Download Overall Survival of Chinese Female Patients with Stage Ⅰ～Ⅲ

Chinese Female Breast Cancer Patients Show A Better Overall Survival Than Their
Male Counterparts
XIA Liangping,1,2 ZHOU Feifei,1,2 GUO Guifang,1,2 WANG Fang,1,2 WANG Xi,1,3YUAN
Zhongyu1,4 and ZHUAN Bei1,2
1 State Key Laboratory of Oncology in South China, Sun Yat-sen Universty Cancer Center,
Guangzhou, Guangdong, 510060, R.P. China
2 VIP Region, Sun Yat-sen University Cancer Center, Guangzhou, Guangdong, 510060, R.P.
China
3 Department of Breast Oncology, Sun Yat-sen University Cancer Center, Guangzhou,
Guangdong, 510060, R.P. China
4 Department of Medical Oncology, Sun Yat-sen University Cancer Center, Guangzhou,
Guangdong, 510060, R.P. China
Corresponding author: XIA Liangping
Email: [email protected]
Tel: +8620-87343107
Mobile: 13926410608
Address: 651 Dongfeng Road East, Guangzhou, Guangdong, China
Abstract:
Backgroud: The aim of this study was to compare the prognosis of MBC and FBC patients
in China and the prognosis of MBC and their corresponding postmenopausal FBC patients.
Methods: Thirty five MBC patients who were treated at the Cancer Center of Sun Yat-sen
University between 1969 and 2004 were enrolled in the study. Seventy FBC patients who
were matched with the MBC patients for TNM stage, year of diagnosis and age at diagnosis
were simultaneously enrolled in the study. A second group comprising 18 MBC patients and
their corresponding 36 matched postmenopausal FBC patients were also enrolled. The whole
group and the postmenopausal groups were compared for five and ten year survival curves.
Results: All the factors that could potentially affect prognosis were balanceable among the
groups except more FBC than MBC patients underwent endocrine therapy and a modified
radical mastectomy. The 5 and 10 year survival values in the whole group were 81.6% and
60.3% for men and 90.7% and 73.5% for women. The difference between the two matched
groups was significant (P = 0.02). The 5 and 10 year survival in the postmenopausal group
were 82.5% and 100% for men and 66.0% and 85.9% for women. The difference between the
two matched groups was insignificant (P = 0.159).
Conclusions: Chinese FBC patients had a better prognosis than Chinese MBC patients.
However, MBC patients and their corresponding postmenopausal FBC patients had a similar
prognosis.
Key words: male breast cancer; female breast cancer; postmenopausal; prognosis
INTRODUCTION
Male breast cancer (MBC) has been investigated only in small single institution
retrospective studies or by extrapolation from female breast cancer studies (1). MBC patients
are generally older than FBC patients at diagnosis, exhibit more frequent lymph node
involvement, present at a more advanced stage, show a predominant proportion of infiltrating
ductal carcinoma and have higher expression levels of estrogen receptor (ER) and/or
progesterone receptor (PR) (1, 2). These differences may be associated with a higher
cancer-specific death rate in MBC (2). It is not clear if there is a difference in prognosis
between MBC and FBC (1, 3, 4). Previous studies have speculated on the possibility of
distinct pathways of oncogenesis in MBC and FBC (5). It has been reported that more FBC
patients are premenopausal in China than in western countries (6). The differences between
MBC and FBC have not been investigated to date and all studies on Chinese MBC have
analyzed small patient populations (21.18±1.10 patients/study; range from 5 to 65 [data not
shown]). The goal of our present study was to compare the prognosis in Chinese MBC and
FBC patients.
Our study is the first prognostic comparison of Chinese male and female breast cancer
patients. This is also the first study in the world comparing the prognosis of MBC patients
with that of postmenopausal FBC patients who are considered clinically similar to MBC
patients (1).
METHODS
The data for our study were obtained from the retrospective breast cancer database at the
Cancer Center of Sun Yat-sen University. The data included all MBC and FBC patients with
stage Ⅰ～Ⅲ breast cancer, diagnosed between June 1, 1969 until November 30, 2004. We
collected data from at least 5 years of follow-up visits.
Inclusion criteria for the study were 1) Availability of accurate TNM staging 2)
Availability of well-documented clinical information 3) Availability of follow-up clinical
information for more than five years 4) StageⅠ～Ⅲ 5) Curative intent. Exclusion criteria for
the study were 1) Presence of metastatic lesions at initial diagnosis. 2) Patient undergone
breast surgery at a different institution. Each MBC patient was carefully matched with two
FBC patients for 1) age at diagnosis (more than 90% patients within ± 2 years) 2) year of
diagnosis (within ± 2 year) and 3) identical clinical stage at diagnosis (7, 8). When more than
two women met the matching criteria, the first two patients were chosen (8). Thirty five MBC
patients and 70 matched FBC patients were enrolled in the study. In the postmenopausal
group, both the matched FBC patients were in the postmenopausal state at diagnosis. The
postmenopausal group enrolled 18 MBC patients and 36 matched FBC patients.
Statistical analysis
The chi-square test or Fisher’s exact test was used to compare the breast cancer
characteristics between men and women for qualitative data and the t-test for quantitative
data. Overall survival was calculated using Kaplan-Meier method. The end points for 5- and
10-year survivals were death, irrespective of the cause. P values <0.05 were considered
statistically significant. Statistical analysis was performed using SPSS13.0 for Windows.
RESULTS
1. The basic characteristics of study groups
We analyzed the basic characteristics of our study groups, including median of age, year
of diagnosis, TNM stage, tumor laterity, skin/nipple involvement, pathological subtypes,
HER2 expression, ER/PR expression, time to diagnosis, and time of follow-up (Table 1). The
first three characteristics (especially the TNM stage which was identical in each matched
group) were the criteria used for matching the MBC and FBC patients. There were no
significant differences in any of these characteristics between the MBC and FBC entire group
as well as the postmenopausal group.
Since all treatment strategies were potential prognostic factors which could affect the
results, we carried out a comparison (Table 2) of treatment strategies including treatment
modalities, adjuvant chemotherapy, postoperative radiotherapy, endocrine treatment, and
surgery (9). We observed that in the FBC group, more patients, both in the whole group and
postmenopausal group, accepted endocrine therapy (P=0.038, P=0.006) and modified radical
mastectomy (P=0.001, P=0.005). The two groups were well matched in all other respects.
2. Survival curves in the two groups
Figure 1 shows the survival curve of the whole group. Whole group 5 and 10 year
survivals were 81.6% and 60.3% for men, and 90.7% and 73.5% for women, respectively.
The difference between the two matched groups was significant (P = 0.02). The
postmenopausal group 5 and 10 year survivals were 82.5% and 100% for men, and 66.0%
and 85.9% for women, respectively. The difference between the two matched groups was not
significant (P = 0.159). Figure 2 represesnts the survival curve of the postmenopausal group.
DISCUSSION
While some previous retrospective studies including case-control studies (7, 8, 10-15)
and population-based studies (3, 4, 15-20) showed prognostic differences between MBC and
FBC, others were inconclusive. This inconsistency may be associated with the extremely low
incidence of MBC, making it impossible to conduct prospective randomized phase Ⅲclinical
trials which are required to answer a question of this nature (20, 21). However, our results
agreed with a previous study (8) and demonstrated that FBC patients had a better prognosis
than MBC patients when the whole group was analyzed. When we analyzed potential
prognostic factors before prognosis analysis, we found that both the groups were comparable.
What then, causes a difference in prognosis between the MBC and FBC groups? MBC occurs
on the average, 10 years later than FBC (22, 23). This makes the impact of comorbidities and
second neoplasms more important and can confound comparative results. To illustrate this
fact, the ‘Adjuvant Online’ program was used to calculate the death risks of two hypothetical
patients who differed only in age (20). It was observed that the 10 year survival in a 63-year
old patient with pT2N1, grade 2 ER+ tumor and minor health problems, and without adjuvant
treatment was 57.7% (with 33.3% and 9.0% death risks from breast cancer and ‘other causes’,
respectively). In another case, a 73-year old patient with the same type of tumor had a 31%
risk of death from breast cancer and a 20.5% risk of death from ‘other causes’.
Approximately 11% of the MBC patients experienced second cancers, the most common of
which were cutaneous melanoma and stomach cancer (24). They also exhibited a high
incidence of cardiovascular, neurological and respiratory diseases. These data suggest that in
these patients, the risk of death from non-specific diseases other than cancer, increases with
an increase in age. This phenomenon existed in clinical practice demonstrated by the French
Cancer Centres study(25). Disease-specific survival (DSS) rather than OS, therefore became
a more suitable marker to study MBC prognosis (7, 8, 11-13, 15, 25-27). With OS as the end
point, there was no difference in 5-year survival between MBC and FBC patients. However,
with DSS as the end point, the same studies showed a significant difference between the two
groups (8). Some studies showed that DSS remained the same in the two groups while OS
was better in FBC patients (7). Since the case-control studies were similar to our study and
matched patients for age at diagnosis, we believe that the risk of comorbidities is similar in
both populations. We therefore believe that the age at diagnosis did not play a role in the
differential prognosis between MBC and FBC patients in our study. Although we did not
calculate DSS in this study, we believe that OS reflects the prognosis of MBC and FBC
patients since the age at diagnosis was matched.
We also investigated the role of ER/PR status and HER2 status in the prognostic
differences between the two groups. Expression levels of ER/PR have been shown to be
higher in MBC patients than in FBC patients (1). However, our data agree with a study
showing that HER2 expression levels are lower in MBC patients than in FBC patients (28).
Since ER/PR and HER2 predict prognosis in breast cancer (29, 30), we believe that this may
play a role in the difference in prognosis between our two study groups. ER/PR status and
HER2 status have been shown to be predictive factors of response to endocrine therapy and
trastuzumab treatment respectively (29). In our study, a lower number of male patients
underwent endocrine therapy, resulting in a lost opportunity to achieve a good outcome. We
showed that MBC patients had a worse 5-year survival rate than FBC patients (81.6% versus
90.7%). We believe that this phenomenon can be overcome when doctors and patients are
educated on the advantages of treating MBC and FBC patients using similar endocrine
therapeutic strategies.
The presence of strongly PR-positive nuclei is a predictor of response to tamoxifen
treatment in premenopausal women with breast cancer (31). Similarly, PR negativity in
postmenopausal women with ER positive and PR-negative tumors is considered a marker of
tamoxifen resistance (32). These data suggest that PR, which is more likely to be expressed in
male breast cancer tumors, would enable these patients to mount an effective response to
endocrine therapy. However, results from a recent study comparing the effects of arimidex
alone, tamoxifen alone or combination treatment may not support this notion (33). Therefore,
although MBC is characterized by higher levels of ER/PR expression and lower levels of
HER2 expression, the significance of this difference in expression levels may be different in
MBC and FBC (34).
We propose that differences in treatment modalities may be the most important factor in
the prognostic difference between the MBC and FBC groups. We demonstrated that more
FBC patients underwent endocrine therapy (P<0.05). Fewer FBC patients accepted surgery
alone as a treatment option (P≈0.05) which may play an important role in the prognostic
difference between the groups. Our data agreed with previous results (35-38) including from
our group [39], showing that more MBC patients underwent radical mastectomy instead of
modified radical mastectomy, which is more common in FBC patients. However, these
studies demonstrated that the two surgery models had an equivalent efficacy and were
therefore unlikely to cause the difference in prognosis between the two groups.
We asked if MBC and postmenopausal FBC had the same prognosis. Based on the
Cancer Incidence Public-Use database of the National Cancer Institute’s Surveillance,
Epidemiology, and End Results (SEER), which includes 381,128 cases of FBC and 2560
cases of MBC, a previous study (1) found that male breast cancer was more like
postmenopausal than premenopausal female breast cancer in the following three aspects (1)
age-frequency distribution, (2) prognostic factor profiles reflective of tumor biology (nuclear
grade and hormone receptor expression), and (3) age specific incidence rate patterns. We
compared the prognosis in the 18 MBC and corresponding 36 postmenopausal FBC patients
enrolled in our study and showed that the 5 and 10 year survival curves of the two groups
were similar. Therefore, although all the factors that could potentially impact prognosis were
similar in the whole group and the postmenopausal group, there was a difference in prognosis
between MBC and FBC patients between the two groups. The lack of a significant prognostic
difference in the postmenopausal group may be related to small patient numbers, and may
result from more younger patients, who usually showed a poorer prognosis than older patients
[19], excluded from the postmenopausal group.
To our knowledge, this is the first study comparing matched male and female breast
cancer patients in China and the first study worldwide directly comparing the prognosis of
MBC and postmenopausal FBC patients. We believe that the long follow up time of 71-116
months and balancing of all the basic characteristics which could potentially impact
prognosis, ensure the results of this study believable. We demonstrated that although FBC
patients had a better 5 and 10 year survival in the whole group, the FBC and MBC groups
showed similar 5 and 10 year survival curves when the population was limited to the
postmenopausal group. We propose that the difference in prognosis between MBC and FBC
patients in this study was closely associated with the different treatment strategies in the two
groups.
ACKNOWLEDGMENTS
We are grateful to all the doctors who performed surgeries and thank the patients for
their participation in this study. We thank Professor Hao Yuantao for the statistical analyses
and Miss Ma Xiu-fang from the Department of Follow-up in our Cancer Center who
collected all the follow-up information. We thank Zhang Jianwei, Chen Zidong, and Li
Pengliang for clinical data collection.
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Table 1. Patient demographics of the four matched groups
Characteristics
Male(N=35)
Female(N=70)
P*
Male(N=18)
Postmenopausal
P**
female(N= 36)
Median
of
age
59(39－78)
58(36－76)
0．461
65(56-78)
65(51-76)
o.682
(range)
Year of diagnosis
0.998
1.000
1969-1979
5（14.3%）
11（15.7%）
2（11.1%）
4（11.1%）
1980-1989
7（20.0%）
14（20.0%）
4（22.2%）
8（22.2%）
1990-1999
13（37.1%）
25（35.7%）
8（44.4%）
16（44.4%）
2000-2004
10（28.6%）
20（28.6%）
4（22.2%）
8（22.2%）
TNM
1.00
1.00
Ⅰ
12（34.3%）
24（34.3%）
9（50.0%）
18（50.0%）
Ⅱ
14（40.0%）
28（40.0%）
8（44.4%）
16（44.4%）
Ⅲ
9（25.7%）
18（25.7%）
1（5.6%）
2（5.6%）
Tumor laterality
0.890
0.561
Left
17（46.6%）
33（47.1%）
7（38.9%）
17（47.2%）
Right
18（51.4%）
37（52.9%）
11（61.1%）
19（52.8%）
Skin/nipple
0.26
1.00
involvement
No
28（80.0%）
67（95.7%）
17（94.4%）
35（97.2%）
Yes
7（20.0%）
3（4.3%）
1（5.6%）
1（2.8%）
Pathological types
Infiltrating
0.517
0.481
29（82.9%）
59（84.3%）
14（77.8%）
29（80.6%）
DISC
2（5.7%）
1（1.4%）
2（11.1%）
1（2.8%）
others
4（11.4%）
10（14.3%）
2（11.1%）
6（16.7%）
N=9
N=18
N=3
N=8
-
7（77.8%）
6（33.3%）
2（66.7%）
3（37.5%）
+
1（11.1%）
6（33.3%）
0
2（25.0%）
++
1（11.1%）
1（5.6%）
1（33.1%）
1（12.5%）
+++
0（0.0%）
5（27.8%）
0
2（25.0%）
N=12
N=25
N=6
N=12
Both negative
1（8.3%）
8（32.0%）
0（0.00%）
3（25.0%）
Both positive
9（75.0%）
13（52.0%）
6（100.0%）
8（66.7%）
2（16.7%）
4（16.0%）
0（0.0%）
1（8.3%）
ductal carcinoma
HER2 expression
ER/PR expression
ER
positive
or
PR
0.033
0．366
0.450
0．676
Time to diagnosis
Median
0．246
12
time,months(Range
(7days-50
6
(2
days-13
years)
years)
71 (18-391)
90(10-474)
0．287
12 (7 days-10
4
(2
days-13
years)
years)
95(29-391)
116(29-257)-
)
Median
follow-up
0．816
0．853
months(range)
* Comparison between MBC and all FBC; ** Comparison of postmenopausal FBC with
matched MBC patients. DISC: Ductal in situ carcinoma.
Table 2. Treatment strategies in the four patient groups
Characteristics
Male(N=35)
Female(N=70)
P*
Male(N=18)
Postmenopausal
P**
FBC(N=36)
Treatment
0．055
0．053
modalities
Comprehensive
Operation only
28（80.0%）
66（94.3%）
12（66.7%）
33（91.7%）
7（20.0%）
4（5.7%）
6（33.3%）
3（8.3%）
Adjuvant
0．165
0．554
chemotherapy
Yes
16（45.7%）
42（60.0%）
6（33.3%）
15（41.7%）
No
19（54.3%）
28（40.0%）
12（66.7%）
21（58.3%）
Neoadjuvant
0．235
0．289
chemotherapy
Yes
5（14.3%）
17（24.3%）
0（0.0%）
No
30（85.7%）
53（75.7%）
18（100.0%） 12（88.9%）
Adjuvant
4（11.1%）
0．622
1．00
radiotherapy
Yes
7（20.0%）
17（24.3%）
3（16.7%）
7（19.4%）
No
28（80.0%）
53（75.7%）
Endocrine therapy
15（83.3%）
29（80.6%）
0．038
0．006
Yes
14（40.0%）
43（61.4%）
6（33.3%）
26（72.2%）
No
21（60.0%）
27（38.6%）
12（66.7%）
10（27.8%）
Operation model
0．001
0．005
RM
30（85.7%）
36（51.4%）
17（94.4%）
18（50.0%）
MRM
3（8.6%）
25（35.7%）
1（5.6%）
13（36.1%）
Others
1（2.9%）
9（12.9%）
0（0.0%）
5（13.9%）
No
1（2.9%）
0（0.0%）
0（0.0%）
0（0.0%）
* Comparison of MBC with all FBC patients; ** Comparison of MBC with matched
postmenopausal FBC patients; .RM: Radical mastectomy; MRM: Modified radical
mastectomy
1.0
Fe ma le
S u rviva l ra te (% )
0.8
0.6
Ma le
0.4
0.2
0.0
0.00
60.00
120.00
180.00
240.00
Tim e (m o n th s )
Figure 1. MBC and FBC survival curves in the whole group
When the whole group was analyzed, the 5 and 10 year survivals were 81.6% and 60.3% for
men, and 90.7% and 73.5% for women, respectively. The difference between the two
matched groups was significant (P = 0.02).
1.0
Fe m a le
0.8
S u rviva l ra te (% )
Ma le
0.6
0.4
0.2
0.0
0.00
60.00
120.00
180.00
240.00
Tim e (m o n th s )
Figure 2. MBC and FBC survival curves in the postmenopausal group
The postmenopausal group comprised 18 MBC patients and 36 matched postmenopausal
FBC patients. The 5 and 10 year survivals were 82.5% and 100% for men, and 66.0% and
85.9% for women, respectively. The difference between the two matched groups was
insignificant (P = 0.159).