Abstract
Effects of socioeconomic status on the long-term survival of 808 women with node-negative breast cancer in Canada and the United States were observed. Ontario and California samples diagnosed between 1988 and 1990 were followed until 2006. Socioeconomic data were taken from population censuses. Compared with their California counterparts, residents of low-income urban areas in Ontario experienced a significant 15-year survival advantage (RR = 1.66 [95% CI: 1.00, 2.76]). In these and other vulnerable, lower-middle- to working-class neighborhoods, significantly more Ontario residents gained access to adjuvant radiation therapy (RR = 1.75 [1.21, 2.53]) which seemed associated with better long-term survival (RR = 1.36 [0.99, 1.86]). This stage-adjusted, historical cohort analysis suggests much greater cancer care equity in Canada than in the United States.
Keywords: adjuvant treatment, California, Canada, health insurance, long-term survival, node-negative breast cancer, Ontario, radiation therapy, socioeconomic factors, United States
Studies of breast cancer survival in diverse Canadian and United States metropolitan areas have tested a health insurance hypothesis and consistently found advantaged survival among Canadians in vulnerable low-income neighborhoods (1–4). None of those studies accounted for stage of disease at diagnosis. This one did. Recent staged analyses observed Canadian advantages in low-income Ontario places versus similar California places on 5-year node-positive breast cancer survival (5). Such Canadian women gained greater access to adjuvant chemo- and radio-therapies (6). Long-term investigations in this field are rare (7), and no previous international comparative study followed patients for more than 5 years. This Ontario-California cohort did. Consistent with a health insurance theory, we hypothesized that significantly more low-income Canadian women with node-negative breast cancer would enjoy long-term survival.
METHODS
A historical cohort of 1,802 women diagnosed between 1988 and 1990 with nonmetastasized, invasive breast cancer in Ontario and California were randomly selected. No significant difference on long-term survival was observed for node-positive disease or for node-negative disease in rural places. So, this study explored its node-negative-specific hypothesis in urban places. Ontario and California cancer registries, respectively, selected 366 and 442 node-negative cases from large (Toronto and San Francisco) and small cities (Windsor and Modesto) (8–10). Census tract-based socioeconomic status measures (“low-income” in Canada and US “poverty”) have defined income deciles (11,12). They aggregated similar low-income areas in both countries. The lowest income deciles were defined in US dollars as follows: Ontario—median low-income household prevalence (34.6%, $20,260) and California—poor (28.7%, $19,190) (13). Socioeconomically vulnerable areas (5th, 7th, and 10th lowest deciles) that demonstrated the poorest US survival were aggregated and defined as follows: Ontario (16.0%, $33,250) and California (10.0%, $30,060). They were similar to previously studied decile areas in Hawaii that were more predominantly represented not only by the poor but also by the near poor (up to 200% of the federal poverty criterion) (2,12). Disease stage and treatments were reliably abstracted from patient charts (average κ coefficient 0.95) (14–16). Cohorts followed until 2006 were able to detect 20% survival differences (α = 0.05 and 1−β = Power = 0.80) (17). All-cause (15-year) survival was used because, although survival is highly accurate in these registries, the underlying cause of death is not (8). Survival rate ratios (RR) were age-adjusted and confidence intervals (95% CI) were based on the Mantel–Haenszel chi-squared test (18,19). Methodological details have been reported (5).
RESULTS
Long-term node-negative breast cancer survival was not associated with income in Ontario, but it was in California. As hypothesized for the lowest income places, significantly advantaged Canadian survival was observed (RR = 1.66), and Canadian women in vulnerable areas were similarly advantaged (RR = 1.35 [95% CI: 1.01, 1.81], not shown in Table 1). These findings did not differ by place size. Analyses among vulnerable samples found that women in such Ontario areas were more likely to have received a lumpectomy than were their counterparts in California (RR = 1.86 [1.37, 2.52]), but the lumpectomy-mastectomy difference was not itself associated with long-term survival. Potentially vulnerable women in Ontario were also more likely to have received adjuvant radiation therapy (age-adjusted rates of 0.427 versus 0.244, RR = 1.75 [1.21, 2.53]) which did seem associated with better long-term survival (RR = 1.36 [0.99, 1.86]). There were no significant between-country difference on tumor size, receipt of adjuvant chemotherapy or on wait-times for initial surgical or adjuvant treatments.
Table 1.
Income group | Ontario |
California |
Ontario versus California |
|||||||
---|---|---|---|---|---|---|---|---|---|---|
n | Rate1 | RR2 | 95% CI3 | n | Rate1 | RR2 | 95% CI3 | RR | 95% CI3 | |
Highest | 43 | 0.522 | 1.00 | — | 44 | 0.570 | 1.00 | — | 0.92 | 0.67, 1.26 |
31 | 0.461 | 0.88 | 0.54, 1.42 | 50 | 0.569 | 1.00 | 0.96, 1.04 | 0.81 | 0.56, 1.16 | |
42 | 0.527 | 1.01 | 0.88, 1.16 | 47 | 0.482 | 0.85 | 0.56, 1.30 | 1.09 | 0.67, 1.78 | |
35 | 0.576 | 1.10 | 0.78, 1.55 | 42 | 0.576 | 1.01 | 0.65, 1.56 | 1.00 | 0.84, 1.20 | |
Middle | 34 | 0.474 | 0.91 | 0.54, 1.52 | 41 | 0.319 | 0.56 | 0.34, 0.92 | 1.49 | 0.88, 2.53 |
36 | 0.550 | 1.05 | 0.78, 1.42 | 47 | 0.521 | 0.91 | 0.65, 1.28 | 1.06 | 0.80, 1.41 | |
35 | 0.493 | 0.94 | 0.55, 1.62 | 44 | 0.394 | 0.69 | 0.45, 1.064 | 1.25 | 0.78, 2.01 | |
46 | 0.530 | 1.02 | 0.65, 1.61 | 41 | 0.477 | 0.84 | 0.53, 1.33 | 1.11 | 0.77, 1.60 | |
28 | 0.571 | 1.09 | 0.77, 1.54 | 45 | 0.479 | 0.84 | 0.54, 1.31 | 1.19 | 0.80, 1.76 | |
Lowest | 36 | 0.502 | 0.96 | 0.60, 1.54 | 41 | 0.302 | 0.60 | 0.37, 0.97 | 1.66 | 1.00, 2.76 |
n, number of incident breast cancer cases; Rate, directly age-adjusted 15-year survival rate; RR, standardized survival rate ratio; CI, confidence interval.
Bolded RRs and CIs are statistically significant.
All rates were directly age-adjusted using this study’s combined Ontario-California population of cases as the standard (age strata: 25–44, 45–54, 55–64, 65–74 and 75 years or older), so all of the rates are directly comparable.
A survival rate ratio of 1.00 is the within-country baseline.
Confidence intervals are based on the Mantel–Haenszel chi-squared test.
90% confidence interval does not include the null (0.48, 0.99).
DISCUSSION
This study found that residents of vulnerable low-income urban areas in Ontario with node-negative breast cancer were significantly advantaged on 15-year survival as compared with similar women in California. Such neighborhoods are more predominantly represented, not only by the poor, but also by the near poor or cyclically poor in middle- to working-class neighborhoods, who are more likely to be inadequately insured in the US (2,12,20). In an era of breast cancer treatment innovations, this study observed that relatively poor women in Ontario gained access to them (lumpectomy and adjuvant radiation therapy) more readily than their counterparts in California, and such access, particularly to adjuvant radiotherapy seemed to matter in terms of their long-term survival chances. These findings are consistent with well known socioeconomic (health insurance)-breast cancer care gradients in the US and nonassociations in Canada (Ontario) (5,21–27).
One might wonder if it could be race/ethnicity, rather than SES that accounts for the observed survival differences. We could not statistically adjust for this factor as the OCR does not code race/ethnicity. We were able, however, to replicate key findings with the following conservative comparison: non-Hispanic white women in California versus the entire diverse sample of women in Ontario. After excluding all racial or ethnic minority group members from the California sample (18 African-American, 33 Hispanic, 19 Asian American and 2 women of other racial/ethnic backgrounds) key socioeconomic gradients were maintain. For example, the 15-year survival gradient seemed as steep or possibly even steeper within California (lowest versus highest income areas RR = 0.48 95% CI: 0.27, 0.84). Furthermore, the Canadian survival advantage seemed also to have been maintained in the lowest income areas (Ontario versus. California lowest income areas RR = 1.84 [90% CI: 1.10, 3.09]). Therefore, we think that race, per se, or race the biologic, rather than the social construction, is probably not a potent alternative explanation for this study’s pattern of findings. This study might also be limited by its focus on all-cause, rather than cancer-specific or disease-free survival. For the following reasons we think not. The underlying cause of “noncancer” deaths can often be directly associated with nontreatment or even with cancer treatment complications (28). And although length of survival is highly accurate in these cancer registries, the underlying cause of death is not (8). Probably of most importance, exploratory analyses, limited to women under the age of 50 (nearly all deaths due to cancer), replicated key findings. Although this study was able to account for a number of important factors (age, income, place, and disease stage at diagnosis), it could not account for notable others such as comorbid conditions and body mass index. Previous studies, however, have suggested that their socioeconomic distributions are probably quite similar in the two, culturally similar, developed nations under study, Canada and the United States (2,4,29–31). Therefore, we think that such factors probably did not potently confound this study’s findings.
CONCLUSION
More inclusive health insurance coverage in Canada versus the United States seems the most plausible explanation for the observed Canadian advantages on treatment access and survival.
Acknowledgments
This work was supported by the Canadian Breast Cancer Research Alliance (Canadian Institutes of Health Research [CIHR] grant no. MOP-67161), the Canadian Cancer Society (National Cancer Institute of Canada grant no. 016160), the Social Sciences and Humanities Research Council of Canada (grant no. 410-2002-0173) as well as a CIHR investigator award and partnership appointment to its first and third investigators. The authors gratefully acknowledge the administrative and logistical assistance of William E. Wright, chief, Cancer Surveillance Section of the California Department of Health Services at the time this study was initiated. We also gratefully acknowledge the research and technical assistance of Carole Herbert (Cancer Care Ontario), Madhan Balagurus-amy, Leah Archambault, Natalie Herbert, Dylan Herbert (University of Windsor) and Mark Allen (California Cancer Registry). This study was reviewed and cleared by the University of Windsor’s research ethics committee as well as the Ontario Cancer Research Network’s research ethics board.
References
- 1.Gorey KM, Holowaty EJ, Fehringer G, Laukkanen E, Richter NL, Meyer CM. An international comparison of cancer survival: relatively poor areas of Toronto, Ontario and three US metropolitan areas. J Public Health Med. 2000;22:343–8. doi: 10.1093/pubmed/22.3.343. [DOI] [PubMed] [Google Scholar]
- 2.Gorey KM, Holowaty EJ, Fehringer G, Laukkanen E, Richter NL, Meyer CM. An international comparison of cancer survival: metropolitan Toronto, Ontario and Honolulu, Hawaii. Am J Public Health. 2000;90:1866–72. doi: 10.2105/ajph.90.12.1866. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Gorey KM, Holowaty EJ, Fehringer G, et al. An international comparison of cancer survival: Toronto, Ontario, and Detroit, Michigan, metropolitan areas. Am J Public Health. 1997;87:1156–63. doi: 10.2105/ajph.87.7.1156. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Gorey KM, Kliewer E, Holowaty EJ, Laukkanen E, Ng EY. An international comparison of breast cancer survival: Winnipeg, Manitoba and Des Moines, Iowa, metropolitan areas. Ann Epidemiol. 2003;13:32–41. doi: 10.1016/s1047-2797(02)00259-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Gorey KM, Luginaah IN, Holowaty EJ, Fung KY, Hamm C. Breast cancer survival in Ontario and California, 1998—2006: socioeconomic inequity remains much greater in the United States. Ann Epidemiol. 2009;19:121–4. doi: 10.1016/j.annepidem.2008.10.010. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Gorey KM, Luginaah IN, Holowaty EJ, Fung KY, Hamm C. Wait times for initial surgical and adjuvant treatment of breast cancer in Canada and the United States: evidence of greater socioeconomic inequity in America. Clin Invest Med. 2009;32:E239–49. doi: 10.25011/cim.v32i3.6113. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Soerjomataram I, Louwman MWJ, Ribot JG, Roukema JA, Coebergh JWW. An overview of prognostic factors for long-term survivors of breast cancer. Breast Cancer Res Treat. 2008;107:309–30. doi: 10.1007/s10549-007-9556-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Hall S, Schulze K, Groome P, Mackillop W, Holowaty E. Using cancer registry data for survival studies: the example of the Ontario Cancer Registry. J Clin Epidemiol. 2006;59:67–76. doi: 10.1016/j.jclinepi.2005.05.001. [DOI] [PubMed] [Google Scholar]
- 9.North American Association of Central Cancer Registries. Data quality assessments. [accessed on January 6, 2009]. Available at: http://www.naaccr.org.
- 10.Wright WE. California Cancer Registry Enhancement for Breast Cancer Research. Berkeley: California Public Health Foundation; 1996. [Google Scholar]
- 11.Statistics Canada. Profiles of census tracts, 1991 (Ontario) Ottawa: 1992. [Google Scholar]
- 12.US Bureau of the Census. 1990 Census of Population and Housing in California: Summary Tape File 3 on CD-ROM. Washington, DC: US Department of Commerce; 1992. [Google Scholar]
- 13.Bank of Canada. Currency of Canada: exchange rates to other major currencies. [accessed on January 6, 2009]. Available at: http://www.bank-banque-canada.ca.
- 14.California Cancer Registry. California Cancer Reporting System standards. 7. I. Sacramento: Department of Health Services, Cancer Surveillance Section; 2003. Cancer Reporting in California: Abstracting and Coding Procedures for Hospitals. [Google Scholar]
- 15.Young JL Jr, Roffers SD, Ries LAG, Fritz AG, Hurlbut AA, editors. NIH pub no 01–4969. Bethesda: National Cancer Institute; 2001. SEER Summary Staging Manual—2000: Codes and Coding Instructions. [Google Scholar]
- 16.National Cancer Institute. NIH pub no 98–1999. 3. Bethesda: National Institutes of Health; 1998. SEER extent of disease—1988 codes and coding instructions. [Google Scholar]
- 17.Fleiss JL. Statistical Methods for Rates and Proportions. 2. New York: John Wiley & Sons; 1981. [Google Scholar]
- 18.Miettinen OS. Estimability and estimation in case-referent studies. Am J Epidemiol. 1976;103:226–35. doi: 10.1093/oxfordjournals.aje.a112220. [DOI] [PubMed] [Google Scholar]
- 19.Mantel N, Haenszel W. Statistical aspects of the analysis of data from retrospective studies of disease. J Natl Cancer Inst. 1959;22:719–48. [PubMed] [Google Scholar]
- 20.Jargowski PA. Poverty and Place: Ghettos, Barrios, and the American City. New York: Russell Sage Foundation; 1997. [Google Scholar]
- 21.Byers TE, Wolf HJ, Bauer KR, et al. The impact of socioeconomic status on survival after cancer in the United States: findings from the National Program of Cancer Registries Patterns of Care Study. Cancer. 2008;113:582–91. doi: 10.1002/cncr.23567. [DOI] [PubMed] [Google Scholar]
- 22.Coburn N, Fulton J, Pearlman DN, Law C, DiPaolo B, Cady B. Treatment variation by insurance status for breast cancer patients. Breast J. 2008;14:128–34. doi: 10.1111/j.1524-4741.2007.00542.x. [DOI] [PubMed] [Google Scholar]
- 23.Foley KL, Kimmick G, Camacho F, et al. Survival disadvantage among Medicaid-insured breast cancer patients treated with breast conserving surgery without radiation therapy. Breast Cancer Res Treat. 2007;101:207–14. doi: 10.1007/s10549-006-9280-2. [DOI] [PubMed] [Google Scholar]
- 24.McDavid K, Tucker TC, Sloggett A, Coleman MP. Cancer survival in Kentucky and health insurance coverage. Arch Intern Med. 2003;163:2135–44. doi: 10.1001/archinte.163.18.2135. [DOI] [PubMed] [Google Scholar]
- 25.Young WW, Marks SM, Kohler SA, Hsu AY. Dissemination of clinical results. Mastectomy versus lumpectomy and radiation therapy. Med Care. 1999;34:1003–17. doi: 10.1097/00005650-199610000-00003. [DOI] [PubMed] [Google Scholar]
- 26.Benk V, Przybysz R, McGowan T, Paszat L. Waiting times for radiation therapy in Ontario. Can J Surg. 2006;49:16–21. [PMC free article] [PubMed] [Google Scholar]
- 27.Goel V, Olivotto I, Hislop TG, et al. Patterns of initial management of node-negative breast cancer in two Canadian provinces. CMAJ. 1997;156:25–35. [PMC free article] [PubMed] [Google Scholar]
- 28.Brown BW, Brauner C, Minnotte MC. Noncancer deaths in white adult cancer patients. J Natl Cancer Inst. 1993;85:979–87. doi: 10.1093/jnci/85.12.979. [DOI] [PubMed] [Google Scholar]
- 29.Ford ES, Mokdad AH. Epidemiology of obesity in the Western Hemisphere. J Clin Endocrinol Metab. 2008;93(11 Suppl 1):S1–8. doi: 10.1210/jc.2008-1356. [DOI] [PubMed] [Google Scholar]
- 30.Wolf-Maier K, Cooper RS, Banegas JR, et al. Hypertension prevalence and blood pressure levels in 6 European countries, Canada, and the United States. JAMA. 2003;289:2363–9. doi: 10.1001/jama.289.18.2363. [DOI] [PubMed] [Google Scholar]
- 31.Gorey KM, Holowaty EJ, Laukkanen E, Fehringer G, Richter NL. Association between socioeconomic status and cancer incidence in Toronto, Ontario: possible confounding of cancer mortality by incidence and survival. Cancer Prev Control. 1998;2:236–41. [PubMed] [Google Scholar]