1721

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

Katrina R. Bauer, MS CTR1 BACKGROUND. Tumor markers are becoming increasingly important in breast can-
Monica Brown, PhD2 cer research because of their impact on prognosis, treatment, and survival, and
Rosemary D. Cress, DrPH1,3 because of their relation to breast cancer subtypes. The triple-negative phenotype
Carol A. Parise, PhD4 is important because of its relation to the basal-like subtype of breast cancer.
Vincent Caggiano, MD4,5 METHODS. Using the population-based California Cancer Registry data, we identi-
fied women diagnosed with triple-negative breast cancer between 1999 and 2003.
1
Public Health Institute/California Cancer Regis- We examined differences between triple-negative breast cancers compared with
try, Sacramento, California. other breast cancers in relation to age, race/ethnicity, socioeconomic status
2
Public Health Institute/Cancer Surveillance Pro- (SES), stage at diagnosis, tumor grade, and relative survival.
gram, Sacramento, California. RESULTS. A total of 6370 women were identified as having triple-negative breast cancer
3 and were compared with the 44,704 women with other breast cancers. Women with tri-
Department of Health Sciences, Division of Epi-
demiology, UC Davis, California. ple-negative breast cancers were significantly more likely to be under age 40 (odds ratio
4
[OR], 1.53), and non-Hispanic black (OR, 1.77) or Hispanic (OR, 1.23). Regardless of
Sutter Institute for Medical Research, Sacra-
stage at diagnosis, women with triple-negative breast cancers had poorer survival than
mento, California.
those with other breast cancers, and non-Hispanic black women with late-stage triple-
5
Sutter Cancer Center/Cancer Surveillance Pro- negative cancer had the poorest survival, with a 5-year relative survival of only 14%.
gram, Sacramento, California.
CONCLUSIONS. Triple-negative breast cancers affect younger, non-Hispanic black
and Hispanic women in areas of low SES. The tumors were diagnosed at later stage
and were more aggressive, and these women had poorer survival regardless of stage.
In addition, non-Hispanic black women with late-stage triple-negative breast can-
cer had the poorest survival of any comparable group. Cancer 2007;109:1721–8.

2007 American Cancer Society.

KEYWORDS: breast neoplasms, estrogen receptors, progesterone receptors, HER2/

The collection of cancer incidence data used in neu, continental population groups, ethnic groups, health disparities.
the study was supported by the California
Department of Health Services as part of the sta-
tewide cancer reporting program mandated by
California Health and Safety Code Section
103885; the National Cancer Institute’s Surveil-
B reast cancer is the most common cancer among women in Cali-
fornia, accounting for approximately one-third of newly diag-
nosed cancers.1 Racial disparities in breast cancer outcomes have
lance, Epidemiology, and End Results Program been well documented,2–7 with African American women having a
under contract N01-PC-35136 awarded to the
Northern California Cancer Center, contract N01- The ideas and opinions expressed herein are those Address for reprints: Katrina R. Bauer, MS,
PC-35139 awarded to the University of Southern
of the author(s) and endorsement by the State of Research Associate IV, California Cancer Registry,
California, and contract N02-PC-15105 awarded
California, Department of Health Services, the Public Health Institute, 1700 Tribute Rd. Ste. 100,
to the Public Health Institute; and the Centers for National Cancer Institute, and the Centers for Dis- Sacramento, CA 95815-4402; Fax: (916) 779-
Disease Control and Prevention’s National Pro- ease Control and Prevention or their Contractors 2608 E-mail: kbauer@ccr.ca.gov
gram of Cancer Registries, under agreement
and Subcontractors is not intended nor should be
U55/CCR921930-02 awarded to the Public Health inferred. Received September 26, 2006; revision received
Institute. December 7, 2006; accepted January 23, 2007.

ª 2007 American Cancer Society

DOI 10.1002/cncr.22618
Published online 26 March 2007 in Wiley InterScience (www.interscience.wiley.com).
1722 CANCER May 1, 2007 / Volume 109 / Number 9
lower incidence of breast cancer compared with
whites but a higher overall mortality.2,8 In California
the relative burden of invasive breast cancer varies by
age and by race/ethnicity. Thus, breast cancer com-
prises nearly one-quarter (24.4%) of all new invasive
cancers in black women aged 20 to 29 years, whereas
it only represents 9.1% in non-Hispanic whites. Simi-
larly, average age-adjusted mortality rates for African
American women less than 50 years of age are
reported at 11.9 deaths per 100,000, or nearly twice
the rate in non-Hispanic whites (6.0 deaths per
100,000). Even after age 50, black women continue to
have the highest mortality rate.2
Determination of estrogen receptor (ER) status of
invasive breast carcinoma is useful as a prognostic
and predictive factor and has become standard prac-
tice in the management of this neoplasm. ER positiv-
ity predicts for response to endocrine therapy such as
antiestrogen (tamoxifen) administration or ovarian
suppression. Similarly, human epidermal growth fac-
tor receptor 2 (HER2) positivity is useful for selecting
targeted therapy with monoclonal antibody (trastu-
zumab) against HER2. Recently, microarray profiling
of invasive breast carcinoma has identified 5 distinct
subtypes of morphologically similar breast cancers
(luminal A, luminal B, normal breast-like, HER2-over-
expressing, and basal-like).9 The basal-like subtype,
accounting for about 15% of breast cancer cases and
characterized by negativity for ER, progesterone re-
ceptor (PR), and HER2, is associated with aggressive
histology, poor prognosis, and unresponsiveness to
the usual endocrine therapies, shorter survival, and
BRCA1-related breast cancer.9–12
Because basal-like breast cancers are ER-, PR-,
and HER2-negative, they are sometimes called ‘triple-
negative,’ although it should be noted that only about
85% of triple-negative phenotypic breast cancers are
deemed to be basal-like when tested by appropriate
immunohistochemical means.13,14 To help develop
treatment strategies for this subtype of breast cancer,
we undertook the present study to better characterize
the triple-negative phenotype with respect to age,
race/ethnicity, socioeconomic status, and survival.
MATERIALS AND METHODS
Case Identification
Data included in this study were identified using the
California Cancer Registry (CCR), a population-based
registry composed of 8 regional registries collecting
cancer incidence and mortality data for the entire
population of California. A state law passed in 1985
mandated the reporting of all newly diagnosed can-
cers in California, and statewide implementation
began January 1, 1988. Cases are reported to the Can-
cer Surveillance Section of the California Department
of Health Services from hospitals and any other facil-
ities providing care or therapy to cancer patients
residing in California.15
First primary cases of invasive, female breast can-
cer (ICDO-3 sites C50.0-C50.9)16 diagnosed between
January 1, 1999, and December 31, 2003, and reported
to the CCR as of April 2006, are presented in these
analyses. A case was defined as triple-negative if ER,
PR, and HER2 were negative and the remaining breast
cancer cases, where tumor marker status was known,
were defined as other breast cancers.
The CCR requires the collection of tumor marker
information from the medical record on the status of
ER and PR for breast cancers diagnosed on or after
January 1, 1990, and the status of HER2 for breast can-
cers diagnosed on or after January 1, 1999.15 ER and
PR status are recorded according to the pathologist’s
interpretation of the assays. ER and PR are considered
negative if immunoperoxidase staining of tumor cell
nuclei is less than 5%. ER and PR status can also be
determined by examining cytosol protein. ER is con-
sidered negative if there are fewer than 3 femtomoles
per milligram of cytosol protein and PR is considered
negative if there are fewer than 5 femtomoles per
milligram of cytosol protein.17 HER2 was assessed
through immunohistochemistry (IHC) or fluorescence
in situ hybridization (FISH). IHC is scored on a quali-
tative scale from 0 to 31, based on interpretation of
staining intensity, with 0 and 11 classified as negative,
21 as borderline, and 31 as positive.18 FISH is scored
on a quantitative scale with less than 2 copies of the
HER2 gene classified as negative.19
Variables
Race/ethnicity was classified into 4 mutually exclusive
categories of Asian-Pacific Islander, Hispanic, non-
Hispanic black, and non-Hispanic white. Race/ethni-
city was based on information obtained from the
medical record, which can be derived from patient
self-identification, assumptions based on personal
appearance, or inferences based on the race/ethnicity
of the parents, birthplace, surname, or maiden name.
Hispanic ethnicity was based on information from the
medical record and computerized comparisons to the
1980 US census list of Hispanic surnames. Patients
identified as Hispanic on the medical record, or
patients identified as white, black, or of unknown race
with a Hispanic surname were classified as Hispanic.
Cases with unknown race/ethnicity, age, or sex were
excluded from these analyses.
Quintile of socioeconomic status (SES) was de-
rived from a principle component analysis using data

from the 2000 US census.20 SES was assigned at the
census block group level (2000 US census) and based
on address at time of initial diagnosis as reported in
the medical record.
Stage at diagnosis was collected from the patient’s
medical record and coded according to the American
Joint Commission on Cancer (AJCC) Cancer Staging
Manual, 6th ed.21 The CCR collected Surveillance,
Epidemiology, and End Results (SEER) extent of disease
(EOD)22 for breast cancer cases diagnosed from 1988
through December 2004. EOD was converted to AJCC
stage at diagnosis using SEER guidelines.23 For logistic
regression and survival analyses, stage III and stage IV
were combined owing to small cell counts. Tumor grade
was collected from the medical record and coded accord-
ing to ICDO-3.16 Tumor size in millimeters was collected
from the medical record according to SEER EOD.22
Statistical Analysis
Proportions and 95% confidence intervals (CI) were
calculated for age, race, SES, and tumor characteristic
comparisons, including AJCC stage and tumor grade.
T-tests were used to detect differences in average age
and tumor size between the 2 breast cancer groups.
Tests of independent proportions were used to detect
differences for age group, race, SES, AJCC stage, and
tumor grade.24 Bivariate and multiple logistic regres-
sion analyses were performed to calculate odds ratios
(OR) and 95% CIs for demographic differences
between triple-negative breast cancers and other
breast cancers. ORs from the multiple logistic regres-
sion were adjusted for age, race, SES, AJCC stage, and
tumor grade. Counts and 5-year relative cumulative
survival, a type of overall survival, were calculated
using SEER*Stat 6.1.4. The actuarial method was used
for relative survival calculations. SAS (Cary, NC) 9.1.3
was used for logistic regression analyses.
RESULTS
Of the 92,358 women with first primary breast cancer
diagnosed between 1999 and 2003, 51,074 (55.3%)
were found to have the 3 markers and 41,284 (44.7%)
were missing 1 or more of the markers. We performed
2 sets of analyses, first comparing triple-negatives to
other breast cancers with known tumor marker status,
and second comparing triple-negatives to other breast
cancers including cases with at least 1 unknown
tumor marker. The bivariate and multivariate compar-
isons were nearly identical, with no differences in sta-
tistical significance with regard to median age, age
groupings, stage, race/ethnicity, SES, and overall rela-
tive 5-year survival. Only those cases with known
tumor marker status were included in these analyses.
Triple-Negative Breast Cancers/Bauer et al. 1723
The triple-negative phenotype was observed in 6370
(12.5%) of the eligible breast cancer cases, and the
remaining 44,704 cases were classified as ‘‘other
breast cancers.’’
Table 1 shows the demographic characteristics of
the 51,074 women with known tumor marker status.
The median age at diagnosis for the triple-negative
group was 54 years, significantly less than 60 years for
the other breast cancer group. Approximately 63% of
women with triple-negative breast cancer were diag-
nosed before age 60, whereas fewer than half of
women with other breast cancer were diagnosed in
that age range. Although the majority of women with
breast cancer were non-Hispanic white, a smaller pro-
portion (62%) was observed among the triple-negative
group when compared with women with other breast
cancers (73%). The percent of non-Hispanic black
women among the triple-negative group was twice
that of the other breast cancer group (P < .001). The
proportion of Hispanic women in the triple-negative
group was also significantly higher than the propor-
tion in the other breast cancer group. No significant
difference was noted for Asian-Pacific Islanders. In
addition, one-quarter of non-Hispanic blacks (24.6%)
were found to have the triple-negative phenotype,
whereas the percent of non-Hispanic whites or Asian-
Pacific Islanders with triple-negative features was low,
10.8% and 11.7%, respectively (data not shown). His-
panics were intermediate at 17.2%.
Among both groups of women the percent of all
breast cancers increased as SES increased, although
women with triple-negative breast cancer had a larger
proportion diagnosed in areas of low SES. Stage at di-
agnosis was significantly different between the 2
groups, with the triple-negative patients presenting at
a more advanced stage. Median tumor size was signif-
icantly larger for the triple-negative group (22 mm
versus 17 mm, P < .001). The vast majority of triple-
negative breast cancers (76%) were classified as poorly
differentiated or undifferentiated, whereas only 28%
of the other breast cancer group were so categorized
(P < .001).
Table 2 shows the adjusted ORs and 95% CIs from
the multiple logistic regression analyses for patient
demographics of triple-negative breast cancers com-
pared with other breast cancers. The odds of having
triple-negative breast cancer increased with younger
age, with women less than age 40 being 1.53 times
more likely than 60 to 69-year-olds to be diagnosed
with triple-negative breast cancer. Non-Hispanic
black women were nearly twice as likely to be diag-
nosed with triple-negative breast cancer when com-
pared with non-Hispanic whites, and Hispanic
women were slightly more likely to be diagnosed with
1724 CANCER May 1, 2007 / Volume 109 / Number 9

TABLE 1
Characteristics of Invasive Breast Cancer Cases in Women in California With Known Tumor Marker Status,
1999–2003

Triple negative N = 6370 Other breast cancers N = 44,704

Characteristics No. (%) No. (%) P*

Total 6370 44704

Age at diagnosis, median 54 60 <.001
<40 778 (12.2) 2534 (5.7) <.001
40–49 1553 (24.4) 8359 (18.7) <.001
50–59 1690 (26.5) 11,415 (25.5) .192
60–64 1108 (17.4) 9616 (21.5) <.001
70–79 817 (12.8) 8671 (19.4) <.001
80 424 (6.7) 4109 (9.2) .027
Race/ethnicity
Non-Hispanic white 3959 (62.2) 32,712 (73.2) <.001
Non-Hispanic black 636 (10.0) 1951 (4.4) <.001
Hispanic 1187 (18.6) 5714 (12.8) <.001
Asian/Pacific Islander 537 (8.4) 4043 (9.0) .319
Other 51 (0.8) 284 (0.6) .44
SES
SES 1, Low 830 (13.0) 4344 (9.7) <.001
SES 2 1180 (18.5) 6701 (15.0) <.001
SES 3 1345 (21.1) 8969 (20.1) .2
SES 4 1479 (23.2) 11,014 (24.6) .116
SES 5, High 1536 (24.1) 13,676 (30.6) <.001
Tumor size in mm, median 22 17 <.001
AJCC stage at diagnosis
Stage I 2088 (32.8) 20,439 (45.7) <.001
Stage II 3099 (48.6) 17,919 (40.1) <.001
Stage III 686 (10.8) 3016 (6.7) .001
Stage IV 248 (3.9) 1440 (3.2) <.001
Unknown 249 (3.9) 1887 (4.2) .409
Tumor grade
Well differentiated 195 (3.1) 10,091 (22.6) <.001
Moderately differentiated 1003 (15.7) 18,786 (42.0) <.001
Poorly differentiated 4526 (71.1) 11,825 (26.5) <.001
Undifferentiated 333 (5.2) 773 (1.7) .004
Unknown 313 (4.9) 3229 (7.2) .039

SES indicates socioeconomic status.

* t-tests were used to test for differences in means for age and tumor size, and tests of independent proportions were used to test for differences for race, SES,
stage, and grade.

triple-negative breast cancer. Compared with women
living in areas of the highest quintile of SES, women
living in areas of lower SES were more likely to be
diagnosed with triple-negative breast cancer than
other breast cancers. However, women in the lowest
level of SES were only marginally significantly more
likely to be triple-negative.
Relative survival for women with triple-negative
breast cancer was poorer than for women with other
types of breast cancer, with 77% of women surviving 5
years after diagnosis, compared with 93% survival for
other breast cancers (Fig. 1). Figure 2 demonstrates
these differences in relative survival by stage at diag-
nosis and by race/ethnicity. Women with triple-nega-
tive breast cancer had consistently poorer survival
when compared with women with other breast can-
cers for each stage and race group. For women diag-
nosed at AJCC stage I (Fig. 2, top), Hispanic women
with triple-negative breast cancers had the worst
5-year cumulative relative survival, although their sur-
vival rates were just over 90%, and the difference was
not statistically significant. For women diagnosed at
stage II (Fig. 2, middle), non-Hispanic whites, Hispa-
nics, and non-Hispanic blacks with triple-negative
breast cancer had statistically significant lower sur-
vival than all race groups among the women with
other breast cancers. In addition, among women with
stage II breast cancers, non-Hispanic black women
had the poorest survival, although the difference was
not significant when compared with other stage II tri-
 Triple-Negative Breast Cancers/Bauer et al. 1725

TABLE 2
Adjusted Odds Ratios* and 95% Confidence Intervals for Patient
Characteristics and Triple-Negative Phenotype Among Women With
Breast Cancer in California, 1999–2003

Adjusted odds
No. (%) ratio 95% CI

Age group at diagnosis

<40 3312 (6.5) 1.53 1.37–1.70
40–49 9912 (19.4) 1.20 1.10–1.31
50–59 1310 5 (25.7) 1.12 1.02–1.22
60–69 10,724 (21.0) 1.00 1.00–1.00
70–79 9488 (18.6) 0.90 0.81–0.99
801 4533 (8.9) 0.98 0.86–1.11
Race/ethnicity
Non-Hispanic white 36,671 (71.8) 1.00 1.00–1.00
Non-Hispanic black 2587 (5.1) 1.77 1.59–1.97
Hispanic 6901 (13.5) 1.23 1.14–1.34 FIGURE 1. Five-year relative survival of triple-negative breast cancers
Asian/Pacific Islander 4580 (9.0) 0.86 0.77–0.95 compared with other breast cancers by stage at diagnosis, California,
Other 335 (0.7) 1.42 1.03–1.97
1999 2003.
SES
SES1, Low 5174 (10.1) 1.12 1.01–1.24
SES2 7881 (15.4) 1.22 1.12–1.34 treatment,26,27 or socioeconomic factors.7,28,29 Other
SES3 10,314 (20.2) 1.14 1.05–1.24 investigations have shown that equal access to medi-
SES4 12,493 (24.5) 1.08 1.00–1.17 cal care does not eliminate completely the survival
SES5, High 15,212 (29.8) 1.00 1.00–1.00
disadvantage for African American women,30–33 and
SES indicates socioeconomic status.
race alone has been suggested as an independent pre-
* Adjusted for age, race, SES, AJCC stage, and tumor grade. dictor for survival.34–36 African American women were
noted to have significantly earlier age at diagnosis,
high grade tumors, and a higher proportion of ER-
ple-negative breast cancers. Non-Hispanic black
negative and PR-negative cancers,3,6,37–42 suggesting
women diagnosed at late stage (Fig. 2, bottom) with
that breast cancer is biologically different in African
triple-negative breast cancer had the poorest survival
American women.
of any other comparable group, with only 14% surviv-
The molecular classification of breast cancer,
ing 5 years after diagnosis, compared with 49% 5-year
based on DNA microarray technology, into luminal,
relative survival among non-Hispanic black women
basal, and HER2 subtypes with distinct differences in
with other breast cancers diagnosed at late stage, as
prognosis and response to therapy, is a vivid illustra-
well as 36% survival among non-Hispanic white and
tion of the heterogeneity of breast cancer. The basal-
37% among Hispanic women with late stage triple-
like subtype, characterized by lack of expression of ER
negative breast cancer.
and PR, low or absent expression of HER2, and IHC
expression for cytokeratins usually expressed in the
basal cells of the breast (CK5 and CK14), is associated
DISCUSSION with aggressive histology, poor clinical outcomes, and
In this large population-based study of invasive breast BRCA1-related breast cancer.9–12 First presented dur-
cancer, we found the triple-negative phenotype to be ing the 2004 American Society of Clinical Oncology
significantly associated with younger age, African annual meeting,43 Carey et al.44 have shown that the
American race/ethnicity, more advanced stage at di- basal-like breast cancer subtype is more prevalent
agnosis, poorly differentiated histology, lower SES, among premenopausal African American women and
and shortened survival. is a contributing factor to the poor prognosis of young
Racial disparities in breast cancer incidence and African American women with breast cancer.
mortality have been well documented in the past, and The present study, based solely on population-
numerous studies have shown that African American based registry data without the benefit of microarray
women have a lower incidence of breast cancer but or IHC confirmation of the basal-like subtype, illus-
worse survival when compared with white women.2–8 trates the value of the triple-negative phenotype as a
Possible explanations advanced for this disparity in surrogate marker for basal-like cancer. Age less than
breast cancer mortality include lack of access to 40 years, being non-Hispanic black and, to a lesser
health insurance and medical care,25 differences in extent, being Hispanic, are clearly the most powerful
1726 CANCER May 1, 2007 / Volume 109 / Number 9
FIGURE 2. Top: Five-year relative survival for women with breast cancer
diagnosed at AJCC stage I, triple-negative breast cancers versus other breast
cancers, California, 1999 2003. Middle: Five-year relative survival for women
with breast cancer diagnosed at AJCC stage II, triple-negative breast cancers
versus other breast cancers, California, 1999 2003. Bottom: Five-year relative
survival for women with breast cancer diagnosed at AJCC stage III-IV, triple-
negative breast cancers versus other breast cancers, California, 1999 2003.
risk factors for this poor prognosis subtype of breast
cancer. Because the triple-negative phenotype is not
amenable to any form of endocrine therapy,
efforts are underway to develop appropriate targeted
therapies.45
We acknowledge the limitations of this study.
First, this is strictly a population-based cancer registry
investigation. Second, histologic grading of tumors, as
well as tests for ER, PR, and HER2, were performed by
a wide variety of laboratories without central review.
Third, almost half the initial study population lacked
information about ER, PR, and HER2, with the latter
constituting the bulk of missing data. In 1999 the CCR
began collection of HER2 results but over 50% of
newly diagnosed breast cancers lacked this test result.
By 2003, HER2 testing of primary breast cancer was
more common and more than 70% of breast cancer
cases were found to have HER2 on record. The results
from our analysis comparing triple-negative cases to
other breast cancers with at least 1 tumor marker
coded as unknown were nearly identical to the com-
parisons between triple-negatives and other breast
cancers with known tumor marker status. Thus, we
feel confident that these 2 groups were fairly compa-
rable. Fourth, our study examined the triple-negative
phenotype without confirmatory microarray or IHC
assays. We recognize that triple-negativity does not
automatically equate with the basal-like breast cancer.
However, the proportion of the triple-negative pheno-
type found in the present study (12.5%) corresponds
well to the reported incidence of the basal-like breast
cancer.12,45,46
Despite these shortcomings, our study is of value
because 1) it includes a sufficiently adequate number
of breast cancer cases; 2) it reflects real-world experi-
ence of a large, statewide cancer registry in an ethni-
cally diverse population; 3) it highlights the importance
of the triple-negative phenotype, now readily available
for all new breast cancer cases, as a surrogate marker
for basal-like breast cancer; 4) it emphasizes the role of
younger age and race/ethnicity (African American and
Hispanic) as important risk factors; and 5) it clearly
reveals the survival disadvantage of the triple-negative
phenotype and may help hasten the development of
specific targeted therapy for this subtype of breast can-
cer. Further research regarding the contribution of
each of the tumor markers is underway with survival
analyses adjusting for multiple risk factors.
REFERENCES
1. American Cancer Society. California Facts and Figures
2006. Oakland, CA: California Division and Public Health
Institute, California Cancer Registry; 2005.
2. Campleman S, Curtis R. Demographic aspects of breast
cancer incidence and mortality in California, 1988–1999.
In: Morris C, Kwong SL, eds. Breast Cancer in California,
2003 Sacramento, CA: California Department of Health Ser-
vices, Cancer Surveillance Section, July 2004.

3. Chu KC, Lamar CA, Freeman HP. Racial disparities in
breast carcinoma survival rates: separating factors that
affect diagnosis from factors that affect treatment. Cancer.
2003;97:2853–2860.
4. Polite BN, Olopade OI. Breast cancer and race: a rising tide
does not lift all boats equally. Perspect Biol Med. 2005;48(1
Suppl):S166–175.
5. Chlebowski RT, Chen Z, Anderson GL, et al. Ethnicity and
breast cancer: factors influencing differences in incidence
and outcome. J Natl Cancer Inst. 2005;97:439–448.
6. Cunningham JE, Butler WM. Racial disparities in female
breast cancer in South Carolina: clinical evidence for a bio-
logical basis. Breast Cancer Res Treat. 2004;88:161–176.
7. Newman LA. Breast cancer in African-American women.
Oncologist. 2005;10:1–14.
8. Ries L, Eisner M, Kosary M. SEER Cancer Statistics Review,
1975–2000. Bethesda, MD: National Cancer Institute, 2003.
9. Perou CM, Sorlie T, Eisen MB, et al. Molecular portraits of
human breast tumours. Nature. 2000;406:747–752.
10. Sorlie T, Tibshirani R, Parker J, et al. Repeated observation
of breast tumor subtypes in independent gene expression
data sets. Proc Natl Acad Sci U S A. 2003;100:8418–8423.
11. Sorlie T, Perou CM, Tibshirani R, et al. Gene expression
patterns of breast carcinomas distinguish tumor subclasses
with clinical implications. Proc Natl Acad Sci U S A.
2001;98:10869–10874.
12. Foulkes WD, Stefansson IM, Chappuis PO, et al. Germline
BRCA1 mutations and a basal epithelial phenotype in
breast cancer. J Natl Cancer Inst. 2003;95:1482–1485.
13. Livasy CA, Karaca G, Nanda R, et al. Phenotypic evaluation
of the basal-like subtype of invasive breast carcinoma. Mod
Pathol. 2006;19:264–271.
14. Kandel MJ, Stadler Z, Masciari S, et al. Prevalence of
BRCA1 mutations in triple negative breast cancer (BC). J
Clin Oncol (Meeting Abstracts). 2006;24(18 Suppl):508.
15. Cancer Reporting in California: Abstracting and Coding
Procedures for Hospitals. California Cancer Reporting Sys-
tem Standards. Vol. I. Sacramento, CA: California Depart-
ment of Health Services, Cancer Surveillance Section, 2006.
16. Fritz AG. International classification of diseases for oncol-
ogy: ICD-O. 3rd ed. Geneva: World Health Organization;
2000.
17. Fritz A.Recording tumor markers in collaborative staging
system site-specific factors. Available from URL: http://
www.cancerstaging.org/cstage/tumormarkers.pdf Accessed
April on 28, 2006.
18. DAKO HERCEPTest Information Web site. Summary of Pro-
cedure, Vol. 2006, October 15, 2003. Available from URL:
http://www.herceptin.com/herceptin/professional/testing/
faqs.jsp Accessed on June 7, 2006.
19. PathVysion. HER-2 DNA probe kit package insert. Vysis,
Downers Grove, CA, February, 2002.
20. Yost K, Perkins C, Cohen R, Morris C, Wright W. Socioeco-
nomic status and breast cancer incidence in California
for different race/ethnic groups. Cancer Causes Control.
2001;12: 703–711.
21. Greene FL, Page DL, Fleming ID, et al. AJCC Cancer Sta-
ging Manual. 6th ed. New York: Springer; 2002.
22. SEER Extent of Disease 1998, Codes and Coding Instruc-
tions. 3rd ed. Bethesda, MD: National Cancer Institute,
National Institutes of Health; 1998.
23. Seiffert JE,National Cancer Institute (U.S.). SEER Program:
Comparative Staging Guide for Cancer. Bethesda, MD: U.S.
Dept. of Health and Human Services Public Health Service
Triple-Negative Breast Cancers/Bauer et al. 1727
National Institutes of Health National Cancer Institute,
1993.
24. Fleiss JL, Levin BA, Paik MC. Statistical Methods for Rates
and Proportions. 3rd ed. Hoboken, NJ: Wiley-Interscience;
2003.
25. Ayanian JZ, Kohler BA, Abe T, Epstein AM. The relation
between health insurance coverage and clinical outcomes
among women with breast cancer. N Engl J Med. 1993;329:
326–331.
26. Breen N, Wesley MN, Merrill RM, Johnson K. The relation-
ship of socio-economic status and access to minimum
expected therapy among female breast cancer patients in
the National Cancer Institute Black-White Cancer Survival
Study. Ethn Dis. 1999;9:111.
27. McWhorter WP, Mayer WJ. Black/white differences in type
of initial breast cancer treatment and implications for sur-
vival. Am J Public Health. 1987;77:1515–1517.
28. Bradley CJ, Given CW, Roberts C. Race, socioeconomic sta-
tus, and breast cancer treatment and survival. J Natl Can-
cer Inst. 2002;94:490–496.
29. Gordon NH. Socioeconomic factors and breast cancer in
black and white Americans. Cancer Metastasis Rev. 2003;22:
55–65.
30. Field TS, Buist DS, Doubeni C, et al. Disparities and sur-
vival among breast cancer patients. J Natl Cancer Inst
Monogr. 2005:88–95.
31. Jatoi I, Becher H, Leake CR. Widening disparity in survival
between white and African-American patients with breast
carcinoma treated in the U. S. Department of Defense
Healthcare system. Cancer. 2003;98:894–899.
32. Wojcik BE, Spinks MK, Optenberg SA. Breast carcinoma
survival analysis for African American and white women
in an equal-access health care system. Cancer. 1998;82:
1310–1318.
33. Albain KS, Unger J, Hutchins LF.Outcome of African Ameri-
cans on Southwest Oncology Group (SWOG) breast cancer
adjuvant therapy trials. San Antonio Breast Cancer Sympo-
sium 2003:21.
34. Joslyn SA, West MM. Racial differences in breast carcinoma
survival. Cancer. 2000;88:114–123.
35. Newman LA, Griffith KA, Jatoi I, Simon MS, Crowe JP, Col-
ditz GA. Meta-analysis of survival in African American and
white American patients with breast cancer: ethnicity com-
pared with socioeconomic status. J Clin Oncol. 2006;24:
1342–1349.
36. Newman LA, Mason J, Cote D, et al. African-American eth-
nicity, socioeconomic status, and breast cancer survival: a
meta-analysis of 14 studies involving over 10,000 African-
American and 40,000 white American patients with carci-
noma of the breast. Cancer. 2002;94:2844–2854.
37. Aziz H, Hussain F, Sohn C, et al. Early onset of breast carci-
noma in African American women with poor prognostic
factors. Am J Clin Oncol. 1999;22:436–440.
38. Furberg H, Millikan R, Dressler L, Newman B, Geradts J.
Tumor characteristics in African American and white
women. Breast Cancer Res Treat. 2001;68:33–43.
39. Henson DE, Chu KC, Levine PH. Histologic grade, stage,
and survival in breast carcinoma: comparison of African
American and Caucasian women. Cancer. 2003;98:908–917.
40. Jones BA, Kasl SV, Howe CL, et al. African-American/white
differences in breast carcinoma: p53 alterations and other
tumor characteristics. Cancer. 2004;101:1293–1301.
41. Newman LA, Alfonso AE. Age-related differences in breast
cancer stage at diagnosis between black and white patients
1728 CANCER May 1, 2007 / Volume 109 / Number 9
in an urban community hospital. Ann Surg Oncol. 1997;4:
655–662.
42. Shavers VL, Harlan LC, Stevens JL. Racial/ethnic variation
in clinical presentation, treatment, and survival among
breast cancer patients under age 35. Cancer. 2003;97:134–
147.
43. Carey LA, Perou CM, Dressler LG, et al. Race and the poor
prognosis basal breast tumor (BBT) phenotype in the
population-based Carolina Breast Cancer Study (CBCS). J
Clin Oncol (Meeting Abstracts). 2004;22(14 Suppl):9510.
44. 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.
45. Nielsen TO, Hsu FD, Jensen K, et al. Immunohistochemical
and clinical characterization of the basal-like subtype of inva-
sive breast carcinoma. Clin Cancer Res. 2004;10:5367–5374.
46. Rodriguez-Pinilla SM, Sarrio D, Honrado E, et al. Prognos-
tic significance of basal-like phenotype and fascin expres-
sion in node-negative invasive breast carcinomas. Clin
Cancer Res. 2006;12:1533–1539.