Comm & Chro Disease

FROM THE ACADEMY

Skin cancer and photoprotection in people of color: A review and recommendations for

physicians and the public

Oma N. Agbai, MD, a Kesha Buster, MD,

b Miguel Sanchez, MD,

c Claudia Hernandez, MD,

d

Roopal V. Kundu, MD, e Melvin Chiu, MD,

f Wendy E. Roberts, MD,

g Zoe D. Draelos, MD,

h

Reva Bhushan, PhD, i Susan C. Taylor, MD,

j and Henry W. Lim, MD

a

Detroit, Michigan; Wichita, Kansas; New York, New York; Chicago and Schaumburg, Illinois;

Los Angeles and Rancho Mirage, California; High Point, North Carolina; and Philadelphia, Pennsylvania

From

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Skin cancer is less prevalent in people of color than in the white population. However, when skin cancer occurs in non-whites, it often presents at a more advanced stage, and thus the prognosis is worse compared with white patients. The increased morbidity and mortality associated with skin cancer in patients of color compared with white patients may be because of the lack of awareness, diagnoses at a more advanced stage, and socioeconomic factors such as access to care barriers. Physician promotion of skin cancer prevention strategies for all patients, regardless of ethnic background and socioeconomic status, can lead to timely diagnosis and treatment. Public education campaigns should be expanded to target communities of color to promote self-skin examination and stress importance of photoprotection, avoidance of tanning bed use, and early skin cancer detection and treatment. These measures should result in reduction or earlier detection of cutaneous malignancies in all communities. Furthermore, promotion of photoprotection practices may reduce other adverse effects of ultraviolet exposure including photoaging and ultraviolet- related disorders of pigmentation. ( J Am Acad Dermatol 2014;70:748-62.)

Key words: basal cell carcinoma; Bowen disease; dermatofibrosarcoma protuberans; dyspigmentation; melanoma; Merkel cell carcinoma; mycosis fungoides; people of color; photoprotection; radiation; skin cancer; skin of color; squamous cell carcinoma; sun protection; sunscreen; ultraviolet.

DEFINITIONS

Abbreviations used:

BCC: basal cell carcinoma DFSP: dermatofibrosarcoma protuberans MED: minimal erythema dose MF: mycosis fungoides MM: malignant melanoma NMSC: nonmelanoma skin cancer POC: people of color SCC: squamous cell carcinoma SEER: Surveillance, Epidemiology, and End

Results SPF: sun-protection factor UV: ultraviolet

Whites: Non-Hispanic individuals of European descent

Blacks: Non-Hispanic individuals of African descent

Hispanics: Individuals who trace their origin or descent to Mexico, Puerto Rico, Cuba, Spanish- speaking Central and South American countries, Spanish-speaking island nations of the Caribbean, and other Spanish cultures. Origin can be considered as the heritage, nationality group, lineage, or country of the person or the person’s parents or ancestors before their arrival in the United States. People who

the Multicultural Dermatology Center, Department of

ermatology, Henry Ford Hospital, Detroit a ; Department of

ermatology, Via Christi Clinic, Wichita b ; Department of

ermatology, New York University Medical Centerc; Depart-

ent of Dermatology, University of Illinois College of Medicine,

hicago d ; Northwestern Center for Ethnic Skin, Department of

ermatology, Northwestern University Feinberg School of

edicine, Chicagoe; Division of Dermatology, University of

alifornia Los Angeles Medical Centerf; Desert Dermatology

ncho Mirage g ; Dermatology Consulting Services, High Point

h ;

merican Academy of Dermatology, Schaumburgi; and Society

ill Dermatology and Cosmetic Center, Philadelphia.j

Funding sources: None.

The authors’ conflict of interest/disclosure statements appear at

the end of the article.

Accepted for publication November 26, 2013.

Reprint requests: Reva Bhushan, PhD, Department of

Evidence-based Research, American Academy of

Dermatology, 930 E Woodfield Rd, Schaumburg, IL 60173.

E-mail: [email protected].

Published online January 30, 2014.

0190-9622/$36.00

� 2014 by the American Academy of Dermatology, Inc. http://dx.doi.org/10.1016/j.jaad.2013.11.038

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identify their origin as Hispanic or Latino may be of any race. This definition of Hispanic fully excludes the Portuguese, Brazilians, or anyone from any other country that speaks Portuguese.1

Asians: Individuals having origins in any of the original peoples of East Asia, Southeast Asia, or the Indian subcontinent, including, for example, Cambodia, China, India, Japan, Korea, Malaysia, Pakistan, the Philippine Islands, Thailand, and Vietnam.1

INTRODUCTION Malignant melanoma (MM) and nonmelanoma

skin cancer (NMSC) account for 40% of all neoplasms in whites, making it the most common malignancy in the United States.2 Skin cancer is most common in whites and in people living in equatorial latitudes.3

The incidence of both MM and NMSC remains significantly lower in people of color (POC) when compared with whites as they are seen in about 5% of Hispanics, 4% of Asians, and 2% of blacks.4,5 Even so, multiple reports have demonstrated heightened morbidity and mortality in minority populations,

6-8

raising public health concerns in these groups. Although there are data detailing incidence of skin cancer in POC, these data are limited. In addition to skin cancer, factors such as photoaging, pigmentary disorders induced or exacerbated by ultraviolet (UV) exposure, and sunburn must be considered in POC. It is estimated that black, Hispanic, and Asian Americans will comprise approximately 50% of the US population by the year 2050.4 These evolving demographics, elevated rates of skin cancer morbidity and mortality in POC, and limited clinical data on additional adverse effects of UV exposure in this population mandate that physicians develop familiarity with the concept of optimized photo- protection for POC. An understanding of the varying clinical presentations of UV-related skin cancers in POC, in addition to relevant topics in photoaging and UV-related disorders of pigmentation, is necessary for adequate management of photoprotection in POC.

BIOLOGICAL BASIS OF SKIN CARCINOGENESIS AND PHOTOAGING IN POC

Few studies have been performed to thoroughly evaluate biological differences between differing ethnic skin types. Skin color is primarily determined by the presence of melanin. Jimbow et al9 reported that dark skin has larger melanocytes that produce more melanin and melanosomes are distributed individually in keratinocytes rather than in aggre- gates. The rarity of cutaneous malignancy in

populations of darker complexions is secondary to photoprotection from a higher amount of epidermal melanin, which filters at least twice as much UV radiation as the epidermis of whites.10 In an in vitro study performed by Kaidbey et al,11 the amount of UV radiation reaching the papillary dermis of whites was greater than that of blacks by approximately 5-fold. The authors proposed that larger and more melanized melanosomes observed in POC absorbed more energy than the melanosomes in white skin, which were smaller, less dense, and lightly mela- nized. Furthermore, the authors estimated that the epidermis of blacks has an intrinsic sun-protection factor (SPF) of 13.4, whereas light skin has an SPF of 3.3.11 Therefore, exposure to UV radiation plays a lesser role in heightening the risk for skin cancer in populations of darker complexions.

Damage to DNA secondary to UV radiation is a major factor in cutaneous photocarcinogenesis and photoaging. However, the correlation of ethnicity and degree of sensitivity to UV rays has not been elucidated. Tadokoro et al12 performed a study evaluating the correlations between melanin content and degree of UVA- and UVB-induced DNA damage in normal-appearing skin of various ethnic groups. DNA damage was found to be most severe in qualitatively light skin. Baseline skin pigmentation and extent of DNA damage were inversely related, as individuals of darker skin tones were able to repair UVA-/UVB-induced DNA damage more rapidly than subjects with fair skin. Even low exposure to UVA/UVB radiation induced some appreciable DNA damage in all skin types, dispelling the myth that those with very dark skin are completely im- mune to UVA-/UVB-induced DNA damage.12

Indeed, NMSC and MM do occur in POC, despite the low relative risk.13 Because of the limited research on skin cancer in POC, there are few resources providing insight on evaluating darkly pigmented lesions in POC. Frequently atypical presentations, together with constitutive dark pigmentation, pose diagnostic challenges in the identification of characteristics such as variation in color within the lesions. Furthermore, certain skin cancers that are pigmented in POC may not be pigmented in whites (such as basal cell carcinoma, which is more likely to be pigmented in darker skin types); therefore, a high index of suspicion in POC is necessary in making the diagnosis.

5

BASAL CELL CARCINOMA Basal cell carcinoma (BCC) is the most prevalent

skin cancer found in whites, Asians, and Hispanics.14

Hispanics are more likely to be given a diagnosis of multiple BCC rather than a single squamous cell

Fig 1. Nonmelanoma skin cancers in people of color. Pigmented basal cell carcinoma in elderly Hispanic man (right lateral orbital rim) (A); middle-aged Asian woman (right cheek) (B); middle-aged Hispanic man (right forehead) (C); and middle-aged Hispanic man (left nasal ala) (D). Hypopigmented mycosis fungoides in Hispanic man (back) (E) and black man (lower aspect of back) (F). G, Metastatic squamous cell carcinoma in black man (right parietal scalp, courtesy of Dr Marc Silverstein, Sacramento, CA).

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carcinoma (SCC).15 In contrast to Hispanic popula- tions, BCC is the second most common skin malig- nancy in blacks after SCC.4,5

The clinical spectrum of disease in BCC shows many parallels among blacks, whites, Asians, and Hispanics. The classic clinical presentation of a solitary pearly papule with central ulceration and rolled borders may be seen in POC, but may pose challenges in the physical examination as the characteristic pearly borders and telangiectasia may not be clinically as apparent in dark skin types (Fig 1). In whites, the majority of patients presenting with BCC are of advancedage([50years),mostcommonlypresenting with asymptomatic solitary translucent nodules with central ulceration.14 Pigmentation is present in over 50% of tumors in POC,4,16 whereas only 5% of BCCs affecting whites have been shown to be pigmented. In Asians, BCCs frequently present as brown to black papules, or have a ‘‘black pearly’’ appearance.17 The clinical presentation of BCCs in Asian skin ranges from nodules to papules, plaques, and ulcers.18 With regards to anatomic distribution, there are significant similarities between POC and whites. Approximately 80% of BCCs in POC were found in the head and neck,19 as has been shown in whites.14 Differential diagnosis for BCC in POC includes seborrheic kera- tosis, blue nevus, trauma, lupus erythematosus, nevus

sebaceous, sarcoidosis, and melanoma.20 Metastasis in BCC is rare in all skin types.14

BCC in blacks Although quite rare, BCC has been reported in the

black population. In a report from Howard University (Washington, DC) from 1960 through 1986, most BCCs were seen in blacks of fairer skin complexion in comparison with those with darker complexions.19 From this, one may conclude that the incidence of BCC may correlate directly with the degree of skin pigmentation, as it is most frequently diagnosed in whites of fairer complexions, and more rarely diagnosed in blacks. A study of skin cancer prevalence was conducted by Asuquo et al21 in a Nigerian teaching hospital between the years of 2000 and 2004. Of 63 cases of skin cancer, BCC was diagnosed in 8% (n = 5) of the cases; 66.7% of the BCC were on the head and neck, and 33.3% on the upper limb. All of these lesions were nodular. BCC was diagnosed only in albinos in this study.21 In a review of 128 black patients with 148 BCCs, Mora and Burris3 (New Orleans, LA) found that the average age of examination (not necessarily onset) was 59 years, with lesions most commonly located on head and neck. Only 2 of these patients had albinism.

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The incidence of BCC in non-sun-exposed skin is equal between whites and blacks.22 Diverse pre- sentations and locations of BCCs have been found in blacks, ranging from superficial BCC to perianal BCC.3,11 BCCs in blacks are often pigmented, and there are reports of BCCs that have arisen in scars, which rarely proceeded to metastasize.3,4,23

BCC in Hispanics One of the most common neoplasms diagnosed in

Hispanics is pigmented BCC.16 Hispanics studied demonstrated significantly lower incidence rates of BCC than non-Hispanic whites regardless of gender.24 Still, a high index of suspicion should be maintained in evaluating pigmented lesions in Hispanics, as BCCs have a propensity to be pig- mented in Hispanic populations and may be mis- diagnosed as melanomas.16 In a study performed by Bigler et al16 (Albuquerque, NM), the incidence of pigmented BCC in Hispanics was found to be twice that of white patients.

Compared with whites, Hispanics with NMSC were shown to have fewer tumors per individual, and fewer Hispanics had more than 1 tumor.24 A registry of skin cancers in New Mexico between the years of 1964 and 1992 showed an average of 1.8 tumors per individual with NMSC among Hispanics, compared with 2.2 tumors per individual with NMSC in whites. Of these, BCC was more common than SCC by 6.6-fold in both Hispanics and whites.24

BCC in Asians Although NMSC is not common in Asians, it is not

extremely rare. In a study by Cheng et al25 studying incidence of NMSC between 1990 and 1999 in Hong Kong, China, the incidence of BCC was 0.32 and 0.92 per 100,000 population. Pigmented BCC was the most common NMSC diagnosed, found in approxi- mately 60% of Chinese patients with skin cancer in the study.25 Multiple or subsequent skin cancers and subtypes of new cancers were seen less often in the Chinese group when compared with the white group.25 Similarly, Sng et al26 reported an increase of skin cancers including BCC, SCC, and MM, in Singapore between the years of 1998 and 2006. The extremities were the most common sites affected by Bowen disease (SCC in situ).27 There is an increased incidence of NMSC in Japanese living in Kauai, Hawaii, which may be secondary to heightened intensity of year-round UV radiation and popularity of outdoor activities, as reviewed by Lee and Lim.28

SQUAMOUS CELL CARCINOMA SCC comprises approximately 20% of all skin

cancers. With MM excluded, approximately 75% of

all deaths from skin cancers are caused by SCC. 29

In blacks and Asian Indians, SCC is the most commonly diagnosed skin cancer. It is the second most commonly diagnosed skin cancer in Hispanics, East Asians (including Japanese and Chinese patients), and whites.5,30 Although actinic keratoses are most commonly diagnosed in white and Japanese pa- tients,31 they are very rare in blacks.32

Riskfactorsfor SCCinPOCincludechronicscarring and inflammatory processes including hidradenitis suppurativa, lupus erythematosus, scars caused by chemical and thermal burns, skin ulcers, and sites of previous radiation.33,34 Immunocompromised pa- tients, including organ transplant recipients, also demonstrate a heightened risk for SCC.35 Among blacks, the greatest predisposing factors for devel- oping SCC include chronic scarring and/or inflamma- tory processes that are observed in 20% to 40% of reported cases.4 In addition, the human papilloma- virus has been linked to the development of SCC, particularly in immunocompromised patients.36 One retrospective study detected human papillomavirus DNA in skin samples of 4.7% of controls, 90.5% of benign warts, 60.4% of precancerous lesions, 59.7% of SCC, and 27.8% of BCC, suggesting a link between viral infection and the development of NMSC.37

Definitive studies have not been performed on the relationship between human papillomavirus infection and NMSC in POC.

SCCs are characteristically firm, superficial, well- demarcated papules or plaques that emerge from a rounded, indurated, and elevated base.29 In POC, SCC is most commonly found in areas that are not typically exposed to the sun, such as the lower extremities and anus. In fact, lower extremity and anogenital SCCs were seen in 15% of SCCs in blacks in a study conducted by Halder and Bang19 in Washington, DC. This is a sharp contrast to the white population, in whom SCCs are characteristically seen in chronically sun-exposed skin.19

SCC in blacks Among black patients given the diagnosis of

SCC, the peak incidence was shown to be in the fifth decade on the lower limbs, followed by the head and neck and then the genitals. The scalp and lip are more often implicated in black women than in men.38 Chronic trauma, ulcers, and scars are the most significant predisposing factors for SCCs in the lower limb and on the scalp, as reported by Amir et al38 (Dar es Salaam, Tanzania) in a study of SCC in Tanzanian patients, where UV radiation was found to be the primary factor predisposing pa- tients to increased risk of SCC in the head and neck. In a study done in Tanzania, smegma of the

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uncircumcised penis was also reported as a risk factor for the majority of cases of SCC developing on the penis in blacks.38 The majority of SCC on the penis were found to be SCC in situ upon histologic analysis in a study performed by Hubbell et al39

(New Orleans, LA). SCC was the most common skin cancer reported

in a Nigerian teaching hospital between 2000 and 2004 by Asuquo et al,

21 where the lower limb was

the most commonly affected anatomic site. SCC manifesting as Marjolin ulcer associated with trau- matic injury of the limb was diagnosed in 7 patients, and associated with a history of burn in 1 patient. SCC involved the external genitalia in 9 patients, 3 of whom had genital warts. The anus was affected in 4 female cases. There were no lesions involving the head and neck regions, and all patients in this study presented with chronic ulcers.21

Several cases of the emergence of SCC within scars of chronic discoid lupus erythematosus in black patients have been reported. Caruso et al40 reported a heightened propensity for SCC to metastasize in black Canadian patients with discoid lupus erythe- matosus. Sun exposure of hypopigmented lesions of discoid lupus erythematosus may have been a predisposing factor.

In blacks, Bowen disease (SCC in situ) typically presents as scaly hyperkeratotic pigmented pla- ques, and may be misdiagnosed as MM. In contrast, Bowen disease lesions are rarely pigmented outside of the groin in whites.41 Black women are affected twice as often as black men, and most frequently in skin that is not sun exposed.19 In a study performed by Mora et al42 in New Orleans, LA, evolution to SCC was noted in 5 of 19 black patients with Bowen disease, leading to death in 3 of these patients. The most common area affected was the lower extremity.42 Mortality of SCC in blacks is as high as 29%, secondary not only to delays in diagnosis and treatment, but also to more aggressive biologic behavior of SCC in this popu- lation.41,43 In blacks, SCC that develops within a chronic scarring process tends to be more aggres- sive and is associated with a 20% to 40% risk of metastasis. In contrast, the rate of metastatic trans- formation of sun-induced SCC in blacks is approx- imately 1% to 4%.4 In a case series on SCC in blacks performed by Mora and Perniciaro

33 (New Orleans,

LA), the highest mortality was observed in cases of perianal SCC. Although most patients with primary SCC have a very good prognosis, the 10-year survival is less than 20% in patients with regional lymph node metastasis, and less than 10% in patients with distant metastasis.29

SCC in Asians Bowen disease and pigmented BCCs are not

uncommonly diagnosed in Asians. Because of their pigmented appearance, as in blacks, these may be misdiagnosed as MM.25 Although NMSC is uncom- mon, it is not rare in the Chinese population in Hong Kong. Cheng et al25 (Hong Kong, China) reported that the incidence of SCC in 1990 was 0.16 per 100,000 population, and in 1999, 0.34. Similarly, in a case-control study performed by Chen et al44 in Taiwan evaluating the association between UV radi- ation exposure from the sun and risk for develop- ment of SCC by gender, exposure at a young age (15-24 years) and cumulative sun exposure were significantly associated with heightened risk of SCC in a dose-related pattern. Cumulative sun exposure was found to be more closely related to increased risk of SCC in women, whereas sun exposure at an early age showed more relevance to SCC risk in men.44 Skin reactions such as redness, burn, and suntan after 2 hours of sun exposure in childhood and adolescence were not associated with increased risk for SCC.44

In a study on skin cancer incidence between 1986 and 1997 among Asians living in Singapore, 2650 BCCs were reported. There was a general increase in skin cancer incidence from 6 per 100,000 person- years (from 1968-1972) to 8.9 per 100,000 person- years (1993-1997). The incidence of BCC increased approximately 3% yearly. Age-standardized inci- dence rates for BCC were greatest in fair-skinned Chinese, followed by Malays and Indians. This trend was also noted for SCC and cutaneous MM.

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MALIGNANT MELANOMA MM is the deadliest type of skin cancer found

across all races and ethnicities. Many melanoma cases are diagnosed in nonhospital settings and thus may be underreported to central cancer registries, which traditionally collect the majority of cases from hospi- tals.46 This could lead to significant underreporting of MM and resultant underestimation of the incidence of melanoma.47 The National Cancer Institute, Division of Cancer Control and Population Sciences, Surveillance Research Program, Cancer Statistics Branch (Bethesda, MD) reports that the incidence of cutaneous MM increased by approximately 6% yearly in the 1970s, slowed to a 3% yearly increase between 1981 and 2000, and has since stabilized.48

Since the late 1980s, the incidence of MM has increased significantly among Hispanics in California, increasing an average of 1.8% yearly in male Hispanics between 1988 and 2001, and 7.3% average yearly between 1996 and 2001.49 In a study conducted by Bergfelt et al,50 the incidence of MM

Fig 2. Melanomas in people of color. A, Lentigo maligna in middle-aged Hispanic woman (vermilion upper and lower lips). Melanoma in middle-aged black woman (right fourth toe) (B); Hispanic woman (left fifth toe) (C); middle-aged Hispanic man (left plantar foot) (D); elderly Hispanic man (right cheek) (E); and Asian woman (side of left leg) (F).

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among Hispanics in Puerto Rico and New Mexico (race not specified) was greater than in US blacks by 1.6- to 3.7-fold. There was a close correlation in anatomic distribution of MM among whites and Hispanics in New Mexico in both men and women. The most common MM distribution in Hispanics from Puerto Rico was the leg, as was seen in black Americans.50 In another study, Vazquez-Botet et al51

reported that nearly half of MM in Hispanic patients in Puerto Rico were found on the extremities, especially the feet, similar to black and Japanese patients. Superficial spreading melanoma was the most com- mon histologic type, followed by acral lentiginous, nodular, and lentigo maligna melanomas.51 More recently, Wu et al52 (New Orleans, LA) reported that incidence rates of MM in the United States were notably higher in females than males in white and Hispanic populations younger than 50 years, and in Asian/Pacific Islanders younger than 40 years. The median age of white and black patients was greater (59-63 years) when compared with Hispanics, Asian/ Pacific Islanders, and American Indians/Alaskan Natives (52-56 years).52 Histologically, acral lentigi- nous melanoma was the most common subtype in blacks, whereas superficial spreading melanoma was most commonly diagnosed in all other ethnic groups studied.52 Incidence rates of acral lentiginous

melanoma were, however, highest in Hispanics. Non-whites demonstrated an increased propensity to present with more advanced MM when compared with whites.52

Typically, MM presents as a dark macule or patch and may have a history of rapid spreading. Suspicion for subungual melanomas is raised when a pig- mented band wider than 3 mm is observed on the nail, extension of pigment to proximal nail fold (Hutchinson sign) and there is pigment variation, rapid growth in size, and the observation of solitary lesions.4 Subungual melanoma is most common on the thumb and first toe. In populations of color, the plantar foot is most commonly affected (Fig 2),53 as it is implicated in 30% to 40% of cases.54 Melanomas found in the oral cavity comprise approximately 7.5% of all melanomas in Asians, where approximately 60% of these develop from lesions of oral melanosis.

The greatest risk factors for the development of MM in whites include periods of high intermittent sunlight exposure (as in sunbathing and indoor tanning), and large cumulative doses of UV radiation from chronic exposure (as seen in outdoor workers).55 Factors in the host that may increase susceptibility to develop- ment of melanoma include a large number of nevi, the presence of dysplastic nevi, freckles, fair complexion, red or blonde hair, and family history of MM.55

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Contrarily, in blacks and Asians, UVradiation does not appear to be a major risk factor, as the majority of melanomas are found in skin that is not typically sun exposed, including palmar, plantar, and subungual skin, and mucous membranes.56 In POC, the risk factors for MM have not been identified, but may be unrelated to sun exposure.57 Specifically, as acral melanomas are identified with similar rates at different latitudes and in varying racial groups, and as they tend to be diagnosed in anatomic sites that are not typically sun exposed, their origin may be unrelated to sun exposure.28

MM in blacks In black Americans, acral lentiginous melanoma is

the most common and deadly form of MM.56,58 Not uncommonly it is misdiagnosed and managed as a tinea nigra, or even talon noir. In a retrospective study performed at Tulane University School of Medicine (New Orleans, LA)58 from 1958 to 1990, 82 patients (including 27 white men, 29 white women, 18 black men, and 8 black women) with a diagnosis of acral lentiginous melanoma were fol- lowed up, and the study showed a trend toward reduced survival in black men. A direct correlation between decreased survival and increased Clark level was also observed. As previously mentioned, the overall incidence of melanoma in the black population is lower than that of whites. Additional types of melanoma found in black Americans include superficial spreading and nodular types.

13

Acral lentiginous melanoma has a poor prognosis secondary to its propensity for deep invasion at presentation, with 5-year survival lower than 50%.59

In a study of skin cancers in a teaching hospital in Nigeria between 2000 and 2004, MM of the skin represented 8% (n = 5) of the 63 histologically diagnosed cutaneous malignancies. All of these MMs were plantar. Three of the 5 cases were clinically advanced nodular melanomas, whereas 2 were ulcerated superficial spreading melanomas.21

MM in Hispanics Pipitone et al60 (Maywood, IL) proposed that

Hispanics had a propensity to present with more advanced disease secondary to the combination of a belief that they are not at risk to sunburn and/or develop skin cancer. Skin cancer prevention mea- sures are typically directed toward non-Hispanic whites, where skin self-examination and sun protec- tion are emphasized.13 Feun et al61 (Miami, FL) reviewed 54 melanoma cases in Hispanic patients; the majority of melanomas were located on the trunk, arm, shoulder, leg, and hip. Although 70% of these patients presented with local disease, 26%

presented with regional and distant lesions. In this study, Hispanics given the diagnosis of melanomas had better treatment outcomes and survival than non-Hispanics.61 This contradicts a handful of other studies that have demonstrated poorer survival in Hispanic populations.57,62,63

MM in Asians In Asian populations, the sole of the foot is the

most common site for MM.28 This is typically acral lentiginous melanoma.28 As in blacks and Hispanics, MMs in Asians have a propensity to be diagnosed at a late stage in comparison with whites.57 In a study done in Taiwan, factors such as age over 55 years, male gender, tumor thickness, and tumor ulceration were generally predictive of a poorer prognosis.64 In a study done in Japan, loss of the p53 gene though deletion mutation was associated with more aggres- sive subtypes of MM.65

Although in whites, number of melanocytic nevi is directly proportional to risk of developing MM,66 this may not be the case in POC. The density of melanocytic nevi is significantly lower in POC than in whites.66 Gallagher et al66 (Vancouver, British Columbia, Canada) found that nevus density in Asians was unrelated to skin color or tendency to burn. These findings may indicate a lack of correla- tion between nevi density and MM in POC; however, further research is needed to clarify this point.

Survival in MM across ethnicities The 5-year survival for melanoma in Hispanic and

black populations has been shown to be consistently lower than in whites.6,53,67 When compared with whites, black and Hispanic populations have a pro- pensity to present with thicker tumors that are more advanced, therefore leading to a worse prognosis. In reviewing several melanoma cases in California, Cockburn et al49 demonstrated that diagnosis of tumors with a thickness greater than 1.5 mm upon presentation increased at 11.6% yearly and 8.9% yearly in Hispanic males and females, respectively. Hu et al62 performed a retrospective analysis of case series in the Florida Cancer Data System, showing that late-stage melanomas were most commonly diagnosed in black and Hispanic patients, at rates of 52% and 26%, respectively. In contrast, late-stage MM was diagnosed at a rate of 16% in white populations.62 In reviewing MM cases in California, blacks are have a higher rate of death in comparison with their white counterparts after adjusting for sex, age, stage, histology, anatomic site, socioeconomic status, and treatment.68 Therefore, the lower survival for blacks with MM is not fully accounted for by discrepancies in socioeconomic standing or access to

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adequate medical care. This leads to a conclusion that more aggressive primary and secondary preven- tion measures are needed for the diagnosis and control of MM across all races, including groups that have a lower risk of developing MM.69

MYCOSIS FUNGOIDES Mycosis fungoides (MF) is more commonly diag-

nosed in whites than in POC. However, incidence and prognosis vary significantly based on race. Weinstock and Gardstein70 used the US Surveillance, Epidemiology, and End Results (SEER) program of the National Cancer Institute to study the incidence of MF in blacks, whites, and Asians in the United States from 1973 to 1992. After adjusting for age, blacks had a higher incidence of MF than whites, with an incidence rate ratio of 1.6. The incidence of MF in Asians was lower than that of whites, with an incidence rate ratio of 0.6. Furthermore, blacks with MF had a worse prognosis than whites, with a mortality ratio of 2.4 compared with whites. In contrast, the mortality ratio of Asians compared with whites was 0.5. The cause for these differences in incidence and mortality are unknown.70 In a more recent study, Criscione and Weinstock71 used the SEER database to study incidence of cutaneous T-cell lymphoma in whites and blacks between 1973 and 2002. The incidence was 9.0 per 1 million person- years in blacks, whereas incidence of cutaneous T-cell lymphoma was 6.1 per 1 million person-years in whites.

MF typically presents as erythematous or hyperpigmented patches in individuals of darker complexion.13 Hypopigmented MF is diagnosed almost exclusively in POC. It typically presents as poorly defined hypopigmented patches (Fig 1).20,72,73 Distribution is typically more central than acral, and mild pruritus is often present.13

Differential diagnosis includes pityriasis alba, tinea versicolor, vitiligo, postinflammatory hypopigmenta- tion, and tinea corporis. Biopsy should be done in cases unresponsive to treatment for the aforemen- tioned conditions, or in patients who exhibit wors- ened disease despite treatment. Multiple biopsy specimens are often needed to confirm the diag- nosis.20 Immunohistochemical analysis often reveals a relative loss of the CD7 antigen.

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OTHER SKIN CANCERS There is limited information on other skin cancers

diagnosed in POC. Dermatofibrosarcoma protuber- ans (DFSP) is a slow-growing spindled cell neoplasm located in the dermis or subcutaneous tissue. It can present as a rare pigmented form that comprises up to 5% of DFSP. The pigmented variant occurs primarily

in blacks. DFSP most commonly presents on the trunk, followed by the upper and lower extremities and the head and neck. Clinically it may resemble a keloid, raising suspicion for keloidlike lesions in blacks that have no clear history of trauma.41 One study conducted in Nigeria reported 5 DFSP in 63 skin cancers diagnosed between 2000 and 2004. Three of these presented with recurrent lesions, and positive margin in 1 patient after initial excision.

21 Pigmented

DFSP may be histologically distinguished from the common variant through the presence of a dendritic cells containing melanin. DFSP tend to have a high local recurrence rate, though there have been reports of distant metastases. Wide excision and close clinical follow-up are indicated.13

Merkel cell carcinoma occurs at a rate of 0.2 and 0.01 per 100,000 in whites and blacks, respectively. Increased sun exposure corresponds with increased incidence, as the face is the most commonly affected site.75 Merkel cell carcinoma is rarely seen in Asians, though there have been case reports associating Merkel cell carcinoma with other skin cancers such as Bowen disease.76

PHOTOAGING AND UV-RELATED DYSPIGMENTATION IN POC

Although skin cancers pose the greatest mortality risk when discussing the need for photoprotection in POC, additional adverse effects of UVexposure, such as photoaging and UV-related exacerbation of pigmentation disorders, must be considered. Up to 95% of the visible signs of aging are a result of exposure to the sun, which starts in childhood and persists throughout life. Clinical signs of photoaging apparent in white skin may be less noticeable in POC of comparable age groups, implying a role of skin color in photoprotection.77 Despite the protective effects of darker skin on photoaging, signs of pho- toaging are still prevalent in POC. Dyspigmentation is more commonly seen in POC, whereas wrinkling is more prevalent in whites. As pigmentation disor- ders such as postinflammatory hyperpigmentation and melasma are generally more prevalent in POC, photoprotection may prevent worsening and recur- rence of these conditions.77

Kotrajaras and Kligman78 (Bangkok, Thailand) reported that significant photodamage manifested as dermal collagen and elastin damage, epidermal atypia and atrophy, and disorders of pigmentation are not uncommonly seen in POC. Similarly, other studies have observed that pigmentary changes may be more common than skin wrinkling with regards to photoaging among Asians.79,80 Chan et al81 (Hong Kong, China) observed that moderate to severe wrinkling becomes evident at around 50 years in

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Asians, 1 or 2 decades later than in age-matched whites.

Chung et al82 (Seoul, South Korea) performed a study evaluating the type and severity of photo- damage in Koreans and observed that women had a propensity to have more wrinkles than men. Seborrheic keratosis was the major pigmentary lesion observed in sun-exposed skin of men, whereas hyperpigmented macules were more often seen in women. Although cigarette smoking was found to be an independent risk factor for wrinkles, this was not so for dyspigmentation.82 There was no correlation between constitutive skin color and development of wrinkles or dyspigmentation. The authors concluded that wrinkling and pigmentary changes are significant manifestations of photoaging in Koreans.

82

Additional cutaneous manifestations of photoag- ing in ethnic skin include development of benign lesions such as solar lentigines and dermatosis papulosa nigra.81,83

SUN-PROTECTION BELIEFS AND PRACTICES IN POC

Although POC are most commonly categorized into skin phototypes IV to VI, it should be noted that ethnic skin colors can span the entire spectrum of skin phototypes.84 Skin examination and photo- protection practices differ between ethnic groups as whites and Hispanics have a greater propensity to use sunscreen than blacks.69 In addition, whites are more likely to perform skin self-examinations than Hispanics. Although blacks and Hispanics show similar practices in performance of skin self- examinations, blacks tend to follow up with derma- tologists less frequently.13 One survey study showed that blacks who self-reported experiencing severe sunburns were 7 times less likely to use sunscreen than their white counterparts who reported experi- encing severe sunburns. Among those surveyed who had severe sunburns in other ethnic groups (eg, Mexican American, other Hispanic, and other races), there was no such difference in sunscreen use.85

Although UV radiation exposure continues to become a more significant causative factor for skin cancer in blacks, discussion of their UV radiation- protection practices remains inadequate. Hall and Rogers86 (Atlanta, GA) analyzed the National Health Interview Survey performed in 1992 (n = 1583), in which approximately 6% of blacks reported marked sensitivity to sunlight with occurrence of severe sunburn, whereas 9% reported mild burning. Of the subjects studied, 53% self-reported a high likeli- hood of wearing protective clothing, sunscreens, or seeking shade. Factors such as educational

background, age, and sunburn history contributed to a tendency toward better photoprotection habits with sunscreens.86 Similarly, Buster et al87

(Birmingham, AL) evaluated a cross-sectional survey data from the National Cancer Institute to evaluate cancer-related knowledge, attitudes, and behaviors. There were 1246 respondents, including whites, blacks, and Hispanics. Blacks perceived their likeli- hood of developing skin cancer in the future as low, and were less likely than whites to recognize that behavior and lifestyle influence the risk of devel- oping skin cancer. Furthermore, blacks and Hispanics were more likely to believe that skin cancer is associated with pain or another symptom. Blacks less frequently viewed regular skin examina- tions as necessary for early detection of skin cancer, and both blacks and Hispanics were more likely to believe that little can be done to decrease the risk of developing skin cancer.87

In a survey performed by the Skin of Color Center in New York, NY, blacks and Hispanics self-reported low sunscreen use, secondary to misconceptions that it is unnecessary to use sun protection to prevent photoaging or skin cancers.77 If used at all, sun- screens were generally insufficiently applied and not reapplied frequently enough. Sanclemente et al88

(Medellin, Colombia) performed a study evaluating sun-protection behavior, skin phenotype, and min- imal erythema dose (MED) in 911 high school students in Colombia. There was significant vari- ability in MEDs among the different phototypes represented in the population, as individuals with fairer skin appeared to respond to UV radiation similar to their darker-skinned colleagues, and some students with darker skin responded similar to what would be expected from someone of lighter skin. This suggested a lack of predictability of MEDs based on skin phototype. In this population, only 10% of students who completed the associated questionnaire reported use of sunscreens or prac- ticed photoprotection.

88

Studies have shown that educational intervention may be helpful in improving photoprotection prac- tices. In a study performed by Kundu et al89

(Chicago, IL), POC (n = 93) were given instruction on how to identify potentially abnormal moles in cutaneous self-examination. Races represented in the study included Asian/Pacific Islander (21.5%), black American (59.1%), Hispanic (15.1%), and multiracial or ‘‘mixed’’ (4.3%). The investigators used self-report questionnaires evaluating attitudes, practices, and beliefs before, immediately after, and 3 months after the educational intervention.89 In all, 21% self-reported a skin phenotype that sometimes burns, and 32% reported at least 1 blistering sunburn

Table I. Recommendations for photoprotection and early detection of skin cancer in people of color

n Seek shade whenever possible.

n Wear sun-protective clothing. n Wear a wide-brimmed hat to shade the face and neck, and shoes that cover the entire foot. n Wear sunglasses with ultraviolet-absorbing lenses. n Apply broad-spectrum sunscreen with a sun-protection factor of 30 or greater. Sunscreens without inorganic filters (titanium dioxide and zinc oxide) are generally better accepted by people of color because of their better cosmesis on dark skin.

n Apply sunscreen to dry skin 15 to 30 minutes before going outdoors. When outdoors, reapply every 2 hours to all exposed skin, and after perspiring or swimming.

n Avoid exposure to indoor tanning beds/lamps. n Take vitamin D supplement. n Perform monthly self-skin examinations, paying close attention to subungual skin, palms, soles, mucous membranes, groin. and perianal area.

Table II. Recommendations for physicians for people of color

n Educate patients:

People of color are at risk for developing skin cancer. Practice sun-protective behaviors. Perform monthly self-skin examinations for those with multiple nevi, or history of skin cancers. Avoid tanning salons. Obtain regular skin examination by a dermatologist.

n Perform a thorough skin examination including areas infrequently exposed to the sun, such as palms, soles, oral mucosa, groin, and perianal area. Regularly ask patients to remove shoes and socks for skin examination.

n Monitor changes in pigmented lesions, including those of mucosal, palmar, plantar, interdigital spaces, and subungual surfaces.

n Advise vitamin D supplementation as indicated. n Refer to dermatologists: Changing pigmented lesions. Nonhealing ulcers. Hyperkeratotic or poorly healing lesions in chronic lesions such as those of discoid lupus erythematosus, or in scars. Atypical appearing keloidal plaques, or those with growth/development with no history of trauma.

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in the past. Of the original 93 subjects, 71 returned for follow-up evaluation after 3 months. Improved knowledge of MM as a skin cancer, and of concern- ing signs for melanoma was observed after the educational intervention. Furthermore, awareness of MM risk was shown to improve and was main- tained at 3 months. Practices such as performance of monthly self-skin checks, particularly of palms, soles, and periungual skin, dramatically improved after the intervention.89

VITAMIN D AND PHOTOPROTECTION Vitamin D has been shown to be beneficial for

bone health, and has been reported to have other potential health effects, including reduction of colo- rectal cancer, and reduction in cardiovascular dis- ease.90 Therefore, the question of whether or not rigorous photoprotection increases the risk of vitamin D deficiency is an important one.

Individual variables such as amount of skin pigmen- tation play a role in determining vitamin D produc- tion. There has been an emergence of vitamin D deficiency and rickets in dark-skinned patients in northern latitudes of the United States and United Kingdom. Meanwhile, similar populations in their countries of origin did not have this problem, which has led to suspicion that increased skin pigmentation may predispose dark-skinned patients to have vitamin D deficiency in certain geographic loca- tions.91 Because POC, especially those of darker skin, may have a higher risk for vitamin D insuffi- ciency secondary to higher skin melanin content,92

vitamin D supplementation should be recommen- ded as part of a photoprotection regimen for POC. Although there have been studies demonstrating decreased serum vitamin D levels in patients with photosensitivity practicing rigorous photoprotec- tion,93-95 regular use of sunscreens did not result in inadequate serum vitamin D level.95-97 It should be

Table III. Melanoma, basal cell carcinoma, squamous cell carcinoma, and Bowen disease in people of color

Skin cancer Pertinent demographics Physical presentation Differential diagnosis in POC Anatomic distribution Major risk factors in POC

Melanoma Median age of diagnosis in all races ranges from 52-63 y

Skin: Dark macules or patches with history of rapid spreading

Nail: Pigmented band [3 mm on the nail

Oral mucosa: Oral melanomas can rise from lesions of oral melanosis

Tinea nigra palmaris, talon noir, pigmented BCC

Commonly in lower extremities and plantar feet

UV radiation NOT a major risk factor

Risk factors for melanoma in POC unknown

BCC Most prevalent skin cancer in Hispanics14; second most common in blacks (in whom SCC is the most common)4,5

Typical: Asymptomatic solitary translucent nodules with pearly borders, rolled borders, and telangiectasia14

POC: Pigmentation in over half of cases; brown/black papules can also present as nodules, plaques, and ulcers

4,16,18

Seborrheic keratosis, blue nevus, trauma, lupus erythematosus, nevus sebaceous, sarcoidosis, and melanoma5,18

Head and neck most common in both whites and POC

15,19

Family history of skin cancer, Fitzpatrick skin type I, and the presence of actinic keratoses, solar lentigines, leukoderma, and elastosis rhomboidalis nuchae, UV radiation

SCC Most common skin cancer in blacks and Asian Indians; second most common in Hispanics, East Asians, and whites (second to BCC); in blacks: peak incidence in forties

Range between well- demarcated scaling pink plaques; firm, superficial, well-demarcated papules/ nodules emerging from round, indurated elevated base; granulomatous or verrucous lesions; and nonhealing ulcers

Lesions can be hypopigmented or hyperpigmented

Actinic keratosis, nummular eczema, inflamed seborrheic keratosis, verruca vulgaris

Typically on the face in white skin; in POC, not uncommon in areas not typically exposed to the sun, including lower extremities and anus

Lower limb/scalp SCC: Chronic scarring and inflammatory processes including hydradenitis suppurativa, lupus erythematosus, chemical/ thermal burns, chronic skin ulcers, chronic trauma sites of previous radiation; immunocompromised patients also at risk

Head/neck SCC: UV radiation Bowen disease Black women affected twice

as often as black men Scaly hyperkeratotic pigmented plaques resembling seborrheic keratoses

Seborrheic keratoses, pigmented BCC, superficial BCC, malignant melanoma, or nonspecific pigmented hyperkeratotic lesions

Areas not typically exposed to the sun: including groin and extremities

See SCC

BCC, Basal cell carcinoma; POC, people of color; SCC, squamous cell carcinoma; UV, ultraviolet.

J A M

A C A D D

E R M

A T O L

A P R IL

2 0 14

7 5 8

A g b a i et

a l

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Agbai et al 759

noted that most of the vitamin D photoprotection studies were done in predominantly white popula- tion, raising a question to their applicability to the broader population. A guideline to follow would be Institute of Medicine recommendations of 400 IU of vitamin D daily for infants up to 1 year old, 600 IU for individuals between 1 and 70 years old, and 800 IU for those older than 70 years.98 The National Institutes of Health provided a listing of food sources of vitamin D, including but not limited to cod liver oil, salmon, tuna, swordfish, and vitamin Defortified dairy products.99

THE SPF AND RECOMMENDATIONS FOR CLINICAL PRACTICE

A recent survey performed by Pourciau et al100

demonstrated a general belief among leaders in photodermatology that photoprotection counseling is warranted in POC. Still, there is a general lack of strong data supporting recommendations on SPF requirements for specific skin phototypes. It is known that a given sunscreen may demonstrate different SPF value in varying skin colors, as demon- strated by Damian et al101 (Sydney, Australia) in 1999. Using a xenon arc lamp with an emission spectrum simulating the UVA and UVB wavelengths of natural sunlight, the investigators found testing a sunscreen product in fair-skinned individuals (who had low MED) yielded higher SPF values compared with testing the same product in dark-skinned sub- jects (with higher MEDs). Because commercial testing of SPF is mandated to be done in fair- skinned individuals,102 SPF values of sunscreens on dark skin therefore may be lower that the SPF values stated in the label.101

Similar to the message on photoprotection for the general population, POC should also be advised to use a daily broad-spectrum sunscreen of at least SPF 30, and practice sun-protective behavior such as seeking shade and use of protective clothing, wide- brimmed hat, and sunglasses (Table I). Sunscreens should be applied liberally and reapplied every 2 hours while outdoors. Furthermore, patients should be advised to avoid tanning salons and intentional tanning with natural sunlight. A thorough skin examination, including examination of nails, oral cavity, gums, palms, soles, groin, and perianal area should be performed regularly by a dermatologist; for those older than 50 years, yearly examination is appropriate. Pigmented lesions on gums and streaks in nails are normal in POC, but should be monitored regularly for changes as malignant transformation can occur. For patients with history of skin NMSC or melanoma, or multiple nevi, monthly self-skin ex- amination is appropriate. Primary care physicians

should be educated on high-risk sites for MM, such as palms and soles (Tables II and III). Efforts are needed to take the diversity in culture, beliefs, and language across ethnicities into account so that photoprotec- tion education can reach the target population of color.

Wendy E. Roberts, MD, serves as a consultant for Allergan Medical, L’Oreal, La Roche-Posay, and NeoStrata, for which she receives honoraria. She also sits on the advisory board and consults for SkinMedica, for which she receives honoraria. She receives stock options from TopMD. She consults for Theraplex, for which she receives no compensation.

In 2013, Susan Taylor, MD, held seats on the advisory boards of Allergan, Beiersdorf, Inc, Excaliard Pharmaceuticals, and Unilever, for which she receives honoraria. She serves as a consultant for Curel Skincare, Pfizer, Schlesinger Associates, and Viviscal. Dr Taylor founded T2 Skincare for which she receives other financial benefit and serves in other roles. She receives grants as an investigator for Hisamitsu Pharmaceutical, Medicis Pharmaceuticals, Noven Pharmaceuticals, and Pfizer. Dr Taylor has received honoraria as a speaker from Allergan, Johnson & Johnson, Kao USA, Merz Pharmaceuticals, and Neostrata.

2012 found Dr Taylor serving as a consultant for Schlesinger Associates and Pfizer for which she received honoraria. She sat on the advisory board for Allergan, Beiersdorf and Excaliard Pharmaceuticals, for which she received honoraria. Dr Taylor founded T2 Skincare for which she received other financial benefit and served in other roles. She is an investigator for Pfizer, Medicis, Noven, and Hisamitsu, for which she receives honoraria. She contracted for Medscape/ WebMD for which she received honoraria. She served as a speaker for Merz Pharmaceuticals and Allergan for which she received honoraria. She receives no compen- sation for her role at the Philadelphia Life Sciences Institute.

In 2011, Dr Taylor was awarded grants as an investigator for Medicis and Noven Pharmaceuticals. She received honoraria for speaking from Elsevier and Johnson & Johnson. Dr Taylor sat on the advisory board for Merz Pharmaceuticals and Beiersdorf and received honoraria for her support. She served as a consultant and received a consulting fee from Tria Beauty and Johnson & Johnson Dr. Taylor has received honoraria as researcher from Johnson & Johnson and Beiersdorf.

Henry W. Lim, MD, serves as a consultant for Ferndale and La Roche-Posay for which he receives honoraria.

Roopal V. Kundu, MD, had no relevant conflict of interest to disclose. Her department receives compensa- tion for pharmaceutical sponsored research that does not benefit her directly.

Oma N. Agbai, MD, Kesha Buster, MD, Miguel Sanchez, MD, Claudia Hernandez, MD, Melvin Chiu, MD, FAAD, Zoe D. Draelos, MD, and Reva Bhushan, PhD, had no relevant conflicts of interest to disclose.

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