Disparities in race/ethnicity and socioeconomic status: risk of mortality of breast cancer patients in the California Cancer Registry, 2000–2010

BMC Cancer

Carol A Parise¹  Vincent Caggiano¹ 

[1] Sutter Institute for Medical Research, 2801 Capitol Ave Suite 400, Sacramento, CA 95816, USA

关键词: Socioeconomic status;    Race/ethnicity;    Breast cancer-specific mortality;    Disparities;   

Others  :  1135464
DOI  :  10.1186/1471-2407-13-449

 received in 2013-03-12, accepted in 2013-09-26,  发布年份 2013

【 摘 要 】

Background

Racial disparities in breast cancer survival have been well documented. This study examines the association of race/ethnicity and socioeconomic status (SES) on breast cancer-specific mortality in a large population of women with invasive breast cancer.

Methods

We identified 179,143 cases of stages 1–3 first primary female invasive breast cancer from the California Cancer Registry from January, 2000 through December, 2010. Cox regression, adjusted for age, year of diagnosis, grade, and ER/PR/HER2 subtype, was used to assess the association of race/ethnicity on breast cancer-specific mortality within strata of stage and SES. Hazard ratios (HR) and 95% confidence intervals were reported.

Results

Stage 1: There was no increased risk of mortality for any race/ethnicity when compared with whites within all SES strata. Stage 2: Hispanics (HR = 0.85; 0.75, 0.97) in the lowest SES category had a reduced risk of mortality.. Blacks had the same risk of mortality as whites in the lowest SES category but an increased risk of mortality in the intermediate (HR = 1.66; 1.34, 2.06) and highest (HR = 1.41; 1.15, 1.73) SES categories. Stage 3: Hispanics (HR = 0.74; 0.64, 0.85) and APIs (HR = 0.64; 0.50, 0.82) in the lowest SES category had a reduced risk while blacks had similar mortality as whites. Blacks had an increased risk of mortality in the intermediate (HR = 1.52; 1.20, 1.92) and highest (HR = 1.53; 1.22, 1.92) SES categories.

Conclusions

When analysis of breast cancer-specific mortality is adjusted for age and year of diagnosis, ER/PR/HER2 subtype, and tumor grade and cases compared within stage and SES strata, much of the black/white disparity disappears. SES plays a prominent role in breast cancer-specific mortality but it does not fully explain the racial/ethnic disparities and continued research in genetic, societal, and lifestyle factors is warranted.

【 授权许可】

   
2013 Parise and Caggiano; licensee BioMed Central Ltd.

【 参考文献 】

• [1]American Cancer Society: California Department of Public Health, California Cancer Registry. California Cancer Facts and Figures 2012. Oakland, CA: American Cancer Society, California Division; 2011.
• [2]Campleman S, Curtis R: Demographic aspects of breast cancer incidence and mortality in California, 1988–1999. In Breast Cancer in California, 2003. Volume July. Edited by Morris C, Kwong SL. Sacramento, CA: California Department of Health Services, Cancer Surveillance Section; 2004.
• [3]Hofer BM, Kwong SL, Allen M, Bates JH, McCusker ME, Snipes KP: Cancer in California, 2008, Special Highlight on Cancer by Race and Ethnicity. Sacramento, CA: California Department of Public Health Cancer Surveillance Section; 2008.
• [4]Ries L, Eisner M, Kosary M: SEER Cancer Statistics Review, 1975–2000. Bethesda, MD: National Cancer Institute; 2003.
• [5]Eley JW, Hill HA, Chen VW, Austin DF, Wesley MN, Muss HB, Greenberg RS, Coates RJ, Correa P, Redmond CK, et al.: Racial differences in survival from breast cancer. Results of the National Cancer Institute Black/White Cancer Survival Study. Jama 1994, 272(12):947-954.
• [6]Swanson GM, Lin CS: Survival patterns among younger women with breast cancer: the effects of age, race, stage, and treatment. J Natl Cancer Inst Monogr 1994, 16:69-77.
• [7]Joslyn SA, West MM: Racial differences in breast carcinoma survival. Cancer 2000, 88(1):114-123.
• [8]Shavers VL, Brown ML: Racial and ethnic disparities in the receipt of cancer treatment. J Natl Cancer Inst 2002, 94(5):334-357.
• [9]Shavers VL, Harlan LC, Stevens JL: Racial/ethnic variation in clinical presentation, treatment, and survival among breast cancer patients under age 35. Cancer 2003, 97(1):134-147.
• [10]Smedley R, Stith A, Nelson : Unequal treatment: Confronting racial and ethnic disparities in healthcare. Washington DC: National Academies Press; 2003.
• [11]Chlebowski RT, Chen Z, Anderson GL, Rohan T, Aragaki A, Lane D, Dolan NC, Paskett ED, McTiernan A, Hubbell FA, et al.: Ethnicity and breast cancer: factors influencing differences in incidence and outcome. J Natl Cancer Inst 2005, 97(6):439-448.
• [12]Hershman D, McBride R, Jacobson JS, Lamerato L, Roberts K, Grann VR, Neugut AI: Racial disparities in treatment and survival among women with early-stage breast cancer. J Clin Oncol 2005, 23(27):6639-6646.
• [13]Bigby J, Holmes MD: Disparities across the breast cancer continuum. Cancer Causes Control 2005, 16(1):35-44.
• [14]Barr DA: Health Disparities in the United States: Social Class, Race, Ethnicity, and Health. Baltimore: The Johns Hopkins Press; 2008.
• [15]Deshpande AD, Jeffe DB, Gnerlich J, Iqbal AZ, Thummalakunta A, Margenthaler JA: Racial disparities in breast cancer survival: an analysis by age and stage. J Surg Res 2009, 153(1):105-113.
• [16]Menashe I, Anderson WF, Jatoi I, Rosenberg PS: Underlying causes of the black-white racial disparity in breast cancer mortality: a population-based analysis. J Natl Cancer Inst 2009, 101(14):993-1000.
• [17]Ademuyiwa FO, Edge SB, Erwin DO, Orom H, Ambrosone CB, Underwood W 3rd: Breast cancer racial disparities: unanswered questions. Cancer Res 2011, 71(3):640-644.
• [18]Raghavan D: Slow progress in cancer care disparities: HIPAA, PPACA, and CHEWBACCA… but were still not there! Oncologist 2011, 16(7):917-919.
• [19]Gapstur SM, Dupuis J, Gann P, Collila S, Winchester DP: Hormone receptor status of breast tumors in black, Hispanic, and non-Hispanic white women. An analysis of 13,239 cases. Cancer 1996, 77(8):1465-1471.
• [20]Joslyn SA: Hormone receptors in breast cancer: racial differences in distribution and survival. Breast Cancer Res Treat 2002, 73(1):45-59.
• [21]Ademuyiwa FO, Olopade OI: Racial differences in genetic factors associated with breast cancer. Cancer Metastasis Rev 2003, 22(1):47-53.
• [22]Bauer KR, Brown M, Cress RD, Parise CA, Caggiano V: Descriptive analysis of estrogen receptor (ER)-negative, progesterone receptor (PR)-negative, and HER2-negative invasive breast cancer, the so-called triple-negative phenotype: a population-based study from the California cancer Registry. Cancer 2007, 109(9):1721-1728.
• [23]Parise CA, Bauer KR, Caggiano V: Variation in breast cancer subtypes with age and race/ethnicity. Crit Rev Oncol Hematol 2010, 76(1):44-52.
• [24]Linden G: The influence of social class in the survival of cancer patients. Am J Public Health Nations Health 1969, 59(2):267-274.
• [25]Fritz AG: International classification of diseases for oncology : ICD-O. 3rd edition. Geneva: World Health Organization, Geneva; 2000:239. vi
• [26]Cancer reporting in California: Abstracting and coding procedures for hospitals. California cancer reporting system standards, Volume I. Sacramento, CA: California Department of Public, Cancer Surveillance and Research Branch; 2008.
• [27]Yost K, Perkins C, Cohen R, Morris C, Wright W: Socioeconomic status and breast cancer incidence in California for different race/ethnic groups. Cancer Causes Control 2001, 12(8):703-711.
• [28]Liu L, Deapen D, Bernstein L: Socioeconomic status and cancers of the female breast and reproductive organs: a comparison across racial/ethnic populations in Los Angeles County, California (United States). Cancer Causes Control 1998, 9(4):369-380.
• [29]Clarke CA, Glaser SL, Keegan TH, Stroup A: Neighborhood socioeconomic status and Hodgkin’s lymphoma incidence in California. Cancer Epidemiol Biomarkers Prev 2005, 14(6):1441-1447.
• [30]Parikh-Patel A, Bates JH, Campleman S: Colorectal cancer stage at diagnosis by socioeconomic and urban/rural status in California, 1988–2000. Cancer 2006, 107(5 Suppl):1189-1195.
• [31]Zell JA, Rhee JM, Ziogas A, Lipkin SM, Anton-Culver H: Race, socioeconomic status, treatment, and survival time among pancreatic cancer cases in California. Cancer Epidemiol Biomarkers Prev 2007, 16(3):546-552.
• [32]Brown M, Tsodikov A, Bauer KR, Parise CA, Caggiano V: The role of human epidermal growth factor receptor 2 in the survival of women with estrogen and progesterone receptor-negative, invasive breast cancer: The California Cancer Registry, 1999–2004. Cancer 2008, 112(4):737-747.
• [33]Ou SH, Zell JA, Ziogas A, Anton-Culver H: Low socioeconomic status is a poor prognostic factor for survival in stage I nonsmall cell lung cancer and is independent of surgical treatment, race, and marital status. Cancer 2008, 112(9):2011-2020.
• [34]Yin D, Morris C, Allen M, Cress R, Bates J, Liu L: Does socioeconomic disparity in cancer incidence vary across racial/ethnic groups? Cancer Causes Control 2010, 21(10):1721-1730.
• [35]Parise CA, Bauer KR, Brown MM, Caggiano V: Breast cancer subtypes as defined by the estrogen receptor (ER), progesterone receptor (PR), and the human epidermal growth factor receptor 2 (HER2) among women with invasive breast cancer in California, 1999–2004. Breast J 2009, 15(6):593-602.
• [36]Bauer K, Parise C, Caggiano V: Use of ER/PR/HER2 subtypes in conjunction with the 2007 St Gallen Consensus Statement for early breast cancer. BMC Cancer 2010, 10:228. BioMed Central Full Text
• [37]Demicheli R, Retsky MW, Hrushesky WJ, Baum M, Gukas ID, Jatoi I: Racial disparities in breast cancer outcome: insights into host-tumor interactions. Cancer 2007, 110(9):1880-1888.
• [38]Gross CP, Smith BD, Wolf E, Andersen M: Racial disparities in cancer therapy: did the gap narrow between 1992 and 2002? Cancer 2008, 112(4):900-908.
• [39]Bach PB, Guadagnoli E, Schrag D, Schussler N, Warren JL: Patient demographic and socioeconomic characteristics in the SEER-Medicare database applications and limitations. Med Care 2002, 40(8 Suppl):IV-19-IV-25.
• [40]Amirikia KC, Mills P, Bush J, Newman LA: Higher population-based incidence rates of triple-negative breast cancer among young African-American women: Implications for breast cancer screening recommendations. Cancer 2011, 117(12):2747-2753.
• [41]Bradley CJ, Given CW, Roberts C: Race, socioeconomic status, and breast cancer treatment and survival. J Natl Cancer Inst 2002, 94(7):490-496.
• [42]Dragun AE, Huang B, Tucker TC, Spanos WJ: Disparities in the application of adjuvant radiotherapy after breast-conserving surgery for early stage breast cancer: impact on overall survival. Cancer 2011, 117(12):2590-2598.
• [43]Bickell NA, Wang JJ, Oluwole S, Schrag D, Godfrey H, Hiotis K, Mendez J, Guth AA: Missed opportunities: racial disparities in adjuvant breast cancer treatment. J Clin Oncol 2006, 24(9):1357-1362.
• [44]Lund MJ, Brawley OP, Ward KC, Young JL, Gabram SS, Eley JW: Parity and disparity in first course treatment of invasive breast cancer. Breast Cancer Res Treat 2008, 109(3):545-557.
• [45]Li CI, Daling JR, Malone KE: Incidence of invasive breast cancer by hormone receptor status from 1992 to 1998. J Clin Oncol 2003, 21(1):28-34.
• [46]van Ravesteyn NT, Schechter CB, Near AM, Heijnsdijk EA, Stoto MA, Draisma G, de Koning HJ, Mandelblatt JS: Race-specific impact of natural history, mammography screening, and adjuvant treatment on breast cancer mortality rates in the United States. Cancer Epidemiol Biomarkers Prev 2011, 20(1):112-122.
• [47]Roach M 3rd, Cirrincione C, Budman D, Hayes D, Berry D, Younger J, Hart R, Henderson IC: Race and survival from breast cancer: based on Cancer and Leukemia Group B trial 8541. Cancer J Sci Am 1997, 3(2):107-112.
• [48]Curtis E, Quale C, Haggstrom D, Smith-Bindman R: Racial and ethnic differences in breast cancer survival: how much is explained by screening, tumor severity, biology, treatment, comorbidities, and demographics? Cancer 2008, 112(1):171-180.
• [49]Du XL, Fang S, Meyer TE: Impact of treatment and socioeconomic status on racial disparities in survival among older women with breast cancer. Am J Clin Oncol 2008, 31(2):125-132.
• [50]Chu QD, Smith MH, Williams M, Panu L, Johnson LW, Shi R, Li BD, Glass J: Race/Ethnicity has no effect on outcome for breast cancer patients treated at an academic center with a public hospital. Cancer Epidemiol Biomarkers Prev 2009, 18(8):2157-2161.
• [51]Vona-Davis L, Rose DP: The influence of socioeconomic disparities on breast cancer tumor biology and prognosis: a review. J Womens Health (Larchmt) 2009, 18(6):883-893.
• [52]Komenaka IK, Martinez ME, Pennington RE Jr, Hsu CH, Clare SE, Thompson PA, Murphy C, Zork NM, Goulet RJ Jr: Race and ethnicity and breast cancer outcomes in an underinsured population. J Natl Cancer Inst 2010, 102(15):1178-1187.
• [53]Byers TE, Wolf HJ, Bauer KR, Bolick-Aldrich S, Chen VW, Finch JL, Fulton JP, Schymura MJ, Shen T, Van Heest S, 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(3):582-591.
• [54]Sprague BL, Trentham-Dietz A, Gangnon RE, Ramchandani R, Hampton JM, Robert SA, Remington PL, Newcomb PA: Socioeconomic status and survival after an invasive breast cancer diagnosis. Cancer 2011, 117(7):1542-1551.
• [55]Newman LA, Griffith KA, Jatoi I, Simon MS, Crowe JP, Colditz GA: Meta-analysis of survival in African American and white American patients with breast cancer: ethnicity compared with socioeconomic status. J Clin Oncol 2006, 24(9):1342-1349.
• [56]Albain KS, Unger JM, Crowley JJ, Coltman CA Jr, Hershman DL: Racial disparities in cancer survival among randomized clinical trials patients of the Southwest Oncology Group. J Natl Cancer Inst 2009, 101(14):984-992.
• [57]Huo D, Ikpatt F, Khramtsov A, Dangou JM, Nanda R, Dignam J, Zhang B, Grushko T, Zhang C, Oluwasola O, et al.: Population differences in breast cancer: survey in indigenous African women reveals over-representation of triple-negative breast cancer. J Clin Oncol 2009, 27(27):4515-4521.
• [58]Stark A, Kleer CG, Martin I, Awuah B, Nsiah-Asare A, Takyi V, Braman M, Quayson SE, Zarbo R, Wicha M, et al.: African ancestry and higher prevalence of triple-negative breast cancer: findings from an international study. Cancer 2010, 116(21):4926-4932.
• [59]Henderson BE, Lee NH, Seewaldt V, Shen H: The influence of race and ethnicity on the biology of cancer. Nat Rev Cancer 2012, 12(9):648-653.
• [60]Jones BA, Patterson EA, Calvocoressi L: Mammography screening in African American women: evaluating the research. Cancer 2003, 97(1 Suppl):258-272.
• [61]Berry DA, Cronin KA, Plevritis SK, Fryback DG, Clarke L, Zelen M, Mandelblatt JS, Yakovlev AY, Habbema JD, Feuer EJ: Effect of screening and adjuvant therapy on mortality from breast cancer. N Engl J Med 2005, 353(17):1784-1792.
• [62]Whitman S, Ansell D, Orsi J, Francois T: The racial disparity in breast cancer mortality. J Community Health 2011, 36(4):588-596.
• [63]Turra CM, Goldman N: Socioeconomic differences in mortality among U.S. adults: insights into the Hispanic paradox. J Gerontol B Psychol Sci Soc Sci 2007, 62(3):S184-S192.
• [64]Patel TA, Colon-Otero G, Bueno Hume C, Copland JA 3rd, Perez EA: Breast cancer in Latinas: gene expression, differential response to treatments, and differential toxicities in Latinas compared with other population groups. Oncologist 2010, 15(5):466-475.
• [65]O’Donnell PH, Dolan ME: Cancer pharmacoethnicity: ethnic differences in susceptibility to the effects of chemotherapy. Clin Cancer Res 2009, 15(15):4806-4814.
• [66]Reding KW, Chen C, Lowe K, Doody DR, Carlson CS, Chen CT, Houck J, Weiss LK, Marchbanks PA, Bernstein L, et al.: Estrogen-related genes and their contribution to racial differences in breast cancer risk. Cancer Causes Control 2012, 23(5):671-681.
• [67]Brawley OW: Is race really a negative prognostic factor for cancer? J Natl Cancer Inst 2009, 101(14):970-971.
• [68]Shavers VL, Fagan P, Jones D, Klein WM, Boyington J, Moten C, Rorie E: The state of research on racial/ethnic discrimination in the receipt of health care. Am J Public Health 2012, 102(5):953-966.
• [69]Wallace TA, Martin DN, Ambs S: Interactions among genes, tumor biology and the environment in cancer health disparities: examining the evidence on a national and global scale. Carcinogenesis 2011, 32(8):1107-1121.
• [70]Bauer KR, Brown M, Creech C, Schlag NC, Caggiano V: Data quality assessment of HER2 in the Sacramento Region of the California Cancer Registry. J Reg Manage 2007, 34(1):4-7.
• [71]Dunnwald LK, Rossing MA, Li CI: Hormone receptor status, tumor characteristics, and prognosis: a prospective cohort of breast cancer patients. Breast Cancer Res 2007, 9(1):R6. BioMed Central Full Text
• [72]Grann VR, Troxel AB, Zojwalla NJ, Jacobson JS, Hershman D, Neugut AI: Hormone receptor status and survival in a population-based cohort of patients with breast carcinoma. Cancer 2005, 103(11):2241-2251.
• [73]Muss HB, Hunter CP, Wesley M, Correa P, Chen VW, Greenberg RS, Eley JW, Austin DF, Kurman R, Edwards BK: Treatment plans for black and white women with stage II node-positive breast cancer. The National Cancer Institute Black/White Cancer Survival Study experience. Cancer 1992, 70(10):2460-2467.
• [74]Harlan LC, Abrams J, Warren JL, Clegg L, Stevens J, Ballard-Barbash R: Adjuvant therapy for breast cancer: practice patterns of community physicians. J Clin Oncol 2002, 20(7):1809-1817.
• [75]Griggs JJ: Role of nonclinical factors in the receipt of high-quality systemic adjuvant breast cancer treatment. J Clin Oncol 2012, 30(2):121-124.
• [76]Rizzo M, Lund MJ, Mosunjac M, Bumpers H, Holmes L, O’Regan R, Brawley OW, Gabram S: Characteristics and treatment modalities for African American women diagnosed with stage III breast cancer. Cancer 2009, 115(13):3009-3015.
• [77]Sail K, Franzini L, Lairson D, Du X: Differences in treatment and survival among African-American and Caucasian women with early stage operable breast cancer. Ethn Health 2012, 17(3):309-323.
• [78]Krieger N: Overcoming the absence of socioeconomic data in medical records: validation and application of a census-based methodology. Am J Public Health 1992, 82(5):703-710.
• [79]Shavers VL: Measurement of socioeconomic status in health disparities research. J Natl Med Assoc 2007, 99(9):1013-1023.
• [80]Bernstein L, Teal CR, Joslyn S, Wilson J: Ethnicity-related variation in breast cancer risk factors. Cancer 2003, 97(1 Suppl):222-229.
• [81]Colditz GA, Rosner BA, Chen WY, Holmes MD, Hankinson SE: Risk factors for breast cancer according to estrogen and progesterone receptor status. J Natl Cancer Inst 2004, 96(3):218-228.
• [82]Ursin G, Bernstein L, Lord SJ, Karim R, Deapen D, Press MF, Daling JR, Norman SA, Liff JM, Marchbanks PA, et al.: Reproductive factors and subtypes of breast cancer defined by hormone receptor and histology. Br J Cancer 2005, 93(3):364-371.
• [83]Ma H, Bernstein L, Pike MC, Ursin G: Reproductive factors and breast cancer risk according to joint estrogen and progesterone receptor status: a meta-analysis of epidemiological studies. Breast Cancer Res 2006, 8(4):R43. BioMed Central Full Text
• [84]Gerend MA, Pai M: Social determinants of Black-White disparities in breast cancer mortality: a review. Cancer Epidemiol Biomarkers Prev 2008, 17(11):2913-2923.
• [85]Shinde SS, Forman MR, Kuerer HM, Yan K, Peintinger F, Hunt KK, Hortobagyi GN, Pusztai L, Symmans WF: Higher parity and shorter breastfeeding duration: association with triple-negative phenotype of breast cancer. Cancer 2010, 116(21):4933-4943.
• [86]Harris HR, Willett WC, Terry KL, Michels KB: Body fat distribution and risk of premenopausal breast cancer in the Nurses’ Health Study II. J Natl Cancer Inst 2011, 103(3):273-278.
• [87]Phipps AI, Chlebowski RT, Prentice R, McTiernan A, Wactawski-Wende J, Kuller LH, Adams-Campbell LL, Lane D, Stefanick ML, Vitolins M, et al.: Reproductive history and oral contraceptive use in relation to risk of triple-negative breast cancer. J Natl Cancer Inst 2011, 103(6):470-477.
• [88]Bernstein L, Lacey JV Jr: Receptors, associations, and risk factor differences by breast cancer subtypes: positive or negative? J Natl Cancer Inst 2011, 103(6):451-453.
• [89]Montoya MJ, Kent EE: Re: Racial disparities in cancer survival among randomized clinical trials of the Southwest Oncology Group. J Natl Cancer Inst 2010, 102(4):277-278.
• [90]Trivers KF, Messer LC, Kaufman JS: Re: Racial disparities in cancer survival among randomized clinical trials of the Southwest Oncology Group. J Natl Cancer Inst 2010, 102(4):278-279.