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Abstract

Breast cancer is the leading cause of cancer death for women worldwide. While breast cancer incidence is lower for many ethnic minority women than for white women, stage at diagnosis and survival are often worse. These disparities are most marked for African–American women, but are also present for Asians, Latinas, Native Americans and Hawaiians. The etiology of ethnic disparities in breast cancer is multifactorial, including differences in tumor characteristics, genetics, access to care and insurance, prevalence of risk factors, screening participation and processes of care, such as timeliness of diagnosis and quality of communication and treatment. This review will examine what is known regarding ethnic differences in all of these areas, what questions remain, and where researchers and policy makers should focus their future efforts.

Keywords

breast cancer ethnicity health disparities review

Worldwide, breast cancer is the leading cause of cancer death for women [1]. The American Cancer Society estimates that there will be 178,480 new cases of female invasive breast cancer and 70,880 female deaths from breast cancer in the USA this year [2]. While white women have the highest incidence of breast cancer, African–Americans have the highest rate of breast cancer death, and Latinas have a disproportionately high rate of breast cancer death for their incidence [2].

Incidence, mortality & stage

Racial/ethnic disparity in breast cancer incidence and mortality has been shown in multiple studies. A prospective study of 156,570 postmenopausal participants in the Women's Health Initiative found that while age-adjusted incidence for all ethnic minority groups is lower than for white women, most of this difference could be accounted for by differences in prevalence of breast cancer risk factors among these groups, except among African–American women. African–Americans, Native–Americans, Hawaiians and Latinas are all at greater risk of death after a breast cancer diagnosis compared with white women, partly because of a greater proportion of advanced-stage disease in nonwhite women compared with white women [3]. A large, retrospective cohort study that examined population-based tumor registry data from 11 registries, and included significant numbers of multiple ethnic minority groups – including African–Americans, Latinas from diverse parts of Latin America, Hawaiians, Native Americans and South Asians – found that nonwhites are more likely than whites to present with advanced (stage IV) disease [3]. In the Women's Health Initiative study, African–American women had both a higher rate of unfavorable tumor characteristics (such as high grade, estrogen-receptor-negative tumors) and a higher rate of breast cancer mortality than white women [4]. In addition, recent analysis of the National Cancer Institutes Surveillance, Epidemiology and End Results (SEER) database, shows that adjustment for within-stage differences in tumor size and lymph node status did not reduce the disparity in mortality between African–American and white women [5]. Recent reports show an overall 7% decrease in invasive cancer between 2002 and 2004 [6,7], which is thought to be partly due to the decline in use of postmenopausal hormone therapy [8]. Incidence rates for African-American women have decreased to a lesser extent than among white women (2.7 vs 6.4%), possibly because African–American women are much less likely to initiate postmenopausal hormone therapy [4].

While data for increased mortality appear to be strong and most consistent for African–Americans [2 –4,9 –11], there are considerable data to show that other ethnic minorities are often diagnosed with advanced-stage disease, putting them at risk for poor breast cancer outcomes. Latinas, while having a lower overall incidence of breast cancer, are more likely to be diagnosed with advanced disease than non-Latina whites [12 –14]. A greater proportion of Latinas who are born outside the USA are diagnosed with advanced-stage disease than for US-born Latinas, which may be due to differences in mammography utilization [15]. Small studies have shown that South Asian women in the USA are diagnosed with more advanced stages than white women [16], that Asian-born Chinese women in the USA have lower rates of breast cancer survival than US-born Chinese women [17] and that West-African-born women in the UK have lower rates of breast cancer survival than UK-born women [18]. Many factors may influence breast cancer diagnosis and advanced stage of diagnosis and decreased survival for nonwhite ethnic minority women, including tumor characteristics, genetics, prevalence of risk factors, access to care and insurance, screening participation, processes of care and communication and treatment. In the remainder of this paper, we will review the existing data in each of these areas.

Tumor characteristics

Differences in breast tumor characteristics lend biological plausibility to the observed heterogeneity of disease presentation and outcome across racial/ethnic groups of women. In addition, tumor characteristics and their impact on prognosis, particularly the absence or presence of particular biomarkers (estrogen receptor [ER], progestin receptor [PR] and HER2neu), have become increasingly important in assisting clinicians to make treatment recommendations [19 –21]. In a case–control study, Carey et al. found premenopausal African–American women to have the highest prevalence of the worst-prognosis tumors compared with postmenopausal African–American women and non-African–American women (39 vs 14 vs 16%, respectively) [22]. The worse-prognosis tumors were defined as basal-like breast cancer subtypes (ER^–, PR^–, HER2^–, cytokeratin 5/6⁺ and/or HER1⁺). Premenopausal African–American women also had the lowest prevalence of the best-prognosis tumors, defined as luminal A subtype (ER⁺ and/or PR⁺, HER2^–) [22]. Among participants in the Women's Health Initiative who developed breast cancer, African–Americans had approximately a fivefold greater chance than whites of having high-grade ER^– tumors [4]. In their 11-tumor registry cohort, Li et al. examined the prevalence of poor-prognosis receptor status tumors (ER^– and PR^–) among a broad range of ethnic groups, and found that African–Americans, Native Americans, multiple Asian groups (Filipinas, Chinese, Koreans, Vietnamese and South Asians) and Latinas from across Latin America all have increased risk of poor-prognosis tumors compared with non-Latina whites [23]. In a recent study of women within a large health-maintenance organization (thus, with equal access to care), Latinas were more likely to have poorly differentiated and ER^– tumors than non-Latina whites [14]. These observed differences in histology and tumor receptor status, as well as in phenotypic disease course (e.g., more advanced-stage tumors and higher mortality rates as described above), introduces the as yet not fully answered question of whether these differences are due to genetics or environmental factors, such as screening utilization, or both. We will explore these potential sources of difference in the remainder of this review.

Genetics

Across populations, younger age at diagnosis and having more first- and second-degree relatives with breast and ovarian cancer is associated with increased risk of carrying a BRCA1 or BRCA2 mutation [24]. In the general population, mutations in the BRCA genes only account for 5–10% of breast cancers [25]. BRCA1 and BRCA2 have the highest prevalence among Ashkenazi Jewish women, but are not limited to this population. Deleterious mutations have been identified in African–American, African, Latina, Chinese and white women without Ashkenazi Jewish heritage [24,26–29]. While heritable susceptibility not accounted for by BRCA genes likely plays a significant role in a large percentage of breast cancer cases, differences attributed to heritable susceptibility due to racial ancestry may be difficult to prove. Apparent differences in heritability can be confounded by differences in known breast cancer risk factors – such as parity, BMI and alcohol intake – which themselves may differ among cultural groups [30].

While, as outlined above, deleterious mutations exist across race/ethnic groups, any screening program for genetic susceptibility to breast cancer should be conscious of the need for culturally and linguistically appropriate patient recruitment and educational programs. Halbert et al. found that while knowledge regarding breast cancer genetics and testing availability is generally low among African–Americans, expectations for high benefit from testing are perhaps misguidedly high [31]. In addition, African–American women may be less willing to participate in BRCA testing [32] or in enrollment in a genetic registry [33]. This could, at least in part, be due to the legacy of the Tuskegee Syphilis Study conducted by the US government from 1932 to 1972, in which African–American men were denied effective treatment for syphilis in an effort to document the natural history of the disease [34]. Mistrust of medical research and testing in the African–American community because of this trial has since been well documented [35,36]. Although less well documented, genetic testing may also be perceived as threatening in immigrant communities, particularly in those with high proportions of undocumented immigrants, where fear of discrimination and even deportation has been shown to negatively impact access to timely healthcare [37,38]. Any efforts to screen for and study genetic susceptibility in these populations must be accompanied by culturally sensitive educational and counseling programs.

Risk factors

Traditional risk factors, such as early menarche, postmenopausal obesity and later initiation of childbearing confer increased risk across racial/ethnic groups. However, the prevalence of these risk factors varies across groups ( Table 1 ). For example, Chinese women are less likely to have a family history of breast cancer, be nulliparous and have a history of benign biopsy [39]. African–Americans, Latinas and Native Americans are more likely to have an early menarche, while white and Asian women are more likely to have late parity and to have ever used postmenopausal hormone therapy [4]. Parity appears to have a dual association for African–American women: high parity is associated with increased risk among younger women (<45 years) and decreased risk among older women [40]. Postmenopausal elevated BMI is prevalent across race/ethnic groups except for Asians [4,41]. For Latinas, obesity is associated with increased risk across the age spectrum, not just for postmenopausal women [42].

Table 1.

Differences in prevalence of traditional risk factors across racial/ethnic groups*.

	Family history (%)	Early menarche (%)	Late† or no parity (%)	History of benign biopsies (%)	PM high BMI (%)	Alcohol intake§ (%)	PMHT use¶ (%)
African–American	12	24	19	19	51	2	26
Asian/Pacific Islander	9–12	21	14–27	17	11	1	29–48
Latina	9	25	18	15	37	2	35
Native American	14	24	14	18	44	3	35
White	14–17	22	19–59	20	28	4	43–54

When estimates were available from multiple sources, a range of percentages is presented (data taken from [4,39]).

†

≥ age 30 years.

≥2 drinks/day.

Prior to 2003.

HT: Hormone therapy; PM: Postmenopausal.

One risk factor that has increasingly become a focus of research is breast density [43]. Women who have more dense breasts are more likely to have a family history of breast cancer, pointing to a potentially genetic contribution to breast cancer risk [44]. Acculturation within an ethnic group may be associated with differences in breast density [45], indicating that there are likely environmental factors influencing breast density as well. As with other risk factors, both genetic and environmental factors probably contribute to the impact of breast density on the development of breast cancer. It appears that breast density is a risk factor across ethnic groups [46,47].

Socioeconomic status

While incidence rates for breast cancer are highest among white women, the risk of developing breast cancer increases with increasing socioeconomic status (SES) such that more-affluent women in all race/ethnic groups have a higher risk than less-affluent women in those same groups [48]. The reasons for this association are not known, but may be mediated by variation in environmental exposures, diet and other risk factors such as breast density. However, when US women who are living in poverty do develop breast cancer, they are more likely to be diagnosed at an advanced stage, are less likely to be treated with breast-conserving surgery and radiation when they have early-stage disease, and are less likely to survive their disease than more affluent women [49]. Certainly, there is a higher proportion of ethnic minority and immigrant women than white women living in poverty in the USA. The impact of low SES on disparities in breast cancer presentation and outcomes is likely mediated by multiple other predictors, ranging from lifestyle risk factors such as parity and breast feeding and physical characteristics such as obesity, to tumor characteristics such as receptor status [50 –53]. Health insurance and adequate access to healthcare also play a role [54,55]. However, lower SES alone does not account for all differences in survival, particularly for African–American women [13,56,57]. In a study of African–American and white women treated in US military healthcare facilities – and thus with equal access to care – African–American women had a 40% higher hazard of breast cancer death than white women, even after adjusting for tumor stage and clinical variables [58]. The authors point out that this difference is smaller than that seen in national data, showing that equitable access to care can decrease disparities in breast cancer mortality; however, their findings are still significant and show that access alone cannot eliminate differences. In their pooled meta-analysis of 20 studies over 25 years, Newman et al. found that even after adjusting for age, stage and socioeconomic status, African–American women have an increased hazard of both overall mortality and of breast cancer-specific mortality compared with whites [57].

Screening participation

Historically, ethnic minority women in the USA are less likely than whites to undergo recommended mammography screening [49,59,60]. During the 1990s, screening rates improved for all groups, and this increased screening has been associated with diagnosis at earlier stages for all groups, although the positive impact appears to be less for African–Americans [61]. The sensitivity of mammography among Asian, Latina and African–American women is similar to white women, and the proportion of advanced-stage disease is similar among women undergoing regular screening mammography [39,62,63]. In other words, most of the differences in advanced-stage tumors among African–American and Latina women are ameliorated by regular screening [60]. However, regardless of screening history, African–American women have more high-grade tumors than white women. In an effort to improve screening rates for poor women, the Centers for Disease Control initiated a program in the early 1990s offering free mammography to qualifying women through the National Breast and Cervical Cancer Early Detection Program (NBCCEDP). The initiation of this program increased mammography screening rates overall, and in particular for Latinas and Asians, a higher proportion of whom had never had previous mammography [64]. However, screening rates continue to be lower overall for African–Americans eligible for the program [65], and for Latinas in general [66]. Other data from the 2003 National Health Interview Survey show that overall screening mammography rates have equalized for African–American and white women; however, while improved from previous years, screening rates still remain lower for Asians, Native Americans and Latinas [67]. Recent data from the Medical Expenditure Panel Survey similarly show Latina and Asian women to have lower screening rates than white women [68].

In addition to the NBCCEDP, there are other factors and interventions that appear to increase screening rates for ethnic minorities. Having health insurance, in particular public insurance, increases screening rates more for Latinas and African–American women than for whites [66]. Having regular medical care increases rates for all groups studied, including Latinas, African–American and Chinese women [69 –72]. As with other preventive behavior, a recommendation from a regular physician increases screening participation for Latinas and African–Americans [73,74]. In addition, because less acculturated Asian immigrants have lower rates of screening [75 –78], culturally and linguistically tailored interventions increase screening rates in those populations [79,80]. For African–Americans, a culturally tailored religious-based intervention is effective in increasing screening rates [81], but an individually tailored interactive computer intervention is more effective to increase screening participation than culturally tailored, passive messages [82]. The religious-based intervention is not effective for Latina participants [81].

Processes of care

Communication of abnormal mammography results

One outcome of screening participation is abnormal mammography results, due to both cancer and false positives, for all women [83]. Unfortunately, physicians do not always communicate adequately with patients regarding abnormal results, despite the fact that there is evidence that good communication of abnormal mammography results improves receipt of appropriate follow-up care [84,85]. In one study, Asian and Latina women reported receiving confusing or conflicting information regarding their mammography result more often than white women [86]; in another, Asian women were less likely than white women to understand that their mammography result was indeed abnormal [87]; and, in a third study, compared with white women, African–American women had twice the chance of not having been notified and not knowing their mammography result [88]. In these studies, the definition of adequate communication varied; however, collectively, it is broadly defined as timely verbal notification and consistent messages about results, as well as need, type and timing of follow-up tests and care. The reasons for this inadequate communication are unclear, but may include language barriers, low health literacy and low financial incentives and time resources on the part of the clinical provider. This documented poor communication may contribute to the observed longer delays in care, and subsequent worse outcomes, for ethnic minorities with breast cancer.

Delays in diagnosis & treatment

African–American, Asian and Latina women have all been shown to have longer delays than whites from screening mammography to diagnosis or resolution of abnormal mammography finding; this has been most robustly documented for African–Americans [89 –94]. In the UK, black and South Asian women have the longest diagnostic delays [95]. African–Americans, Native Americans and Latinas also all experience greater delays from diagnosis to treatment [91 –93,96,97]. For Latinas, language barriers appear to contribute to both diagnostic and treatment delays [89,96]. Other apparent contributors to delay include scheduling difficulties, physician inaction (e.g., not contacting patients, or not ordering follow-up tests) and patient lack of knowledge or understanding [98,99]. These differential delays in care, and the sometimes inadequate communication of abnormal results and need for follow-up, may in fact contribute substantially to differences in presentation in tumor size and stage, and perhaps even to mortality differences. Thus, improvement in the delivery of healthcare in the form of timely action and appropriate communication may improve breast cancer outcomes. One study of a successful intervention to increase timely follow-up of breast abnormalities using a care-management model and a patient navigator demonstrated that personalized interventions can decrease diagnostic delays [100].

Treatment disparities

Although less well studied, there appear to be concerning disparities in receipt of appropriate treatment for ethnic minorities. In two studies, African–American and Latina women were less likely than whites to undergo appropriate adjuvant therapy despite equal rates of referral to medical oncologists [101]. In another, African–Americans were less likely to undergo adjuvant or hormone therapy [102]. In a third study, African–Americans were 24% less likely than whites to undergo radiotherapy after breast-conserving surgery [103]. It has been hypothesized that lower white blood cell counts in African–Americans contribute to longer duration of lower-dose treatment [104]; however, it is unclear whether this is a causal relationship, and it cannot explain all of the inadequate treatment outlined above.

It is difficult to determine from these studies whether patients are being offered treatment and refusing or not being offered the same types of treatments across racial/ethnic groups for similar stages of disease. Although knowledge regarding treatment-specific prognosis appears to be low for all women (48% of women with DCIS or stage I breast cancer knew that mastectomy and lumpectomy with radiation had the same 5-year survival), it may be even lower for African–American women (24%) than for white women (52%) [105]. This type of difference may be impacted by education, health literacy and the clinician' ability to communicate well with patients from many different sociocultural groups regarding treatment choices. One study of audiotaped conversations between oncologists and newly diagnosed breast cancer patients found that physicians gave more medical information to younger, well-educated and white patients than to older, less educated or nonwhite patients [106]. In addition, physicians engaged in more relationship building with white patients than with nonwhite patients. These somewhat subtle differences in communication could have a substantive impact on treatment decisions and outcomes.

Future perspective

Disparities exist for ethnic minorities for both the type of breast cancer and across the care spectrum. This has been studied best and is most marked for African–American women; however, particularly in the areas of disease stage, tumor characteristics and processes of care, there are considerable data to suggest differences for other ethnic minorities in the USA. The root causes for these disparities appear to be multifactorial, ranging from biologic to environmental to healthcare processes. Thus, solutions will need to be multifaceted.

Executive summary

Incidence, mortality & stage

African–Americans have a lower incidence of breast cancer than whites, but the highest breast cancer mortality of all ethnic groups.

Ethnic minorities, particularly African–Americans and Latinas, are more likely than whites to be diagnosed at younger ages and present with advanced-stage disease.

Immigrant women – Chinese, South Asian and Latina – tend to present at advanced stages and have poorer outcomes than their US-born counterparts.

Tumor characteristics

Among women with breast cancer, African–Americans, Asians and Latinas have all been shown to have a higher prevalence of estrogen-receptor-negative tumors than whites.

Premenopausal African–American women have a higher prevalence of basal-type tumors, which have poor survival prognosis.

Genetics

Deleterious mutations in the BRCA1 and BRCA2 genes have been found in many different ethnic populations, including Africans, African–Americans, Asians, Latinas and whites.

Differences in breast cancer incidence and outcomes attributed to heritable susceptibility due to racial ancestry may be confounded by differences in known breast cancer risk factors that often differ among cultural groups.

Risk factors

White, Asian, African and Latina women differ in their prevalence of breast cancer risk factors.

Breast density has emerged as a significant risk factor for breast cancer; higher breast density is associated with higher risk.

Breast density appears to be a risk factor across ethnic populations.

Socioeconomic status

Across ethnic groups, higher socioeconomic status is associated with a higher incidence of breast cancer.

Living in poverty is associated with advanced stage at diagnosis and higher breast cancer mortality.

Adjustment for socioeconomic status does not account for all of the differences among ethnic groups in breast cancer survival, particularly for African–Americans.

Screening participation

African–American, Asian and Latina women all historically have slightly lower rates of mammography screening than whites in the USA. Differences across groups are primarily in the frequency of screening.

National programs aimed at low-income uninsured women have increased screening rates, particularly for Latinas and Asians.

Having health insurance, regular medical care, a recommendation for screening from a physician, and culturally and individually tailored interactive interventions all increase participation in mammography screening for ethnic minority women.

Processes of care

Ethnic minorities appear to experience inadequate communication with their clinicians when they have abnormal mammography results requiring evaluation.

African–American, Asian and Latina women have all been shown to have longer delays than whites from screening mammography to diagnosis or resolution of abnormal mammography findings.

A care-management model with patient navigators has been shown to decrease diagnostic delays.

Treatment disparities are understudied, but do appear to exist for ethnic minorities compared with whites for adjuvant, hormone and radiation therapy.

Future perspective

The disparities that exist for ethnic minorities, particularly for African–Americans, but also for Asians and Latinas, are present across the disease and care spectrum, and appear to be multifactorial.

More research is needed to delineate the contribution of hereditary susceptibility, tumor biology and breast density to these disparities.

Screening participation is the only area in which interventions to decrease disparities have been adequately studied; a large-scale national program has been successful, but there is still room for improvement to implement other intervention strategies on a broad scale.

Other areas, such as communication, diagnostic delays and treatment disparities, deserve more attention to develop interventions to equalize and improve the quality of care across ethnic groups.

Research in the following areas has the potential for being fruitful toward the aim of eliminating ethnic breast cancer disparities. First, there is a need for more research to delineate the contribution of genetics and hereditary susceptibility, particularly for premenopausal African–American women without deleterious BRCA mutations. Next, we need a better understanding of breast density as a risk factor in different ethnic groups, the contribution of genetics and environment to breast density, and mechanisms for gene–environment interactions. Much work has already been done in the area of screening participation; what is needed now is improved translation of proven interventions that optimize screening participation into clinical and public health practice. Other areas, such as communication of abnormal mammography results, diagnostic delays and treatment disparities, deserve more attention to develop interventions that will both equalize and improve the quality of care across ethnic groups. Significant advances have been made in breast cancer diagnosis, treatment and survival in the past 15 years. In order for women of all ethnicities to benefit equally from these and future advances, researchers, clinicians and policy makers will need to focus more attention on the diverse etiologies of ethnic differences in breast cancer and on interventions to eliminate those disparities.

Footnotes

Supported by the NCI-funded Breast Cancer Surveillance Consortium co-operative agreement U01CA63740 (KK) and the American Cancer Society MRSG-06–253–01 (LSK and KK). The authors have no other relevant affiliations or financial involvement with any organization or entity with a financial interest in or financial conflict with the subject matter or materials discussed in the manuscript apart from those disclosed.

No writing assistance was utilized in the production of this manuscript.

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Ethnic Disparities in Breast Cancer

Abstract

Keywords

Incidence, mortality & stage

Tumor characteristics

Genetics

Risk factors

Socioeconomic status

Screening participation

Processes of care

Communication of abnormal mammography results

Delays in diagnosis & treatment

Treatment disparities

Future perspective

Footnotes

References