Society of Black Academic Surgeons
Race and recurrence in women who undergo neoadjuvant
chemotherapy for breast cancer
Marissa Howard-McNatt, M.D.a,*, Julia Lawrence, M.D.b, Susan A. Melin, M.D.b,
Edward A. Levine, M.D.a, Perry Shen, M.D.a, John H. Stewart IV, M.D.a
aDepartment of Surgical Oncology, Wake Forest School of Medicine, Medical Center Boulevard, Winston-Salem, NC
27157, USA;bDepartment of Medical Oncology, Wake Forest School of Medicine, Winston-Salem, NC, USA
BACKGROUND: Black women can have worse outcomes than white women with breast cancer. We
examined survival in black and white women who received neoadjuvant chemotherapy.
METHODS: We identified 98 women with stage II or III breast cancer who underwent neoadjuvant
chemotherapy. Women with inflammatory breast cancer, T4 disease, or metastases were excluded. Data
were analyzed using the Fisher exact test and Kaplan-Meier method.
RESULTS: From the cohort, 69 women were included. The median follow-up was 6.2 years. The
estrogen receptor status was similar. White women tended to overexpress human epidermal growth fac-
tor receptor 2 (HER2) (P 5.091). The pretreatment T stage was T3. All women received similar neoad-
juvant chemotherapy. The 5-year progression-free survival was better for white women compared with
black women (78% vs 58%, P 5 .05). The 5-year overall survival was similar (P 5 .095).
CONCLUSIONS: The pretreatment characteristics of women receiving neoadjuvant chemotherapy
were similar. Black women had a worse disease-free survival. The overall survival was the same.
? 2013 Elsevier Inc. All rights reserved.
Black women who are diagnosed with breast cancer
have been reported to have worse outcomes than white
women.1,2The Surveillance Epidemiology and End Results
database noted that the 5-year survival rate in black women
was 71%, whereas in white women it was 86%. Although
the incidence of breast cancer is lower in black women,2,3
they can present with a larger tumor size,4–6an increased
number of positive axillary lymph7nodes, and a more
advanced stage than white women.4–6
When women present with large breast cancers, the
treatment options include mastectomy or neoadjuvant che-
motherapy followed by surgery. Neoadjuvant chemother-
apy is an accepted means of treating locally advanced
breast cancer.8National Surgical Adjuvant Breast and
Bowel Project Protocols B-18 and B-27 showed compara-
ble rates of disease-free and overall survival in patients
undergoing neoadjuvant chemotherapy compared with
adjuvant treatment.9–11However, a clear advantage of neo-
adjuvant chemotherapy is that it can convert patients with
large tumors to candidates for breast conservation.12Racial
differences in women receiving neoadjuvant chemotherapy
have not been examined. We sought to examine survival in
black and white women who received neoadjuvant chemo-
therapy for breast cancer.
Patients were selected from our existing prospective
institutional review board–approved databases. All women
aged 18 or older who received neoadjuvant chemotherapy
The authors declare no conflicts of interest.
E-mail address: firstname.lastname@example.org
Manuscript received June 7, 2012; revised manuscript January 23, 2013
0002-9610/$ - see front matter ? 2013 Elsevier Inc. All rights reserved.
The American Journal of Surgery (2013) 205, 397-401
from 1999 to 2011 were included in this study. Women with
inflammatory breast cancer, T4 disease, or metastatic
disease at the time of diagnosis were excluded.
All patients in the study received neoadjuvant chemo-
therapy after cancer diagnosis. Women with T1 and T2
disease received chemotherapy to downsize the tumor size
in order to undergo a lumpectomy secondary to the ratio of
breast to tumor size. Women with T3 or N2 disease
underwent chemotherapy because of large bulky disease.
The neoadjuvant chemotherapy regimens were selected at
the discretion of the medical oncologist, with patients
receiving anthracycline, taxane, or both. Patients who were
candidates received trastuzumab when their tumor was
found to be HER2 positive and after it became available in
2005. There were no delays or discontinuation in the receipt
of chemotherapy in either group. Radiation was adminis-
tered for all patients who underwent breast conservation.
The dose of radiation was 50 Gy to the entire breast with
6-MV photons followed by an electron beam boost of 16
Gy to the tumor bed. Patients with 3 or more positive nodes
or extracapsular extension also underwent irradiation to the
supraclavicular area (45 Gy) and axilla (50 Gy). Hormone
receptor–positive patients received adjuvant endocrine
therapy with tamoxifen or an aromatase inhibitor. After
completing chemotherapy, patients went to the operating
room for a mastectomy or a lumpectomy as per their
personal choice. Patients with a positive margin after
breast-conserving surgery were re-excised to achieve clear
margins. Margins were re-excised if there was ductal
carcinoma in situ or an invasive tumor ,1 mm from the
cut surface or tumor on ink.
Local-regional recurrence was defined as chest wall
recurrence and/or any regional lymph node basin (axillary,
supraclavicular, or infraclavicular) recurrence. Distant re-
currence was any tumor outside of these regions. Women
who developed metastatic disease were given additional
chemotherapy as per the medical oncologist.
The Kaplan-Meier method was used to generate survival
curves for the time to disease-free survival and overall
survival from the date of diagnosis. Follow-up extended
past 10 years for some patients, but Kaplan-Meier plots
were truncated at 5 years. Fisher exact tests were used to
evaluate differences between groups.
From the initial cohort of98 women, 69 met the inclusion
criteria. The median follow-up of the survivors was 6.2
years. In our cohort, there were 14 (20%) black women and
55 (80%) white women. The mean age was 51 years (49
years for blacks vs 52 years for whites). Table 1 shows the T
and N stage for black and white patients treated with neoad-
in both groups. Black women tended to have larger tumors,
but this did not reach statistical significance (P 5 .095).
There was no difference between estrogen (P 5.76) or pro-
gesterone (P 5.550) or HER2-positive (P 5.091) receptor
status between the 2 groups (Table 1).
All women underwent a similar neoadjuvant chemother-
apy regimen, with the majority receiving anthracycline and
taxane. Of the 18 patients who were HER2 positive, 33%
received trastuzumab. The majority of patients received
adjuvant radiation therapy.
The most common pretreatment stage was T3. There
was similar downsizing of the tumors between black and
white women (P 5.5) (Table 2). A pathologic complete re-
sponse was achieved in 6 (8.6%) of the patients. Black
women were more likely to have a pathologic complete re-
sponse compared with white women (14% vs 7%). Mastec-
tomy and breast-conservation rates were similar between
the 2 groups (P 5 .1219).
Of the 69 patients, 18 (24.6%) had a local regional
recurrence or died after 5 years of receiving treatment.
Black women had 6 local recurrences, whereas white
women experienced 12 recurrences. The 5-year disease-
free survival was better for white women compared with
with breast cancer
Tumor characteristics of Black and White women
Black (%)White (%)P value
included in test)
398The American Journal of Surgery, Vol 205, No 4, April 2013
black women (78% white vs 58% black, P 5 .05; (Fig. 1).
However, the 5-year overall survival was statistically
similar between the 2 groups (80% white vs 60% black,
P 5 .095; Fig. 2). We also analyzed survival for all
triple-negative patients with regard to race and survival.
We found no difference in progression-free or overall sur-
vival when comparing black and white patients with
triple-negative tumors (Fig. 3 & Fig. 4).
Neoadjuvant chemotherapy is an acceptable treatment
for women who present with locally advanced breast
cancer. It can downstage these tumors and enable women
to become candidates for breast-conserving surgery.8–10
Black women who can present with larger tumors can
greatly benefit from using neoadjuvant chemotherapy.
Disease-free survival was worse in black women. There
was a trend toward better overall survival in white women.
We found that the pretreatment tumor characteristics of
tumor size and receptor status were similar between white
and black women. Some studies have found an increased
tumors in black women.3,13DNA microarray profiles can be
used to classify breast tumors into distinct biologic sub-
types.14,15Because this testing may not often be feasible
in the clinical setting, these subtypes can be approximated
by classifying the estrogen, progesterone, and HER2 recep-
tors.16The basal-like subset can be defined as Estrogen Re-
ceptor (ER) negative, Progesterone receptor (PR) negative,
that the basal-like breast cancer subtype was more prevalent
among premenopausal black women (39%) compared with
postmenopausal black women (14%) and white women
(16%) of any age (P , .001).13Despite the fact that the
mean age was 49 years among our black cohort, suggesting
ceptor status may be caused by the small sample size.
We also analyzed disease-free and overall survival
between black and white women with ER-negative breast
cancers. There was no difference in disease-free or overall
survival between these 2 groups. Basal-like breast cancers
tend to exhibit more aggressive features such as an
increased nuclear grade and histologic grade, increased
aldehyde dehydrogenase activity, and a higher proliferative
Comparison of pre- and post-treatment clinical T and N stage with pathologic response to chemotherapy
P value Black (%)White (%)Black (%)White (%)
Unknown (not included in test)
0 2 (14.3)
Progression-free survival by race.
Overall survival by race.
M. Howard-McNatt et al. Women and neoadjuvant chemotherapy 399
index.3,7,17Our cohorts, regardless of race, showed similar
poor outcomes if they had basal-like breast cancers.
Our results show that black women have worse disease-
freesurvivalbutsimilar overall survivalcomparedwithwhite
women receiving neoadjuvant chemotherapy. Woodward
et al18looked at breast cancer patients treated with mastec-
tomy and doxorubicin-based chemotherapy and found worse
overall survival rate in black women compared withHispanic
and white women who received adjuvant and neoadjuvant
chemotherapy (adjuvant hazard ratio 5 1.39, P 5.018; neo-
adjuvant hazard ratio 5 1.37, P 5 .02). They contributed
this to tumor biology and socioeconomic factors, such as
less frequent screening mammograms, less aggressive treat-
ment, and failure to seek medical care. Our cohort had statis-
between the 2 races.All patientsreceivedthe standardofcare
once they were in our institution. However, the sole HER2-
amplified breast cancer patient of African descent did not
receive trastuzumab. This patient was seen at our institution
before the widespread use of trastuzumab in the adjuvant set-
ting. Overall, the findings of similar overall survival between
treatments and compliance of our patients to therapies. We
attribute our compliance to the use of patient navigators for
underrepresented and underinsured women with breast can-
cer. The implementation of a patient navigator program has
been shown to improve the quality of care and compliance
to treatment.19At our institution, the navigators spend an
average of 35 minutes in face-to-face contact dealing mainly
with education and social issues. Patient navigation is so
important that it is a required standard for cancer center ap-
proval by the American College of Surgeons Commission
The limitation of our study is the small sample size and its
retrospective nature from a single institution. If we look
overall survival between women receiving neoadjuvant che-
motherapy. Other factors may contribute to decreased
disease-free survival including young age and tumor biology.
Additional subgroup analysis was not performed because the
numbers became too small to achieve significance.
In summary, we found no difference in overall survival
between black and white women who received neoadjuvant
chemotherapy. However, black women had decreased
disease-free survival. This cohort will continue to be fol-
lowed in an effort to identify determinants of differences in
survival. Neoadjuvant chemotherapy should be offered to all
women regardless of race to downstage large breast tumors.
1. Ries L, Eisner M, Kosary M. SEER Cancer Statistics Review,
1973–1999. Bethesda, MD: National Cancer Institute; 2002.
2. Ries L, Eisner M, Kosary M. SEER Cancer Statistics Review,
1975–2000. Bethesda, MD: National Cancer Institute;; 2003.
3. Newman LA. Breast cancer in African-American women. Oncologist
4. Chen VW, Correa P, Kurman RJ, et al. Histological characteristics of
breast carcinoma in blacks and whites. Cancer Epidemiol Biomarkers
5. Weiss SE, Tarter PI, Ahmed S, et al. Ethnic differences in risk and
prognostic factors for breast cancer. Cancer 1995;76:268–74.
6. Joslyn SA, West MM. Racial differences in breast carcinoma survival.
7. Elledge RM, Clark GM, Chamness GC, et al. Tumor biologic factors
and breast cancer prognosis among white, Hispanic, and black women
in the United States. J Natl Cancer Inst 1994;86:705–12.
8. Sweeting RS, Klauber-DeMore N, Meyers MO, et al. Young women
with locally advanced breast cancer who achieve breast conservation
after neoadjuvant chemotherapy have a low local recurrence rate.
Am Surg 2011;77:850–5.
9. Fisher B, Brown A, Mamounas E, et al. Effect of preoperative chemo-
therapy on local-regional disease in women with operable breast can-
cer: findings from the National Surgical Adjuvant Breast and Bowel
Project B-18. J Clin Oncol 1997;15:2483–93.
10. Rastogi P, Anderson SJ, Bear HD, et al. Preoperative chemotherapy:
updates of National Surgical Adjuvant Breast and Bowel Project
Protocols B-18 and B-27. J Clin Oncol 2008;26:778–85.
11. Bear HD, Anderson S, Smith RE, et al. Sequential preoperative or
postoperative docetaxel added to preoperative doxorubicin plus cyclo-
phosphamide for operable breast cancer: National Surgical Adjuvant
Breast and Bowel Project Protocol B-27. J Clin Oncol 2006;24:
Triple-negative patients’ progression-free survival by
Triple-negative patients’ overall survival by race.
400The American Journal of Surgery, Vol 205, No 4, April 2013
12. Beriwal S, Schwartz GF, Komarnicky L, et al. Breast-conserving ther- Download full-text
apy after neoadjuvant chemotherapy: long-term results. Breast J 2006;
survival in the Carolina Breast Cancer Study. JAMA 2006;295:2492–502.
14. Perou CM, Sorlie T, Eisen MB, et al. Molecular portraits of human
breast tumours. Nature 2000;406:747–52.
15. Sorlie T, Perou CM, Tibshirani R, et al. Gene expression patterns of
breast carcinomas distinguish tumor subclasses with clinical implica-
tions. Proc Natl Acad Sci U S A 2001;98:10869–74.
16. Brenton JD, Carey LA, Ahmed AA, et al. Molecular classification and
molecular forecasting of breast cancer. Ready for clinical application?
J Clin Oncol 2005;23:7350–60.
17. DeBrot M, Rocha RM, Soares FA, et al. Prognostic impact of the
cancer stem cell related markers ALDH1 and EZH2 in triple negative
and basal-like breast cancers. Pathology 2012;44:303–12.
18. Woodward WA, Huang EH, McNeese MD, et al. African-American
race is associated with a poorer overall survival rate for breast cancer
patients treated with mastectomy and doxorubicin-based chemother-
apy. Cancer 2006;107:2662–8.
19. Weber JJ, Mascarenhas DC, Bellin LS, et al. Patient navigation and the
quality of breast cancer care: an analysis of the Breast Cancer Care
Quality Indicators. Ann Surg Oncol 2012;19:3251–6.
20. Commission of Cancer, Cancer Program Standards 2012: Ensuring
Patient-Centered Care, v1.0. Available at: http://www.facs.org/cancer/
coc/cocprogramstandards2012.pdf. Accessed January 7, 2013.
M. Howard-McNatt et al. Women and neoadjuvant chemotherapy401