Disparities in breast cancer treatment and outcomes: Biological, social, and health system determinants and opportunities for research

Oncologist

Volumn 18, Issue 9, 2013, Pages 986-993

  Wheeler, Stephanie B ^a,b   Reeder Hayes, Katherine E ^b,c   Carey, Lisa A ^b,c  

^a University of North Carolina at Chapel Hill   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Access to care; Breast cancer; Cancer care quality; Disparities; Race

Indexed keywords

CYCLIN E; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ESTROGEN RECEPTOR; HORMONE RECEPTOR; PROGESTERONE; PROTEIN P16; PROTEIN P53;

ARTICLE; BEHAVIOR; BREAST CANCER; CANCER HORMONE THERAPY; CANCER INCIDENCE; CANCER MORTALITY; COMORBIDITY; ETHNICITY; HEALTH CARE QUALITY; HEALTH DISPARITY; HEALTH INSURANCE; HUMAN; MAMMOGRAPHY; OUTCOME ASSESSMENT; PARTIAL MASTECTOMY; PRIORITY JOURNAL; PROSTATE CANCER; RACE; SENTINEL LYMPH NODE BIOPSY; SOCIAL ASPECT; SOCIOECONOMICS;

ACCESS TO CARE; BREAST CANCER; CANCER CARE QUALITY; DISPARITIES; RACE;

AFRICAN CONTINENTAL ANCESTRY GROUP; BREAST NEOPLASMS; EUROPEAN CONTINENTAL ANCESTRY GROUP; FEMALE; HEALTHCARE DISPARITIES; HUMANS; MIDDLE AGED; SEER PROGRAM; SOCIAL CLASS; TREATMENT OUTCOME; UNITED STATES;

EID: 84884556628     PISSN: 10837159     EISSN: 1549490X     Source Type: Journal    
DOI: 10.1634/theoncologist.2013-0243     Document Type: Article

References (102)

1. Banerjee M, George J, Yee C et al. Disentangling the effects of race on breast cancer treatment. Cancer 2007;110:2169-2177.
2. Bickell NA, Mendez J, Guth AA. The quality of early-stage breast cancer treatment: What can we do to improve? Surg Oncol Clin N Am 2005;14:103-117, vi.
3. Bickell NA, Wang JJ, Oluwole S et al. Missed opportunities: Racial disparities in adjuvant breast cancer treatment. J Clin Oncol 2006;24:1357-1362.
4. Bickell NA, LePar F, Wang JJ et al. Lost opportunities: Physicians' reasons and disparities in breast cancer treatment. J Clin Oncol 2007;25:2516-2521.
5. Bigby J, Holmes MD. Disparities across the breast cancer continuum. Cancer Causes Control 2005;16:35-44.
6. Bowen RL, Stebbing J, Jones LJ. A review of the ethnic differences in breast cancer. Pharmacogenomics 2006;7:935-942.
7. Chen AY, Halpern MT, Schrag NM et al. Disparities and trends in sentinel lymph node biopsy among early-stage breast cancer patients (1998-2005). J Natl Cancer Inst 2008;100:462-474.
8. Freedman RA, He Y, Winer EP et al. Trends in racial and age disparities in definitive local therapy of early-stage breast cancer. J Clin Oncol 2009;27: 713-719.
9. Gerend MA, Pai M. Social determinants of black-white disparities in breast cancer mortality: A review. Cancer Epidemiol Biomarkers Prev 2008; 17:2913-2923.
10. Haggstrom DA, Quale C, Smith-Bindman R. Differences in the quality of breast cancer care among vulnerable populations. Cancer 2005;104:2347-2358.
11. Lund MJ, Brawley OP, Ward KC et al. Parity and disparity in first course treatment of invasive breast cancer. Breast Cancer Res Treat 2008;109:545-557.
12. Masi CM, Olopade OI. Racial and ethnic disparities in breast cancer: A multilevel perspective. Med Clin North Am 2005;89:753-770.
13. Shavers VL, Brown ML. Racial and ethnic disparities in the receipt of cancer treatment. J Natl Cancer Inst 2002;94:334-357.
14. Tammemagi CM. Racial/ethnic disparities in breast and gynecologic cancer treatment and outcomes. Curr Opin Obstet Gynecol 2007;19:31-36.
15. Bach PB, Schrag D, Brawley OW et al. Survival of blacks and whites after a cancer diagnosis. JAMA 2002;287:2106-2113.
16. Fast Stats: An interactive tool for access to SEER cancer statistics. Surveillance Research Program, NationalCancerInstitute.Availableat, http://seer.cancer. gov/faststats. Accessed August 4, 2013.
17. Vogel VG. Epidemiology, genetics, and risk evaluation of postmenopausal women at risk of breast cancer. Menopause 2008;15(suppl):782-789.
18. Colditz GA, Baer HJ, Tamimi RM. Chapter 51:Breast cancer. In: Schottenfeld D, Fraumeni JF Jr. eds. Cancer Epidemiology and Prevention. 3rd ed. New York, NY: Oxford University Press, 2006:995-1012.
19. American Cancer Society. Cancer Facts & Figures for African Americans: 2009-2010. Available at http://www.cancer.org/acs/groups/content/@ nho/documents/document/cffaa2009-2010pdf. pdf. Accessed August 4, 2013.
20. Edwards BK, Brown ML, Wingo PA et al. Annual report to the nation on the status of cancer, 1975-2002, featuring population-based trends in cancer treatment. J Natl Cancer Inst 2005;97:1407-1427.
21. Feenstra C. Healthy people 2010. Mich Nurse 2000;73:14-15.
22. Movsas B, Moughan J, Owen J et al. Who enrolls onto clinical oncology trials? A radiation Patterns Of Care Study analysis. Int J Radiat Oncol Biol Phys 2007;68:1145-1150.
23. Gross CP, Filardo G, Mayne ST et al. The impact of socioeconomic status and race on trial participation for older women with breast cancer. Cancer 2005;103:483-491.
24. Anders C, Carey LA. Understanding and treating triple-negative breast cancer. Oncology (Williston Park) 2008;22:1233-1239; discussion 1239-1240,1243.
25. Smith-Bindman R, Miglioretti DL, Lurie N et al. Does utilization of screening mammography explain racial and ethnic differences in breast cancer? Ann Intern Med 2006;144:541-553.
26. Carey LA, Perou CM, Livasy CA et al. Race, breast cancer subtypes, and survival in the Carolina Breast Cancer Study. JAMA 2006;295:2492-2502.
27. O'Brien KM, Cole SR, Tse CK et al. Intrinsic breast tumor subtypes, race, and long-term survival in the Carolina Breast Cancer Study. Clin Cancer Res 2010;16:6100-6110.
28. Demicheli R, Retsky MW, Hrushesky WJ et al. Racial disparities in breast cancer outcome: Insights into host-tumor interactions. Cancer 2007;110: 1880-1888.
29. Lund MJ, Trivers KF, Porter PL et al. Race and triple negative threats to breast cancer survival: A population-based study in Atlanta, GA Breast Cancer Res Treat 2009;113:357-370.
30. Porter PL, Lund MJ, Lin MG et al. Racial differences in the expression of cell cycle-regulatory proteins in breast carcinoma. Cancer 2004;100:2533-2542.
31. Caudle AS, Gonzalez-Angulo AM, Hunt KK et al. Predictors of tumor progression during neoadjuvant chemotherapy in breast cancer. J Clin Oncol 2010;28:1821-1828.
32. Magai C, Consedine NS, Adjei BA et al. Psychosocial influences on suboptimal adjuvant breast cancer treatment adherence among African American women: Implications for education and intervention. Health Educ Behav 2008;35:835-854.
33. Maloney N, Koch M, Erb D et al. Impact of race on breast cancer in lower socioeconomic status women. Breast J 2006;12:58-62.
34. Mobley LR, Kuo TM, Clayton LJ et al. Mammography facilities are accessible, so why is utilization so low? Cancer Causes Control 2009;20:1017-1028.
35. Blackman DJ, Masi CM. Racial and ethnic disparities in breast cancer mortality: Are we doing enough to address the root causes? J Clin Oncol 2006;24:2170-2178.
36. Millikan RC, Newman B, Tse CK et al. Epidemiology of basal-like breast cancer. Breast Cancer Res Treat 2008;109:123-139.
37. Peppercorn J, Perou CM, Carey LA. Molecular subtypes in breast cancer evaluation and management: Divide and conquer. Cancer Invest 2008;26: 1-10.
38. Schneider BP, Winer EP, Foulkes WD et al. Triple-negative breast cancer: Risk factors to potential targets. Clin Cancer Res 2008;14:8010-8018.
39. Wildiers H, Brain EG. Adjuvant chemotherapy in elderly patients with breast cancer: Where are we? Curr Opin Oncol 2005;17:566-572.
40. Chen VW, Correa P, Kurman RJ et al. Histological characteristics of breast carcinoma in blacks and whites. Cancer Epidemiol Biomarkers Prev 1994;3: 127-135.
41. Fejerman L, Ziv E. Population differences in breast cancer severity. Pharmacogenomics 2008;9: 323-333.
42. Kang SP, Martel M, Harris LN. Triple negative breast cancer: Current understanding of biology and treatment options. Curr Opin Obstet Gynecol 2008;20:40-46.
43. Andre F, Pusztai L. Molecular classification of breast cancer: Implications for selection of adjuvant chemotherapy. Nat Clin Pract Oncol 2006;3:621-632.
44. Munoz M, Estevez LG, Alvarez I et al. Evaluation of international treatment guidelines and prognostic tests for the treatment of early breast cancer. Cancer Treat Rev 2008;34:701-709.
45. Morris GJ, Mitchell EP. Higher incidence of aggressive breast cancers in African-American women: A review. J Natl Med Assoc 2008;100:698-702.
46. Huo D, Ikpatt F, Khramtsov A 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: 4515-4521.
47. Yang XR, Sherman ME, Rimm DL et al. Differences in risk factors for breast cancer molecular subtypes in a population-based study. Cancer Epidemiol Biomarkers Prev 2007;16:439-443.
48. Chen F, Chen GK, Stram DO et al. A genomewide association study of breast cancer in women of African ancestry. Hum Genet 2013;132:39-48.
49. Bickell NA. Race, ethnicity, and disparities in breast cancer: Victories and challenges. Womens Health Issues 2002;12:238-251.
50. Breen N, Wagener DK, Brown ML et al. Progress in cancer screening over a decade: Results of cancer screening from the 1987, 1992, and 1998 National Health Interview Surveys. J Natl Cancer Inst 2001;93:1704-1713.
51. Baquet CR, Commiskey P. Socioeconomic factors and breast carcinoma in multicultural women. Cancer 2000;88(suppl):1256-1264.
52. Du XL, Fang S, Vernon SW et al. Racial disparities and socioeconomic status in association with survival in a large population-based cohort of elderly patients with colon cancer. Cancer 2007;110:660-669.
53. 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;31:125-132.
54. Ren XS, Amick BC, Williams DR. Racial/ethnic disparities in health: The interplay between discrimination and socioeconomic status. Ethn Dis 1999;9:151-165.
55. Canto MT, Anderson WF, Brawley O. Geographic variation in breast cancer mortality for white and black women: 1986-1995. CA Cancer J Clin 2001;51:367-370.
56. Schleinitz MD, DePalo D, Blume J et al. Can differences in breast cancer utilities explain disparities in breast cancer care? J Gen Intern Med 2006;21: 1253-1260.
57. Ashing-Giwa KT, Padilla G, Tejero J et al. Understanding the breast cancer experience of women: A qualitative study of African American, Asian American, Latina and Caucasian cancer survivors Psychooncology 2004;13:408-428.
58. Wagner L, Lacey MD. The hidden costs of cancer care: An overview with implications and referral resources for oncology nurses. Clin J Oncol Nurs 2004;8:279-287.
59. Warren JL, Yabroff KR, Meekins A et al. Evaluation of trends in the cost of initial cancer treatment. J Natl Cancer Inst 2008;100:888-897.
60. Lee DW, Stang PE, Goldberg GA et al. Resource use and cost of diagnostic workup of women with suspected breast cancer. Breast J 2009;15:85-92.
61. USA Today/Kaiser Family Foundation/Harvard School of Public Health National Survey of Households Affected by Cancer [Publication No. 7591]. Available at http://kaiserfamilyfoundation.files.wordpress.com/ 2013/01/7591.pdf. Accessed August 4, 2013.
62. Polacek GN, Ramos MC, Ferrer RL. Breast cancer disparities and decision-making among U.S. women. Patient Educ Couns 2007;65:158-165.
63. Talcott JA, Spain P, Clark JA et al. Hidden barriers between knowledge and behavior: The North Carolina prostate cancer screening and treatment experience. Cancer 2007;109:1599-1606.
64. Carpenter WR, Reeder-Hayes K, Bainbridge J et al. The role of organizational affiliations and research networks in the diffusion of breast cancer treatment innovation. Med Care 2011;49:172-179.
65. Wheeler SB, Carpenter WR, Peppercorn J, etal. Predictors of timing of adjuvant chemotherapy in older women with hormone receptor-negative, stages II-III breast cancer. Breast Cancer Res Treat 2012;131:207-216.
66. Wheeler SB, Carpenter WR, Peppercorn J et al. Structural/organizationalcharacteristicsofhealthser-vices partly explain racial variation in timeliness of radiation therapy among elderly breast cancer patients. Breast Cancer Res Treat 2012;133:333-345.
67. Punglia RS, Weeks JC, Neville BA et al. Effect of distance to radiation treatment facility on use of radiation therapy after mastectomy in elderly women. Int J Radiat Oncol Biol Phys 2006;66:56-63.
68. Bach PB, Pham HH, Schrag D et al. Primary care physicians who treat blacks and whites. N Engl J Med 2004;351:575-584.
69. Jerome-D'Emilia B, Begun JW. Diffusion of breast conserving surgery in medical communities. Soc Sci Med 2005;60:143-151.
70. Vernon SW, Vogel VG, Halabi S et al. Breast cancer screening behaviors and attitudes in three racial/ethnic groups. Cancer 1992;69:165-174.
71. Gooden K, Howard D, Carpenter W et al. The effect of hospital and surgeon volume on racial differences in recurrence-free survival after radical prostatectomy. Med Care 2008;46:1170-1176.
72. Morris AM, Wei Y, Birkmeyer NJ et al. Racial disparities in late survival after rectal cancer surgery. J Am Coll Surg 2006;203:787-794.
73. Earle CC, Neumann PJ, Gelber RD et al. Impact of referral patterns on the use of chemotherapy for lung cancer. J Clin Oncol 2002;20:1786-1792.
74. Bradley CJ, Given CW, Roberts C. Disparities in cancer diagnosis and survival. Cancer 2001;91:178-188.
75. Hershman DL, Unger JM, Barlow WE et al. Treatment quality and outcomes of African American versus white breast cancer patients: Retrospective analysis of Southwest Oncology studies S8814/ S8897. J Clin Oncol 2009;27:2157-2162.
76. Newman LA, Martin IK. Disparities in breast cancer. Curr Probl Cancer 2007;31:134-156.
77. Sateren WB, Trimble EL, Abrams J et al. How sociodemographics, presence of oncology specialists, and hospital cancer programs affect accrual to cancer treatment trials. J Clin Oncol 2002;20:2109-2117.
78. Tejeda HA, Green SB, Trimble EL et al. Representation of African-Americans, Hispanics, and whites in National Cancer Institute cancer treatment trials. J Natl Cancer Inst 1996;88:812-816.
79. Mitchell KW, Carey LA, Peppercorn J. Reporting of race and ethnicity in breast cancer research: Room for improvement. Breast Cancer Res Treat 2009;118:511-517.
80. Reeder-Hayes KE, Bainbridge J, Meyer AM et al. Race and age disparities in receipt of sentinel lymph node biopsy for early-stage breast cancer. Breast Cancer Res Treat 2011;128:863-871.
81. Halpern MT, Chen AY, Marlow NS et al. Disparities in receipt of lymph node biopsy among earlystage female breast cancer patients. Ann Surg Oncol 2009;16:562-570.
82. Payne R, Medina E, Hampton JW. Quality of life concerns in patients with breast cancer: Evidence for disparity of outcomes and experiences in pain management and palliative care among African-American women. Cancer 2003;97(suppl):311-317.
83. Demissie S, Silliman RA, Lash TL, Adjuvanttamoxifen: Predictors of use, side effects, and discontinuation in older women. J Clin Oncol 2001;19:322-328.
84. Owusu C, Buist DS, Field TS et al. Predictors of tamoxifen discontinuation among older women with estrogen receptor-positive breast cancer. J Clin Oncol 2008;26:549-555.
85. Hershman DL, Kushi LH, Shao T et al. Early discon-tinuation and nonadherence to adjuvant hormonal therapy in a cohort of 8,769 early-stage breast cancer patients. J Clin Oncol 2010;28:4120-4128.
86. Barron TI, Connolly R, Bennett K et al. Early discontinuation of tamoxifen: A lesson for oncologists. Cancer 2007;109:832-839.
87. Kimmick G, Anderson R, Camacho F et al. Adjuvant hormonal therapy use among insured, low-income women with breast cancer. J Clin Oncol 2009; 27:3445-3451.
88. Partridge AH, Wang PS, Winer EP et al. Nonadherence to adjuvant tamoxifen therapy in women with primary breast cancer. J Clin Oncol 2003;21:602-606.
89. Partridge AH, Non-adherencetoendocrinetherapy for breast cancer. Ann Oncol 2006;17:183-184.
90. Partridge AH, LaFountain A, Mayer E et al. Adherence to initial adjuvant anastrozole therapy among women with early-stage breast cancer. J Clin Oncol 2008;26:556-562.
91. Ziller V, Kalder M, Albert US et al. Adherence to adjuvant endocrine therapy in postmenopausal women with breast cancer. Ann Oncol 2009;20:431-436.
92. Lash TL, Fox MP, Westrup JL et al. Adherence to tamoxifen over the five-year course. Breast Cancer Res Treat 2006;99:215-220.
93. Nekhlyudov L, Li L, Ross-Degnan D et al. Fiveyear patterns of adjuvant hormonal therapy use, persistence, and adherence among insured women with early-stage breast cancer. Breast Cancer Res Treat 2011;130:681-689.
94. Kohler RE, Wheeler SB, Reeder-Hayes KE et al. Endocrine therapy use among Medicaid-insured breast cancer survivors with hormone receptorpositive tumors. J Clin Oncol 2012;30(suppl):6017a.
95. Hershman DL, Shao T, Kushi LH et al. Early discontinuation and non-adherence to adjuvant hormonal therapy are associated with increased mortality in women with breast cancer. Breast Cancer Res Treat 2011;126:529-537.
96. Shavers VL, Shavers BS. Racism and health inequity among Americans. J Natl Med Assoc 2006; 98:386-396.
97. Dignam JJ, Redmond CK, Fisher B et al. Prognosis among African-American women and white women with lymph node negative breast carcinoma: Findings from two randomized clinical trials of the National Surgical Adjuvant Breast and Bowel Project (NSABP). Cancer 1997;80:80-90.
98. Yood MU, Johnson CC, Blount A et al. Race and differences in breast cancer survival in a managed care population. J Natl Cancer Inst 1999;91:1487-1491.
99. Smith K, Wray L, Klein-Cabral M et al. Ethnic disparities in adjuvant chemotherapy for breast cancer are not caused by excess toxicity in black patients. Clin Breast Cancer 2005;6:260-266.
100. Newman LA, Theriault R, Clendinnin N et al. Treatment choices and response rates in AfricanAmerican women with breast carcinoma. Cancer 2003;97(suppl):246-252.
101. Dawood S, Broglio K, Kau SW et al. Triple receptor-negative breast cancer: The effect of race on response to primary systemic treatment and survival outcomes. J Clin Oncol 2009;27:220-226.
102. Tichy JR DA, Anders CK, Carey LA. Race, Response to Chemotherapy, and Outcome within Clinical Breast Cancer Subtypes. Cancer Res 2011; 71(suppl 3):nr P2-14-01a.