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Article first published online: 20 FEB 2002
Copyright © 2002 American Cancer Society
Volume 94, Issue 4, pages 1175–1182, 15 February 2002
How to Cite
Lin, S. S., Clarke, C. A., Prehn, A. W., Glaser, S. L., West, D. W. and O'Malley, C. D. (2002), Survival differences among Asian subpopulations in the United States after prostate, colorectal, breast, and cervical carcinomas . Cancer, 94: 1175–1182. doi: 10.1002/cncr.10319
A portion of the cancer incidence and survival data was collected by the Northern California Cancer Center under contract N01-CN-65107 with the National Cancer Institute, National Institutes of Health, and with support of the California Cancer Registry, a project of the Cancer Surveillance Section, California Department of Health Services, under subcontract 050M-8701/8-S1522 with the Public Health Institute.
The content of this publication does not necessarily reflect the views or policies of the U.S. Department of Health and Human Services or the California Department of Health Services, nor does mention of trade names, commercial products, or organizations suggest endorsement by the U.S. Government or the State of California.
- Issue published online: 20 FEB 2002
- Article first published online: 20 FEB 2002
- Manuscript Accepted: 15 OCT 2001
- Manuscript Revised: 12 OCT 2001
- Manuscript Received: 13 JUN 2001
Information is limited for Asian subgroups regarding survival after diagnosis of the common cancers amenable to routine screening. The authors examined survival after carcinomas of the prostate, colon/rectum, breast, and cervix separately for Chinese, Japanese, Filipinos, and non-Hispanic whites in the United States.
Using data from the Surveillance, Epidemiology, and End Results program, the authors compared the distributions of stage at diagnosis and computed 5-year cause specific survival probabilities, overall and by stage of disease, for cancer patients whose diagnosis was in 1988–1994 and who were observed through 1997.
Among males, Filipinos were more likely to be diagnosed with advanced stage colorectal and prostate carcinomas than other Asians and non-Hispanic whites; they also experienced worse survival after these cancers. This survival deficit occurred across all stages of colorectal carcinoma and remained apparent within distant stage prostate carcinoma. Among females, Chinese were less likely to receive diagnoses of early stage colorectal carcinoma than Japanese and Filipinas. In addition, their survival was consistently lower across more advanced stages of disease. Chinese also experienced somewhat worse survival after diagnosis of early stage cervical carcinoma. Japanese were more likely to be diagnosed with early stage carcinomas but also tended to experience better survival after prostate, colorectal, and breast carcinomas regardless of stage.
Chinese, Japanese, and Filipinos experienced unequal survival after these screenable carcinomas, indicating that certain groups may benefit from more aggressive screening efforts. The heterogeneity of cancer outcomes observed within the community classified as Asian reinforces the need for cancer statistics to be reported for disaggregated subgroups. Cancer 2002;94:1175–82. © 2002 American Cancer Society.
Carcinomas amenable to routine screening (prostate, colon/rectum, breast, and cervix) should be characterized by earlier stage diagnosis and more favorable prognosis with an associated survival benefit.1 However, to the extent that benefits have been identified, survival has been shown to vary among racial/ethnic groups,2–7 indicating a potentially troubling disparity in access to screening resources. To date, studies of racial/ethnic differences in cancer survival have focused on black and white populations,7–17 and recent research has included Hispanics and American Indians.18–24 However, information on cancer survival in Asian and Pacific Islander (API) subgroups remains limited, even as these populations are increasing in the United States.25, 26 The few publications involving specific API subgroups have noted relative survival after prostate, breast, colon, and rectum carcinomas to be higher among Japanese but lower among Filipinos than other racial/ethnic groups.2–6, 27, 28 However, most of these reports2, 4–6 did not account for possible confounding by stage of disease at diagnosis. Moreover, all of the reports, including those providing stage specific information,3, 27, 28 have relied on potentially biased relative survival rates based on expected rates that were produced from U.S. life table data not specific to these API subgroups.29 It is recommended that if reliable information on cause of death is available, it should be used to compute survival.30
Data on survival for specific racial/ethnic groups are essential for clinicians and public health researchers and practitioners to identify populations who may not be receiving adequate screening or treatment.31 Survival statistics by race/ethnicity also pave the road for further research regarding sociodemographic or clinical factors responsible for disparities in survival. To provide such information for the major screenable cancers in the three largest U.S. Asian subgroups with attention to the limitations of the earlier publications, we computed population-based cause specific survival probabilities, which are more accurate than relative survival rates, by stage for carcinomas of the prostate, colon/rectum, breast, and cervix for Chinese, Japanese, Filipinos, and non-Hispanic whites. We also compared the stage at diagnosis among the racial/ethnic groups because this distribution indicates the efficacy of screening in a given group and examined stage specific survival because stage is a strong predictor of survival after cancer diagnosis.
Cancer survival data were obtained from the population-based Surveillance, Epidemiology, and End Results (SEER) program, which covers the states of Connecticut, Hawaii, Iowa, New Mexico and Utah, and the metropolitan areas of Atlanta, Detroit, San Francisco/Oakland, Seattle/Puget Sound, San Jose/Monterey, and Los Angeles.7, 32, 33 The latter two registries joined the SEER program in 1992. Together, all SEER regions include approximately 43% of the U.S. Chinese population, 49% of U.S. Filipinos, and 60% of U.S. Japanese.7, 32–34
Cases for analysis were Chinese, Japanese, Filipinos, and non-Hispanic whites (hereafter called “whites”) living in a SEER catchment area when diagnosed with an invasive tumor of the breast, prostate, cervix, colon, or rectum during the period January 1, 1988 through December 31, 1994. This time frame was chosen because the staging scheme based on the American Joint Committee on Cancer TNM system (AJCC staging) for breast, cervical, and colorectal carcinomas was used consistently by SEER during this period.35, 36 For breast carcinomas, only female patients were considered. For all cancer sites, we excluded second and later malignancies, tumors not confirmed microscopically, and those diagnosed at death or during autopsy; together, the excluded cases accounted for between 4% (cervix) and 20% (colon/rectum) of all study subjects. For colorectal carcinoma, 90% of the excluded diagnoses were not first primary malignancies, partially reflecting SEER rules that define tumors arising in each segment of the colon and rectum as separate diagnoses rather than recurrences (30% of the 90% arose from first primaries of the colon or rectum). Cases with unknown causes of death (< 2%) were excluded from cause specific survival analyses. The final study population is shown in Table 1.
|Cancer site||Race/ethnicity||No. of patientsa||No. of cause specific deaths (%)b||SEER historic stage at diagnosis (%)c|
|SEER-modified AJCC stage at diagnosis (%)c|
|Colon/rectum (male)d||Chinese||737||226 (31)||26||30||23||16||5|
|Colon/rectum (female)d||Chinese||635||222 (35)||22||30||27||14||8|
|Breast (female)d||Chinese||1219||176 (14)||41||41||7||4||8|
Each regional SEER registry conducts active and passive follow-up of cancer patients for vital status using linkages with state and national death indices, Health Care Financing Administration files, driver's license registration files, voter registration files, Social Security Administration files, national credit agency records, and other databases, as well as contact with patients, hospitals and physicians' offices. The SEER program requires that at least 95% of patients have a report of vital status within the 18 months before data release.7, 16 Patients in this analysis were followed for vital status through December 31, 1997.
As death due to the cancer of interest was the end point for these analyses, underlying cause of death was obtained from registry data, which were abstracted from death certificates, and was assigned using International Classification of Disease, 9th revision codes37 185.0–185.9 for prostate, 153.0–154.1 for colon/rectum, 174.0–175.9 for breast, and 180.0–180.9 for cervix.
Stage of Disease
For colorectal, breast, and cervical carcinomas, tumor stage at diagnosis was defined using the SEER-modified AJCC staging scheme, 3rd edition (1988+),38 which allows for a more detailed analysis than the SEER historic staging scheme (local, regional, distant). Both staging schemes are either obtained directly from the patients' records or defined using the detailed extent of disease information collected by SEER, which describes tumor size, clinical extension to other organs, and lymph node status.36, 38 The relations between AJCC stage and SEER historic stage, and their TNM equivalents, are presented in Table 2 to facilitate comparison to other reports. For prostate carcinoma, data are presented using SEER historic stage, because AJCC staging is unreliable due to coding changes over time; in addition, a large proportion of cases (> 40%) were not staged using the AJCC scheme because of unknown extent of disease information (data not shown).
|SEER-modified AJCC stage||SEER historic stage||TNM equivalentc|
|0||In situ, local||Tis, N0, M0|
|I||Local||T1–T2, N0, M0|
|II||Local, regional, distant||T3–T4, N0, M0|
|III||Regional, distant||any T, N1–N2, M0|
|IV||Distant||any T, any N, M1|
|0||In situ, local||Tis, N0, M0|
|I||Local, regional||T1, N0, M0|
|II||Local, regional||T0–T2, N0–N1, M0 T3, N0, M0|
|III||Regional, distant||T0–T2, N2, M0 T3, N1–N2, M0 T4, any N, M0 any T, N3, M0|
|IV||Distant||any T, any N, M1|
|0||In situ||Tis, N0, M0|
|I||Local, regional||T1, N0, M0|
|II||Regional||T2, N0, M0|
|III||Regional||T3, any N, M0 T1–T2, N1, M0|
|IV||Regional, distant||T4, any N, M0 any T, any N, M1|
The Mantel–Haenszel chi-square test39 was used to determine statistical significance (P values < 0.05) of differences in stage distributions across racial/ethnic groups. Five-year cause specific survival probabilities, which represent the probabilities of not dying of the cancers of interest for 5 years or more after diagnosis, were computed via the actuarial method using the SAS lifetest procedure with 1-year intervals (survival probabilities computed using 6-month intervals did not differ from those computed using 1-year intervals).40 Ninety-five percent confidence intervals were calculated to determine the precision of each survival estimate. However, because these intervals were not adjusted for multiple comparisons, we caution against using them to assess statistical significance between groups. In the subsequent sections, we will highlight racial/ethnic survival differences exceeding 5%.
Distributions of study subjects by stage are presented by race/ethnicity in Table 1. Among males with prostate and colorectal carcinomas, Filipinos were significantly less likely than other racial/ethnic groups to receive a diagnosis of localized or Stage I disease. Among females with a colorectal carcinoma diagnosis, the proportions of Stage I disease were lowest among Chinese and whites. For breast and cervical carcinomas, Chinese and Filipinas were significantly less likely than Japanese and whites to receive a diagnosis of Stage I disease.
Cause Specific Deaths
Table 1 also shows the number of cause specific deaths by race/ethnicity. Among males, Filipinos had the highest proportion of cancer deaths. Among females with colorectal carcinoma, Chinese and whites had higher proportions of deaths than Japanese and Filipinas. For breast carcinoma, Japanese females had a lower proportion of deaths than the other racial/ethnic groups, whereas for cervical carcinoma, they experienced a slightly higher proportion of cancer deaths.
Table 3 presents the 5-year cause specific survival probabilities and 95% confidence intervals by cancer site and race/ethnicity for all stages combined. For all groups, survival probabilities generally were high for prostate and breast carcinoma but lower for colorectal carcinoma. Among males, Filipinos had poorer survival after prostate and colorectal carcinomas than the other racial/ethnic groups, particularly Chinese and Japanese. Among females, Chinese and whites had poorer 5-year survival after colorectal carcinoma than Japanese or Filipinas. Japanese females also had better survival after breast carcinoma and slightly worse survival after cervical carcinoma, although these latter survival probabilities were based on few patients.
|Cancer site||Race/ethnicity||Survival (95% CI)|
Stage specific 5-year survival probabilities and 95% confidence intervals are presented in Table 4. In general, survival was relatively favorable for all racial/ethnic groups diagnosed with localized or Stage I disease. Among males with prostate carcinoma diagnosed at local or regional stages, survival was similar for all racial/ethnic groups; however, within distant stage disease, survival was poorer among Filipinos than Chinese and Japanese, and poorest among whites. For colorectal carcinoma, the relatively worse survival observed for Filipino males (Table 3) persisted across the stages for which we had adequate data but appeared to be more marked at Stages II and III. Survival after distant stage prostate and colorectal carcinomas was notably higher among Japanese males than for any of the other racial/ethnic groups.
|Cancer site||Race/ethnicity||SEER historic stage at diagnosis (95% CI)|
|Prostate||Chinese||97.0 (95.5–98.6)||93.6 (89.3–97.9)||51.3 (40.7–62.0)||96.2 (92.0–100.0)|
|Japanese||96.5 (95.4–97.7)||91.1 (88.0–94.1)||59.7 (51.8–67.6)||87.2 (80.9–93.4)|
|Filipino||95.1 (93.3–96.9)||89.7 (85.6–93.8)||45.1 (37.0–53.3)||83.3 (76.8–89.8)|
|Whiteb||95.4 (95.2–95.6)||91.5 (91.1–91.9)||35.9 (34.6–37.2)||87.1 (86.4–87.8)|
|SEER-modified AJCC stage at diagnosis|
|Colon/rectum (male)||Chinese||94.6 (90.7–98.5)||79.8 (73.8–85.7)||57.2 (49.0–65.4)||—||64.9 (45.9–83.9)|
|Japanese||92.3 (89.2–95.5)||83.5 (78.9–88.2)||64.5 (58.5–70.6)||—||68.8 (52.3–85.4)|
|Filipino||89.2 (83.0–95.4)||74.4 (65.9–82.9)||46.0 (37.2–54.9)||—||—|
|White||92.1 (91.5–92.8)||78.0 (77.1–78.9)||55.5 (54.2–56.7)||6.3 (5.4–7.1)||52.4 (49.2–55.6)|
|Colon/rectum (female)||Chinese||93.1 (88.7–97.5)||72.1 (65.1–79.1)||58.7 (50.6–66.8)||—||—|
|Japanese||94.7 (91.6–97.8)||82.7 (77.7–87.7)||63.7 (57.2–70.2)||—||—|
|Filipina||93.9 (88.7–99.1)||87.1 (79.4–94.8)||65.9 (55.8–76.0)||—||—|
|White||92.7 (92.0–93.3)||78.5 (77.6–79.4)||56.7 (55.4–58.0)||8.4 (7.5–9.3)||42.9 (39.7–46.0)|
|Breast (female)||Chinese||96.5 (94.7–98.4)||85.9 (82.6–89.3)||55.5 (43.1–67.9)||—||83.3 (75.2–91.4)|
|Japanese||97.9 (96.9–98.9)||90.5 (88.0–93.0)||62.4 (49.2–75.7)||36.0 (23.8–48.1)||93.2 (88.8–97.5)|
|Filipina||97.3 (95.6–99.0)||85.8 (82.8–88.8)||61.9 (49.2–74.6)||—||86.3 (78.7–93.9)|
|White||96.9 (96.7–97.1)||85.2 (84.7–85.6)||59.3 (57.6–60.9)||22.3 (20.8–23.9)||85.8 (84.9–86.8)|
|Cervix||Chinese||86.0 (77.9–94.2)||65.9 (47.2–84.5)||—||—||—|
|White||93.7 (92.8–94.5)||64.3 (60.5–68.1)||51.9 (48.1–55.7)||21.7 (17.4–26.1)||72.3 (67.1–77.6)|
Among females with colorectal carcinoma, survival after Stage II or III disease was worse among Chinese and whites but slightly better among Filipinas. For Stage II breast carcinoma, all groups had slightly worse survival than Japanese; Chinese also had worse survival after Stage III disease. For cervical carcinoma, Chinese females experienced poorer survival after Stage I disease, although that was based on few subjects.
This descriptive study presents population-based breast, prostate, colorectal, and cervical carcinoma survival statistics separately for Chinese, Japanese, and Filipino populations with attention to cause-of-death information and stage at diagnosis based on consistent staging schemes. We have found notable differences in the stage distribution and survival after four screenable cancers among these three large U.S. Asian populations.
Filipino males experienced worse survival than did Chinese and Japanese for both prostate and colorectal carcinoma, particularly for distant stage disease. The finding that their survival was more comparable after early stage disease supports a need for enhanced efforts targeting screening in this group. However, interpretation of survival differences for early stage prostate cancer is unclear because there is currently no clear evidence that the most widely used screening modality for prostate carcinoma, prostate specific antigen, improves survival after prostate carcinoma.
The data presented here for colorectal and breast carcinomas among Asian females indicate that Chinese may benefit from more aggressive screening for colorectal carcinoma, and both Chinese and Filipinas may benefit from additional screening for breast carcinoma. Of note, Chinese females experienced somewhat worse survival after diagnosis of early stage cervical carcinoma. Although there have been studies addressing cervical carcinoma early detection among Chinese women,41, 42 to date, studies of cervical carcinoma survival in Chinese women have only examined the role of human papillomavirus (HPV); these studies have shown no association of HPV with survival.43, 44
The relatively favorable survival after prostate, colorectal, and breast carcinomas among Japanese is consistent with earlier stage diagnosis. However, the better survival among Japanese within more advanced stage disease also suggests less aggressive tumors or differential treatment. Further research is needed to understand the relation between cancer screening, treatment, and survival in specific racial/ethnic subgroups.
In a prior analysis of breast carcinoma diagnosed in 1985–1991 in the San Francisco Bay Area, we showed that Filipinas experienced worse 5-year relative survival (77%) than did Chinese (85%) or Japanese (86%) women, primarily because of differences for local stage disease.27 Since that time, survival after breast carcinoma has improved for Japanese and Filipinas, but not for Chinese women (data not shown),29 such that in the current data, survival was highest for Japanese and similar among Chinese and Filipinas. Future analysis might address the reasons for the lack of improvement in survival among Chinese women.
We found that racial/ethnic variations in survival after these common screenable carcinomas were partially explained by differences in stage at diagnosis, although considerable survival differences occurred in the advanced stages of disease. Factors in addition to stage, such as age, are likely to influence differences in survival among the racial/ethnic groups. Younger age is associated with worse stage specific survival after breast or prostate carcinoma, whereas older age leads to poor stage specific survival after cervical and colorectal carcinoma.29 Although the ethnic patterns in survival noted here could reflect differences in distributions of age at diagnosis among the study groups, considerable evidence indicates that age is unlikely to explain all of our observed ethnic survival patterns. Among males with prostate carcinoma, Filipinos tended to be older at diagnosis than Japanese and Chinese, whereas for males with colorectal carcinoma, Filipinos were younger at diagnosis than Japanese;29 these age patterns are not consistent with what would be expected if age explained the observed survival patterns. Among females with breast carcinoma, Japanese were older at diagnosis than Chinese or Filipinas; however, the survival patterns among the three Asian subgroups were similar across age (data not shown),29 suggesting that age would not explain the better overall survival among Japanese. In addition, the survival deficits for Filipino men and Chinese women with distant stage disease may be attributable to differing degrees of tumor aggressiveness, extent of disease, and responsiveness to treatment within the staging categories.45
The survival statistics presented in this report point to the importance of identifying specific sociodemographic and clinical factors contributing to the observed racial/ethnic patterns in survival among the Asian subgroups. Modification of factors such as lack of access to regular screening, lifestyle practices, or inadequate treatment could translate into meaningful public health and clinical interventions. For example, a recent report on breast and cervical carcinoma screening showed that whereas 21% of U.S. Japanese women older than age 40 years never had a mammogram, this proportion was 26–28% among Chinese and Filipino women.46 Studies of API women have shown that lack of regular screening for breast and cervical carcinoma is associated with having no health insurance coverage, concerns over cost, embarrassment, perceived inconvenience and lack of time, traditional beliefs regarding health and disease, as well as beliefs that screening is not necessary in the absence of symptoms.41, 42, 46–52 Evidence also suggests that the lower breast and cervical carcinoma screening rates among API women are partly attributable to physicians not recommending or performing these routine tests.53
Sociodemographic, lifestyle, and other health-related behaviors and beliefs influencing cancer survival show intergenerational differences within the API groups.41, 42, 49–51, 53 The three U.S. Asian groups studied here differ in geographic and cultural origins, and in immigration patterns and degree of acculturation. The number of Japanese immigrants to the U.S. was highest between 1900 and 1910, whereas large waves of Chinese and Filipinos immigrants entered the U.S. after the 1965 Immigration and Naturalization Act.54, 55 In 1992, greater than 70% of Japanese in the U.S. were U.S. born, whereas only 37% of U.S. Chinese and 36% of U.S. Filipinos were U.S. born.54 Because previous research has identified that certain traditional beliefs may be barriers to receiving timely screening,41, 42, 46–52 the longer residence and the higher degree of acculturation of U.S. Japanese54 may contribute to their better survival patterns. Further research into the relation of the immigration and acculturation experiences to cancer survival is needed to identify specific subgroups (e.g., foreign born) at increased risk of dying from screenable cancers. Because SEER data on nativity are not complete among the Asian subgroups, we did not include this information in our analysis.
Our results may be affected to some extent by racial/ethnic misclassification in the SEER database56–59; for example, we found that San Francisco–Oakland area cancer patients misclassified by the SEER registry as Vietnamese (36%) identified themselves as Chinese.59 Similar problems may affect other API subgroups, but to our knowledge, there have been no other published studies of misclassification in these populations. Our results also may be affected by misclassification of cause-of-death information on death certificates.60 However, racial/ethnic survival patterns remained the same regardless of whether cause specific deaths, all cancer deaths, or all deaths were considered as the outcome (data not shown), indicating that misclassification, if any, is likely random across the racial/ethnic groups shown here.
The relative paucity of research on cancer survival in U.S. Asian subgroups may reflect the perception that cancer survival among Asians is favorable compared with that of other racial/ethnic groups.24 However, our study demonstrates that the aggregation of Asian subgroups obscures survival disparities in specific groups. Reporting survival statistics for APIs as a group would have masked the survival deficit for Filipino men with prostate and colorectal carcinomas and for Chinese women with colorectal carcinoma. Recently, the Institute of Medicine released a request for U.S. cancer data on minority groups, particularly disaggregated API groups.61 Our findings support the importance of reporting and interpreting cancer statistics and results from analytic studies for specific API subgroups. In addition, they show that aggregating health data across racial/ethnic populations can produce study results and statistics that are not meaningful or applicable in a public health or clinical setting.
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