin cancer noted in the black population and tends to occur in sun-protected sites and in areas of chronic scarring processes and chronic inflammation, such as burn scars, ulcers, discoid lupus erythematosus, lupus vulgaris, and hidradenitis suppurativa.6,7,9,10 These SCCs tend to be more aggressive and are associated with a 20% to 40% risk of metastasis compared with a 1% to 4% risk of metastasis for sun-induced cancer in immunocompetent black patients.7 Mortality from SCC in African Americans is as high as 29%.10 Interestingly, while the skin cancers found in black OTRs in our cohort were consistent in that they were found in non–sun-exposed areas, the predominant type of malignant neoplasm diagnosed in the present study was SCCIS. There were no black patients with SCC. It is possible that all lesions were diagnosed in the in situ stage owing to the established referral system whereby our transplant medicine counterparts send all OTRs for screening and establishment of dermatologic care. Hence, as a part of their posttransplantation treatment, all OTRs within our health system, including those who are nonwhite, receive a total-body skin examination, including examination of the genitalia, and are counseled regarding risk factors and followed at least yearly in our dermatology clinic. This finding suggests that all OTRs, regardless of race, should be referred for routine skin evaluation because it may lead to earlier diagnosis and better outcomes.

Most SCCISs in black OTRs were found in the groin-genital area. All of these patients endorsed a history of clinically evident CA-VV, and 2 of 3 lesions tested positive for high-risk HPV types 16 or 18. In both immunocompetent and immunosuppressed patients, HPV has been linked to the development of SCC.12-14 One study of transplant patients detected HPV viruses in up to 90% of SCCs.15 Another study of nonimmunosuppressed patients found HPV DNA in skin biopsy specimens of 4.7% of controls, 90.5% of warts, 60.4% of precancerous lesions, and 59.7% of SCCs.16 This potential association between HPV and SCCIS warrants careful examination of the groin, genitalia, and perianal area in search of early lesions. In addition, documentation of HPV history may help identify those who are at risk for SCC. This finding also suggests that there may be significant differences in risk factors pertaining to the development of cutaneous malignant neoplasms between white and black OTRs. With the advent of the HPV vaccine, the prevalence of cervical cancer is expected to decrease. A concomitant decrease in CA-VV, and consequently cutaneous SCC-SCCIS, may follow suit. This questions whether OTRs with a history of CA-VV or HPV should be vaccinated in efforts to decrease their risk of SCC development, or, perhaps, HPV vaccination should be administered to all patients prior to transplantation. Finally, genital SCCIS related to HPV is slow growing, taking approximately 10 years to progress into invasive disease.17 Hence, genital SCCs or those of viral etiology may have different biologically aggressiveness behavior than those of solar etiology, which may further explain the early diagnosis of skin cancer in the black population in our study. Additional studies are needed to determine if SCC-SCCIS lesions harbor viral changes on a molecular level and, if they do, in what manner this translates clinically.

Two BCCs were diagnosed among black patients, and both occurred after a decade of immunosuppression. One was an indolent variant of BCC found on the back and diagnosed after 21 years of immunosuppression. The other lesion occurred after 10 years of immunosuppression on the nasal tip of a patient with multiple risk factors for skin cancer development, including a photosensitizing disorder, porphyria cutanea tarda, and a heart transplant, which requires the greatest degree of immunosuppression. Because sun exposure is the most common predisposing factor in the development of BCC, these findings question the utility of extensive photoprotection counseling in black OTRs, particularly those with darker skin types.9

By contrast, most skin cancers in Asians (83.3%) were found on sun-exposed areas and had a shorter time to development when compared with skin cancers in blacks. The lesions included 1 SCC, 3 SCCISs, 1 BCC, and 1 sebaceous carcinoma, with all lesions located on the face except for 1 SCCIS, which was identified in the groin. The median time to skin cancer development among Asians was conspicuously earlier than in the black organ transplant population, at 4 years vs 8 years. Three-quarters of the Asian patients who developed skin cancer grew up in equatorial Southeast Asia. It has been shown that UV radiation is a significant risk factor for skin cancer development in Asians. One study18 of a Singapore Cancer Registry between 1968 and 1997 found that fairer Chinese patients had a 2-fold greater incidence of skin cancer than Malaysians and Indians with darker skin. Another study found the incidence of BCC to be 2 times greater among Japanese who live in Kauai, Hawaii, secondary to intense UV exposure and greater participation in outdoor activities.19 Thus, Asian patients in the present study had increased lifetime sun exposure from living in areas with intense UV radiation, which may explain the shorter time to skin cancer development.

Few conclusions can be drawn from the Hispanic patients because of the limited data. There were 2 nonmelanoma skin cancers identified in sun-exposed locations and 2 on the lower extremities in patients with a history of VV or CA. Additional studies with larger sample sizes are needed to ascertain any trends or conclusions.

Although the sample size is small, a few recommendations can be made regarding posttransplant dermatologic care for nonwhite OTRs. All patients, regardless of race, should receive, at minimum, a baseline total-body skin examination and counseling regarding risk factors and photoprotection. This examination should include a thorough inspection of the genitalia, groin, and perianal regions, particularly among black patients. A history of HPV, CA, or VV should be obtained from all patients. Education and counseling regarding the importance of photoprotection should be provided to all Asian patients, especially those who grew up in equatorial locales. Patients with any of these risk factors may warrant closer monitoring.

This study is limited by its short duration of follow-up, retrospective design, small proportion of patients with skin cancer as noted herein, and, thus, possible lack of generalizability to larger populations. It raises many questions. The optimal frequency of follow-up, the efficacy of the HPV vaccine in preventing future SCCISs and SCCs, the biologic aggressiveness of virally-induced SCCISs and SCCs compared with sun-induced SCCISs and SCCs, and the effects of sun exposure and utility of photoprotective behaviors in blacks, particularly those with darker skin types, are still largely unknown. Future studies are needed to address these areas.

Conclusions

This study sought to describe demographic and skin cancer characteristics among nonwhite OTRs. A large number of SCCISs were observed in black OTRs on sun-protected areas whereas most nonmelanoma skin cancers occurred on sun-exposed areas in Asians. The increased rate of SCCISs compared with SCCs observed in blacks is possibly due to close follow-up in a medical-surgical transplant dermatology center where all OTRs are referred to dermatology and receive a comprehensive evaluation that includes examination of the genitalia or due to different biological aggressiveness of genital or virally induced SCCISs. Risk factors for blacks likely differ from those of Asians and may include a history of HPV infection in blacks compared with sun exposure history and/or emigration from equatorial locales in Asians. Nonwhite organ transplant patients represent a unique group with specialized medical needs; thus, more knowledge on risk factors, appropriate screening methods, and counseling points are essential for providing comprehensive dermatologic care for these patients.

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Article Information

Corresponding Author: Christina Lee Chung, MD, Department of Dermatology, Drexel University, 219 N Broad St, Fourth Floor, Philadelphia, PA 19107 (christina.chung@drexelmed.edu).

Accepted for Publication: July 21, 2016.

Published Online: September 21, 2016. doi:10.1001/jamadermatol.2016.3328

Author Contributions: Drs Pritchett and Chung had full access to all of the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis.

Study concept and design: Doyle, Shaver, Abdelmalek, Cusack, Chung.

Acquisition, analysis, or interpretation of data: All authors.

Drafting of the manuscript: Pritchett, Doyle, Miller, Chung.

Critical revision of the manuscript for important intellectual content: Doyle, Shaver, Miller, Abdelmalek, Cusack, Malat, Chung.

Statistical analysis: Pritchett, Shaver, Miller, Malat.

Administrative, technical, or material support: Pritchett, Doyle, Abdelmalek, Cusack, Chung.

Study supervision: Doyle, Shaver, Abdelmalek, Cusack, Chung.

Conflict of Interest Disclosures: None reported.

Additional Contributions: We thank Jennifer Hawkins, RMA, the transplant clinical coordinator at Drexel University, who helped log clinical information and tracked patients, and Rohit Nijhawan, MD, a resident at Drexel University who was integral in helping to establish the Center for Transplant Patients. They were not compensated for their contributions.

References
1.
United Network for Organ Sharing. https://optn.transplant.hrsa.gov/data/view-data-reports/national-data/#. Accessed May 9, 2016.
2.
Berg  D, Otley  CC.  Skin cancer in organ transplant recipients: Epidemiology, pathogenesis, and management.  J Am Acad Dermatol. 2002;47(1):1-17.PubMedGoogle ScholarCrossref
3.
Euvrard  S, Kanitakis  J, Claudy  A.  Skin cancers after organ transplantation.  N Engl J Med. 2003;348(17):1681-1691.PubMedGoogle ScholarCrossref
4.
Zwald  FO, 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(2):253-261.PubMedGoogle ScholarCrossref
5.
Gogia  R, Binstock  M, Hirose  R, Boscardin  WJ, Chren  MM, Arron  ST.  Fitzpatrick skin phototype is an independent predictor of squamous cell carcinoma risk after solid organ transplantation.  J Am Acad Dermatol. 2013;68(4):585-591.PubMedGoogle ScholarCrossref
6.
Buoy  AG, Yoo  S, Alam  M,  et al.  Distribution of skin type and skin cancer in organ transplant recipients.  Arch Dermatol. 2010;146(3):344-346.PubMedGoogle ScholarCrossref
7.
Agbai  ON, Buster  K, Sanchez  M,  et al.  Skin cancer and photoprotection in people of color: a review and recommendations for physicians and the public.  J Am Acad Dermatol. 2014;70(4):748-762.PubMedGoogle ScholarCrossref
8.
Kailas  A, Solomon  JA, Mostow  EN, Rigel  DS, Kittles  R, Taylor  SC.  Gaps in the understanding and treatment of skin cancer in people of color.  J Am Acad Dermatol. 2016;74(5):1020-1021.PubMedGoogle ScholarCrossref
9.
Battie  C, Gohara  M, Verschoore  M, Roberts  W.  Skin cancer in skin of color: an update on current facts, trends, and misconceptions.  J Drugs Dermatol. 2013;12(2):194-198.PubMedGoogle Scholar
10.
Gloster  HM  Jr, Neal  K.  Skin cancer in skin of color.  J Am Acad Dermatol. 2006;55(5):741-760.PubMedGoogle ScholarCrossref
11.
US Census Bureau. 2010 Census data. http://www.census.gov/2010census/data/. Accessed April 14, 2016.
12.
Karagas  MR, Nelson  HH, Sehr  P,  et al.  Human papillomavirus infection and incidence of squamous cell and basal cell carcinomas of the skin.  J Natl Cancer Inst. 2006;98(6):389-395.PubMedGoogle ScholarCrossref
13.
Arron  ST, Jennings  L, Nindl  I,  et al; Viral Working Group of the International Transplant Skin Cancer Collaborative (ITSCC) & Skin Care in Organ Transplant Patients, Europe (SCOPE).  Viral oncogenesis and its role in nonmelanoma skin cancer.  Br J Dermatol. 2011;164(6):1201-1213.PubMedGoogle ScholarCrossref
14.
Schmidt  SA, Hamilton-Dutoit  SJ, Farkas  DK, Steiniche  T, Sørensen  HT.  Human papillomavirus and the incidence of nonmelanoma and melanoma skin cancer using cervical conization as a surrogate marker: a nationwide population-based Danish cohort study.  Ann Epidemiol. 2015;25(4):293-296.e2.PubMedGoogle ScholarCrossref
15.
Connolly  K, Manders  P, Earls  P, Epstein  RJ.  Papillomavirus-associated squamous skin cancers following transplant immunosuppression: one Notch closer to control.  Cancer Treat Rev. 2014;40(2):205-214.PubMedGoogle ScholarCrossref
16.
Iftner  A, Klug  SJ, Garbe  C,  et al.  The prevalence of human papillomavirus genotypes in nonmelanoma skin cancers of nonimmunosuppressed individuals identifies high-risk genital types as possible risk factors.  Cancer Res. 2003;63(21):7515-7519.PubMedGoogle Scholar
17.
Wright  TC  Jr.  Cervical cancer screening in the 21st century: is it time to retire the PAP smear?  Clin Obstet Gynecol. 2007;50(2):313-323.PubMedGoogle ScholarCrossref
18.
Koh  D, Wang  H, Lee  J, Chia  KS, Lee  HP, Goh  CL.  Basal cell carcinoma, squamous cell carcinoma and melanoma of the skin: analysis of the Singapore Cancer Registry data 1968-97.  Br J Dermatol. 2003;148(6):1161-1166.PubMedGoogle ScholarCrossref
19.
Chuang  TY, Reizner  GT, Elpern  DJ, Stone  JL, Farmer  ER.  Nonmelanoma skin cancer in Japanese ethnic Hawaiians in Kauai, Hawaii: an incidence report.  J Am Acad Dermatol. 1995;33(3):422-426.PubMedGoogle ScholarCrossref
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