Breast Cancer Screening by Asian-American Women in a Managed Care Environment Shin-Ping Tu, MD, MPH, Stephen H. Taplin, MD, MPH, William E. Barlow, PhD, Edward J. Boyko, MD, MPH Context:
Cross-sectional surveys show that Asian-American women are less likely to have had screening mammograms.
Objective:
To prospectively assess mammography screening by Asian-American women in a program with mailed recommendations and no out-of-pocket costs.
Design:
Two prospective cohort studies.
Setting:
A nonprofit health care system where women members ⱖ 40 years old are surveyed for breast cancer risk factors and enrolled into a screening program on survey completion.
Participants: Program enrollment—All Asian-American women identified through a compilation of Asian surnames (Chinese, Japanese, Vietnamese, and Korean) and a random sample of 2000 women with non-Asian surnames, who were mailed a survey from May 1988 to April 1995. Mammogram participation—All Asian-American women and a random sample of 3000 women with non-Asian surnames, enrolled in the screening program and were mailed a first recommendation for screening from May 1988 to April 1994. Main Outcome Measures:
Odds of program enrollment and mammogram use within one year (participation) by Asian-American women compared to non-Asian controls.
Results:
Compared to controls, Asian-American women were less likely to enroll in Breast Cancer Screening Program (BCSP) (odds ratio 0.53; 95% CI 0.43, 0.64). In aggregate, AsianAmerican women had similar mammogram participation rates. Among older ChineseAmerican women participation was lower compared to controls (odds ratio 0.66; 95% CI 0.44, 0.97).
Conclusion:
Participation in mammography screening (program enrollment and participation) by Asian-American women was not necessarily enhanced by the removal of financial barriers. Variations of screening behavior among Asian-American women may be obscured when analyzed in aggregate. Medical Subject Headings (MeSH): screening, mammography, Asians (Asian Americans), utilization (Am J Prev Med 1999;17(1):55– 61) © 1999 American Journal of Preventive Medicine
Introduction
A
sian and Pacific Islanders are one of the fastest growing and most diverse minority groups in the United States.1,2 From 1980 to 1990, the number of Asian and Pacific Islanders almost doubled, and it is projected that by the year 2050, Asian and From the Department of Medicine (Tu, Boyko), University of Washington, Seattle, WA; Center for Health Studies (Taplin, Barlow), Group Health Cooperative of Puget Sound, Seattle, WA; Department of Family Medicine (Taplin), University of Washington, Seattle, WA; Department of Biostatistics (Barlow), University of Washington, Seattle, WA; Seattle Epidemiologic Research and Information Center (Boyko), Veterans Affairs Puget Sound Health Care System, Seattle, WA. Address correspondence and reprints to Shin-Ping Tu, MD, MPH, Box 359780, Division of General Internal Medicine, Harborview Medical Center, 325 Ninth Ave, Seattle, WA 98104. E-mail:
[email protected]
Am J Prev Med 1999;17(1) © 1999 American Journal of Preventive Medicine
Pacific Islanders will comprise 10% of the U.S. population. Highly heterogeneous, Asian and Pacific Islanders include persons from 28 Asian countries and 25 Pacific Island cultures.3 Based on the 1990 census, 95% of Asian and Pacific Islanders were Asian Americans with Chinese (23.8%), Filipinos (20.4%), Japanese (12.3%), Asian Indians (11.8%), Koreans (11.6%), and Vietnamese (8.9%) representing the largest proportions. Although the incidence of breast cancer among Asian Americans is low compared to white women, breast cancer is the most common major malignancy among several Asian-American and Asian ethnic female populations.4 –10 The implications of this disease to the health of Asian-American women is even more sobering as increasing evidence demonstrates that breast cancer
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risk rises after migration to the U.S.11,12 For AsianAmerican women born in the U.S., the risk approaches that of the white population.13 Few national studies have assessed mammography screening rates of Asian-American women. Data from the National Health Interview Survey showed that women in the Asian/Other category were one half as likely to have ever had a mammogram.14 Similarly, 1994 statistics from California reveal Asian/Other women reported the lowest proportion of mammography use in the previous 2 years compared to non-Hispanic whites, African Americans, and Hispanics.5 The heterogeneity of Asian Americans reflects not only varying ethnic groups but also different migration histories to the U.S. Given that this will limit the usefulness of aggregated data on Asian Americans, ethnic-specific information is necessary to accurately reflect the health behaviors of Asian Americans.15 Surveys conducted on specific Asian ethnic groups demonstrated low mammography screening rates by Vietnamese and ChineseAmerican women.16,17 Recent studies continue to identify low utilization by Vietnamese-American women; however, data on Chinese-American women have been less consistent.7,18 –21 Similarly, data from Hawaii and California indicated low utilization by Filipino and Japanese-American women, although one study suggested a trend of increased screening in recent years.22,23 The association between mammogram use and factors such as low level of education, poor English fluency, and lack of health insurance has been documented by these studies.7,16 –21 However, mammography use may have been confounded in some of these studies by the presence of financial deterrents, because screening may have required out-of-pocket costs even for those with insurance. Therefore, screening differences between Asian Americans and the white population need to be evaluated in settings without financial barriers. Group Health Cooperative of Puget Sound (GHC) is a nonprofit health maintenance organization (HMO) in Washington state with over 360,000 enrollees and a Breast Cancer Screening Program (BCSP) requiring no out-of-pocket costs. With non-Asian women as the referent group, this study compared the enrollment of four Asian-American ethnic groups (Chinese, Japanese, Vietnamese, and Korean) into the BCSP. In addition, mammography screening by these four groups, individually and in aggregate, was assessed prospectively using a computerized database with screening recommendations and subsequent mammogram participation.
Methods Design Two prospective cohort studies of Asian-American and non-Asian control women enrolled in a prepaid health 56
plan. The cohorts were followed for BCSP enrollment and completion of the first BCSP-recommended screening mammogram.
Setting The BCSP is a program requiring no out-of-pocket costs for GHC enrollees. Women aged 40 and above are eligible for this program and are mailed a clinical survey in English to determine their breast cancer risk factors (Figure 1).24,25 The survey did not include information on ethnicity, education, marital status, or length of residence in the U.S. In the first year of the program, survey completion rate was 84% for the population as a whole.26 Women who completed the questionnaire were stratified to four different risk levels,27 and sent a letter specifying their recommended interval for comprehensive breast cancer screening. This included a clinical breast exam, mammogram, and breast self-exam instructions. Through a computerized reminder system, women were then mailed a recommendation to schedule a screening mammogram.
Outcome Measure One outcome of interest was program enrollment in the BCSP. To benefit from BCSP, women had to return the survey to receive recommendations automatically from the program. Using the computerized data, receipt of the survey by BCSP was compared between women from the different ethnic groups. Another outcome of interest was mammogram participation when recommended for the first time through BCSP. Mammogram participation among all eligible risk groups was defined as completing a mammogram within 12 months of the mailed recommendation.
Study Population The general GHC population reflects the demography of the regional area: 91% Caucasians; 4% Asian and Pacific Islanders; and 3% African Americans.26 Members of GHC have different types of health insurance, with the majority insured through private insurance. Others are covered through Medicare, Medicaid, and Basic Health Plan (a subsidized health insurance plan for low-income persons residing in Washington State). Program Enrollment. Eligible women were GHC members aged 40 years and over. The study period was limited to survey mailing dates of May 1, 1988 to April 30, 1995. Asian-American women were identified using surname lists purchased from a marketing company that compiled the names and addresses of Asians residing in the Seattle area and classified by ethnicity.28 Additional lists from the literature and the Northern California Cancer Institute also contributed to the final pool.29 –31 A total of 1212 Asian-American women were
American Journal of Preventive Medicine, Volume 17, Number 1
Figure 1. Flow charts of program enrollment and mammogram participation. GHC ⫽ Group Health Cooperative of Puget Sound; BCSP ⫽ Breast Cancer Screening Program.
identified. For controls, 2000 women were randomly selected from 57,215 women with non-Asian surnames. Age at the time of the survey and the date of survey were extracted for analysis. Using GHC’s general enrollment database, dates of enrollment and termination at GHC were also obtained.
Asian surnames, 3000 women were then randomly selected as controls. Dates of enrollment and termination at GHC as well as type of health care insurance were extracted for the analyses from GHC’s general enrollment database.
Mammogram Participation. This study constituted a different cohort of women from those included in the assessment of program enrollment. Eligible subjects were women aged 40 and above, enrolled with BCSP, had no prior history of breast cancer and were mailed a BCSP recommendation for the first time between May 1, 1988 and April 30, 1994 to schedule an appointment for mammography screening. To accommodate time for the completion and recording of mammograms into the BCSP database, the study period was limited to April 1994. Participants of other breast cancer screening intervention studies conducted at GHC were also excluded. Using the surname lists, 677 Asian-American women were identified. Surnames not specific for Asian ethnicity or Asian ethnic groups (e.g., Lee, Park) were classified separately. From 44,993 eligible women with non-
Statistical Analysis The Mann-Whitney tests, chi-square tests, and logistic regression were conducted using SPSS statistical programs. When appropriate, the StatXact-3 program was used for Fisher’s exact test. Program Enrollment. Mean age and duration of enrollment with GHC were compared for Asian-American women and controls using the Mann-Whitney test. To evaluate the effect of ethnicity and other covariates on BCSP enrollment, unconditional logistic regression (forward stepwise) was performed. Analysis was restricted to women who remained GHC members for at least 1 year after the survey mailing date. Mammogram Participation. Bivariate analysis was conducted in relation to mammogram participation for Am J Prev Med 1999;17(1)
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Table 1. Program enrollment—Demographic characteristics and likelihood of enrollment into the breast cancer screening program
Ethnicity
N
% Response
Controls Chinese Japanese Korean Vietnamese Asian
1473 495 223 33 106 857
81.5 67.1 76.2 72.7 72.6 70.4
Mean age
Mean GHC enrollment (months)
OR (95% CI)
45.5 45.3 45.4 44.1 45.0 45.2
48 43 70a 31 30 55
Referent 0.46 (0.37, 0.58) 0.67 (0.48, 0.95) 0.62 (0.28, 1.35) 0.62 (0.39, 0.97) 0.53 (0.43, 0.64)
a P ⬍ 0.001 compared with general GHC women. OR ⫽ odds ratio adjusted for age and years of enrollment with GHC; GHC ⫽ Group Health Cooperative of Puget Sound.
each ethnic group and the following independent variables: age, age group (40 to 49, 50 to 64, and 65 or more), years of GHC enrollment prior to mammography recommendation, enrollment for one or more years after recommendation, study year (year mammography recommendation was mailed), type of health care insurance (private, low income, Medicare), BCSP assigned risk level, first-degree relative with breast cancer, previous breast biopsy, nulliparity at age 30, menarche before age 11, menopause at 55 or older, and prior mammogram. Continuous variables were tested by the Mann-Whitney test and categorical data with the chi-square test. Logistic regression was then performed to estimate the odds of mammogram participation by Asian-American women compared to controls. Each Asian ethnic group was modeled separately and in aggregate as an Asian-American group. Women with nonspecific Asian surnames were analyzed separately. The independent variables listed above were tested as covariates in the forward stepwise logistic model. Age was initially entered as a continuous variable then categorized into age groups. Potential confounders were tested using backward stepwise modeling and adjusted for in the final logistic models. To assess for effect modification, first-order interaction terms between ethnic group and the independent variables were tested in the logistic regression models and included when inclusion improved the model significantly.
Results Program Enrollment. Eight hundred fifty-seven AsianAmerican women and 1473 controls were included in the analyses. The mean ages of the women were similar by ethnic group, but the mean length of enrollment with GHC varied (Table 1). Women in the control group had the highest response rate and subsequent enrollment in BCSP. Compared to controls, AsianAmerican women in aggregate and by ethnic groups were less likely to respond to the survey (Table 1). 58
Enrollment with GHC for more than 10 years positively predicted survey completion (odds ratio 1.66, 95% CI 1.22 to 2.26) and subsequent enrollment into BCSP. Mammogram Participation. Demographic and enrollment characteristics of the women are presented in Table 2. Asian-American women in aggregate and by ethnic subgroup had lower prior mammogram use compared to controls. Risk factors for breast cancer identified by BCSP showed a lower proportion of Chinese, Korean, and Vietnamese-American women in the highest risk level. The unadjusted odds of mammogram participation by Asian-American women in aggregate or by ethnic group did not differ significantly from that of controls except for Korean-American women (Table 3). After controlling for potential confounding factors (age group, enrollment with BCSP for at least 1 year, years of enrollment with GHC, study year, BCSP risk level, first-degree relative with breast cancer, previous biopsy, and prior mammogram), in aggregate the adjusted odds of mammogram participation by Asian-American women also did not differ from controls (Table 3). In subgroup analysis, distinct patterns emerged. In the adjusted logistic model of mammogram participation by Chinese-American women and controls, the first-order interaction term of age as a continuous variable and ethnicity was statistically significant (P ⫽ 0.01). When modeled separately by age group, older Chinese-American women, aged 50 years and above, had significantly lower mammogram participation compared to controls of their own age group (Table 3). Japanese-American women and women with nonspecific surnames had similar odds of mammogram participation as controls. Korean-American women were less likely to participate in mammography screening while Vietnamese-American women were more likely to undergo screening (Table 3). The sample sizes of these latter two groups were small and no statistically significant differences were detected.
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Table 2. Mammogram participation—Demographic and GHC enrollment characteristics
N Age (yr)
Mean (s.d.) Median
Control
Chinese
Japanese
2716 53.9 (12.4) 51
308 51.1a (10.7) 50
243 54.3 (12.1) 53
Korean
Vietnamese
Nonspecific
Asian
27 51.8 (9.7) 51
58 51.4 (8.5) 50.0
311 53.9 (11.8) 51.0
636 52.4b (11.1) 50.0
Age group (%)
40–49 yrs 50–64 yrs ⱖ65 yrs
40.3 38.6 21.1
43.5b 43.5 13.0
37.4 37.4 25.1
37.0c 48.1 14.8
32.8b 58.6 8.6
36.7 43.7 19.6
39.9 42.8 17.3
GHC enrollment (%) (year)
⬍1 1–5 5–10 10 or more Missing Yes No
7.1 29.3 21.1 41.8 0.8 93.0 7
6.5 33.1 22.4 37.0 1.0 89.6b 10.4
3.7a 24.7 16.0 55.1 0.4 94.7 5.3
7.4b,c 33.3 40.7 18.5 0.0 81.5b,c 18.5
20.7a,c 37.9 10.3 27.6 3.4 89.7c 10.3
6.8 34.4 19.6 37.6 1.6 91.3 8.7
6.9 30.3 19.7 42.3 0.9 91.2 8.8
Study year (%)
1988 1989 1990 1991 1992 1993
29.7 19.6 12.5 12.6 14.5 11.2
25.6a 12.3 11.0 14.0 22.1 14.9
37.9b 14.0 14.4 10.3 15.2 8.2
33.3c 11.1 11.1 11.1 18.5 14.8
25.9 13.8 17.2 20.7 10.3 12.1
27.3 17.7 13.5 10.6 14.8 16.1
30.7a 13.1 12.9 13.1 18.2 12.1
Insurance (%)
Low income Medicare Private 1 2 3 No Yes
0.8 4.1 95.1 1.5 12 86.5 42.6 57.4
6.5a 2.9 90.6 0.3c 9.7 89.9 54.2a 45.8
0.4c 2.9 96.7 1.2c 1.03 88.5 50.2b 49.8
0.0c 0.0 100.0 0c 3.7 96.3 63b 37
5.2a,c 0.0 94.8 0c 5.2 94.8 60.3b 39.7
2.6b,c 2.6 94.9 3.5b 11.6 84.9 47.9 52.1
3.8a 2.5 93.7 0.6b 9.3 90.1 53.6a 46.4
Enrolled 1 year (%)
Risk level (%) Prior mammorgram (%)
P ⬍ 0.001 (chi-square or Mann-Whitney test) compared to controls. P ⬍ 0.05 (chi-square or Mann-Whitney test) compared to controls. c 1 or 2 cells with expected count of ⬍5. GHC ⫽ Group Health Cooperative of Puget Sound; s.d. ⫽ standard deviation; Enrolled 1 year ⫽ enrolled for at least a year with breast cancer screening program after recommendation for mammography screening; Study year ⫽ the year that mammography recommendation was mailed to subject; Insurance ⫽ type of health insurance; Risk level ⫽ GHC Breast Cancer Screening Program risk level. a
b
Discussion To date, the pioneering studies on breast cancer screening by Asian-American women have been crosssectional and self-reported surveys.5,7,14,16 –22 These studies have contributed to the understanding of breast cancer screening by Asian Americans; however, by nature of their design, the internal validity and generalizability of the results may be limited. As more data emerge, the screening practices of Asian-American women present a picture that is increasingly more complex. This study is the first to report actual, not self-reported, prospective use of mammography screening by Asian-American women after a recommendation. It is also unique because financial barriers, which have been associated with low screening rates, were not a deterrent for participants of this study. Despite the lack of financial barriers, Asian-American women in this HMO were less likely to enroll into a breast cancer screening program. This finding may be associated with the level of English proficiency and literacy, because enrollment relied on the completion
of an English survey. It is also possible that other nonfinancial factors such as culture and logistic factors may contribute to this discrepancy. Although limited to a restricted spectrum of Asian ethnic groups, variations in mammogram participation were identified. In aggregate, Asian-American women had similar mammogram participation as controls; however, this analytic approach obscured the different screening patterns of the ethnic groups. Only when studied separately were the variations revealed among these Asian-American women. For Chinese-American women, our results provide new insights to previous reports of mammography utilization by this ethnic group. In a cross-sectional survey, Lee et al.20 found similar proportions of women who reported having ever had a mammogram in the 40 – 49 (69%) and 50 –74 (72%) age group. In our study, compared to non-Asians, older Chinese-American women with health insurance requiring no out-ofpocket cost were significantly less likely to participate in mammography screening when recommended to do Am J Prev Med 1999;17(1)
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Table 3. Mammogram participation with first BCSP recommendation Referent Controls (n ⫽ 2680) 1.00 Controls (n ⫽ 2680) 1.00 Controls (n ⫽ 2680) 1.00 Age group 40–49 (n ⫽ 1081) 1.00 50–64 (n ⫽ 1035) 1.00 ⱖ65 (n ⫽ 564) 1.00 Controls (n ⫽ 2680) 1.00 Controls (n ⫽ 2680) 1.00 Controls (n ⫽ 2680) 1.00
Crude odds ratio (95% CI)
Adjusted odds ratioa (95% CI)
Asian (n ⫽ 626) 0.93 (0.78, 1.11) Nonspecific Asian names (n ⫽ 305) 1.11 (0.87, 1.40) Chinese (n ⫽ 303) 0.86 (0.68, 1.09)
Asian (n ⫽ 626) 0.95 (0.80, 1.14) Nonspecific Asian names (n ⫽ 305) 1.13 (0.88, 1.44) Chineseb (n ⫽ 303) Age group 40–49 (n ⫽ 133) 1.23 (0.84, 1.80) 50–64 (n ⫽ 313) 0.66 (0.44, 0.97) ⱖ65 (n ⫽ 39) 0.43 (0.21, 0.90) Japanese (n ⫽ 241) 1.07 (0.82, 1.41) Vietnamese (n ⫽ 55) 1.63 (0.93, 2.88) Korean (n ⫽ 27) 0.43 (0.18, 1.02)
Japanese (n ⫽ 241) 1.01 (0.78, 1.32) Vietnamese (n ⫽ 55) 1.52 (0.88, 2.63) Korean (n ⫽ 27) 0.40 (0.17, 0.91)
a Adjusted for: age group, enrollment with BCSP for at least 1 year, years of enrollment with GHC, study year, BCSP risk level, first-degree relative with breast cancer, previous biopsy, and prior mammorgram. b Modeled separately by age group and adjusted for: enrollment with BCSP for at least 1 year, years of enrollment with GHC, study year, BCSP risk level, first-degree relative with breast cancer, previous biopsy, and prior mammogram. BCSP ⫽ Breast Cancer Screening Program; GHC ⫽ Group Health Cooperative to Puget Sound.
so. This finding merits additional evaluation because cultural issues may be involved and older women may be more likely to retain cultural barriers such as modesty.32,33 Logistic barriers, such as transportation and scheduling challenges, may also prevent them from getting to screening sites. Mammogram participation by Japanese-American women was similar to controls. This finding is consistent with two interpretations. First, Japanese-Americans migrated relatively earlier to the US. Second, there may be cultural differences between Chinese and JapaneseAmericans resulting in the different participation rates. Due to the small samples of Vietnamese and KoreanAmerican women, results for these groups are inconclusive and may be subject to misclassification bias. However, the results do support the need for additional studies. An important strength of this study is the documented enrollment and screening, which eliminates acquiescence bias (i.e., over-reporting of a behavior perceived as desirable).21Another strength is the prospective tracking of screening mammograms following a recommendation. Although this study is unique, our results may be limited in their generalizability. Women enrolled with GHC may not be representative of the general U.S., Asian-American, or other staff model HMO populations. Another limitation is the lack of ethnic identifiers in the database. Choi et al.30 demonstrated high spec60
ificity for Chinese surname lists; however, potential misclassification based on surnames persist.15 Although multiple sources were used to compile the surname lists, surnames may have been omitted resulting in some Asian-Americans classified as controls. Due to the low proportion of Asian-Americans in GHC, this misclassification would not appreciably bias the results and any given bias would be towards the null hypothesis. In addition, Asian-American women identified using surnames comprised 2.1% of the eligible GHC population. Because the study excluded Filipinos, Asian Indians, and other Southeast Asians (who make up 42% of Asian and Pacific Islanders in the Seattle Metropolitan area),34 our participants are representative of the Asian and Pacific Islanders in GHC. Potential misclassification due to interracial and interethnic marriages may also have resulted. The extent of such misclassification in GHC is unknown. The effect and magnitude of this bias, differential or nondifferential, remains to be determined. Nonspecific surnames were analyzed separately for mammogram participation. Although sub-optimal, this method provided some assurance that exclusion of women with nonspecific surnames from the aggregated Asian-American group did not affect the results significantly. However, this approach did not contribute to additional information for the individual ethnic groups. Reports in the literature indicate an association
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between self-reported screening, socioeconomic status, English proficiency, and the degree of acculturation among immigrant women.7,8,16 –21 Due to the lack of such data from BCSP, the impact of socioeconomic status and acculturation could not be adjusted for in the logistic models of this study. Although the study has several potential limitations, our results indicate that participation in mammography screening by Asian-American women may not necessarily be enhanced by removal of financial barriers alone. In order to enhance use of mammography screening by ethnic women, cancer prevention efforts need to address non-financial factors. This study supports the need to conduct surveillance of mammography screening for more reliable data on Asian-American women. Due to the diversity of Asian-Americans, surveillance must be conducted by ethnic groups rather than in aggregate. Additional studies are also needed to profile Asian-American women who under-utilize screening mammography and to develop culturally and linguistically meaningful resources to enhance their breast cancer screening activities. This research was supported in part by the American Cancer Society’s Primary Care Physician’s Career Development Award, a fellowship grant and EPC 97-010 from the Department of Veterans Affairs, Group Health Cooperative of Puget Sound, and NCI #UOICA 63731.
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