Skip to main content
Top
Published in: Cancer Causes & Control 10/2008

01-12-2008 | Original Paper

Race/ethnicity and breast cancer estrogen receptor status: impact of class, missing data, and modeling assumptions

Authors: Nancy Krieger, Jarvis T. Chen, James H. Ware, Afamia Kaddour

Published in: Cancer Causes & Control | Issue 10/2008

Login to get access

Abstract

Objective

To test whether reported associations between race/ethnicity and breast cancer estrogen receptor (ER) status are inflated due to missing ER data, lack of socioeconomic data, and use of the odds ratio (OR) rather than the prevalence ratio (PR).

Methods

We geocoded and added census tract socioeconomic data to all cases of primary invasive breast cancer (n = 42,420) among women diagnosed between 1998 and 2002 in two California cancer registries (San Francisco Bay Area; Los Angeles County) and analyzed the data using log binomial regression.

Results

Adjusting for socioeconomic position and tumor characteristics, in models using the imputed data, reduced the PR for the black versus white excess risk of being ER− from 1.76 (95% CI: 1.66, 1.86; adjusted for age and catchment area) to 1.47 (95% CI: 1.38, 1.56). The latter parameter estimate was 16% greater (i.e., 1.56) in models excluding women with missing ER data, and was 43% greater when estimated using the OR (i.e., 1.82).

Conclusion(s)

Studies on race/ethnicity and ER status that fail to account for missing data and socioeconomic data and report the OR are likely to yield inflated estimates of racial/ethnic disparities in ER status.
Literature
1.
go back to reference Althuis MD, Fergenbaumm JH, Garcia-Closas M, Brinton LA, Madigan MP, Sherman ME (2004) Etiology of hormone receptor-defined breast cancer: a systematic review of the literature. Cancer Epidemiol Biomarkers Prev 13:1558–1568PubMed Althuis MD, Fergenbaumm JH, Garcia-Closas M, Brinton LA, Madigan MP, Sherman ME (2004) Etiology of hormone receptor-defined breast cancer: a systematic review of the literature. Cancer Epidemiol Biomarkers Prev 13:1558–1568PubMed
3.
go back to reference Chlebowski RT, Chen Z, Anderson GL et al (2005) Ethnicity and breast cancer: factors influencing differences in incidence and outcome. J Natl Cancer Inst 97:439–448PubMedCrossRef Chlebowski RT, Chen Z, Anderson GL et al (2005) Ethnicity and breast cancer: factors influencing differences in incidence and outcome. J Natl Cancer Inst 97:439–448PubMedCrossRef
4.
go back to reference Stanford JL, Szklo M, Brinton LA (1986) Estrogen receptors and breast cancer. Epidemiol Rev 8:42–59PubMed Stanford JL, Szklo M, Brinton LA (1986) Estrogen receptors and breast cancer. Epidemiol Rev 8:42–59PubMed
5.
go back to reference Morris GJ, Naidu S, Topham AK et al (2007) Differences in breast carcinoma characteristics in newly diagnosed African-American and Caucasian patients—a single-institution compilation compared with the National Cancer Institute’s Surveillance, Epidemiology, and End Results Database. Cancer 110:876–884. doi:10.1002/cncr.22836 PubMedCrossRef Morris GJ, Naidu S, Topham AK et al (2007) Differences in breast carcinoma characteristics in newly diagnosed African-American and Caucasian patients—a single-institution compilation compared with the National Cancer Institute’s Surveillance, Epidemiology, and End Results Database. Cancer 110:876–884. doi:10.​1002/​cncr.​22836 PubMedCrossRef
6.
go back to reference Watlington AT, Byers T, Mouchawar J, Sauaia A, Ellis J (2007) Does having insurance affect differences in clinical presentation between Hispanic and non-Hispanic white women with breast cancer? Cancer 109:2093–2099. doi:10.1002/cncr.22640 PubMedCrossRef Watlington AT, Byers T, Mouchawar J, Sauaia A, Ellis J (2007) Does having insurance affect differences in clinical presentation between Hispanic and non-Hispanic white women with breast cancer? Cancer 109:2093–2099. doi:10.​1002/​cncr.​22640 PubMedCrossRef
7.
go back to reference Woods SE, Luking R, Atkins B, Engel A (2006) Association of race and breast cancer stage. J Natl Med Assoc 98:683–686PubMed Woods SE, Luking R, Atkins B, Engel A (2006) Association of race and breast cancer stage. J Natl Med Assoc 98:683–686PubMed
9.
go back to reference Porter PL, Lund MJ, Lin MG et al (2004) Racial differences in the expression of cell cycle regulatory proteins in breast carcinoma - Study of young African American and white women in Atlanta, Georgia. Cancer 100:2533–2542. doi:10.1002/cncr.20279 PubMedCrossRef Porter PL, Lund MJ, Lin MG et al (2004) Racial differences in the expression of cell cycle regulatory proteins in breast carcinoma - Study of young African American and white women in Atlanta, Georgia. Cancer 100:2533–2542. doi:10.​1002/​cncr.​20279 PubMedCrossRef
11.
go back to reference Ziv E, Tice J, Smith-Bindman R, Shepherd J, Cummings S, Kerlikowske K (2004) Mammographic density and estrogen receptor status of breast cancer. Cancer Epidemiol Biomarker Prev 13:2090–2095 Ziv E, Tice J, Smith-Bindman R, Shepherd J, Cummings S, Kerlikowske K (2004) Mammographic density and estrogen receptor status of breast cancer. Cancer Epidemiol Biomarker Prev 13:2090–2095
13.
go back to reference Li CI, Malone KE, Daling JR (2002) Differences in breast cancer hormone receptor status and histology by race and ethnicity among women 50 years of age and older. Cancer Epidemiol Biomarker Prev 11:601–607 Li CI, Malone KE, Daling JR (2002) Differences in breast cancer hormone receptor status and histology by race and ethnicity among women 50 years of age and older. Cancer Epidemiol Biomarker Prev 11:601–607
14.
go back to reference Miller BA, Hankey BF, Thomas TL (2002) Impact of sociodemographic factors, hormone receptor status, and tumor grade on ethnic differences in tumor stage and size for breast cancer in US women. Am J Epidemiol 155:534–545. doi:10.1093/aje/155.6.534 PubMedCrossRef Miller BA, Hankey BF, Thomas TL (2002) Impact of sociodemographic factors, hormone receptor status, and tumor grade on ethnic differences in tumor stage and size for breast cancer in US women. Am J Epidemiol 155:534–545. doi:10.​1093/​aje/​155.​6.​534 PubMedCrossRef
16.
18.
go back to reference Stanford JL, Greenberg RS (1989) Breast cancer incidence in young women by estrogen receptor status and race. Am J Public Health 79:71–73PubMed Stanford JL, Greenberg RS (1989) Breast cancer incidence in young women by estrogen receptor status and race. Am J Public Health 79:71–73PubMed
19.
go back to reference Stanford JL, Szklo M, Boring CC et al (1987) A case-control study of breast cancer stratified by estrogen receptor status. Am J Epidemiol 125:184–194PubMed Stanford JL, Szklo M, Boring CC et al (1987) A case-control study of breast cancer stratified by estrogen receptor status. Am J Epidemiol 125:184–194PubMed
23.
go back to reference Elmore JG, Moceri VM, Carter D, Larson EB (1998) Breast carcinoma tumor characteristics in black and white women. Cancer 83:2509–2515. doi:10.1002/(SICI)1097-0142(19981215)83:12<2509::AID-CNCR15>3.0.CO;2-V Elmore JG, Moceri VM, Carter D, Larson EB (1998) Breast carcinoma tumor characteristics in black and white women. Cancer 83:2509–2515. doi:10.1002/(SICI)1097-0142(19981215)83:12<2509::AID-CNCR15>3.0.CO;2-V
24.
go back to reference Krieger N, van den Eeden SK, Zava D, Okamoto A (1997) Race/ethnicity, social class, and prevalence of breast cancer prognostic biomarkers: a study of white, black, and Asian women in the San Francisco Bay Area. Ethn Dis 7:137–149PubMed Krieger N, van den Eeden SK, Zava D, Okamoto A (1997) Race/ethnicity, social class, and prevalence of breast cancer prognostic biomarkers: a study of white, black, and Asian women in the San Francisco Bay Area. Ethn Dis 7:137–149PubMed
25.
go back to reference Weiss SE, Tartter PI, Ahmed S et al (1995) Ethnic differences in risk and prognostic factors for breast cancer. Cancer 76:268–274. doi: 10.1002/1097-0142(19950715)76:2<268::AID-CNCR2820760217>3.0.CO;2-1 Weiss SE, Tartter PI, Ahmed S et al (1995) Ethnic differences in risk and prognostic factors for breast cancer. Cancer 76:268–274. doi: 10.1002/1097-0142(19950715)76:2<268::AID-CNCR2820760217>3.0.CO;2-1
26.
go back to reference Gordon NH (1995) Association of education and income with estrogen receptor status in primary breast cancer. Am J Epidemiol 142:796–803PubMed Gordon NH (1995) Association of education and income with estrogen receptor status in primary breast cancer. Am J Epidemiol 142:796–803PubMed
27.
go back to reference Chen VW, Correa P, Kurman RJ et al (1994) Histological characteristics of breast carcinoma in blacks and whites. Cancer Epidemiol Biomarkers Prev 3:127–135PubMed Chen VW, Correa P, Kurman RJ et al (1994) Histological characteristics of breast carcinoma in blacks and whites. Cancer Epidemiol Biomarkers Prev 3:127–135PubMed
28.
go back to reference Ansell D, Whitman S, Lipton R, Cooper R (1993) Race, income, and survival from breast cancer at two public hospitals. Cancer 72:2974–2978. doi:10.1002/1097-0142(19931115)72:10<2974::AID-CNCR2820721019>3.0.CO;2-M Ansell D, Whitman S, Lipton R, Cooper R (1993) Race, income, and survival from breast cancer at two public hospitals. Cancer 72:2974–2978. doi:10.1002/1097-0142(19931115)72:10<2974::AID-CNCR2820721019>3.0.CO;2-M
29.
go back to reference Crowe JP Jr, Gordon NH, Hubay CA, Pearson OH, Marshall JS, McGuire WL (1986) The interaction of estrogen receptor status and race in predicting prognosis for stage I breast cancer patients. Surgery 100:599–605PubMed Crowe JP Jr, Gordon NH, Hubay CA, Pearson OH, Marshall JS, McGuire WL (1986) The interaction of estrogen receptor status and race in predicting prognosis for stage I breast cancer patients. Surgery 100:599–605PubMed
30.
go back to reference Schafer JL (1997) Analysis of incomplete multivariate data. Chapman and Hall, Boca Raton Schafer JL (1997) Analysis of incomplete multivariate data. Chapman and Hall, Boca Raton
31.
go back to reference Greenland S, Finkle WD (1995) A critical look at methods for handling missing covariates in epidemiologic regression analyses. Am J Epidemiol 142:1255–1264PubMed Greenland S, Finkle WD (1995) A critical look at methods for handling missing covariates in epidemiologic regression analyses. Am J Epidemiol 142:1255–1264PubMed
36.
go back to reference Thomson CS, Hole DJ, Twelves CJ, Brewster DH, Black RJ, Scottish Cancer Therapy Network (2001) Prognostic factors in women with breast cancer: distribution by socioeconomic status and effect on differences in survival. J Epidemiol Community Health 55:308–315. doi:10.1136/jech.55.5.308 PubMedCrossRef Thomson CS, Hole DJ, Twelves CJ, Brewster DH, Black RJ, Scottish Cancer Therapy Network (2001) Prognostic factors in women with breast cancer: distribution by socioeconomic status and effect on differences in survival. J Epidemiol Community Health 55:308–315. doi:10.​1136/​jech.​55.​5.​308 PubMedCrossRef
39.
go back to reference Krieger N (2003) Does racism harm health? did child abuse exist before 1962?—on explicit questions, critical science, and current controversies: an ecosocial perspective. Am J Public Health 93:194–199PubMed Krieger N (2003) Does racism harm health? did child abuse exist before 1962?—on explicit questions, critical science, and current controversies: an ecosocial perspective. Am J Public Health 93:194–199PubMed
40.
go back to reference Ernst W, Harris B (eds) (1999) Race, science, and medicine, 1700–1960. Routledge, London Ernst W, Harris B (eds) (1999) Race, science, and medicine, 1700–1960. Routledge, London
42.
go back to reference Krieger N (2004) Ecosocial theory. In: Anderson N (ed) Encyclopedia of health and behavior. Sage, Thousand Oaks, CA, pp 292–294 Krieger N (2004) Ecosocial theory. In: Anderson N (ed) Encyclopedia of health and behavior. Sage, Thousand Oaks, CA, pp 292–294
44.
go back to reference Davies HT, Crombie IK, Tavakoli M (1998) When can odds ratios mislead? BMJ 316:989–991PubMed Davies HT, Crombie IK, Tavakoli M (1998) When can odds ratios mislead? BMJ 316:989–991PubMed
46.
go back to reference Greenland S, Thomas DC, Morgenstern H (1986) The rare-disease assumption revisited: a critique of “estimators of relative risk for case-control studies”. Am J Epidemiol 124:869–883PubMed Greenland S, Thomas DC, Morgenstern H (1986) The rare-disease assumption revisited: a critique of “estimators of relative risk for case-control studies”. Am J Epidemiol 124:869–883PubMed
49.
go back to reference Krieger N, Chen JT, Waterman PD, Rehkopf DH, Yin R, Coull BA (2006) Race/ethnicity and changing US socioeconomic gradients in breast cancer incidence: California and Massachusetts, 1978–2002. Cancer Causes Control 17:217–226. doi:10.1007/s10552-005-0408-1 PubMedCrossRef Krieger N, Chen JT, Waterman PD, Rehkopf DH, Yin R, Coull BA (2006) Race/ethnicity and changing US socioeconomic gradients in breast cancer incidence: California and Massachusetts, 1978–2002. Cancer Causes Control 17:217–226. doi:10.​1007/​s10552-005-0408-1 PubMedCrossRef
51.
53.
go back to reference Stewart SL, Swallen KC, Glaser SL, Horn-Ross PL, West DW (1999) Comparison of methods for classifying Hispanic ethnicity in a population-based cancer registry. Am J Epidemiol 149:1063–1071PubMed Stewart SL, Swallen KC, Glaser SL, Horn-Ross PL, West DW (1999) Comparison of methods for classifying Hispanic ethnicity in a population-based cancer registry. Am J Epidemiol 149:1063–1071PubMed
55.
go back to reference Clegg LX, Reichman ME, Hankey BF et al (2007) Quality of race, Hispanic ethnicity, and immigrant status in population-based cancer registry data: implications for health disparity studies. Cancer Causes Control 18:177–187PubMedCrossRef Clegg LX, Reichman ME, Hankey BF et al (2007) Quality of race, Hispanic ethnicity, and immigrant status in population-based cancer registry data: implications for health disparity studies. Cancer Causes Control 18:177–187PubMedCrossRef
56.
go back to reference Krieger N, Waterman P, Lemieux K, Zierler S, Hogan JW (2001) On the wrong side of the tracts? Evaluating the accuracy of geocoding in public health research. Am J Public Health 91:1114–1116PubMed Krieger N, Waterman P, Lemieux K, Zierler S, Hogan JW (2001) On the wrong side of the tracts? Evaluating the accuracy of geocoding in public health research. Am J Public Health 91:1114–1116PubMed
57.
go back to reference Krieger N, Chen JT, Waterman PD, Rehkopf DH, Subramanian SV (2005) Painting a truer picture of US socioeconomic and racial/ethnic health inequalities: the Public Health Disparities Geocoding Project. Am J Public Health 95:312–323. doi:10.2105/AJPH.2003.032482 PubMedCrossRef Krieger N, Chen JT, Waterman PD, Rehkopf DH, Subramanian SV (2005) Painting a truer picture of US socioeconomic and racial/ethnic health inequalities: the Public Health Disparities Geocoding Project. Am J Public Health 95:312–323. doi:10.​2105/​AJPH.​2003.​032482 PubMedCrossRef
58.
go back to reference Krieger N, Chen JT, Waterman PD, Rehkopf DH, Subramanian SV (2003) Race/ethnicity, gender, and monitoring socioeconomic gradients in health: a comparison of area-based socioeconomic measures—The Public Health Disparities Geocoding Project. Am J Public Health 93:1655–1671PubMed Krieger N, Chen JT, Waterman PD, Rehkopf DH, Subramanian SV (2003) Race/ethnicity, gender, and monitoring socioeconomic gradients in health: a comparison of area-based socioeconomic measures—The Public Health Disparities Geocoding Project. Am J Public Health 93:1655–1671PubMed
59.
go back to reference Krieger N, Chen JT, Waterman PD, Soobader MJ, Subramanian SV, Carson R (2002) Geocoding and monitoring of US socioeconomic inequalities in mortality and cancer incidence: does the choice of area-based measure and geographic level matter?: The Public Health Disparities Geocoding Project. Am J Epidemiol 156:471–482. doi:10.1093/aje/kwf068 PubMedCrossRef Krieger N, Chen JT, Waterman PD, Soobader MJ, Subramanian SV, Carson R (2002) Geocoding and monitoring of US socioeconomic inequalities in mortality and cancer incidence: does the choice of area-based measure and geographic level matter?: The Public Health Disparities Geocoding Project. Am J Epidemiol 156:471–482. doi:10.​1093/​aje/​kwf068 PubMedCrossRef
61.
go back to reference King G, Honaker J, Joseph A, Scheve K (2001) Analyzing incomplete political science data: an alternative algorithm for multiple imputation. Am Pol Sci Review 95: 49–69 King G, Honaker J, Joseph A, Scheve K (2001) Analyzing incomplete political science data: an alternative algorithm for multiple imputation. Am Pol Sci Review 95: 49–69
63.
66.
go back to reference SAS Institute (2001) SAS language reference, Version 8. SAS Institute, Cary, NC SAS Institute (2001) SAS language reference, Version 8. SAS Institute, Cary, NC
68.
go back to reference Davey Smith G (2000) Learning to live with complexity: ethnicity, socioeconomic position, and health in Britain and the United States. Am J Public Health 90:1694–1698 Davey Smith G (2000) Learning to live with complexity: ethnicity, socioeconomic position, and health in Britain and the United States. Am J Public Health 90:1694–1698
69.
go back to reference Galobardes B, Lynch J, Davey Smith G (2007) Measuring socioeconomic position in health research. Br Med J 81–82:21–37 Galobardes B, Lynch J, Davey Smith G (2007) Measuring socioeconomic position in health research. Br Med J 81–82:21–37
70.
go back to reference Goodman AH (2000) Why genes don’t count (for racial differences in health). Am J Public Health 90:1699–1702PubMedCrossRef Goodman AH (2000) Why genes don’t count (for racial differences in health). Am J Public Health 90:1699–1702PubMedCrossRef
71.
go back to reference Parra EJ, Kittles RA, Shriver MD (2004) Implications of correlations between skin color and genetic ancestry for biomedical research. Nature Genetics 36(suppl):S54–S60. doi:10.1038/ng1440 Parra EJ, Kittles RA, Shriver MD (2004) Implications of correlations between skin color and genetic ancestry for biomedical research. Nature Genetics 36(suppl):S54–S60. doi:10.​1038/​ng1440
75.
go back to reference Petitti D (2004) Commentary: hormone replacement therapy and coronary heart disease: four lessons. Int J Epidemiol 33:461–463. doi: 10.1093/ije/dyh192 Petitti D (2004) Commentary: hormone replacement therapy and coronary heart disease: four lessons. Int J Epidemiol 33:461–463. doi: 10.​1093/​ije/​dyh192
76.
go back to reference Lawlor DA, Davey Smith G, Ebrahim S (2004) Commentary: The hormone replacement-coronary heart disease conundrum: is this the death of observational epidemiology? Int J Epidemiol 33:464–467. doi:10.1093/ije/dyh124 PubMedCrossRef Lawlor DA, Davey Smith G, Ebrahim S (2004) Commentary: The hormone replacement-coronary heart disease conundrum: is this the death of observational epidemiology? Int J Epidemiol 33:464–467. doi:10.​1093/​ije/​dyh124 PubMedCrossRef
77.
go back to reference Krieger N (2007) Why epidemiologists cannot afford to ignore poverty. Epidemiology 18:658–663PubMed Krieger N (2007) Why epidemiologists cannot afford to ignore poverty. Epidemiology 18:658–663PubMed
78.
go back to reference Prentice RL, Chlebowski RT, Stefanick ML, Mansons JE, Langer RD, Pettinger M, Hendrix SL, Hubbell FA, Kooperberg C, Kuller LH, Lane DS, McTiernan A, O’Sullivan MJ, Rossouw JE, Anderson GL (2008). Conjugated equine estrogens and breast cancer risk in the Women’s Health Initiative clinical trial and observational study. Am J Epidemiol 167:1407–1415. doi:10.1093/aje/kwn090 PubMedCrossRef Prentice RL, Chlebowski RT, Stefanick ML, Mansons JE, Langer RD, Pettinger M, Hendrix SL, Hubbell FA, Kooperberg C, Kuller LH, Lane DS, McTiernan A, O’Sullivan MJ, Rossouw JE, Anderson GL (2008). Conjugated equine estrogens and breast cancer risk in the Women’s Health Initiative clinical trial and observational study. Am J Epidemiol 167:1407–1415. doi:10.​1093/​aje/​kwn090 PubMedCrossRef
80.
go back to reference Ravdin PM, Cronin KA, Howlader N, Berg CD, Chlebowski RT, Feuer EJ, Edwards BK, Berry DA (2007) The decrease in breast-cancer incidence in 2003 in the United States. New Engl J Med 356:1670–1674. doi:10.1056/NEJMsr070105 PubMedCrossRef Ravdin PM, Cronin KA, Howlader N, Berg CD, Chlebowski RT, Feuer EJ, Edwards BK, Berry DA (2007) The decrease in breast-cancer incidence in 2003 in the United States. New Engl J Med 356:1670–1674. doi:10.​1056/​NEJMsr070105 PubMedCrossRef
81.
go back to reference Kim S, Egerter S, Cubbin C, Takahashi ER, Braveman P (2007) Potential implications of missing income data in population-based surveys: an example from a postpartum survey in California. Public Health Reports 122:753–764PubMed Kim S, Egerter S, Cubbin C, Takahashi ER, Braveman P (2007) Potential implications of missing income data in population-based surveys: an example from a postpartum survey in California. Public Health Reports 122:753–764PubMed
82.
go back to reference Chen JT, Kaddour A, Krieger N (2008) Re: Kim et al, “Potential Implications of missing income data in population-based surveys”. Public Health Reports 123:260PubMed Chen JT, Kaddour A, Krieger N (2008) Re: Kim et al, “Potential Implications of missing income data in population-based surveys”. Public Health Reports 123:260PubMed
Metadata
Title
Race/ethnicity and breast cancer estrogen receptor status: impact of class, missing data, and modeling assumptions
Authors
Nancy Krieger
Jarvis T. Chen
James H. Ware
Afamia Kaddour
Publication date
01-12-2008
Publisher
Springer Netherlands
Published in
Cancer Causes & Control / Issue 10/2008
Print ISSN: 0957-5243
Electronic ISSN: 1573-7225
DOI
https://doi.org/10.1007/s10552-008-9202-1

Other articles of this Issue 10/2008

Cancer Causes & Control 10/2008 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine