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© 2003 American Society for Clinical Oncology Asian Ethnicity–Related Differences in Gastric Cancer Presentation and Outcome Among Patients Treated at a Canadian Cancer Center
From the Division of Medical Oncology and Division of Epidemiology, British Columbia Cancer Agency; and Division of Gastroenterology, Department of Medicine, University of British Columbia, Vancouver, British Columbia, Canada; and Department of Epidemiology, Harvard School of Public Health, Boston, MA. Address reprint requests to Sharlene Gill, MD, MPH, Medical Oncology, Mayo Clinic, 200 First St SW, Rochester, MN 55905; email: gill.sharlene{at}mayo.edu.
Purpose: Differences in stage-stratified survival have been reported between Asian and Western populations with gastric cancer. This study examines differences in presentation and outcomes among Asian and non-Asian patients evaluated and treated at a Canadian institution. Patients and Methods: We reviewed 2,043 patients (159 Asians and 1,884 non-Asians) with gastric adenocarcinoma treated between 1978 and 1997. Overall survival was examined by the Kaplan-Meier method, and multivariable analysis by Cox proportional hazards was used to identify whether Asian ethnicity had independent prognostic significance for survival. Results: Median survival was 13.1 months for Asians and 11.1 months for non-Asians (P = .0016). Asian patients were younger and had a greater proportion of signet ring cell histology but were less likely to have proximal disease. Signet ring cell histology did not adversely affect survival. By multivariable analysis, proximal location, poor differentiation, and extent of disease were independently associated with worse survival. Survival was improved with curative resection, palliative resection, and palliative chemotherapy. Asian ethnicity was not independently associated with survival (hazard ratio, 0.89; 95% confidence interval, 0.74 to 1.08). Although a similar proportion of patients underwent curative resection, an interaction was observed between Asian ethnicity and efficacy of resection, with Asians achieving a greater benefit as compared with non-Asians even when adjusted for age and location. Conclusion: The disparity between Eastern and Western gastric cancer survival is not explained by the hypothesis of ethnicity-related differences in tumor biology. Although it is not an independent predictor of survival, Asian ethnicity is associated with distinct characteristics at presentation and more favorable outcomes after curative surgery.
DESPITE ITS declining incidence, gastric cancer remains an aggressive malignancy responsible for 12% of all cancer deaths worldwide.1 In the year 2001, 25,000 new cases of gastric cancer were diagnosed in the United States and Canada, with more than 15,000 related deaths.2,3 Survival outcomes differ considerably between Western and Asian population-based series, with overall 5-year survival rates of 10% to 15% in the United States and Canada2,4 as compared with 45% to 50% in Japan.5 These differences persist when stratified for stage of disease.6 More favorable outcomes have also been reported in studies from other Asian centers including Taiwan and Korea.7,8 Three hypotheses have been proposed to explain this observed disparity: stage migration, differences in treatment, and the different disease hypothesis, which implicates race-related differences in tumor biology, behavior, and host-tumor interactions.9 Attempts to further elucidate Asian versus Western survival differences with multi-institutional and multinational comparisons have been confounded by inherent inconsistencies in the approach to assessment, treatment, and follow-up. In a multivariable comparison of prognostic features between cohorts in Tokyo and Munich, persistent differences in survival were attributed to institution-related variability, which could not be accounted for in the analysis.10 Migrant studies have been used as well. A retrospective comparison of 312 Japanese patients from Honolulu with 3,176 Japanese patients in Tokyo demonstrated higher stage-stratified survival in the Tokyo cohort, thus suggesting that higher Asian survival rates may not be attributable to a different disease hypothesis.11 A contrasting viewpoint was offered by the authors of a population-based cancer registry study, which reported superior adjusted survival rates among Southern California patients of Asian descent.12 This analysis, however, included patients treated at more than 75 separate institutions, and possible heterogeneity in health care access and treatment was acknowledged but could not be controlled. The British Columbia Cancer Agency (BCCA) is the centralized cancer center for the Canadian province of British Columbia (BC), serving a population recognized to be ethnically diverse. Universal health insurance provides comprehensive medical access to all residents, and treatment policies are fairly standardized in accordance with provincial practice guidelines. A 20-year retrospective cohort study was therefore conducted to evaluate Asian ethnicity–related differences in gastric cancer characteristics and outcomes and to determine whether Asian ethnicity is an independent predictor of improved survival in patients with gastric cancer.
Study Design and Subjects All patients with histologic confirmation of invasive gastric adenocarcinoma treated at the BCCA from January 1, 1978, to December 31, 1997, were identified. Patients with in situ disease and gastric lymphoma, sarcoma, or neuroendocrine tumors were excluded. After institutional ethics approval, cases were identified using the BC Cancer Registry, and BCCA medical records were accessed to obtain supplemental clinical data. Abstracted data parameters included age at diagnosis, sex, place of birth, date of diagnosis, histopathology (World Health Organization classification), location (proximal including cardia, body including fundus, lesser curvature and greater curvature, and distal including antrum and pylorus), date of last follow-up, vital status, and, if deceased, date and cause of death. To minimize variability in the completeness of clinical and pathologic tumor-node-metastasis staging and to account for temporal differences in the American Joint Committee of Cancer staging definitions, extent of disease was categorized as localized (T1, T2, or T3 and node-negative), regional (T4 or node-positive), or distant (M1).12 Treatment was recorded as a categorical variable for surgery: curative intent, defined as resection with no residual tumor (R0), versus palliative intent (R1 or R2) versus no resection, and as a dichotomized variable for chemotherapy and radiotherapy (coded as ever received within a year of referral). Ethnicity was defined as Asian versus non-Asian as identified by patient report or, where required, through linkage of distinctive surnames using common surnames of BC residents born in China/Hong Kong/Taiwan, Japan, Korea, Vietnam, and the Philippines.
Statistical Analysis To answer the primary question of the independent prognostic effect of ethnicity, the association between Asian ethnicity and survival was evaluated by the Cox proportional hazards model15 with stepwise selection, using the Efron method of approximation for tied events. All variables with significant univariate associations to Asian ethnicity or overall survival were included as potential confounders. Proportional hazards assumptions were validated by graphical methods. A secondary analysis was performed to examine for a differential effect of treatment by ethnicity. Terms for an Asian-by-treatment interaction for surgery, chemotherapy, and radiation were included in the Cox model. P values were two-sided, with values less than .05 considered to be statistically significant. Adjusted hazard ratios (HRs) with accompanying 95% confidence intervals (CIs) were reported, and referent categories were selected as the lowest risk category for prognostic variables and the no-treatment categories for treatment-related variables.
Patient Characteristics Two thousand forty-three patients with gastric adenocarcinoma were identified. The total number of deaths observed was 1,899, with a mean follow-up of 18.5 months (7% censored with a mean follow-up of 8.2 years). One hundred fifty-nine (8%) of the 2,043 subjects were Asian, with the majority born in a foreign country (Table 1  ). Asians constituted a greater proportion of the total cohort in the second decade of the analysis (10.6% v 4.4%), consistent with increases in Asian migration observed during the study period. The characteristics of Asian and non-Asian patients are listed in Table 2. At presentation, Asians were younger (P < .0001), with a higher proportion of distal gastric cancers (P < .0001) and adenocarcinomas with a signet ring cell histology (P = .0006). No statistically significant difference was observed between the two groups for sex, histologic grade, and extent of disease at diagnosis. For the purposes of excluding small but potentially meaningful differences in T and N stage distributions, the strata of localized or regional extent were further examined. There were no significant ethnicity-related differences in the proportion of patients across subgroups for T stage (T1 to T4, P = .836) and N stage (N1 to N3, P = .453). Patients of Asian ethnicity were more likely to have received systemic chemotherapy (P = .0001). The proportion of patients treated with curative surgery, palliative surgery, and radiation therapy was similar in the two groups.
Survival For the entire cohort, median survival was 11.3 months, with a 5-year cancer specific survival rate of 14% and an overall survival rate of 12%. Five-year overall survival was 19.3% for Asians and 11.4% for non-Asians (P = .0016), with Asians experiencing a 2-month-longer median survival (Fig 1 ). As detailed in Table 3, additional patient variables significant for improved survival on univariate analysis were younger age, decade of diagnosis, distal site, limited extent of disease, and lower histologic grade. Signet ring cell histology did not confer a worse survival. For treatment-related variables, both curative resection and palliative resection were associated with an improvement in median survival when compared with no surgery. In a subgroup comparison stratified by ethnicity, differences in survival favored patients of Asian descent within several covariable strata (Table 3).
However, in a multivariable analysis adjusting for age, decade of diagnosis, location, histology, extent, grade, and treatment, Asian ethnicity was not independently associated with a survival benefit (HR, 0.89; 95% CI, 0.74 to 1.08). Only tumor location, grade, extent, surgery, and chemotherapy remained significant as predictors of overall survival (Table 4 ).
Effect of Treatment According to Ethnicity As previously reported, chemotherapy and surgery with both curative intent and palliative intent were observed to significantly improve survival. Recognizing that this study period preceded our currently recommended practice of adjuvant chemoradiation for gastric cancer, the use of chemotherapy in this population was largely limited to patients with nonresectable advanced disease and most commonly used a fluorouracil-based regimen. Palliative chemotherapy was associated with a significant improvement in median survival for both a regional and metastatic extent presentation (19.8 months v 13.5 months, P < .001 and 7.0 months v 4.2 months, P < .001, respectively). Radiation therapy was not statistically associated with survival. No significant interaction was observed between Asian ethnicity and chemotherapy effect or radiotherapy effect.
A differential effect of the survival benefit from resection with curative intent was observed to favor Asians versus non-Asians. As reflected in Fig 2
This single-institution review describes the effect of Asian ethnicity in gastric cancer while controlling for previous disparities in classification of stage of disease and heterogeneity of treatment. The 5-year survival rate of 12% is well within the range of published survival estimates for patients treated at a North American institution.4 At diagnosis, Asian patients were younger than their non-Asian counterparts, with a lower proportion of proximal tumors, consistent with findings from previous studies of ethnicity-related differences in gastric cancer.12,16 An increasing proximal shift has been recognized in the United States and Europe since the 1970s.17,18 A similar pattern has not yet been observed in Asia.19,20 Gastric cardia tumors are believed to have a distinct etiology from distal tumors and may share a mode of carcinogenesis more in common with tumors of the gastroesophageal junction and lower esophagus. Although lower esophageal tumors were not included in this review, tumors of the gastroesophageal junction are typically recorded by the cancer registry as gastric cardia tumors and may contribute to the proximal predominance among non-Asians. In our analysis, as has been reported previously,12,21 proximal tumors were associated with a worse survival when compared with distal tumors. An ethnicity-related difference in histology was also observed with signet ring cell cancers more common among Asians. Typically regarded as an aggressive histologic subtype,22 studies of the prognostic significance of signet ring cell histology have been conflicting.23–25 In our analysis, this histology did not adversely influence survival. Patients of Asian descent were observed to receive chemotherapy more often than non-Asians. This is likely a reflection of their younger age, which is an important factor when selecting patients for palliative chemotherapy.26 The use of chemotherapy was a significant predictor of survival by multivariable analysis and was associated with a 3- to 6-month improvement in survival for patients with advanced disease. When compared with no surgery, palliative resection was also associated with a survival benefit. Although conclusions regarding the benefits of palliative chemotherapy or resection cannot be drawn from nonrandomized data, it is notable that our results are similar to results from randomized trials of chemotherapy versus best supportive care27–30 and findings from previous nonrandomized studies of palliative resection.31–33 Our center’s experience further supports the use of palliative chemotherapy and surgical interventions in appropriately selected patients with advanced disease. No ethnicity-related differences were observed in the proportion of patients with resectable disease, with approximately 40% of patients in both groups treated by surgery with curative intent, which is again consistent with the 37% to 48% resectability rates reported in the literature.34 Surgery remains the primary treatment modality for gastric cancer. Although complete removal of N1 and N2 lymph nodes (D2 resection) is the standard gastrectomy procedure in Japan, the Western experience with D2 resections has been contentious. When compared with a D1 resection (removal of N1 lymph nodes) in two Western randomized trials, D2 resection was associated with increased operative morbidity and mortality and no improvement in survival.35,36 In practice, less than 10% of patients in the United States have a D2 lymphadenectomy, with the majority undergoing either a D0 (55% to 60%) or D1 dissection (35% to 40%).21,37 Similar to the United States experience, extended lymphadenectomy is not the standard of practice in BC.38 Perhaps one of the most interesting findings in this analysis was the observation of an improved survival for Asian patients after a complete resection among patients treated by the same surgical community. The median survival of 24 months observed in non-Asians after resection is similar to the 27-month survival reported in the surgery-alone arm of the recent Southwest Oncology Group adjuvant chemoradiation trial,37 but less than the 41 months observed among Asians in our cohort. Although all patients did not have surgery at the same institution and complete uniformity of surgical practice cannot be guaranteed, we believe that these differences cannot be wholly ascribed to treatment variability. Patients were treated by a similar group of surgeons, and it is improbable that surgeons were biased to pursue more extensive surgery for their Asian patients as compared with their non-Asian patients. In a recent small series, ethnicity-related differences in survival after gastrectomy were largely attributed to differences in tumor location.39 In addition to a higher proportion of distal tumors, Asian patients in our cohort were also younger. However, evidence of a differential efficacy for curative resection persisted when these factors were adjusted for in a multivariable analysis. It is possible that this survival difference may be accounted for by potential residual confounders not included in our analysis. One such ethnicity-related factor that may affect surgical outcomes is body mass index (BMI). Asian populations, including migrants, commonly have a lower BMI when compared with Caucasians,40,41 and a lower BMI has been implicated as a favorable predictor for both decreased postoperative morbidity and improved disease-free survival after gastric cancer surgery.42,43 As definitive conclusions cannot be drawn from analyses of smaller subgroups, additional studies would be required to validate this hypothesis. The primary goal of this study was to determine the prognostic effect of Asian ethnicity in gastric cancer. An ethnicity-related difference in tumor biology has been suggested as an explanation of superior East Asian survival rates.9 To date, attempts to further advance this hypothesis at a molecular level have been inconclusive. In a comparison of gastric tumors from British and Japanese patients, no differences were identified in the expression of c-erb-B2 or p53.44,45 More recently, the frequency of microsatellite instability (MSI) in 18 gastrectomy specimens from Japan was compared with 20 specimens from American patients of European descent.46 Although a higher frequency of MSI was observed in the Japanese specimens, this difference was not significant and, moreover, none of the Japanese specimens met criteria for a high frequency of MSI instability, the phenotype associated with more favorable outcomes.47 From our analysis, Asian ethnicity was univariately associated with improved survival. However, it was not observed to be an independent predictor of survival when confounding prognostic factors, particularly age and site, were adjusted for in a multivariable analysis. Limitations of this retrospective analysis should be recognized. First, when not available by patient report, the determination of Asian ethnicity required identification using distinctive surnames, which raises the possibility of random misclassification with an associated potential bias of the HR toward the null value. It is important to note that surname linkage is an accepted methodology for ascertainment of ethnicity48–50 and that we were blinded to patient outcomes at the time of ethnicity classification. Second, the preponderance of published data supporting improved survival among Asians comes from Japanese study populations. Only 24% of patients in our Asian cohort were Japanese, with the majority being of Chinese descent. The potential for heterogeneous disease behavior among Pacific Islander and Southeast Asian ethnic subgroups cannot be entirely excluded. Recognizing that different disease patterns have been identified in India compared with Japan, patients from the Indian subcontinent were not included in our Asian subset.51 It is also somewhat reassuring that observed disease characteristics among Asians, including predominance of distal site, are consistent with the Japanese experience and likely reflect the similar epidemiology of gastric cancer among Chinese and Japanese populations.52 Finally, was this series adequately powered for our primary analysis to exclude a meaningful improvement in survival for Asian patients? In the multivariable analysis, the adjusted HR for Asian ethnicity was 0.89, with a 95% CI of 0.74 to 1.08. Thus the true estimate of effect may include an HR of less than 1.0. However, even if we assume the lower limit of this CI to be the true effect, a 26% proportional reduction in mortality would only improve a 5-year survival estimate of 12% to 20%. This would be insufficient to account for the disparity with Asian survival rates, which remain three-fold greater than North American rates. Alternate explanations, particularly differences in diagnosis and treatment, should continue to be pursued. In conclusion, distinct characteristics are recognized among Asian patients presenting with gastric cancer. In the clinical setting, patients with advanced gastric cancer do seem to benefit from palliative chemotherapy and surgery, regardless of ethnic background. Although Asian ethnicity was not observed to be an independent predictor of survival, it was associated with a superior survival after curative resection when compared in a multivariable analysis with that of non-Asians. This finding warrants ongoing study, including an evaluation of the effect of BMI for patients with early-stage gastric cancer.
We thank Dr G. Hislop at Cancer Control Research, BCCA, for his input with ethnicity identification. We also thank Drs J. Telford and S. Mohanty at the Harvard School of Public Health for their assistance with data analysis.
S.G. is currently funded by a fellowship from the Canadian Association of Medical Oncologists and the Canadian Institute of Health Research. Presented at the Thirty-Eighth Annual Meeting of the American Society of Clinical Oncology, May 16–19, 2002, Orlando, FL.
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Copyright © 2003 by the American Society of Clinical Oncology, Online ISSN: 1527-7755. Print ISSN: 0732-183X
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ABSTRACT
INTRODUCTION
2 statistic for categorical variables and the Student’s t test for continuous variables. Median survival and 5-year survival were presented according to the Kaplan-Meier method
