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

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, MDa

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

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Skin cancer is less prevalent in people of color than in the white population. However, when skin canceroccurs in non-whites, it often presents at a more advanced stage, and thus the prognosis is worse comparedwith white patients. The increased morbidity and mortality associated with skin cancer in patients of colorcompared with white patients may be because of the lack of awareness, diagnoses at a more advancedstage, and socioeconomic factors such as access to care barriers. Physician promotion of skin cancerprevention strategies for all patients, regardless of ethnic background and socioeconomic status, can lead totimely diagnosis and treatment. Public education campaigns should be expanded to target communities ofcolor to promote self-skin examination and stress importance of photoprotection, avoidance of tanning beduse, and early skin cancer detection and treatment. These measures should result in reduction or earlierdetection of cutaneous malignancies in all communities. Furthermore, promotion of photoprotectionpractices 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; skincancer; skin of color; squamous cell carcinoma; sun protection; sunscreen; ultraviolet.

DEFINITIONS
Abbreviations used:
BCC: basal cell carcinomaDFSP: dermatofibrosarcoma protuberansMED: minimal erythema doseMF: mycosis fungoidesMM: malignant melanomaNMSC: nonmelanoma skin cancerPOC: people of colorSCC: squamous cell carcinomaSEER: Surveillance, Epidemiology, and End

ResultsSPF: sun-protection factorUV: ultraviolet

Whites: Non-Hispanic individuals of Europeandescent

Blacks: Non-Hispanic individuals of Africandescent

Hispanics: Individuals who trace their origin ordescent 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 consideredas the heritage, nationality group, lineage, or countryof the person or the person’s parents or ancestorsbefore their arrival in the United States. People who

the Multicultural Dermatology Center, Department of

ermatology, Henry Ford Hospital, Detroita; Department of

ermatology, Via Christi Clinic, Wichitab; Department of

ermatology, New York University Medical Centerc; Depart-

ent of Dermatology, University of Illinois College of Medicine,

hicagod; 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 Mirageg; Dermatology Consulting Services, High Pointh;

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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http://dx.doi.org/10.1016/j.jaad.2013.11.038

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VOLUME 70, NUMBER 4Agbai et al 749

identify their origin as Hispanic or Latino may be ofany race. This definition of Hispanic fully excludesthe Portuguese, Brazilians, or anyone from any othercountry that speaks Portuguese.1

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

INTRODUCTIONMalignant melanoma (MM) and nonmelanoma

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

The incidence of both MM and NMSC remainssignificantly lower in people of color (POC) whencompared with whites as they are seen in about 5%of Hispanics, 4% of Asians, and 2% of blacks.4,5 Evenso, multiple reports have demonstrated heightenedmorbidity and mortality in minority populations,6-8

raising public health concerns in these groups.Although there are data detailing incidence of skincancer in POC, these data are limited. In addition toskin cancer, factors such as photoaging, pigmentarydisorders induced or exacerbated by ultraviolet (UV)exposure, and sunburn must be considered in POC.It is estimated that black, Hispanic, and AsianAmericans will comprise approximately 50% of theUS population by the year 2050.4 These evolvingdemographics, elevated rates of skin cancermorbidity and mortality in POC, and limited clinicaldata on additional adverse effects of UV exposure inthis population mandate that physicians developfamiliarity with the concept of optimized photo-protection for POC. An understanding of the varyingclinical presentations of UV-related skin cancers inPOC, in addition to relevant topics in photoaging andUV-related disorders of pigmentation, is necessaryfor adequate management of photoprotection inPOC.

BIOLOGICAL BASIS OF SKINCARCINOGENESIS AND PHOTOAGING INPOC

Few studies have been performed to thoroughlyevaluate biological differences between differingethnic skin types. Skin color is primarily determinedby the presence of melanin. Jimbow et al9 reportedthat dark skin has larger melanocytes that producemore melanin and melanosomes are distributedindividually in keratinocytes rather than in aggre-gates. The rarity of cutaneous malignancy in

populations of darker complexions is secondary tophotoprotection from a higher amount of epidermalmelanin, which filters at least twice as much UVradiation as the epidermis of whites.10 In an in vitrostudy performed by Kaidbey et al,11 the amount ofUV radiation reaching the papillary dermis of whiteswas greater than that of blacks by approximately5-fold. The authors proposed that larger and moremelanized melanosomes observed in POC absorbedmore energy than the melanosomes in white skin,which were smaller, less dense, and lightly mela-nized. Furthermore, the authors estimated that theepidermis of blacks has an intrinsic sun-protectionfactor (SPF) of 13.4, whereas light skin has an SPF of3.3.11 Therefore, exposure to UV radiation plays alesser role in heightening the risk for skin cancer inpopulations of darker complexions.

Damage to DNA secondary to UV radiation is amajor factor in cutaneous photocarcinogenesis andphotoaging. However, the correlation of ethnicityand degree of sensitivity to UV rays has not beenelucidated. Tadokoro et al12 performed a studyevaluating the correlations between melanin contentand degree of UVA- and UVB-induced DNA damagein normal-appearing skin of various ethnic groups.DNA damage was found to be most severe inqualitatively light skin. Baseline skin pigmentationand extent of DNA damage were inversely related, asindividuals of darker skin tones were able to repairUVA-/UVB-induced DNA damage more rapidly thansubjects with fair skin. Even low exposure toUVA/UVB radiation induced some appreciableDNA damage in all skin types, dispelling the myththat those with very dark skin are completely im-mune to UVA-/UVB-induced DNA damage.12

Indeed, NMSC and MM do occur in POC, despitethe low relative risk.13 Because of the limitedresearch on skin cancer in POC, there are fewresources providing insight on evaluating darklypigmented lesions in POC. Frequently atypicalpresentations, together with constitutive darkpigmentation, pose diagnostic challenges in theidentification of characteristics such as variation incolor within the lesions. Furthermore, certain skincancers that are pigmented in POC may not bepigmented in whites (such as basal cell carcinoma,which is more likely to be pigmented in darker skintypes); therefore, a high index of suspicion in POC isnecessary in making the diagnosis.5

BASAL CELL CARCINOMABasal 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 ofmultiple BCC rather than a single squamous cell

Fig 1. Nonmelanoma skin cancers in people of color. Pigmented basal cell carcinoma inelderly 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 nasalala) (D). Hypopigmented mycosis fungoides in Hispanic man (back) (E) and black man (loweraspect 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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APRIL 2014750 Agbai et al

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 showsmany parallels among blacks, whites, Asians, andHispanics. The classic clinical presentation of a solitarypearly papule with central ulceration and rolledborders may be seen in POC, butmay pose challengesin the physical examination as the characteristic pearlyborders and telangiectasia may not be clinically asapparent in dark skin types (Fig 1). In whites, themajority of patients presenting with BCC are ofadvancedage ([50years),most commonlypresentingwith asymptomatic solitary translucent nodules withcentral ulceration.14 Pigmentation is present in over50% of tumors in POC,4,16 whereas only 5% of BCCsaffectingwhites have been shown to be pigmented. InAsians, BCCs frequently present as brown to blackpapules, or have a ‘‘black pearly’’ appearance.17 Theclinical presentation of BCCs in Asian skin ranges fromnodules to papules, plaques, and ulcers.18 Withregards to anatomic distribution, there are significantsimilarities between POC and whites. Approximately80% of BCCs in POC were found in the head andneck,19 as has been shown in whites.14 Differentialdiagnosis for BCC in POC includes seborrheic kera-tosis, blue nevus, trauma, lupus erythematosus, nevus

sebaceous, sarcoidosis, andmelanoma.20Metastasis inBCC is rare in all skin types.14

BCC in blacksAlthough quite rare, BCC has been reported in the

black population. In a report from HowardUniversity (Washington, DC) from 1960 through1986, most BCCs were seen in blacks of fairer skincomplexion in comparison with those with darkercomplexions.19 From this, onemay conclude that theincidence of BCC may correlate directly with thedegree of skin pigmentation, as it is most frequentlydiagnosed in whites of fairer complexions, and morerarely diagnosed in blacks. A study of skin cancerprevalence was conducted by Asuquo et al21 in aNigerian teaching hospital between the years of 2000and 2004. Of 63 cases of skin cancer, BCC wasdiagnosed in 8% (n = 5) of the cases; 66.7% of theBCC were on the head and neck, and 33.3% on theupper limb. All of these lesions were nodular. BCCwas diagnosed only in albinos in this study.21 In areview of 128 black patients with 148 BCCs, Moraand Burris3 (New Orleans, LA) found that theaverage age of examination (not necessarily onset)was 59 years, with lesions most commonly locatedon head and neck. Only 2 of these patients hadalbinism.

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

BCC in HispanicsOne of themost common neoplasms diagnosed in

Hispanics is pigmented BCC.16 Hispanics studieddemonstrated significantly lower incidence rates ofBCC than non-Hispanic whites regardless ofgender.24 Still, a high index of suspicion should bemaintained in evaluating pigmented lesions inHispanics, as BCCs have a propensity to be pig-mented in Hispanic populations and may be mis-diagnosed as melanomas.16 In a study performed byBigler et al16 (Albuquerque, NM), the incidence ofpigmented BCC in Hispanics was found to be twicethat of white patients.

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

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

extremely rare. In a study by Cheng et al25 studyingincidence of NMSC between 1990 and 1999 in HongKong, China, the incidence of BCC was 0.32 and 0.92per 100,000 population. Pigmented BCC was themost common NMSC diagnosed, found in approxi-mately 60% of Chinese patients with skin cancer inthe study.25 Multiple or subsequent skin cancers andsubtypes of new cancers were seen less often in theChinese group when compared with the whitegroup.25 Similarly, Sng et al26 reported an increaseof skin cancers including BCC, SCC, and MM, inSingapore between the years of 1998 and 2006. Theextremities were the most common sites affected byBowen disease (SCC in situ).27 There is an increasedincidence of NMSC in Japanese living in Kauai,Hawaii, which may be secondary to heightenedintensity of year-round UV radiation and popularityof outdoor activities, as reviewed by Lee and Lim.28

SQUAMOUS CELL CARCINOMASCC comprises approximately 20% of all skin

cancers. With MM excluded, approximately 75% of

all deaths from skin cancers are caused by SCC.29 Inblacks and Asian Indians, SCC is the most commonlydiagnosed skin cancer. It is the second mostcommonly diagnosed skin cancer in Hispanics, EastAsians (including Japanese and Chinese patients),and whites.5,30 Although actinic keratoses are mostcommonly diagnosed in white and Japanese pa-tients,31 they are very rare in blacks.32

Risk factors for SCC inPOC includechronic scarringand inflammatory processes including hidradenitissuppurativa, lupus erythematosus, scars caused bychemical and thermal burns, skin ulcers, and sites ofprevious radiation.33,34 Immunocompromised pa-tients, including organ transplant recipients, alsodemonstrate a heightened risk for SCC.35 Amongblacks, the greatest predisposing factors for devel-oping SCC include chronic scarring and/or inflamma-tory processes that are observed in 20% to 40% ofreported cases.4 In addition, the human papilloma-virus has been linked to the development of SCC,particularly in immunocompromised patients.36 Oneretrospective study detected human papillomavirusDNA in skin samples of 4.7% of controls, 90.5% ofbenignwarts, 60.4% of precancerous lesions, 59.7% ofSCC, and 27.8% of BCC, suggesting a link betweenviral infection and the development of NMSC.37

Definitive studies have not been performed on therelationship betweenhumanpapillomavirus infectionand NMSC in POC.

SCCs are characteristically firm, superficial, well-demarcated papules or plaques that emerge from arounded, indurated, and elevated base.29 In POC,SCC is most commonly found in areas that are nottypically exposed to the sun, such as the lowerextremities and anus. In fact, lower extremity andanogenital SCCs were seen in 15% of SCCs in blacksin a study conducted by Halder and Bang19 inWashington, DC. This is a sharp contrast to the whitepopulation, in whom SCCs are characteristically seenin chronically sun-exposed skin.19

SCC in blacksAmong black patients given the diagnosis of

SCC, the peak incidence was shown to be in thefifth decade on the lower limbs, followed by thehead and neck and then the genitals. The scalp andlip are more often implicated in black women thanin men.38 Chronic trauma, ulcers, and scars are themost significant predisposing factors for SCCs in thelower limb and on the scalp, as reported by Amiret al38 (Dar es Salaam, Tanzania) in a study of SCCin Tanzanian patients, where UV radiation wasfound 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 riskfactor for the majority of cases of SCC developingon the penis in blacks.38 The majority of SCC on thepenis were found to be SCC in situ upon histologicanalysis 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 and2004 by Asuquo et al,21 where the lower limb wasthe most commonly affected anatomic site. SCCmanifesting as Marjolin ulcer associated with trau-matic injury of the limb was diagnosed in 7patients, and associated with a history of burn in1 patient. SCC involved the external genitalia in 9patients, 3 of whom had genital warts. The anuswas affected in 4 female cases. There were nolesions involving the head and neck regions, andall patients in this study presented with chroniculcers.21

Several cases of the emergence of SCC withinscars of chronic discoid lupus erythematosus in blackpatients have been reported. Caruso et al40 reporteda heightened propensity for SCC to metastasize inblack Canadian patients with discoid lupus erythe-matosus. Sun exposure of hypopigmented lesions ofdiscoid lupus erythematosus may have been apredisposing factor.

In blacks, Bowen disease (SCC in situ) typicallypresents as scaly hyperkeratotic pigmented pla-ques, and may be misdiagnosed as MM. In contrast,Bowen disease lesions are rarely pigmentedoutside of the groin in whites.41 Black womenare affected twice as often as black men, and mostfrequently in skin that is not sun exposed.19 In astudy performed by Mora et al42 in New Orleans,LA, evolution to SCC was noted in 5 of 19 blackpatients with Bowen disease, leading to death in 3of these patients. The most common area affectedwas the lower extremity.42 Mortality of SCC inblacks is as high as 29%, secondary not only todelays in diagnosis and treatment, but also to moreaggressive biologic behavior of SCC in this popu-lation.41,43 In blacks, SCC that develops within achronic scarring process tends to be more aggres-sive and is associated with a 20% to 40% risk ofmetastasis. 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 blacksperformed by Mora and Perniciaro33 (New Orleans,LA), the highest mortality was observed in cases ofperianal SCC. Although most patients with primarySCC have a very good prognosis, the 10-yearsurvival is less than 20% in patients with regionallymph node metastasis, and less than 10% inpatients with distant metastasis.29

SCC in AsiansBowen disease and pigmented BCCs are not

uncommonly diagnosed in Asians. Because of theirpigmented appearance, as in blacks, these may bemisdiagnosed as MM.25 Although NMSC is uncom-mon, it is not rare in the Chinese population in HongKong. Cheng et al25 (Hong Kong, China) reportedthat the incidence of SCC in 1990 was 0.16 per100,000 population, and in 1999, 0.34. Similarly, in acase-control study performed by Chen et al44 inTaiwan 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 weresignificantly associated with heightened risk of SCCin a dose-related pattern. Cumulative sun exposurewas found to be more closely related to increasedrisk of SCC in women, whereas sun exposure at anearly age showed more relevance to SCC risk inmen.44 Skin reactions such as redness, burn, andsuntan after 2 hours of sun exposure in childhoodand adolescence were not associated with increasedrisk for SCC.44

In a study on skin cancer incidence between 1986and 1997 among Asians living in Singapore, 2650BCCs were reported. There was a general increase inskin 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 increasedapproximately 3% yearly. Age-standardized inci-dence rates for BCC were greatest in fair-skinnedChinese, followed by Malays and Indians. This trendwas also noted for SCC and cutaneous MM.45

MALIGNANT MELANOMAMM is the deadliest type of skin cancer found

across all races and ethnicities. Manymelanoma casesare diagnosed in nonhospital settings and thus maybe underreported to central cancer registries, whichtraditionally collect the majority of cases from hospi-tals.46 This could lead to significant underreporting ofMM and resultant underestimation of the incidence ofmelanoma.47 The National Cancer Institute, Divisionof Cancer Control and Population Sciences,Surveillance Research Program, Cancer StatisticsBranch (Bethesda, MD) reports that the incidenceof cutaneous MM increased by approximately 6%yearly in the 1970s, slowed to a 3% yearly increasebetween 1981 and 2000, and has since stabilized.48

Since the late 1980s, the incidence of MM hasincreased significantly among Hispanics inCalifornia, increasing an average of 1.8% yearly inmale Hispanics between 1988 and 2001, and 7.3%average yearly between 1996 and 2001.49 In a studyconducted 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 by1.6- to 3.7-fold. There was a close correlation inanatomic distribution of MM among whites andHispanics in New Mexico in both men and women.Themost commonMMdistribution in Hispanics fromPuerto Rico was the leg, as was seen in blackAmericans.50 In another study, Vazquez-Botet et al51

reported that nearly half of MM inHispanic patients inPuerto Rico were found on the extremities, especiallythe 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 Morerecently, Wu et al52 (New Orleans, LA) reported thatincidence rates of MM in the United States werenotably higher in females than males in white andHispanic populations younger than 50 years, and inAsian/Pacific Islanders younger than 40 years. Themedian age of white and black patients was greater(59-63 years) when compared with Hispanics, Asian/Pacific Islanders, and American Indians/AlaskanNatives (52-56 years).52 Histologically, acral lentigi-nous melanoma was the most common subtype inblacks, whereas superficial spreading melanoma wasmost commonly diagnosed in all other ethnic groupsstudied.52 Incidence rates of acral lentiginous

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

Typically, MM presents as a dark macule or patchand may have a history of rapid spreading. Suspicionfor subungual melanomas is raised when a pig-mented band wider than 3 mm is observed on thenail, extension of pigment to proximal nail fold(Hutchinson sign) and there is pigment variation,rapid growth in size, and the observation of solitarylesions.4 Subungual melanoma is most common onthe thumb and first toe. In populations of color, theplantar foot is most commonly affected (Fig 2),53 as itis implicated in 30% to 40% of cases.54 Melanomasfound in the oral cavity comprise approximately 7.5%of all melanomas in Asians, where approximately60% of these develop from lesions of oral melanosis.

The greatest risk factors for the development ofMMin whites include periods of high intermittent sunlightexposure (as in sunbathing and indoor tanning), andlarge cumulative doses of UV radiation from chronicexposure (as seen in outdoor workers).55 Factors inthe host that may increase susceptibility to develop-ment ofmelanoma include a large number of nevi, thepresence 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 notappear to be a major risk factor, as the majority ofmelanomas are found in skin that is not typically sunexposed, including palmar, plantar, and subungualskin, and mucous membranes.56 In POC, the riskfactors for MM have not been identified, but may beunrelated to sun exposure.57 Specifically, as acralmelanomas are identifiedwith similar rates at differentlatitudes and in varying racial groups, and as they tendto be diagnosed in anatomic sites that are not typicallysun exposed, their origin may be unrelated to sunexposure.28

MM in blacksIn black Americans, acral lentiginous melanoma is

the most common and deadly form of MM.56,58 Notuncommonly it is misdiagnosed and managed as atinea nigra, or even talon noir. In a retrospectivestudy performed at Tulane University School ofMedicine (New Orleans, LA)58 from 1958 to 1990,82 patients (including 27 white men, 29 whitewomen, 18 black men, and 8 black women) with adiagnosis of acral lentiginous melanoma were fol-lowed up, and the study showed a trend towardreduced survival in black men. A direct correlationbetween decreased survival and increased Clarklevel was also observed. As previously mentioned,the overall incidence of melanoma in the blackpopulation is lower than that of whites. Additionaltypes of melanoma found in black Americansinclude superficial spreading and nodular types.13

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

In a study of skin cancers in a teaching hospital inNigeria between 2000 and 2004, MM of the skinrepresented 8% (n = 5) of the 63 histologicallydiagnosed cutaneous malignancies. All of theseMMs were plantar. Three of the 5 cases wereclinically advanced nodular melanomas, whereas 2were ulcerated superficial spreading melanomas.21

MM in HispanicsPipitone et al60 (Maywood, IL) proposed that

Hispanics had a propensity to present with moreadvanced disease secondary to the combination of abelief that they are not at risk to sunburn and/ordevelop skin cancer. Skin cancer prevention mea-sures are typically directed toward non-Hispanicwhites, 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 thetrunk, arm, shoulder, leg, and hip. Although 70% ofthese patients presented with local disease, 26%

presented with regional and distant lesions. In thisstudy, Hispanics given the diagnosis of melanomashad better treatment outcomes and survival thannon-Hispanics.61 This contradicts a handful of otherstudies that have demonstrated poorer survival inHispanic populations.57,62,63

MM in AsiansIn Asian populations, the sole of the foot is the

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

Although inwhites, number of melanocytic nevi isdirectly proportional to risk of developing MM,66 thismay not be the case in POC. The density ofmelanocytic nevi is significantly lower in POC thanin whites.66 Gallagher et al66 (Vancouver, BritishColumbia, Canada) found that nevus density inAsians was unrelated to skin color or tendency toburn. 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 ethnicitiesThe 5-year survival for melanoma in Hispanic and

black populations has been shown to be consistentlylower than in whites.6,53,67 When compared withwhites, black and Hispanic populations have a pro-pensity to present with thicker tumors that are moreadvanced, therefore leading to a worse prognosis. Inreviewing several melanoma cases in California,Cockburn et al49 demonstrated that diagnosis oftumors with a thickness greater than 1.5 mm uponpresentation increased at 11.6% yearly and 8.9%yearly in Hispanic males and females, respectively.Hu et al62 performed a retrospective analysis of caseseries in the Florida Cancer Data System, showingthat late-stage melanomas were most commonlydiagnosed in black and Hispanic patients, at ratesof 52% and 26%, respectively. In contrast, late-stageMM was diagnosed at a rate of 16% in whitepopulations.62 In reviewing MM cases in California,blacks are have a higher rate of death in comparisonwith their white counterparts after adjusting for sex,age, stage, histology, anatomic site, socioeconomicstatus, and treatment.68 Therefore, the lower survivalfor blacks with MM is not fully accounted for bydiscrepancies in socioeconomic standing or access to

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

MYCOSIS FUNGOIDESMycosis fungoides (MF) is more commonly diag-

nosed in whites than in POC. However, incidenceand prognosis vary significantly based on race.Weinstock and Gardstein70 used the USSurveillance, Epidemiology, and End Results (SEER)program of the National Cancer Institute to study theincidence of MF in blacks, whites, and Asians in theUnited States from 1973 to 1992. After adjusting forage, blacks had a higher incidence of MF thanwhites,with an incidence rate ratio of 1.6. The incidence ofMF in Asians was lower than that of whites, with anincidence rate ratio of 0.6. Furthermore, blacks withMF had a worse prognosis than whites, with amortality ratio of 2.4 compared with whites. Incontrast, the mortality ratio of Asians comparedwith whites was 0.5. The cause for these differencesin incidence and mortality are unknown.70 In a morerecent study, Criscione and Weinstock71 used theSEER database to study incidence of cutaneous T-celllymphoma in whites and blacks between 1973 and2002. The incidence was 9.0 per 1 million person-years in blacks, whereas incidence of cutaneousT-cell lymphoma was 6.1 per 1 million person-yearsin whites.

MF typically presents as erythematous orhyperpigmented patches in individuals of darkercomplexion.13 Hypopigmented MF is diagnosedalmost exclusively in POC. It typically presents aspoorly defined hypopigmented patches(Fig 1).20,72,73 Distribution is typically more centralthan acral, and mild pruritus is often present.13

Differential diagnosis includes pityriasis alba, tineaversicolor, vitiligo, postinflammatory hypopigmenta-tion, and tinea corporis. Biopsy should be done incases unresponsive to treatment for the aforemen-tioned conditions, or in patients who exhibit wors-ened disease despite treatment. Multiple biopsyspecimens are often needed to confirm the diag-nosis.20 Immunohistochemical analysis often revealsa relative loss of the CD7 antigen.74

OTHER SKIN CANCERSThere is limited information on other skin cancers

diagnosed in POC. Dermatofibrosarcoma protuber-ans (DFSP) is a slow-growing spindled cell neoplasmlocated in the dermis or subcutaneous tissue. It canpresent as a rare pigmented form that comprises up to5% of DFSP. The pigmented variant occurs primarily

in blacks. DFSP most commonly presents on thetrunk, followed by the upper and lower extremitiesand the head and neck. Clinically it may resemble akeloid, raising suspicion for keloidlike lesions inblacks that have no clear history of trauma.41 Onestudy conducted inNigeria reported 5DFSP in 63 skincancers diagnosed between 2000 and 2004. Three ofthese presented with recurrent lesions, and positivemargin in 1 patient after initial excision.21 PigmentedDFSP may be histologically distinguished from thecommon variant through the presence of a dendriticcells containing melanin. DFSP tend to have a highlocal recurrence rate, though there have been reportsof distant metastases.Wide excision and close clinicalfollow-up are indicated.13

Merkel cell carcinoma occurs at a rate of 0.2 and0.01 per 100,000 in whites and blacks, respectively.Increased sun exposure corresponds with increasedincidence, as the face is the most commonly affectedsite.75 Merkel cell carcinoma is rarely seen in Asians,though there have been case reports associatingMerkel cell carcinoma with other skin cancers suchas Bowen disease.76

PHOTOAGING AND UV-RELATEDDYSPIGMENTATION IN POC

Although skin cancers pose the greatest mortalityrisk when discussing the need for photoprotection inPOC, additional adverse effects of UVexposure, suchas photoaging and UV-related exacerbation ofpigmentation disorders, must be considered. Up to95% of the visible signs of aging are a result ofexposure to the sun, which starts in childhood andpersists throughout life. Clinical signs of photoagingapparent in white skin may be less noticeable in POCof comparable age groups, implying a role of skincolor in photoprotection.77 Despite the protectiveeffects of darker skin on photoaging, signs of pho-toaging are still prevalent in POC. Dyspigmentationis more commonly seen in POC, whereas wrinklingis more prevalent in whites. As pigmentation disor-ders such as postinflammatory hyperpigmentationand 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 manifestedas dermal collagen and elastin damage, epidermalatypia and atrophy, and disorders of pigmentationare not uncommonly seen in POC. Similarly, otherstudies have observed that pigmentary changes maybemore common than skin wrinklingwith regards tophotoaging among Asians.79,80 Chan et al81 (HongKong, China) observed that moderate to severewrinkling becomes evident at around 50 years in

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

Chung et al82 (Seoul, South Korea) performed astudy evaluating the type and severity of photo-damage in Koreans and observed that women had apropensity to have more wrinkles than men.Seborrheic keratosis was the major pigmentarylesion observed in sun-exposed skin of men,whereas hyperpigmented macules were more oftenseen in women. Although cigarette smoking wasfound to be an independent risk factor for wrinkles,this was not so for dyspigmentation.82 There was nocorrelation between constitutive skin color anddevelopment of wrinkles or dyspigmentation. Theauthors concluded that wrinkling and pigmentarychanges are significant manifestations of photoagingin Koreans.82

Additional cutaneous manifestations of photoag-ing in ethnic skin include development of benignlesions such as solar lentigines and dermatosispapulosa nigra.81,83

SUN-PROTECTION BELIEFS ANDPRACTICES IN POC

Although POC are most commonly categorizedinto skin phototypes IV to VI, it should be noted thatethnic skin colors can span the entire spectrum ofskin phototypes.84 Skin examination and photo-protection practices differ between ethnic groupsas whites and Hispanics have a greater propensity touse sunscreen than blacks.69 In addition, whites aremore likely to perform skin self-examinations thanHispanics. Although blacks and Hispanics showsimilar practices in performance of skin self-examinations, blacks tend to follow up with derma-tologists less frequently.13 One survey study showedthat blacks who self-reported experiencing severesunburns were 7 times less likely to use sunscreenthan their white counterparts who reported experi-encing severe sunburns. Among those surveyed whohad 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 tobecome a more significant causative factor for skincancer in blacks, discussion of their UV radiation-protection practices remains inadequate. Hall andRogers86 (Atlanta, GA) analyzed the National HealthInterview Survey performed in 1992 (n = 1583), inwhich approximately 6% of blacks reported markedsensitivity to sunlight with occurrence of severesunburn, whereas 9% reported mild burning. Ofthe subjects studied, 53% self-reported a high likeli-hood of wearing protective clothing, sunscreens, orseeking shade. Factors such as educational

background, age, and sunburn history contributedto a tendency toward better photoprotection habitswith sunscreens.86 Similarly, Buster et al87

(Birmingham, AL) evaluated a cross-sectional surveydata from the National Cancer Institute to evaluatecancer-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 thatbehavior and lifestyle influence the risk of devel-oping skin cancer. Furthermore, blacks andHispanics were more likely to believe that skincancer 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 tobelieve that little can be done to decrease the risk ofdeveloping skin cancer.87

In a survey performed by the Skin of Color Centerin New York, NY, blacks and Hispanics self-reportedlow sunscreen use, secondary to misconceptionsthat it is unnecessary to use sun protection to preventphotoaging or skin cancers.77 If used at all, sun-screens were generally insufficiently applied and notreapplied frequently enough. Sanclemente et al88

(Medellin, Colombia) performed a study evaluatingsun-protection behavior, skin phenotype, and min-imal erythema dose (MED) in 911 high schoolstudents in Colombia. There was significant vari-ability in MEDs among the different phototypesrepresented in the population, as individuals withfairer skin appeared to respond to UV radiationsimilar to their darker-skinned colleagues, andsome students with darker skin responded similarto what would be expected from someone of lighterskin. This suggested a lack of predictability of MEDsbased on skin phototype. In this population, only10% of students who completed the associatedquestionnaire reported use of sunscreens or prac-ticed photoprotection.88

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

(Chicago, IL), POC (n = 93) were given instructionon how to identify potentially abnormal moles incutaneous self-examination. Races represented inthe study included Asian/Pacific Islander (21.5%),black American (59.1%), Hispanic (15.1%), andmultiracial or ‘‘mixed’’ (4.3%). The investigatorsused self-report questionnaires evaluating attitudes,practices, and beliefs before, immediately after, and3 months after the educational intervention.89 In all,21% self-reported a skin phenotype that sometimesburns, 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 ondark skin.

n Apply sunscreen to dry skin 15 to 30 minutes before going outdoors. When outdoors, reapply every 2 hours to all exposedskin, 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 subungualsurfaces.

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 forfollow-up evaluation after 3 months. Improvedknowledge of MM as a skin cancer, and of concern-ing signs for melanoma was observed after theeducational intervention. Furthermore, awarenessof MM risk was shown to improve and was main-tained at 3 months. Practices such as performance ofmonthly self-skin checks, particularly of palms,soles, and periungual skin, dramatically improvedafter the intervention.89

VITAMIN D AND PHOTOPROTECTIONVitamin D has been shown to be beneficial for

bone health, and has been reported to have otherpotential health effects, including reduction of colo-rectal cancer, and reduction in cardiovascular dis-ease.90 Therefore, the question of whether or notrigorous photoprotection increases the risk ofvitamin 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 Ddeficiency and rickets in dark-skinned patients innorthern latitudes of the United States and UnitedKingdom. Meanwhile, similar populations in theircountries of origin did not have this problem, whichhas led to suspicion that increased skin pigmentationmay predispose dark-skinned patients to havevitamin D deficiency in certain geographic loca-tions.91 Because POC, especially those of darkerskin, 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 demonstratingdecreased serum vitamin D levels in patients withphotosensitivity practicing rigorous photoprotec-tion,93-95 regular use of sunscreens did not result ininadequate 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 allraces ranges from 52-63 y

Skin: Dark macules orpatches with history ofrapid spreading

Nail: Pigmented band[3mm on the nail

Oral mucosa: Oralmelanomas can rise fromlesions of oral melanosis

Tinea nigra palmaris, talonnoir, pigmented BCC

Commonly in lowerextremities and plantarfeet

UV radiation NOT a major riskfactor

Risk factors for melanoma inPOC unknown

BCC Most prevalent skin cancer inHispanics14; second mostcommon in blacks (inwhom SCC is the mostcommon)4,5

Typical: Asymptomaticsolitary translucentnodules with pearlyborders, rolled borders,and telangiectasia14

POC: Pigmentation in overhalf of cases; brown/blackpapules can also presentas nodules, plaques, andulcers4,16,18

Seborrheic keratosis, bluenevus, trauma, lupuserythematosus, nevussebaceous, sarcoidosis,and melanoma5,18

Head and neck mostcommon in both whitesand POC15,19

Family history of skin cancer,Fitzpatrick skin type I, andthe presence of actinickeratoses, solar lentigines,leukoderma, and elastosisrhomboidalis nuchae, UVradiation

SCC Most common skin cancer inblacks and Asian Indians;second most common inHispanics, East Asians, andwhites (second to BCC); inblacks: peak incidence inforties

Range between well-demarcated scaling pinkplaques; firm, superficial,well-demarcated papules/nodules emerging fromround, indurated elevatedbase; granulomatous orverrucous lesions; andnonhealing ulcers

Lesions can behypopigmented orhyperpigmented

Actinic keratosis, nummulareczema, inflamedseborrheic keratosis,verruca vulgaris

Typically on the face in whiteskin; in POC, notuncommon in areas nottypically exposed to thesun, including lowerextremities and anus

Lower limb/scalp SCC:Chronic scarring andinflammatory processesincluding hydradenitissuppurativa, lupuserythematosus, chemical/thermal burns, chronic skinulcers, chronic trauma sitesof previous radiation;immunocompromisedpatients also at risk

Head/neck SCC: UV radiationBowen disease Black women affected twice

as often as black menScaly hyperkeratoticpigmented plaquesresembling seborrheickeratoses

Seborrheic keratoses,pigmented BCC, superficialBCC, malignant melanoma,or nonspecific pigmentedhyperkeratotic lesions

Areas not typically exposedto the sun: including groinand extremities

See SCC

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

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noted that most of the vitamin D photoprotectionstudies were done in predominantly white popula-tion, raising a question to their applicability to thebroader population. A guideline to follow would beInstitute of Medicine recommendations of 400 IU ofvitamin D daily for infants up to 1 year old, 600 IU forindividuals between 1 and 70 years old, and 800 IUfor those older than 70 years.98 The NationalInstitutes of Health provided a listing of food sourcesof vitamin D, including but not limited to cod liveroil, salmon, tuna, swordfish, and vitamin Defortifieddairy products.99

THE SPF AND RECOMMENDATIONS FORCLINICAL PRACTICE

A recent survey performed by Pourciau et al100

demonstrated a general belief among leaders inphotodermatology that photoprotection counselingis warranted in POC. Still, there is a general lack ofstrong data supporting recommendations on SPFrequirements for specific skin phototypes. It isknown that a given sunscreen may demonstratedifferent SPF value in varying skin colors, as demon-strated by Damian et al101 (Sydney, Australia) in1999. Using a xenon arc lamp with an emissionspectrum simulating the UVA and UVB wavelengthsof natural sunlight, the investigators found testing asunscreen product in fair-skinned individuals (whohad low MED) yielded higher SPF values comparedwith testing the same product in dark-skinned sub-jects (with higher MEDs). Because commercialtesting of SPF is mandated to be done in fair-skinned individuals,102 SPF values of sunscreens ondark skin therefore may be lower that the SPF valuesstated in the label.101

Similar to the message on photoprotection for thegeneral population, POC should also be advised touse a daily broad-spectrum sunscreen of at least SPF30, and practice sun-protective behavior such asseeking shade and use of protective clothing, wide-brimmed hat, and sunglasses (Table I). Sunscreensshould be applied liberally and reapplied every 2hours while outdoors. Furthermore, patients shouldbe advised to avoid tanning salons and intentionaltanning with natural sunlight. A thorough skinexamination, including examination of nails, oralcavity, gums, palms, soles, groin, and perianal areashould be performed regularly by a dermatologist;for those older than 50 years, yearly examination isappropriate. Pigmented lesions on gums and streaksin nails are normal in POC, but should be monitoredregularly for changes as malignant transformationcan occur. For patients with history of skin NMSC ormelanoma, or multiple nevi, monthly self-skin ex-amination is appropriate. Primary care physicians

should be educated on high-risk sites for MM, such aspalms and soles (Tables II and III). Efforts are neededto take the diversity in culture, beliefs, and languageacross ethnicities into account so that photoprotec-tion education can reach the target population ofcolor.

Wendy E. Roberts, MD, serves as a consultant forAllergan Medical, L’Oreal, La Roche-Posay, and NeoStrata,for which she receives honoraria. She also sits on theadvisory board and consults for SkinMedica, for which shereceives honoraria. She receives stock options fromTopMD. She consults for Theraplex, for which she receivesno compensation.

In 2013, Susan Taylor, MD, held seats on theadvisory boards of Allergan, Beiersdorf, Inc, ExcaliardPharmaceuticals, and Unilever, for which she receiveshonoraria. She serves as a consultant for Curel Skincare,Pfizer, Schlesinger Associates, and Viviscal. Dr Taylorfounded T2 Skincare for which she receives otherfinancial benefit and serves in other roles. She receivesgrants as an investigator for Hisamitsu Pharmaceutical,Medicis Pharmaceuticals, Noven Pharmaceuticals, andPfizer. Dr Taylor has received honoraria as a speakerfrom Allergan, Johnson & Johnson, Kao USA, MerzPharmaceuticals, and Neostrata.

2012 found Dr Taylor serving as a consultantfor Schlesinger Associates and Pfizer for which shereceived honoraria. She sat on the advisory board forAllergan, Beiersdorf and Excaliard Pharmaceuticals, forwhich she received honoraria. Dr Taylor founded T2Skincare for which she received other financial benefitand served in other roles. She is an investigator forPfizer, Medicis, Noven, and Hisamitsu, for which shereceives honoraria. She contracted for Medscape/WebMD for which she received honoraria. She servedas a speaker for Merz Pharmaceuticals and Allergan forwhich she received honoraria. She receives no compen-sation for her role at the Philadelphia Life SciencesInstitute.

In 2011, Dr Taylor was awarded grants as aninvestigator for Medicis and Noven Pharmaceuticals.She received honoraria for speaking from Elsevier andJohnson & Johnson. Dr Taylor sat on the advisory boardfor Merz Pharmaceuticals and Beiersdorf and receivedhonoraria for her support. She served as a consultantand received a consulting fee from Tria Beauty andJohnson & Johnson Dr. Taylor has received honoraria asresearcher from Johnson & Johnson and Beiersdorf.

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

Roopal V. Kundu, MD, had no relevant conflict ofinterest to disclose. Her department receives compensa-tion for pharmaceutical sponsored research that does notbenefit 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 norelevant conflicts of interest to disclose.

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