Racial and Ethnic Healthcare Disparities in Skin Cancer in the United States: A Review of Existing Inequities, Contributing Factors, and Potential Solutions

Abstract

Objective

Racial and ethnic health disparities affect the diagnosis and management of melanoma and nonmelanoma skin cancers, leading to deleterious outcomes. Non-Hispanic White patients make up the majority of skin cancers cases, yet racial and ethnic minorities have poorer prognoses and outcomes. The skin cancer literature is fragmented with regards to potential contributors to these healthcare disparities. In this article, we provide a comprehensive review of the skin cancer literature to briefly quantify racial and ethnic inequities, highlight contributing factors, and propose practical changes that can be made.

Methods

A PubMed search was completed to identify articles related to racial and ethnic health care disparities in the context of melanoma, basal cell carcinoma, squamous cell carcinoma, Merkel cell carcinoma, and dermatofibrosarcoma protuberans.

Results

Relative to non-Hispanic White patients, patients of racial and ethnic minorities have differing clinical presentations of skin cancers and genetic risk factors. Insurance, access to specialty care, cultural beliefs, and available educational resources further contribute to racial and ethnic disparities.

Limitations

We are limited to the level of detail provided in the existing literature, and at some times are unable to distinguish race of Hispanic populations. We also acknowledge that there are different nationalities grouped under these broad labels as well as multi-racial populations that may not be accounted for.

Conclusion

Awareness of and familiarization with innate factors and potentially more modifiable contributors can help inform efforts to close the observed gap in racial and ethnic inequities.

Racial and ethnic disparities affect healthcare outcomes in dermatology across a range of skin conditions including skin cancer.1-3 Melanoma and non-melanoma skin cancers (NMSC), while more common in non-Hispanic White populations, present with later stage disease and worse prognoses and outcomes in racial and ethnic minorities.4 The etiology of this gap is complex and multi-factorial, and the literature remains fragmented on the subject.

In this article, we aim to provide a comprehensive review of the skin cancer literature to briefly quantify racial and ethnic inequities, then highlight contributing factors and propose practical changes that can be made. For the purposes of this review, we consider patients of a racial minority to be any non-White/non-Caucasian patient, which we further categorize into Black, Asian, and Native Americans/Alaskan Natives. We consider Hispanic patients to be part of an ethnic minority. As this is a review of the existing literature, at times we may be unable to distinguish between White Hispanic or non-White Hispanic populations. Additionally, we recognize that there are different nationalities grouped under these broad labels. We also acknowledge that multi-racial populations are becoming increasing common, yet much of the literature we review may not account for that.

EPIDEMIOLOGY OF SKIN CANCER DISPARITIES

The incidence of newly-diagnosed melanomas in the United States is higher in non-Hispanic White patients (26 per 100,000 individuals) compared to Native Americans/Alaskan Natives (7.4), Hispanics (4.6), Asians (1.3), and non-Hispanic Blacks (1.0).5 Yet, non-White patients comprise a higher proportion of more severe disease.6-8 Compared to White patients, Black patients are more likely to present with late-stage melanomas that are deeper and have higher incidences of regionally advanced or distant disease.9,10 The percent of melanoma cases initially diagnosed at Stage III/IV was twice as high for Black and Native American patients compared to White patients.9, 11-14 Asian American and Pacific Islander individuals were also found to have worse Breslow depth, more lymph node involvement, and higher stage at diagnosis.15 Even when diagnosed at the same stage, Hispanic, Native American, Asian, and Black patients have greater the risk of mortality than White patients.13,15,16,17 Despite changes to screening guidelines and advancements in immunotherapy, this discrepancy significantly worsened from before 2000 to 2010 and beyond.18

Reliable incidence data on basal cell carcinoma (BCC) and cutaneous squamous cell carcinoma (SCC) is limited as registry data does not exist for either cancers, but BCC is the most common skin cancer for every race and ethnicity.19,20 Additionally outcome measures for BCCs in skin of color patients is poorly documented, likely due to the slow growth and low rates of metastases for BCCs in general.21,22 A single-institution review of both BCCs and SCCs did find that preoperative lesion size did not differ among White, Hispanic, or Asian patients.23 Despite no initial size difference, Hispanic and Black patients tend to develop SCC tumors in anatomic locations associated with more advanced disease at initial presentation, including the penis, perianal region, and lower legs.24-28 SCCs that develop in chronic inflammation or scars have higher rates of metastasis and these account for 20-40% of SCCs that develop in Black patients.29,30 Overall SCC-specific mortalities for Black and Hispanic men are worse than that of White men.26,31

In addition to BCCs and SCCs, other less common NMSCs include Merkel cell carcinomas and dermatofibrosarcoma protuberans (DFSP). The overwhelming majority of Merkel cell carcinomas occur in White patients with all non-White patients making up only 3.5 percent of cases.32 Yet, Black race was independently associated with advanced-stage disease at the time of initial diagnosis, and non-Hispanic Blacks had the lowest survival rates.32,33 The incidence of primary DFSP among Black patients is twice that of White patients, with limited data on other races and ethnicities.34-36 Black patients with DFSP were at a 1.7 times higher risk for all-cause death compared to White patients. This was partially attributed to increased tumor size as Black patients were 1.8-fold more likely to present with large tumors.34,35

While differing clinical presentations of skin cancers is one facet of the racial and ethnic disparities aforementioned, other factors such as access to care, insurance inequities, patient perceptions, and physician training all contribute to the observed disparities as well.3 Given previous literature provides scattered data regarding possible etiologies of these inequities and actional steps to address them, we intend for this article to provide a comprehensive overview of the various levels of inequity that contribute to racial and ethnic gaps in skin cancer morbidity and mortality. These factors can serve as potential targets for change in research, trainee recruitment, access to care, and public education campaigns.

CONTRIBUTING FACTORS

Early detection and extirpation of cancerous lesions generally reduces associated morbidity and mortality.37 The shortcomings in timely diagnoses, time to definitive treatment, and prognoses that disproportionately negatively impact racial and ethnic minorities can be explained by both intrinsic (e.g., genetics) and extrinsic factors. Increased awareness of external contributors highlights potential focus areas for improvement and intervention.

Clinical presentations of skin cancers. One recognized cause for delayed diagnosis of skin cancers in skin of color patients is the unique and dissimilar clinical presentations as compared to those in Caucasians. Fifty percent of BCCs in skin of color patients present with pigmentation, which may mask the “translucent” characteristic of BCCs and potentially make arborizing telangiectasias less obvious.6,23,24,28 SCCs have a wide range of clinical presentations in skin of color patients and more often occur in non-sun exposed areas, like the anogenital region that may be missed on skin exams more commonly.6,11,22,38

Similar to SCCs, melanomas in skin of color patients have a predilection for sun-protected areas with an increased frequency in acral and mucosal sites, when compared to non-Hispanic White patients.11,39,40 In the Native American and Alaskan Native populations, acral lentiginous melanomas occur 4.1 times more often than in non-Hispanic White populations.41 Acral lentiginous melanomas are more often missed on examination and are an independent predictor of poor survival.42,43 Additionally, mucosal and acral lentiginous melanomas are more difficult to treat surgically and with immunotherapy, potentially prolonging planning time and lowering success rates.44

Merkel cell carcinoma is rare amongst non-Hispanic White populations, and there is minimal literature comparing how clinical presentations may differ by race. One case report in a Black male described a Merkel cell carcinoma masquerading as an epidermoid cyst.45 A Merkel cell carcinoma in association with Bowen’s disease was reported in a Japanese woman.46

For DFSPs, the pigmented variant occurs primarily in Black patients. They can be mistaken for keloids, which can make them difficult to diagnosis as keloids themselves commonly occurs in skin of color patients.6,47

Educational material and knowledge gap. Few resources provide images of lesions on darker pigmented skin, despite differences in clinical presentations.48,49 Having access to clinical images of skin cancers in patients of higher Fitzpatrick skin types improves diagnostic confidence.50 Much of the learned pattern recognition and exposure needed for accurate clinical diagnoses occurs during residency training. Yet, more than 30 percent of chief residents and program directors denied having didactic sessions that focused on skin of color and only about a quarter of programs reported having lectures on skin of color from an acknowledged expert.51 Geographic region and degree of local diversity may affect whether residents feel their curriculum sufficiently exposes and educates them on patients with skin of color. A recent small study did find that the percent of residents who felt that they treated a patient population diverse in skin types ranged from 50 to 87.5% which is an improvement from prior studies.52 Therefore, graduates of some residency programs may actually feel more comfortable both recognizing and treating skin cancers in patients of racial and ethnic minorities compared to other residents of other programs.

Research is the catalyst for evolving medical knowledge and clinician education. While diversity within United States clinical trials for psoriasis, acne, and eczema has grown, Black patients remain underrepresented in cancer drug trials.53,54 For instance, in the CheckMate-067 Phase 3 trial (nivolumab plus ipilimumab versus ipilimumab alone), no participants were Black, <1.1 percent were of Asian descent, and 0.1 percent were Native American/Alaskan Native.55 No literature has been published analyzing the barriers to recruiting underserved populations to dermatologic-specific research.56 Reported barriers to medical research in general include mistrust of the medical community, geographic impediments, culturally incompetent designs, lack of time, and low socioeconomic status.56

Patient education. Many people of color believe they are invulnerable to skin cancer.57 They are less likely to perform self-examinations, especially in sun-protected areas.1, 58-60 Hispanic patients are also less likely to visit a physician for a total body skin exam, and Blacks and Hispanics have a reduced likelihood to seek medical evaluation for suspicious skin lesions.61 Black and Hispanic patients practice less sun safety habits, citing limited discussions on sun safety and minimal sunburn history.62 Sociocultural values towards skin color also affect sun-protective behaviors. Black and Hispanic patients were less likely to believe that lifestyle could affect their skin cancer risk.3 Meanwhile, Chinese women who grew up in China preferred lighter skin and avoided sun-seeking behaviors versus those raised by Euro-American culture.63 Linguistic acculturation and community-level barriers may also play a role. Being of Hispanic ethnicity increases the probability of living in a neighborhood with a higher incidence of late-stage melanomas.64 One reason for this may be that compared with English-acculturated Hispanics, Spanish-acculturated Hispanics had lower levels of perceived skin cancer risk.65

Patient education may be improved through provider education and counseling. Although minority patients are responsive to education regarding skin examinations, they are less likely to be counseled by providers to do so.66-67 Additionally, previous public awareness campaigns have not focused on educating all skin types. Most campaigns emphasize that sunlight is a significant factor in skin cancer pathogenesis, but are less likely to highlight that skin cancers can still occur in areas shielded from the sun, which is even more common in skin of color.68

Cultural competency and workforce diversity. Skin of color patients prefer racial concordance in their dermatology provider, but dermatology remains one of the least diverse specialties. More than 13 percent of Americans are Black, but Black dermatologists comprise of only 3 percent of all dermatologists. Similarly, 4.2 percent of dermatologists are Hispanic or Latinx, but make up more than 18 percent of the general U.S. population.69-72 These numbers were only marginally better for dermatology residents, though still underwhelming. For instance, only 0.2 percent of dermatology residents in 2014 were Native American/Alaskan Native.73 A recent study found that despite underrepresented minorities pursing research fellowship more often, publishing more, and completing the same number of away rotations and interviews they have lower match rates than their White counterparts.74 This matters as Black and Hispanic physicians more often practice were there are higher percentages of Black and Hispanic residents, respectively.75 Even after accounting for the racial and ethnic makeup of a community, Black and Hispanic physicians treated significantly higher proportions of Black and Hispanic patients, respectively. Overall, non-White physicians cared for over 50 percent of racial and ethnic minority patients.76

The genitalia, the perianal area, and the ocular and oral mucosa were the least frequently inspected anatomic sites on skin exams, even in a high-risk skin cancer clinic.77,78 On surveys, skin of color patients more often reported that White dermatologists inadvertently avoided physical contact and performed cursory examinations. This has been interpreted by patients to be both a risk factor for missed diagnoses and a sign of disrespect and racial insensitivity.69,79 Cultural sensitivity and shared life experiences largely influence why patients of color rate more positive experiences with dermatologists of color.69 For example, use of complementary and alternative medicine is prevalent in Native American and Alaskan Native populations. Resistance to understanding or immediately discussing non-Western medicine therapies can create a wedge in physician-patient relationships and potentially reducing the quality of care.80 Race-discordance between the doctor and patient may further exacerbate miscommunications and overlook sociocultural influences.67,79

Access to dermatologists. Patients of a racial or ethnic minority are less likely to see a dermatologist, which carries downstream effects.1, 81-83 Barriers to care can lengthen the time to accurate diagnosis and appropriate management, such that patients of a non-White race/ethnicity have a longer time to definitive surgical treatment.84 Insurance type, poverty level, concentration of specialists, and hours of operation all contribute to restricted patient access.64,85 Racial and ethnic minority patients with melanoma are more likely to have Medicaid or no insurance. Medicaid patients seeking dermatologic care have lower new patient acceptance rates and longer wait times.86 Compared to those with private insurance, patients with Medicaid have more than three times the odds of being diagnosed with a late-stage melanoma.87 Having Medicaid also increases delays for definitive surgical treatment for melanoma.88 Lack of medical insurance was associated with advanced-stage Merkel cell carcinoma at the time of diagnosis.32 Similarly, no insurance or Medicaid insurance predicted mortality in patients with DFSP.35 Native Americans/Alaskan Natives have even greater access limitations. The Indian Health Service (IHS) provides medical care to federally recognized tribes and overall has improved access of care. However, IHS remains underfunded and has reduced access to specialty care.89

Dermatologists and Mohs micrographic surgeons are geographically maldistributed, with most practicing in or near well-resourced communities and academic centers.90-92 Studies showed that living near a greater density of dermatologists was associated with better outcomes for both melanoma and Merkel cell carcinoma.32,93,94 While people of color tend to live in urban areas, barriers to access may inequitably restrict specialty care.10,95 One study reported that zip codes with higher percentages of Black residents had an average of 1.02 dermatologists (1 per 39,367.50 people) compared to zip codes with a low percentage of Black residents which averaged 2.94 dermatologists (1 per 13,999.88 people).96 Another study reported that despite hospital proximity, Black patients were more likely to get treated at lower quality hospitals with less variety in payor type.67 Additionally, compared to non-Hispanic White patients, Black and Hispanic patients were more likely to use the emergency department for dermatologic care.97

Risk factors. The medical community recognizes that increased exposure to sunlight generally worsens the risk for skin cancer. This includes people who work outdoors for a living due to prolonged exposure to the sun.98 Yet construction workers with darker skin types were found to use less sun protective behaviors.99 Japanese patients living in Hawaii have a greater incidence of NMSC compared to Japanese patients in Japan, which is felt to be secondary to the higher intensity of UV radiation and an enlarged participation in outdoor activities.100 This supports the importance of sun protection even for skin of color patients.

Despite this, UV exposure from sunlight may not be the prevailing risk factor for the majority of skin of color patients, as evidenced by the fact they have a heightened risk of skin cancers occurring in sun-protected areas. For these patients, a multitude of other risk factors may play a role. For example, human immunodeficiency virus (HIV) disproportionately affects Black patients in the United States, and immunosuppression from HIV is associated with an increased risk of melanoma.101,102 Risk factors for SCC in skin of color patients include human papilloma virus (HPV), ulcers, chronic scarring, inflammatory processes (e.g., lupus erythematosus).25,30,103-107

Innate factors like genetics may also contribute to differing presentations and outcomes. Acral and mucosal melanomas more often have KIT mutations and less often have BRAF mutations compared to melanoma on sun-damaged skin.108-110 Melanomas in Black patients were found to have a high Ki-67 expression (a marker of tumor proliferation), low-level of p53 staining (a cell cycle regulator), and high microvessel density (a marker of angiogenesis), suggesting a different biologic basis and behavior, which may contribute to differing presentations and outcomes.1,1,1 One study did find that when insurance was controlled for, acral melanoma prognosis was based on stage at time of presentation, irrespective of race.112 This suggests that at least for acral melanoma race-specific genetics is not the sole contributing factor.

SUGGESTIONS FOR IMPROVEMENT

Given the racial/ethnic differences in skin cancer outcomes and the various amendable contributors, opportunities exist to intervene and reduce the current disparities. Some blueprints for reducing racial disparities in skin cancer have been suggested. Increasing diversity in the dermatology workforce is key. Having dermatologists of color may improve cultural competency and patient-doctor relationships. It may also encourage more diversity in clinical research, which leads to improved provider education on patients with skin of color.

Efforts to increase the representation of minorities in dermatology residencies have been the focus of the American Academy of Dermatology (AAD). Action items include increasing exposure to dermatology to medical students who are under-represented in medicine such as with formal mentorship programs and interest groups.113-114 Reconfiguring selection criteria to remove systemic bias against racial minorities have also been discussed by the AAD’s Diversity Task Force.115 Underrepresent minorities are more likely to take out loans when applying for dermatology residency.74 Alleviating financial constraints by offering stipends for underrepresented minority students on dermatology away rotations, waiving resident application fees, and offering video interviews to relieve travel costs have been proposed as well.115 In the COVID-19 era, unique challenges, such as lack of externships, and how that affects unrepresented minority applicants will need to be considered.116 Not only should recruitment efforts focus on increasing diversity at the level of students and residents, but we also need to consider increasing diversity at higher levels of faculty rank. At every rank, there was a lower number of underrepresented in medicine minority faculty with department chairs being the least diverse.117 More than 50 percent of underrepresented minority students identified lack of support as a barrier, and reported they were encouraged to seek other specialties more reflective of their community.118 The more diverse faculty and higher-ranking faculty that are represented, the greater opportunities there are for mentorship and inspiring medical students and residents of racial and ethnic minorities to apply.

The training received during residency is inherent to dermatologist education and competency level. Ensuring adequate exposure to skin of color patients and adding focused lectures to the curriculum during residency is especially valuable. When dermatologic conditions are shown using images of skin of color, diagnostic accuracy improves.119 Externships to areas that target underserved minorities may be options for further broadening exposure. Additionally, the Skin of Color Society has multiple opportunities for residents to find mentorship and apply for grants that can support research fellowships and projects aimed at improving awareness of skin of color dermatology.120 These more in-depth experiences should not replace incorporating images of all skin types during one’s standard residency teaching. Education objectives need to not only enhance trainee’s recognition of pathologies in all skin types, but also improve cultural competency. Integrating didactics that address cultural disconnects and provide tools to approach culturally sensitive encounters may also improve the cultural competency of dermatology’s incoming workforce.

Patient educational interventions have been shown to improve sun protective behaviors and utilization of skin examinations in skin of color patients, especially when culturally relevant campaigns are employed.66,121 In a study instructing patients on how to identify abnormal skin lesions, participants’ performance of self-skin checks, including of acral and periungual skin, improved and was sustained months later.122 Video-based interventions that include Spanish versions have been successfully used to increase skin cancer awareness among Hispanic populations.123,124 Involving primary care physicians and community organizations, such as churches, may further improve awareness and early detection.125,126 Community-based participatory research is especially important for American Indian/Alaskan Native patients as each tribe is a sovereign nation with unique priorities, laws, and histories.127 What works for one community may not work for another.

Extending and improving access is a vital though more complex undertaking. Increasing trainee diversity may itself expand access, as minority physicians are more likely to provide race-concordant care and practice in underserved areas.95 Incentives to attract dermatologists to practice in high-minority areas, such as loan forgiveness, have been proposed.95 Additionally, dermatologists with higher proportions of minority race/ethnicity patients have lower Merit-Based Incentive Payment System scores, determined by various performance metrics.128 Therefore, adjusting reimbursements models to account for socioeconomic dynamics may encourage dermatologists to treat more underserved patients. Dermatologists may also participate in programs that subsidize or provide free healthcare to underserved populations. Many of these “outreach” programs have had success, but are limited in their examples.129 Ethnic skin centers are another way to not only increase access, but also to educate residents on skin of color. Over the past 20 years, 15 academic ethnic skin centers have been established.120 In cities where a higher percentage of the population are persons of color, ethnic skin centers offer expertise and care through high-volume clinics. The AAD has a grant-sponsored Native American Health Service Resident Rotation program that takes place at the HIS. Residents provide dermatologic care to the Navajo Nation population, helping to increase access and potential foster sustained interest in providing care in areas of need.130 Teledermatology is an appealing option, especially after its recent growth in utilization during the COVID-19 pandemic. Telemedicine can reach a higher proportion of underserved patient population with lower no-show rates and quicker definitive management than even conventional referrals.131,132 However, studies in telemedicine’s use in improving ethnic minority access are limited.133 Additionally, private insurance companies, Medicaid, and Medicare currently restrict coverage of telemedicine and its use. Working to push legislation that expands reimbursement would increase teledermatology’s appeal.134

CONCLUSION

Later stages at time of diagnosis, delayed time to treatment, and unfavorable outcomes in skin of color patients provide evidential support for calls to action focused on reducing racial and ethnic disparities in skin cancer. Genetics and differing clinical presentations do not simply account for the totality of these disparaging statistics. Modifiable factors such as environmental exposures, socioeconomics, and barriers to access are important though less straightforward targets for change. Improving clinician education and cultural competency, increasing workforce diversity within our specialty, and improving patient perception of skin cancer risk while integrating multicultural approaches to future skin cancer campaigns should be considered and potentially pursued. Hopefully increased awareness and recognition of these various contributors to the observed racial and ethnic disparities will enhance dermatologists’ growing efforts to reduce these healthcare inequities.