Minority Adult Survivors of Childhood Cancer: A Comparison of Long-Term Outcomes, Health Care Utilization, and Health-Related Behaviors From
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《临床肿瘤学》
the Department of Pediatrics, East Tennessee State University Quillen College of Medicine, Johnson City, St Jude Children’s Research Hospital, Memphis, TN
Department of Pediatrics, University of California, Los Angeles, CA
Department of Pediatrics, University of Minnesota, Minneapolis, MN
Cancer Prevention Research Program, Fred Hutchinson Cancer Research Center, Seattle, WA
Department of Family and Community Medicine
Department of Pediatrics, The University of Texas Southwestern Medical Center at Dallas, TX
Department of Pediatrics, University of California, San Francisco, CA
Children's Hospital of Alabama Birmingham, AL
the Children's Hospital of Philadelphia, PA
ABSTRACT
PURPOSE: To determine the influence of race/ethnicity on outcomes in the Childhood Cancer Survivor Study (CCSS).
PATIENTS AND METHODS: Of CCSS adult survivors in the United States, 443 (4.9%) were black, 503 (5.6%) were Hispanic and 7,821 (86.6%) were white. Mean age at interview, 26.9 years (range, 18 to 48 years); mean follow-up, 17.2 years (range, 8.7 to 28.4 years). Late mortality, second malignancy (SMN) rates, health care utilization, and health status and behaviors were assessed for blacks and Hispanics and compared with white survivors.
RESULTS: Late mortality rate (6.5%) and 15-year cumulative incidence of SMN (3.5%) were similar across racial/ethnic groups. Minority survivors were more likely to have lower socioeconomic status (SES); final models were adjusted for income, education, and health insurance. Although overall health status was similar, black survivors were less likely to report adverse mental health (females: odds ratio [OR], 0.6; 95% CI, 0.4 to 0.9; males: OR, 0.5; 95% CI, 0.3 to 0.8). Differences in health care utilization and behaviors noted: Hispanic survivors were more likely to report a cancer center visit (females: OR, 1.5; 95% CI, 1.1 to 2.0; males: OR, 1.7; 95% CI, 1.2 to 2.3); black females were more likely (OR, 1.6; 95% CI, 1.1 to 2.4), and Hispanic females less likely to have a recent Pap smear (OR, 0.7; 95% CI, 0.5 to 1.0); black and Hispanic survivors were less likely to report smoking; black survivors were less likely to report problem drinking.
CONCLUSION: Adjusted for SES, adverse outcomes in CCSS were not associated with minority status. Importantly, black survivors reported less risky behaviors and better preventive practices. Hispanic survivors had equitable access to cancer related care.
INTRODUCTION
Childhood cancer survivors are at risk for myriad late morbidities related to their cancer treatment. Recent studies from the Childhood Cancer Survivor Study (CCSS) reported an excess mortality attributable to second malignant neoplasms (SMNs), cardiovascular and pulmonary disease, diminished health status, lack of medical follow-up, and inadequate cancer screening.1-4 These studies compared minorities as a single group, without providing a detailed analysis between race and ethnic groups. Other than studies focusing on 5- and 10-year survival rates,5,6 there is little literature addressing the influence of race and ethnicity on long-term health outcomes of childhood cancer survivors. The need for further study among minority populations was highlighted in the recent landmark Institute of Medicine report, Childhood Cancer Survivorship: Improving Care and Quality of Life.7
Compared with whites, blacks and Hispanic minorities are considered vulnerable populations for adverse health outcomes in both the general US population8,9 and medical oncology.10-12 Socioeconomic differences contribute to the health disparities of minority populations.10,12 The higher prevalence of comorbid conditions in black adults is associated with poorer outcomes in medical oncology settings.13 Hispanics are the minority population least likely to comply with cancer screening recommendations and are the most likely to be uninsured.14-19
The CCSS provides the unique opportunity to investigate the association of race and ethnicity in health outcomes and health care in long-term survivors of childhood cancer. Importantly, it represents the largest population of minority survivors in North America and includes diversity in geographic locales and socioeconomic status (SES). This analysis compares differences in long-term health outcomes, health care utilization, health practices, and health behaviors between adult black, Hispanic, and white survivors of childhood cancer.
PATIENTS AND METHODS
Patient Selection
CCSS is a multi-institutional study of individuals who survived 5 years after treatment for childhood cancer. The present report from the CCSS is restricted to individuals 18 years age who participated in the study and met the following eligibility criteria: (a) diagnosis of leukemia, brain tumor, Hodgkin's disease, non-Hodgkin's lymphoma, kidney tumor, neuroblastoma, soft tissue sarcoma, or bone tumor; (b) diagnosis and initial treatment at one of 26 collaborating CCSS institutions; (c) diagnosis date between January 1, 1970, and December 31, 1986; (d) age younger than 21 years at diagnosis; and (e) survival at least 5 years from diagnosis. The CCSS protocol and contact documents were reviewed and approved by the human subjects committee at each participating institution. A detailed description of the methodology and cohort characteristics has been reported previously.20 Copies of the baseline questionnaire and the treatment abstraction form are available for review at www.cancer.umn.edu/ccss.
Of the 20,602 childhood cancer survivors included in the cohort, 3,035 (14.7%) were lost to follow-up. Among the 17,567 participants located, 14,370 (81.8%) completed a baseline questionnaire, including 9,726 of participants who were 18 years or older at time of interview. Due to differences in health care systems, survivors living in Canada were excluded from this analysis (n = 693). The cohort examined here was based on patients' self-report of race and ethnicity.
Outcomes
Late mortality is defined by the percentage of participants in the cohort who have died as a result of any cause.1 Patients who died before contact had questionnaires completed by a parent or another relative. The date of death was obtained from National Death Index records. Reports and dates of new cancers were verified by review of medical records. Only conditions confirmed as SMNs were included in this analysis.
Six domains of health status were assessed as described previously: general health, mental health, functional impairment, limitations of activity, pain resulting from cancer or its treatment, and anxiety or fears related to cancer or its treatment.2 Self-reported health care utilization for survivors was measured over the previous 2 years for a variety of different types of medical care as described previously.4 Positive health practices included dental care and sex-specific cancer screening health behaviors and practices.3
Risky health behaviors included current smoking status, physical activity and alcohol intake. Respondents' answers for these behaviors were stratified as defined in previous literature.21-24
Independent Variables
Demographic variables considered in the analysis included the age at time of baseline questionnaire and sex. SES variables included health insurance, highest level of education, and household income. Cancer-related variables included cancer diagnosis, age at diagnosis, interval from diagnosis, and cancer treatment.
Analysis
To compare sociodemographic and cancer treatment variables between race groups, two-sample t tests were used for continuous variables, and 2 tests were performed for categoric variables. The number of deaths was determined for black, Hispanic, and white participants, stratified by sex and adjusted for cancer diagnosis. Poisson regression models were used to compare the incidence of death in blacks and Hispanics with white participants, stratified by sex, and adjusted for age and cancer diagnosis. For living respondents, date of questionnaire completion was used as the end point for calculation of person-years, the start point for all patients being 5 years after date of cancer diagnosis. The same data were used to construct Kaplan-Meier survival curves.
Poisson regression models were used to compare SMN incidence among black, Hispanic and white survivors, stratified by age and sex. The number of person-years at risk for the cohort was calculated using the 5-year anniversary of the first cancer diagnosis as the start point, and the date of SMN diagnosis, death, or questionnaire completion as the end point. The observed number of SMNs in each group was compared with the expected number, computed using data from the Surveillance, Epidemiology, and End Results (SEER) database.
The prevalence of adverse outcomes in each of the health status domains, health care utilization, and health behaviors were determined for respondents. Logistic regression models with these outcomes as the dependent variables were used to compare blacks and Hispanics to white respondents. To estimate odds ratios (OR) with 95% CIs for these outcomes, subjects were stratified by sex and adjusted for age and cancer diagnosis. Analyses were performed with and without the following SES variables: health insurance, household income, and level of education. Because the primary aim was to evaluate differences on the basis of race and ethnicity, the final models were adjusted for these three SES variables. Data were analyzed with SAS version 9.0 (SAS Institute, Cary, NC) with two-tailed statistical tests.
RESULTS
In comparison with white survivors, blacks and Hispanics were less likely to have a college education, more likely to have lower household incomes, more likely to be uninsured, and were younger at time of interview. There were differences in cancer diagnoses and thus treatment between the three racial/ethnic groups (Table 1).
The late mortality was 6.5% (31 of 474) in blacks and 6.2% (33 of 536) in Hispanics enrolled in CCSS (Fig 1). These rates were comparable to the 6.6% late death rate in white survivors. Black female survivors had a lower late mortality rate compared with Hispanic or white females, or males of either race (OR, 0.3; 95% CI, 0.1 to 0.7; P = .008). Late mortality caused by SMN occurred in 2.7% (13 of 474) black and 3.0% (16 of 536) Hispanic survivors compared with 3.5% (293 of 8,360) white survivors (P = not significant).
Table 2 lists the percentage of survivors with moderate to severe adverse health status outcomes, medical visits within the previous 2 years, positive health practices, and risky health behaviors. Table 3 provides the OR estimates with 95% CI for these outcomes, stratified by sex and adjusted for age at baseline interview, cancer diagnosis, and SES variables. Compared with white survivors, black survivors were less likely to report mental health problems (male: OR, 0.5; 95% CI, 0.3 to 0.8; female: OR, 0.6; 95% CI, 0.4 to 0.9). In order to explore the differences in reporting of mental health symptoms, subdomains were compared. Both black men and women were less likely to report anxiety (male: OR, 0.4; 95% CI, 0.2 to 0.9; female: OR, 0.5; 95% CI, 0.2 to 0.9) and adverse mental health in at least one domain (male: OR, 0.5; 95% CI, 0.3 to 0.8; female: OR, 0.6; 95% CI, 0.4 to 0.9). Male black survivors were also less likely to report adverse global mental health (OR, 0.4; 95% CI, 0.2 to 0.8) and depression (OR, 0.5; 95% CI, 0.3 to 0.9).
When models were unadjusted for SES, there were some significant differences in health status outcomes. In contrast to the model adjusted for SES, the unadjusted model indicates that black females report adverse mental health (OR, 0.8; 95% CI, 0.5 to 1.2) at similar rates as whites and Hispanics. They were also more likely to report functional impairment (OR, 1.7; 95% CI, 1.2 to 2.5). Without SES adjustment, black males reported similar adverse mental health (OR, 0.6; 95% CI, 0.4 to 1.0), and were more likely to report limitations of activity (OR, 1.7; 95% CI, 1.1 to 2.5). Hispanic males, in models without SES adjustment, were more likely to report adverse general health (OR, 1.9, 95% CI, 1.4 to 2.8), functional impairment (OR, 1.9, 95% CI, 1.3 to 2.8), and any adverse health status (OR, 1.4; 95% CI, 1.1 to 1.8) compared with white survivors. There were no significant differences in health status for Hispanic females with or without adjustment for SES.
The only difference in medical care utilization between models with or without SES was that black males were less likely to report general medical contact (OR, 0.6; 95% CI, 0.5 to 0.9) when adjustment was not made for SES. The differences found in positive practices or risky behaviors did not vary with adjustment for SES.
DISCUSSION
The role of race and ethnicity in health outcomes is an important focus in reducing health disparities, particularly related to cancer.10 This study compares the health outcomes and health care utilization of blacks and Hispanics to whites from the largest cohort of adult survivors of childhood cancer in the United States. Importantly, there are no comparable sources of data currently available that include a sizeable population of long-term survivors of childhood cancer from geographically and socioeconomically diverse settings. In the general population, blacks and Hispanics have an excess risk of all-cause mortality.25 Race and ethnicity are composite terms that encompass socioeconomic, sociocultural, and environmental factors. The interrelationship of race and ethnicity with SES is complex. Though some have suggested that adjusting for SES "closes the gap,"26,27 other studies suggest a persistent disparity in mortality at all levels of SES.11,12,28,29
There were several notable study findings. Similar to the general population, black and Hispanic survivors were more likely to have lower SES. Despite these differences, unadjusted rates of late mortality and SMNs were similar across race and ethnic groups. Adjusted for SES, health status and health care utilization patterns were similar across groups. Notably blacks reported better preventive practices and were less likely to engage in risky behaviors. Black females were the subgroup in the cohort with the lowest mortality rate, the highest compliance with cancer screening, and the greatest avoidance of high-risk behaviors. The following discussion highlights these key findings.
These data, although reassuring for minority populations, apply to a relatively young minority population who may not yet have experienced premorbid health conditions that disproportionately affect black and Hispanic adults.13 Additional follow-up time is required to assess the influence of potential comorbidities combined with the late effects of cancer treatment exposures. SMNs are a major contributor to the late mortality of childhood cancer survivors.1 Epidemiologic data document higher incidence and mortality rates for many adult onset malignancies in racial and ethnic minorities.9-13,25 However, our study is the first to evaluate the association of race and ethnicity with SMN; rates of SMNs were similar among the three groups.
Health status is known to be significantly diminished for the CCSS young adult cohort compared to the general population.2 After adjusting for SES indicators, we found little significant difference in health status on the basis of race or ethnicity. Importantly, black survivors were less likely to report symptoms of adverse mental health.
Lower SES is associated with an increased risk of adverse mental health in the general population and in the CCSS cohort.2 In the general population, it is still controversial whether race, after adjusting for SES, is associated with adverse mental health.30-32 In our study, with SES adjustment, the rate of adverse mental health was significantly lower in blacks than whites, while the rate in Hispanics was similar to whites. The lower prevalence of mental health problems in adult black survivors in our cohort may suggest a difference in resilience or coping.33,34 Alternatively, there may be a racial difference in interpreting and reporting of symptoms of anxiety or depression.
This study yielded unexpected findings regarding the pattern of medical care reported by adult minority survivors of childhood cancer. We previously found that although 87% of adult survivors reported some general medical contact, only 42% and 19%, respectively, reported a cancer-related medical visit or a cancer center visit in the previous two years.4 In that analysis of the entire CCSS cohort 20% of the adult survivors did not have a general physical, cancer-related medical visit, or a visit at a cancer center. Reflecting the influence on SES indicators, survivors without health insurance were almost 2.5 times as likely to report this lack of care as those with insurance. In the present study, we found that regardless of SES, black female and Hispanic male survivors had less general contact with the medical system, yet had equitable use of cancer-related services compared with white survivors. In fact, both male and female Hispanic survivors were more likely to report a visit to a cancer center than white survivors. In our survivor cohort, regardless of SES, hospitalization and emergency room utilization was similar for all three racial/ethnic groups.
These findings contrast with reports of lower rates of outpatient health care utilization by minority groups in the general population14,16,18,35-40 and in survivors of adult cancers.10 Enrollment in childhood cancer protocols, with a uniformity of care, 41,42 may facilitate the development of a therapeutic alliance and an acculturation with the medical system that subsequently extends into adulthood for minority survivors. Thus, the cancer experience during childhood may remove some of the traditional barriers to health care experienced by blacks and Hispanics in the general population.43
Lack of compliance with follow-up and screening services has been suggested as one of the primary contributing factors to higher mortality rates among adult minority oncology patients.13,44,45 Cultural beliefs such as fatalism instill that there is little an individual can do to alter fate or prevent cancer. In the CCSS cohort black female survivors were more likely to report compliance with sex-specific screening in comparison with white survivors; these compliance rates mimic those reported by black women nationally after decades of targeted community programs in this population.10 Conversely, lower Pap smear screening rates in Hispanic survivors in our cohort mirrors findings in the general Hispanic population.12,46 Significantly lower rates of mammography and clinical breast exam are recognized among non-English speakers regardless of ethnicity.47 Therefore, acculturation, English language use, and belief systems such as fatalism need to be recognized by providers as deterrents to cancer screening among Hispanic survivors, as has been reported in the general population.16,19,48-54
Both black and Hispanic survivors were significantly less likely to report smoking in comparison with whites. Smoking prevalence rates were also lower than those for blacks and Hispanics in the general population (blacks, 22.5%; Hispanics, 23.4%) in the Behavioral Risk Factor Surveillance System Survey.55 Emmons et al previously reported from the CCSS cohort that black survivors were less likely to initiate smoking.56 Whereas Hispanic and white survivors reported alcohol-related behavior similar to the general young adult population,55 black survivors were much less likely to report binge drinking. The explanation for these findings need to be further explored, but may be explained by sociocultural differences in coping mechanisms and subsequent risk behaviors in Hispanic and white survivors compared with blacks. It is important to better understand these differences and screen for alcohol-related problems in Hispanic and white survivors.
Several limitations should be appreciated when interpreting the provocative findings of this study. Reporting of race/ethnicity and all outcomes were subject to the bias of self-report. Although this is the largest national cohort of adult black and Hispanic survivors of childhood cancer, the race, ethnic status, and SES of nonparticipants is not known. Thus, there may be a selection bias in the participation rate of minority survivors. We also note that black and Hispanic survivors were relatively well insured, compared with the general US population, suggesting an economic sampling bias.14 We recognize that this is an English-speaking population of Hispanics and hence a more acculturated group. Consequently, participation in the CCSS may select for minorities who were more motivated to comply with health care recommendations. Also, study numbers precluded evaluation of other important vulnerable ethnic groups such as Native Americans and Asians. Lastly, the cross-sectional study design used for this analysis has inherent limitations. Nevertheless, this study provides the most comprehensive evaluation to date of the influence of race and ethnicity on the long-term outcomes and practices of survivors. This article represents outcomes and practices of minority survivors at time of enrollment to the CCSS. There is a richness provided by longitudinally following a cohort to better understand the trends in the outcomes as well as changes in behaviors over time. Because the CCSS cohort is periodically surveyed (currently every 2 years), longitudinal data will be available within the next 1 to 2 years.
In summary, this analysis of a large cohort of black and Hispanic young adults who survived childhood cancer indicates that risk for adverse health outcomes is comparable to that of white survivors when corrected for SES. However, childhood survivors as a group are at risk for socioeconomic disadvantages57,58 that may impair health access as they age.
Authors' Disclosures of Potential Conflicts of Interest
The authors indicated no potential conflicts of interest.
NOTES
Supported by Grant No. U024-CA-55727-05 from the Department of Health and Human Services and funding to the University of Minnesota from the Children's Cancer Research Fund, and the University of California, Los Angeles, Jonsson Comprehensive Cancer Seed Grant Fund.
S.M.C. and J.C. contributed equally to the preparation of this manuscript.
Presented as abstracts/poster at the Pediatric Academic Societies Meeting, San Francisco, CA, May 1, 2004, and the Eighth International Conference on Long-Term Complications of Treatment of Children and Adolescents for Cancer, Niagra-on-the-Lake, Ontario, Canada, June 25, 2004.
Authors' disclosures of potential conflicts of interest are found at the end of this article.
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Department of Pediatrics, University of California, Los Angeles, CA
Department of Pediatrics, University of Minnesota, Minneapolis, MN
Cancer Prevention Research Program, Fred Hutchinson Cancer Research Center, Seattle, WA
Department of Family and Community Medicine
Department of Pediatrics, The University of Texas Southwestern Medical Center at Dallas, TX
Department of Pediatrics, University of California, San Francisco, CA
Children's Hospital of Alabama Birmingham, AL
the Children's Hospital of Philadelphia, PA
ABSTRACT
PURPOSE: To determine the influence of race/ethnicity on outcomes in the Childhood Cancer Survivor Study (CCSS).
PATIENTS AND METHODS: Of CCSS adult survivors in the United States, 443 (4.9%) were black, 503 (5.6%) were Hispanic and 7,821 (86.6%) were white. Mean age at interview, 26.9 years (range, 18 to 48 years); mean follow-up, 17.2 years (range, 8.7 to 28.4 years). Late mortality, second malignancy (SMN) rates, health care utilization, and health status and behaviors were assessed for blacks and Hispanics and compared with white survivors.
RESULTS: Late mortality rate (6.5%) and 15-year cumulative incidence of SMN (3.5%) were similar across racial/ethnic groups. Minority survivors were more likely to have lower socioeconomic status (SES); final models were adjusted for income, education, and health insurance. Although overall health status was similar, black survivors were less likely to report adverse mental health (females: odds ratio [OR], 0.6; 95% CI, 0.4 to 0.9; males: OR, 0.5; 95% CI, 0.3 to 0.8). Differences in health care utilization and behaviors noted: Hispanic survivors were more likely to report a cancer center visit (females: OR, 1.5; 95% CI, 1.1 to 2.0; males: OR, 1.7; 95% CI, 1.2 to 2.3); black females were more likely (OR, 1.6; 95% CI, 1.1 to 2.4), and Hispanic females less likely to have a recent Pap smear (OR, 0.7; 95% CI, 0.5 to 1.0); black and Hispanic survivors were less likely to report smoking; black survivors were less likely to report problem drinking.
CONCLUSION: Adjusted for SES, adverse outcomes in CCSS were not associated with minority status. Importantly, black survivors reported less risky behaviors and better preventive practices. Hispanic survivors had equitable access to cancer related care.
INTRODUCTION
Childhood cancer survivors are at risk for myriad late morbidities related to their cancer treatment. Recent studies from the Childhood Cancer Survivor Study (CCSS) reported an excess mortality attributable to second malignant neoplasms (SMNs), cardiovascular and pulmonary disease, diminished health status, lack of medical follow-up, and inadequate cancer screening.1-4 These studies compared minorities as a single group, without providing a detailed analysis between race and ethnic groups. Other than studies focusing on 5- and 10-year survival rates,5,6 there is little literature addressing the influence of race and ethnicity on long-term health outcomes of childhood cancer survivors. The need for further study among minority populations was highlighted in the recent landmark Institute of Medicine report, Childhood Cancer Survivorship: Improving Care and Quality of Life.7
Compared with whites, blacks and Hispanic minorities are considered vulnerable populations for adverse health outcomes in both the general US population8,9 and medical oncology.10-12 Socioeconomic differences contribute to the health disparities of minority populations.10,12 The higher prevalence of comorbid conditions in black adults is associated with poorer outcomes in medical oncology settings.13 Hispanics are the minority population least likely to comply with cancer screening recommendations and are the most likely to be uninsured.14-19
The CCSS provides the unique opportunity to investigate the association of race and ethnicity in health outcomes and health care in long-term survivors of childhood cancer. Importantly, it represents the largest population of minority survivors in North America and includes diversity in geographic locales and socioeconomic status (SES). This analysis compares differences in long-term health outcomes, health care utilization, health practices, and health behaviors between adult black, Hispanic, and white survivors of childhood cancer.
PATIENTS AND METHODS
Patient Selection
CCSS is a multi-institutional study of individuals who survived 5 years after treatment for childhood cancer. The present report from the CCSS is restricted to individuals 18 years age who participated in the study and met the following eligibility criteria: (a) diagnosis of leukemia, brain tumor, Hodgkin's disease, non-Hodgkin's lymphoma, kidney tumor, neuroblastoma, soft tissue sarcoma, or bone tumor; (b) diagnosis and initial treatment at one of 26 collaborating CCSS institutions; (c) diagnosis date between January 1, 1970, and December 31, 1986; (d) age younger than 21 years at diagnosis; and (e) survival at least 5 years from diagnosis. The CCSS protocol and contact documents were reviewed and approved by the human subjects committee at each participating institution. A detailed description of the methodology and cohort characteristics has been reported previously.20 Copies of the baseline questionnaire and the treatment abstraction form are available for review at www.cancer.umn.edu/ccss.
Of the 20,602 childhood cancer survivors included in the cohort, 3,035 (14.7%) were lost to follow-up. Among the 17,567 participants located, 14,370 (81.8%) completed a baseline questionnaire, including 9,726 of participants who were 18 years or older at time of interview. Due to differences in health care systems, survivors living in Canada were excluded from this analysis (n = 693). The cohort examined here was based on patients' self-report of race and ethnicity.
Outcomes
Late mortality is defined by the percentage of participants in the cohort who have died as a result of any cause.1 Patients who died before contact had questionnaires completed by a parent or another relative. The date of death was obtained from National Death Index records. Reports and dates of new cancers were verified by review of medical records. Only conditions confirmed as SMNs were included in this analysis.
Six domains of health status were assessed as described previously: general health, mental health, functional impairment, limitations of activity, pain resulting from cancer or its treatment, and anxiety or fears related to cancer or its treatment.2 Self-reported health care utilization for survivors was measured over the previous 2 years for a variety of different types of medical care as described previously.4 Positive health practices included dental care and sex-specific cancer screening health behaviors and practices.3
Risky health behaviors included current smoking status, physical activity and alcohol intake. Respondents' answers for these behaviors were stratified as defined in previous literature.21-24
Independent Variables
Demographic variables considered in the analysis included the age at time of baseline questionnaire and sex. SES variables included health insurance, highest level of education, and household income. Cancer-related variables included cancer diagnosis, age at diagnosis, interval from diagnosis, and cancer treatment.
Analysis
To compare sociodemographic and cancer treatment variables between race groups, two-sample t tests were used for continuous variables, and 2 tests were performed for categoric variables. The number of deaths was determined for black, Hispanic, and white participants, stratified by sex and adjusted for cancer diagnosis. Poisson regression models were used to compare the incidence of death in blacks and Hispanics with white participants, stratified by sex, and adjusted for age and cancer diagnosis. For living respondents, date of questionnaire completion was used as the end point for calculation of person-years, the start point for all patients being 5 years after date of cancer diagnosis. The same data were used to construct Kaplan-Meier survival curves.
Poisson regression models were used to compare SMN incidence among black, Hispanic and white survivors, stratified by age and sex. The number of person-years at risk for the cohort was calculated using the 5-year anniversary of the first cancer diagnosis as the start point, and the date of SMN diagnosis, death, or questionnaire completion as the end point. The observed number of SMNs in each group was compared with the expected number, computed using data from the Surveillance, Epidemiology, and End Results (SEER) database.
The prevalence of adverse outcomes in each of the health status domains, health care utilization, and health behaviors were determined for respondents. Logistic regression models with these outcomes as the dependent variables were used to compare blacks and Hispanics to white respondents. To estimate odds ratios (OR) with 95% CIs for these outcomes, subjects were stratified by sex and adjusted for age and cancer diagnosis. Analyses were performed with and without the following SES variables: health insurance, household income, and level of education. Because the primary aim was to evaluate differences on the basis of race and ethnicity, the final models were adjusted for these three SES variables. Data were analyzed with SAS version 9.0 (SAS Institute, Cary, NC) with two-tailed statistical tests.
RESULTS
In comparison with white survivors, blacks and Hispanics were less likely to have a college education, more likely to have lower household incomes, more likely to be uninsured, and were younger at time of interview. There were differences in cancer diagnoses and thus treatment between the three racial/ethnic groups (Table 1).
The late mortality was 6.5% (31 of 474) in blacks and 6.2% (33 of 536) in Hispanics enrolled in CCSS (Fig 1). These rates were comparable to the 6.6% late death rate in white survivors. Black female survivors had a lower late mortality rate compared with Hispanic or white females, or males of either race (OR, 0.3; 95% CI, 0.1 to 0.7; P = .008). Late mortality caused by SMN occurred in 2.7% (13 of 474) black and 3.0% (16 of 536) Hispanic survivors compared with 3.5% (293 of 8,360) white survivors (P = not significant).
Table 2 lists the percentage of survivors with moderate to severe adverse health status outcomes, medical visits within the previous 2 years, positive health practices, and risky health behaviors. Table 3 provides the OR estimates with 95% CI for these outcomes, stratified by sex and adjusted for age at baseline interview, cancer diagnosis, and SES variables. Compared with white survivors, black survivors were less likely to report mental health problems (male: OR, 0.5; 95% CI, 0.3 to 0.8; female: OR, 0.6; 95% CI, 0.4 to 0.9). In order to explore the differences in reporting of mental health symptoms, subdomains were compared. Both black men and women were less likely to report anxiety (male: OR, 0.4; 95% CI, 0.2 to 0.9; female: OR, 0.5; 95% CI, 0.2 to 0.9) and adverse mental health in at least one domain (male: OR, 0.5; 95% CI, 0.3 to 0.8; female: OR, 0.6; 95% CI, 0.4 to 0.9). Male black survivors were also less likely to report adverse global mental health (OR, 0.4; 95% CI, 0.2 to 0.8) and depression (OR, 0.5; 95% CI, 0.3 to 0.9).
When models were unadjusted for SES, there were some significant differences in health status outcomes. In contrast to the model adjusted for SES, the unadjusted model indicates that black females report adverse mental health (OR, 0.8; 95% CI, 0.5 to 1.2) at similar rates as whites and Hispanics. They were also more likely to report functional impairment (OR, 1.7; 95% CI, 1.2 to 2.5). Without SES adjustment, black males reported similar adverse mental health (OR, 0.6; 95% CI, 0.4 to 1.0), and were more likely to report limitations of activity (OR, 1.7; 95% CI, 1.1 to 2.5). Hispanic males, in models without SES adjustment, were more likely to report adverse general health (OR, 1.9, 95% CI, 1.4 to 2.8), functional impairment (OR, 1.9, 95% CI, 1.3 to 2.8), and any adverse health status (OR, 1.4; 95% CI, 1.1 to 1.8) compared with white survivors. There were no significant differences in health status for Hispanic females with or without adjustment for SES.
The only difference in medical care utilization between models with or without SES was that black males were less likely to report general medical contact (OR, 0.6; 95% CI, 0.5 to 0.9) when adjustment was not made for SES. The differences found in positive practices or risky behaviors did not vary with adjustment for SES.
DISCUSSION
The role of race and ethnicity in health outcomes is an important focus in reducing health disparities, particularly related to cancer.10 This study compares the health outcomes and health care utilization of blacks and Hispanics to whites from the largest cohort of adult survivors of childhood cancer in the United States. Importantly, there are no comparable sources of data currently available that include a sizeable population of long-term survivors of childhood cancer from geographically and socioeconomically diverse settings. In the general population, blacks and Hispanics have an excess risk of all-cause mortality.25 Race and ethnicity are composite terms that encompass socioeconomic, sociocultural, and environmental factors. The interrelationship of race and ethnicity with SES is complex. Though some have suggested that adjusting for SES "closes the gap,"26,27 other studies suggest a persistent disparity in mortality at all levels of SES.11,12,28,29
There were several notable study findings. Similar to the general population, black and Hispanic survivors were more likely to have lower SES. Despite these differences, unadjusted rates of late mortality and SMNs were similar across race and ethnic groups. Adjusted for SES, health status and health care utilization patterns were similar across groups. Notably blacks reported better preventive practices and were less likely to engage in risky behaviors. Black females were the subgroup in the cohort with the lowest mortality rate, the highest compliance with cancer screening, and the greatest avoidance of high-risk behaviors. The following discussion highlights these key findings.
These data, although reassuring for minority populations, apply to a relatively young minority population who may not yet have experienced premorbid health conditions that disproportionately affect black and Hispanic adults.13 Additional follow-up time is required to assess the influence of potential comorbidities combined with the late effects of cancer treatment exposures. SMNs are a major contributor to the late mortality of childhood cancer survivors.1 Epidemiologic data document higher incidence and mortality rates for many adult onset malignancies in racial and ethnic minorities.9-13,25 However, our study is the first to evaluate the association of race and ethnicity with SMN; rates of SMNs were similar among the three groups.
Health status is known to be significantly diminished for the CCSS young adult cohort compared to the general population.2 After adjusting for SES indicators, we found little significant difference in health status on the basis of race or ethnicity. Importantly, black survivors were less likely to report symptoms of adverse mental health.
Lower SES is associated with an increased risk of adverse mental health in the general population and in the CCSS cohort.2 In the general population, it is still controversial whether race, after adjusting for SES, is associated with adverse mental health.30-32 In our study, with SES adjustment, the rate of adverse mental health was significantly lower in blacks than whites, while the rate in Hispanics was similar to whites. The lower prevalence of mental health problems in adult black survivors in our cohort may suggest a difference in resilience or coping.33,34 Alternatively, there may be a racial difference in interpreting and reporting of symptoms of anxiety or depression.
This study yielded unexpected findings regarding the pattern of medical care reported by adult minority survivors of childhood cancer. We previously found that although 87% of adult survivors reported some general medical contact, only 42% and 19%, respectively, reported a cancer-related medical visit or a cancer center visit in the previous two years.4 In that analysis of the entire CCSS cohort 20% of the adult survivors did not have a general physical, cancer-related medical visit, or a visit at a cancer center. Reflecting the influence on SES indicators, survivors without health insurance were almost 2.5 times as likely to report this lack of care as those with insurance. In the present study, we found that regardless of SES, black female and Hispanic male survivors had less general contact with the medical system, yet had equitable use of cancer-related services compared with white survivors. In fact, both male and female Hispanic survivors were more likely to report a visit to a cancer center than white survivors. In our survivor cohort, regardless of SES, hospitalization and emergency room utilization was similar for all three racial/ethnic groups.
These findings contrast with reports of lower rates of outpatient health care utilization by minority groups in the general population14,16,18,35-40 and in survivors of adult cancers.10 Enrollment in childhood cancer protocols, with a uniformity of care, 41,42 may facilitate the development of a therapeutic alliance and an acculturation with the medical system that subsequently extends into adulthood for minority survivors. Thus, the cancer experience during childhood may remove some of the traditional barriers to health care experienced by blacks and Hispanics in the general population.43
Lack of compliance with follow-up and screening services has been suggested as one of the primary contributing factors to higher mortality rates among adult minority oncology patients.13,44,45 Cultural beliefs such as fatalism instill that there is little an individual can do to alter fate or prevent cancer. In the CCSS cohort black female survivors were more likely to report compliance with sex-specific screening in comparison with white survivors; these compliance rates mimic those reported by black women nationally after decades of targeted community programs in this population.10 Conversely, lower Pap smear screening rates in Hispanic survivors in our cohort mirrors findings in the general Hispanic population.12,46 Significantly lower rates of mammography and clinical breast exam are recognized among non-English speakers regardless of ethnicity.47 Therefore, acculturation, English language use, and belief systems such as fatalism need to be recognized by providers as deterrents to cancer screening among Hispanic survivors, as has been reported in the general population.16,19,48-54
Both black and Hispanic survivors were significantly less likely to report smoking in comparison with whites. Smoking prevalence rates were also lower than those for blacks and Hispanics in the general population (blacks, 22.5%; Hispanics, 23.4%) in the Behavioral Risk Factor Surveillance System Survey.55 Emmons et al previously reported from the CCSS cohort that black survivors were less likely to initiate smoking.56 Whereas Hispanic and white survivors reported alcohol-related behavior similar to the general young adult population,55 black survivors were much less likely to report binge drinking. The explanation for these findings need to be further explored, but may be explained by sociocultural differences in coping mechanisms and subsequent risk behaviors in Hispanic and white survivors compared with blacks. It is important to better understand these differences and screen for alcohol-related problems in Hispanic and white survivors.
Several limitations should be appreciated when interpreting the provocative findings of this study. Reporting of race/ethnicity and all outcomes were subject to the bias of self-report. Although this is the largest national cohort of adult black and Hispanic survivors of childhood cancer, the race, ethnic status, and SES of nonparticipants is not known. Thus, there may be a selection bias in the participation rate of minority survivors. We also note that black and Hispanic survivors were relatively well insured, compared with the general US population, suggesting an economic sampling bias.14 We recognize that this is an English-speaking population of Hispanics and hence a more acculturated group. Consequently, participation in the CCSS may select for minorities who were more motivated to comply with health care recommendations. Also, study numbers precluded evaluation of other important vulnerable ethnic groups such as Native Americans and Asians. Lastly, the cross-sectional study design used for this analysis has inherent limitations. Nevertheless, this study provides the most comprehensive evaluation to date of the influence of race and ethnicity on the long-term outcomes and practices of survivors. This article represents outcomes and practices of minority survivors at time of enrollment to the CCSS. There is a richness provided by longitudinally following a cohort to better understand the trends in the outcomes as well as changes in behaviors over time. Because the CCSS cohort is periodically surveyed (currently every 2 years), longitudinal data will be available within the next 1 to 2 years.
In summary, this analysis of a large cohort of black and Hispanic young adults who survived childhood cancer indicates that risk for adverse health outcomes is comparable to that of white survivors when corrected for SES. However, childhood survivors as a group are at risk for socioeconomic disadvantages57,58 that may impair health access as they age.
Authors' Disclosures of Potential Conflicts of Interest
The authors indicated no potential conflicts of interest.
NOTES
Supported by Grant No. U024-CA-55727-05 from the Department of Health and Human Services and funding to the University of Minnesota from the Children's Cancer Research Fund, and the University of California, Los Angeles, Jonsson Comprehensive Cancer Seed Grant Fund.
S.M.C. and J.C. contributed equally to the preparation of this manuscript.
Presented as abstracts/poster at the Pediatric Academic Societies Meeting, San Francisco, CA, May 1, 2004, and the Eighth International Conference on Long-Term Complications of Treatment of Children and Adolescents for Cancer, Niagra-on-the-Lake, Ontario, Canada, June 25, 2004.
Authors' disclosures of potential conflicts of interest are found at the end of this article.
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