Health Disparities and the Cancer Survivor Victoria S. Blindera and Jennifer J. Griggsb Disparities on the basis of race and ethnicity have been described in a variety of survivorship outcomes, including late and long-term effects of treatment, surveillance and health maintenance, and psychosocial outcomes. However, the current body of literature is limited in scope and additional research is needed to better define and address disparities among cancer survivors. Semin Oncol 40:796-803 & 2013 Elsevier Inc. All rights reserved.

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acial and ethnic disparities exist with respect to cancer stage at diagnosis, survival, morbidity, mortality, and quality of life.1–10 Minorities tend to be diagnosed with more advanced disease, are more likely to receive inferior treatment compared to non-Hispanic whites, and experience greater morbidity and mortality related to cancer and its treatment.4,5,9–11 Racial and ethnic disparities also have been identified in the survivorship period. Although disparities have been described in cancer treatment, outcomes, and quality of life according to race and ethnicity, age, gender, geography, and disability status, this article focuses on the available literature addressing racial and ethnic disparities in late and long-term effects of cancer and its treatment, including quality of life in the survivorship period. Despite the recent increase in research about late and long-term effects of cancer therapy, the literature is limited with regard to possible disparities in these outcomes. Some studies include race/ethnicity as a covariate, but many do not report race or ethnicity at all, and very few address disparities

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Departments of Epidemiology and Biostatistics and of Medicine, Memorial Sloan-Kettering Cancer Center, New York, NY. b Departments of Internal Medicine, University of Michigan Medical School and Health Management and Policy, School of Public Health, University of Michigan, Ann Arbor, MI. Supported in part by the American Cancer Society (MRSGT-11-00201-CPHPS, Dr Blinder) and the American Society of Clinical Oncology (Career Development Award, Dr Blinder). Financial disclosures: The authors have no relevant financial interests to disclose. Address correspondence to Victoria Blinder, MD, MSc, Center for Health Policy and Outcomes, Department of Epidemiology and Biostatistics, Memorial Sloan-Kettering Cancer Center, 300 E 66th St, 14th Floor, New York, NY 10065. E-mail: [email protected] 0093-7754/ - see front matter & 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1053/j.seminoncol.2013.09.003

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directly. Moreover, the majority of studies that focus on disparities include blacks, Hispanics, and whites only; Asian Americans and other minority and immigrant groups are understudied. The literature also does not address disparities in several late and longterm effects, such as neuropathy, cardiovascular toxicity associated with radiation, or rates of treatment-related leukemia. Differences in treatment, such as undertreatment of blacks,11,12 and poorer long-term survival rates among blacks may account for the lack of disparities demonstrated in certain late and long-term effects. Nonetheless, it is likely that the literature on disparities in survivorship outcomes fails to adequately describe the problems faced by minority populations.

LATE AND LONG-TERM EFFECTS Cardiovascular Outcomes Anthracycline-related cardiomyopathy is an uncommon but serious complication of chemotherapy. Limited data from retrospective chart reviews indicate that blacks may be at increased risk.13,14 A large retrospective analysis of survivors of pediatric cancers treated with anthracyclines showed that the relative risk of cardiotoxicity (congestive heart failure, decreased ejection fraction, or sudden cardiac death) was 1.7 among blacks compared to whites.14 A smaller retrospective study confirmed this increased risk in black adults treated with anthracyclines with an odds ratio of 2.93.13 This study was limited by the fact that the sample of blacks was compared to a sample of unknown racial and age composition from another study.13 The etiology of the apparent increase in cardiotoxicity remains unknown, but one possibility is that polymorphisms in enzymes that determine the drugs’ pharmacokinetics and/or pharmacodynamics may increase exposure to the cardiotoxic metabolite in

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the catalytic pathway.15 Additional research is needed to better assess ethnic differences in the rate of cardiotoxicity and to understand the etiologies of these differences in order to enhance identification of those at risk and to put into place preventive and surveillance strategies.

Second Malignancies Current studies are limited with regard to possible racial/ethnic disparities in the incidence of second malignancies; most studies do not include race/ ethnicity as a variable. We do not know whether treatment-related malignancies, such as secondary leukemias or radiation-related cancers, are more common among some racial/ethnic groups than others. With respect to second malignancies that arise, not as a result of treatment, but due to the same constellation of risk factors, data also are limited. In one study of survivors of head and neck cancer, investigators examined the impact of neighborhood characteristics on the incidence of second primary malignancies.16 They created an index of “neighborhood deprivation,” which included education, unemployment, poverty, single-parent households, and lack of a vehicle available for use. Participants with high neighborhood deprivation had a higher risk of developing a second primary malignancy compared to those with low/moderate neighborhood deprivation (hazard ratio [HR] 2.99; 95% confidence interval [CI], 1.46-6.11) controlling for race, age, income, smoking status, sex, cancer treatment, and cancer stage. Race was not associated with the development of second malignancies, but the study sample was primarily non-Hispanic white (82%). Non-whites were aggregated into a single category (“other”), and no information was provided about the composition of that group. In a study of breast cancer survivors who had participated in two studies undertaken by the National Surgical Adjuvant Breast and Bowel Project, investigators compared the rates of various different “disease-free survival” events in blacks and whites.17 Approximately 6% of the 4,936 participants were black. The investigators found no significant differences between blacks and whites in the rate of contralateral breast cancer or second primary cancer. Overall, data with respect to the development of second malignancies in minorities are extremely limited. In light of the disparities that have been demonstrated in stage at diagnosis, treatment, and survival, this area of research merits additional study.

Gonadal Dysfunction and Infertility Data are limited with respect to disparities in gonadal dysfunction and infertility associated with cancer treatment. Most research has focused on

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disparities in referral patterns, although these data also are limited. In a study of 918 cancer survivors who underwent treatment with the potential to affect fertility, no significant differences were found in access to fertility counseling by an oncologist.18 In contrast, in a single-institution, retrospective, cohort study 26% of white women who had a new cancer diagnosis and were eligible for fertility preservation had a fertility preservation consultation compared to 13% of non-white women.19 However, after controlling for age, insurance status (insured v uninsured), parity, and cancer type (breast v other cancer), the difference between whites and nonwhites was not statistically significant. Another single-institution series compared the characteristics of women referred for fertility preservation prior to chemotherapy or radiation to those referred for assisted reproduction technology after treatment.20 No significant differences were found in referral patterns by race/ethnicity. These findings are limited by the fact that women who were never referred to a fertility practice were not included in the study. Additional research is needed to understand whether or not disparities exist in access to fertility preservation services for cancer survivors and to improve the availability of these treatments.

Osteoporosis Osteopenia and osteoporosis are both a direct consequence of endocrine therapies for some cancers and an indirect consequence of chemotherapy, at least in part due to the impact of chemotherapy on gonadal function. Few studies have addressed disparities in loss of bone mineral density and associated fractures among cancer survivors. Increased skin pigmentation is associated with lower levels of vitamin D, and blacks have lower levels of serum vitamin D compared to whites.21 In a study of women undergoing adjuvant treatment for breast cancer, blacks and Hispanics had higher rates of vitamin D deficiency (defined in this study as serum 25-hydroxyvitamin D level o20 ng/mL) than non-Hispanic whites.22 Although vitamin D is thought to play an important role in increasing bone strength, white women in the general population appear to be at increased risk of osteoporosis compared to non-whites. Whether this risk pattern persists among cancer survivors is not known. Among men with prostate cancer, blacks have a higher hip bone density and similar spine bone density compared to whites, but the two groups have similar declines in bone density of both the hip and the spine as a result of androgen-deprivation therapy. This finding may indicate that the factors leading to lower risk of osteoporosis among healthy blacks may not protect this group against therapy-related bone

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loss.23 In a study of primarily Hispanics and nonHispanic whites undergoing androgen-deprivation therapy for prostate cancer, Hispanics were less likely than non-Hispanic whites to undergo recommended osteoporosis management (odds ratio [OR] 0.39; 95% CI, 0.18–0.86), defined as having undergone dualenergy x-ray absorptiometry (DXA) within 2 years before their last treatment with androgen-deprivation therapy or to be receiving treatment with a bisphosphonate, calcitonin, calcium, or vitamin D.24 The authors advised caution in interpreting these results as race/ethnicity was unknown for 16% of the study sample. If true, however, this statistic is concerning, as studies of osteoporosis in the general population indicate that, while minorities are less likely to be diagnosed with osteoporosis or to suffer a hip fracture, non-whites who are diagnosed with a fracture are more likely to die within 6 months of the fracture and less likely to be ambulatory at 6 months.25 Disparities in osteoporosis screening are further described in the next section.

HEALTHCARE: SURVEILLANCE, SCREENING FOR OTHER CANCERS, AND PREVENTIVE CARE Surveillance Breast Cancer Various studies have examined mammography use among breast cancer survivors, with mixed conclusions regarding whether or not race/ethnicity is associated with this outcome. In one study, race/ ethnicity was not associated with the likelihood of reporting a mammogram within the last year among women aged 30 years or older.26 However, women who were uninsured or had only public insurance (Medicaid or Medicare without a private supplement) were less likely to have undergone a mammogram. Lack of a usual healthcare provider, age ≥75 years, and longer time since diagnosis all were associated with not having a mammogram. Another study of elderly breast cancer survivors found that blacks and those who were dually eligible for Medicaid and Medicare were less likely to undergo surveillance mammography within a year of finishing treatment than were whites and those eligible for Medicare only.27 Those who underwent lumpectomy and radiation therapy also were more likely to undergo surveillance mammography than those in whom radiation therapy was omitted after breast-conserving surgery. In multivariable analysis, treatment type remained a significant predictor of mammography, whereas race and dual eligibility were no longer significant. The investigators concluded that the likelihood of undergoing mammography was greater for

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those who underwent lumpectomy with radiation (the standard of care for women of all ages during the study period), regardless of race or dual public insurance eligibility. However, they acknowledged that because dual eligible, black women are less likely to undergo radiation therapy after breast conserving therapy; additional research is needed to understand and address these disparities. In a third study, which examined mammography use among Medicare beneficiaries, black and other non-white breast cancer survivors both were less likely to have undergone a mammogram a year after their diagnosis compared to whites (OR 0.74; 95% CI, 0.65–0.85 for blacks v OR 0.69; 95% CI, 0.53–0.92 for other non-whites).28

Colorectal Cancer A recent systematic review of racial and ethnic disparities in surveillance colonoscopies after treatment for colorectal cancer identified eight relevant studies.29 Of these, four demonstrated a statistically significant disparity in receipt of a surveillance colonoscopy between blacks and whites, with blacks less likely to undergo standard surveillance.29–33 Three of these studies were based on Medicare claims data33 or a combination of Surveillance Epidemiology and End Results (SEER) and Medicare data.30,31 The fourth study was based on health maintenance organization data.32 Four other studies identified in the review demonstrated disparities in receipt of surveillance colonoscopy between whites and non-whites, but these trends were not statistically significant.34–37 In a more recent study, not included in the aforementioned review due to its publication date, blacks were significantly less likely than whites to receive surveillance colonoscopies and carcinoembryonic antigen (CEA) testing.38 However, no significant difference was found between the two groups in primary care doctor visits. Conversely, no significant differences were found between Hispanics and non-Hispanic whites in receipt of either surveillance colonoscopy or CEA testing, but Hispanics were more likely than nonHispanic whites to see a primary care doctor as recommended. Another study, which included only Medicaid beneficiaries, showed no significant difference in receipt of surveillance colonoscopy between blacks and whites.39 However, less than half of the patients in the study sample had undergone a surveillance colonoscopy within 3–18 months of surgery for colorectal cancer, indicating that poverty may be more important than race/ethnicity in determining who undergoes appropriate surveillance.

Screening for Other Cancers Many studies have used the SEER-Medicare database to examine receipt of routine primary care and

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preventive services among cancer survivors. One study of Medicare beneficiaries diagnosed with colorectal cancer showed that blacks and other nonwhites were less likely to undergo mammograms compared to whites during year 2 after diagnosis (OR 0.71; 95% CI, 0.57–0.88 v OR 0.70; 95% CI 0.55–0.88 for blacks and other non-whites, respectively).40 However, in a sample of long-term colorectal cancer survivors followed for 5 years, there was no significant relationship between receipt of mammography and race, although survivors with a higher socioeconomic status were more likely to undergo mammography (OR 1.09; 95% CI, 1.02–1.17).41 Similarly, socioeconomic status but not race was significantly associated with cervical cancer screening (OR 1.12; 95% CI, 1.05–1.19).41 Data are equivocal with respect to colorectal cancer screening (colonoscopy, sigmoidoscopy, or fecal occult blood testing). A study of Medicare recipients who were survivors of breast cancer showed that blacks were less likely than whites to undergo colorectal cancer screening (OR 0.81; 95% CI, 0.70–0.94),28 but among prostate cancer survivors, no difference was seen in colorectal cancer screening by race/ ethnicity.42 Little information is available regarding prostate cancer screening among survivors of other cancers. Although several analyses comparing cancer survivors to participants without a history of cancer controlled for race/ethnicity, these studies did not directly compare prostate cancer screening between different racial/ethnic groups.43–45

Preventive Care Vaccination Within the general population, racial/ethnic disparities have been demonstrated in receipt of influenza vaccination among elderly patients, and a similar trend might be expected among cancer survivors.46 However, a study of Medicare beneficiaries with advanced colorectal cancer found no significant difference in influenza vaccination rates between blacks and whites. However, patients with a higher socioeconomic status were more likely to be vaccinated.47 While patients with advanced cancer appear to differ from the general population with respect to nonclinical predictors of vaccination, long-term cancer survivors mirror non-cancer patients in this regard. Long-term survivors of colorectal cancer differed in vaccination rates according to both race and socioeconomic status (OR 1.25; 95% CI, 1.08–1.46 for whites compared to nonwhites; OR 1.07; 95% CI, 1.03–1.11 for socioeconomic status).41 Similarly, black breast cancer survivors were less likely than whites to receive an influenza vaccine during the second year after their

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cancer diagnosis (OR 0.47; 95% CI, 0.41–0.53),28 and black prostate cancer survivors were less likely to be vaccinated than white survivors 1 or 5 years after diagnosis (OR 0.41; 95% CI, 0.35–0.48 v OR 0.43; 95% CI, 0.35–0.51 for 1 and 5 years, respectively).42

Bone Mineral Density Monitoring and Cholesterol Screening Similar findings have been seen with respect to bone health and cholesterol screening. Black cancer survivors were less likely than whites to undergo DXA screening in the second year after their cancer diagnosis,28,40 but neither race nor socioeconomic status was associated with receipt of DXA in longterm studies.41 Similarly, black survivors of breast or colorectal cancer were less likely than whites to undergo cholesterol screening in the short term,28,40 but when colorectal cancer survivors were followed for 5 years there was no significant association between either race or socioeconomic status and cholesterol screening.41 Among prostate cancer survivors, no difference was seen in cholesterol screening by race or ethnicity either 1 or 5 years after diagnosis.42

Smoking Cessation No significant racial or ethnic differences have been found in the likelihood of currently smoking in an analysis of 10,035 breast cancer survivors.48 However, a study that selected for cancer survivors who were smokers at the time of their diagnosis found that Hispanics were significantly less likely to stop smoking than non-Hispanic whites.49 There was no significant difference between blacks and nonHispanic whites in the rate of smoking cessation.

QUALITY OF LIFE Quality of life encompasses several domains, including physical, psychological, and social wellbeing. Racial and ethnic differences have been demonstrated in each of these domains among cancer survivors as described below.

Physical Well-Being Pain that persists after cancer and its treatment exerts powerful negative effects on quality of life, physical function, the ability to perform one’s role functions, and the ability to enjoy life. The existing literature provides compelling evidence that there are disparities in pain control between white and black cancer survivors in the United States. In a subset of women enrolled in the Women’s Health Initiative-Observational Study, 4,161 white women and 431 black women with a history of breast cancer

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responded to questions regarding health-related quality of life. Black survivors had small but significantly lower levels of physical functioning and general health.50 In one of the few studies to examine survivors of cancers other than solely breast cancer, a population-based sample of 199 patients with a variety of solid tumors (including breast cancer) was surveyed about the presence and severity of chronic pain, disability, and depressive symptoms.51 Overall, 20% of respondents reported chronic pain. Black respondents reported greater pain severity as well as greater disability related to pain and more depressive symptoms. As described earlier, few studies have included immigrants or women of other races. In one of the few studies of Asians living in the United States,52 a qualitative study of women with breast cancer using focus group methodology demonstrated that Chinese immigrants were less likely to seek medical care for management of physical symptoms, such as vasomotor side effects of endocrine therapy or pain following radiation therapy, than were Chinese-Americans or non-Hispanic white women. In a study of a diverse sample of 804 breast cancer survivors enrolled in the Health, Eating, Activity, and Lifestyle (HEAL) Study, physical well-being, measured using the Medical Outcomes Study SF-36, was significantly lower among blacks than among nonHispanic whites and Hispanics.1 Advancing age among racial and ethnic minorities was found in one study to have an impact on physical functioning among elderly survivors of a variety of cancers. However, once comorbidity was included in the analyses, age was no longer an independent factor associated with racial and ethnic differences in physical functioning.53 Particular attention to those survivors living with multiple medical problems may thus be warranted among majority and minority populations alike.

Psychological Well-Being Mental Health Racial and ethnic differences in the prevalence of depression following cancer have been demonstrated in diverse patient samples. For example, in a subset of participants in the HEAL study described above,1 blacks had significantly higher (more favorable) mental health scores compared with nonHispanic and Hispanic whites. Reassuringly, in a large longitudinal study of 677 low-income breast cancer survivors (252 non-Hispanic whites and 425 Hispanics) enrolled in Medicaid in California, depression was no more prevalent among Hispanics than non-Hispanics.54

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Despite the reassuring finding that depression may not be significantly more prevalent among Hispanics in the United States, a large systematic review and meta-analysis that included 18 studies with primarily Hispanics and Asians/Pacific Islanders with a wide variety of cancers demonstrated significantly higher levels of distress and poorer social quality of life among Hispanics than majority group patients and Asian/Pacific Islander patients.55

Concerns About Recurrence Concerns about recurrence appear to be lower among blacks than among other cancer survivors. In a subset of participants in the HEAL study described above,1 blacks had significantly better mental health scores and lower fear of recurrence scores than did Hispanics and non-Hispanic whites. This finding was confirmed in a diverse populationbased sample of 1,837 black, Hispanic, and nonHispanic white women in Los Angeles and Detroit who were surveyed within a year of being diagnosed with early-stage breast cancer.56 Race and ethnicity, as well as degree of acculturation among Hispanics, were independently associated with worry about cancer recurrence. Black women had the lowest levels of worry and low-acculturated Hispanics the highest. Better symptom management, greater understanding of information, and perceived greater coordination of care accounted for some of the racial and ethnic differences and may represent targets for interventions in low-acculturated Hispanics.

Social Well-Being Sexual Health Sexual dysfunction in the cancer survivor has become an increasing concern for both clinicians and researchers. Erectile dysfunction is a common complication of treatment for prostate cancer. The Prostate Cancer Outcomes Study, a population-based cohort study, surveyed black, Hispanic, and nonHispanic white men over a period of 5 years after a diagnosis of prostate cancer.57 No significant ethnic differences were noted among patients treated with primary radiotherapy. Among those who underwent prostatectomy, erectile dysfunction was more common in non-Hispanic whites than blacks and Hispanics, but blacks were more likely than non-Hispanic whites to say that sexual function was a “moderate-to-big problem” 60 months after diagnosis, and Hispanics were more likely than nonHispanic whites to report the same at 6 and 12 months. Similar results were found in the Cancer of the Prostate Strategic Urologic Research Endeavor (CaPSURE) study, which compared health related

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quality of life in black and white men right after treatment and after 1 year.58 Black men had better sexual function but worse sexual bother than white men just after treatment, but no significant differences were identified at 1 year. Relatively few studies have addressed disparities in sexual health among survivors of breast or gynecologic cancers. One study reported that whites were more likely than blacks to say that breast cancer had a negative impact on their sex lives.59 However, in a study of cervical cancer survivors sexual inactivity was more common among nonwhites than whites.60 A third study included 261 survivors of breast and gynecologic cancers, of whom 63% were white and 33% were black. No significant differences were found by ethnicity in interest in receiving care to address sexual issues, likelihood of seeing a physician to address these issues, or willingness to be contacted to address sexual issues.61 Hispanic women may be more vulnerable to sexual health problems than other racial/ethnic groups. In the above-described study of low-income breast cancer survivors enrolled in Medicaid in California, Hispanics were significantly more likely to report problems with sexual function than nonHispanic whites.54 Treatment factors, such as rates of chemotherapy receipt and rates of mastectomy, did not explain the differences in sexual health. It is possible that lower levels of information support provided to Hispanic women as identified by other investigators62 account in part for the differences in sexual health among ethnic groups.

Employment Outcomes Returning to work after a cancer diagnosis and cancer treatment permits patients and their families to return to normalcy, helps patients retain a sense of contributing to society and to their families, and allows them to maintain their standard of living. Little research has been done on the impact of cancer and its treatment on employment outcomes among racial and ethnic minorities. The research that has been done has been restricted to patients who have been treated for breast cancer.63,64 Significant are the findings that low-income women, Hispanics and non-Hispanics alike,64 and low acculturated Hispanics63 are at high risk of job loss after cancer; among Hispanics, receipt of adjuvant chemotherapy appears to be a particularly important risk factor for job loss.63

SUMMARY Ethnic and racial disparities have been demonstrated in a variety of survivorship outcomes. However, the current body of literature is limited in scope and

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likely underestimates the magnitude of the problem. It is likely that the disparities in stage at presentation, treatment, and survival, also may be demonstrated in additional survivorship outcomes. The challenge for investigators is to identify these and to develop strategies to eliminate these differences. The large databases of patients who have participated in clinical trials represent a rich resource that has remained poorly utilized in this regard and would be a good place to start.

Acknowledgment The authors gratefully acknowledge Sang-Hee Min for assistance with reference management and manuscript preparation.

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Health disparities and the cancer survivor.

Disparities on the basis of race and ethnicity have been described in a variety of survivorship outcomes, including late and long-term effects of trea...
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