Download The role of surgery in the manage- ment of metastatic breast cancer?

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The role of surgery in the management of metastatic breast cancer?
Authors
A. Steyaert, A. Smeets, I. Cadron, H. Wildiers, M.R. Christiaens
Key words
Surgery, stage IV breast cancer, primary tumor, metastasis
Summary
Although metastatic breast cancer has a bad
prognosis, the median survival of these patients
has improved over the last 25 years. This review
considers the role of surgical excision of the
primary tumor and resection of metastases in
patients with limited metastatic disease. There is
emerging evidence that for women with stage IV
breast cancer, resection of the primary tumor with
negative margins significantly improves survival,
especially in patients with solitary bone metasta-
Introduction
Nowadays, surgical treatment in patients with metastatic breast cancer is limited to palliative indications as these patients will ultimately die of their
disease (overall survival of 2% at 20 years of followup) and aggressive approaches lead to useless patient
distress and morbidity.
However, it is important to realize that over the past
25 years, the median survival of these patients has
improved significantly from 15 months in patients diagnosed between 1974-1979 to 51 months in patients
diagnosed between 1995 and 2000.1 This improved
survival is a consequence of patients presenting with
minimal metastatic disease on the one hand and
more effective therapies on the other hand.2
These findings force us to re-evaluate the role of
surgical excision of the primary tumor in metastatic
patients and to consider a resection of metastases for
patients with limited metastatic disease.
The role of surgery of the primary tumor in
stage IV breast cancer patients
Three theories concerning the development of distant metastasis in breast cancer have emerged in the
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sis. For lung, liver, brain and sternum metastases,
surgical resection of the metastasis seems to be
associated with a greater median survival time
and 5-year survival rate. The best candidates for
surgery might be patients with a good response
to systemic treatment, a long disease free interval
after treatment of the primary tumor and a single
site of metastases or metastases confined to one
organ, provided that a complete excision of all
metastases can be obtained.
(BJMO 2009;Vol 3;5:184-190)
first half of the 20th century, each of them having
different implications for the treatment of patients.
The first theory, also known as the Halsted theory,
states that breast cancer starts as a local disease and
that tumor cells spread from the primary tumor to
axillary lymph nodes and then to metastatic sites.3
This view justifies an aggressive local therapy for local control of disease in the breast and the regional
lymph nodes.
Secondly, the Fisher theory, states that breast cancer
is a systemic disease and that tumors which have
the capacity to metastasize, will do so even before
diagnosis.4 This view justifies an aggressive systemic
therapy because the only hope for definitive cure is
treatment of the (micro)metastasis. Local control
according to this theory would have no effect on
overall survival.
Neither theory is correct as demonstrated in different clinical trials. The National Surgical Adjuvant
Breast and Bowel Project breast carcinoma B-04
study (NSABP-B-04) showed no benefit of radical
mastectomy over less radical surgery which brings
in doubt the Halsted theory.5 On the other hand
the significant reduction of the relative risk of death
from breast cancer due to mammographic screening
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compromises the systemic theory. Early detection of
breast cancer does have an influence on the reduction of mortality and randomized controlled trials
show a link between local control and overall survival in breast cancer, again bringing in doubt the
validity of the systemic theory.6,7
The third theory, depicted as the Spectrum theory, is
basically a blend of both the Halsted and the Fisher
theory and states that the exact moment of metastasis to distant sites is unknown at the time of diagnosis.8,9 This theory emphasizes the importance
of locoregional and systemic treatment through a
multimodal approach.
Recently however, new molecular-based hypotheses
of development of metastasis in breast cancer, tumor immunology and tumor growth influence our
view on the metastatic development and progression
in breast cancer which is crucial in deciding whether surgery is indicated in these patients. Today,
there is still limited understanding of the molecular
mechanisms of metastasis but, according to Lang
and colleagues, three new hypotheses can be distinguished.10 The first, known as the parallel evolution
model, states that circulating or disseminated tumor
cells are found early in tumorigenesis and are independent of the primary tumor. This theory justifies a surgical treatment of stage IV patients with
an intact primary and a minimal metastatic burden.
A second model based on the gene expression profile
of the primary tumor, states that the metastatic potential is an inherent, genetic predetermined property that is expressed very early and that tumor cells
are programmed to metastasize to a certain site in
the presence of a favorable microenvironment. This
model justifies an optimal local and systemic treatment to target the circulating tumor cells. The third
hypothesis, depicted as the breast cancer stem cell
model, states that specialized tumor-initiating cancer cells have the exclusive potential to metastasize.
This theory justifies effective treatment directed at
the stem cell population and surgical treatment of
the primary tumor.
New insights into the interaction between metastases and the host are also crucial in making a decision whether surgical intervention is appropriate in
stage IV patients. A study of Danna et al indicated
that, although patients with bulky primary tumors
are immunosuppressed, primary tumor removal reverses immune suppression even in the presence of
extensive metastatic disease.11 They concluded that
reducing tumor burden either by surgery or by other
conventional techniques could augment the efficacy
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of immunotherapy which justifies surgical treatment
in a metastatic breast cancer patient. Removal of the
primary tumor seems to restore immune competence by removing a potentially dependent relationship between the primary tumor and its metastases.
This has already been shown in other carcinoma’s.
The South Western Oncology group (SWOG) trial examined the benefit of nephrectomy in patients with
stage IV renal cell carcinoma, who were randomized
to interleukin therapy, with or without nephrectomy.12 In this study, the overall median survival increased from 8 months without nephrectomy, to 11
months for patients who underwent nephrectomy,
suggesting that aggressive locoregional treatment
may contribute to a prolonged survival. The same
benefit of surgical treatment was described in patients with colorectal and gastric cancer, for which a
reduction in tumor burden has been reported to be
effective in terms of increased survival.13,14
A potential argument against resection of the intact
primary is the tumor dormancy theory. This theory
states that removal of the primary tumor results in
a proliferation of metastases by induction of angiogenesis, reduction of apoptosis and release of growth
factors in response to surgical wounding. This theory however has never been proven by clinical studies
(only level 4 evidence to support this theory) and is
not seen in clinical practice.10
The main limitations in evaluating whether surgical
treatment of the primary tumor in stage IV breast
cancer patients is indicated, are selection biases in
favor of operated patients and limited information
on tumor characteristics and adjuvant therapy.
A first study was conducted by Khan and colleagues.15 It is a retrospective review of data from the
National Cancer Data Base (NCDB) between 1990
and 1993. A total of 16,023 patients were included
of whom 6,861 (42.8%) received no operation and
9,162 (57.2%) underwent either partial (N= 3,513)
or total (N= 5,649) mastectomy. The authors concluded that there is a statistically significant survival advantage in women undergoing surgery at
the primary site, especially when negative margins
were obtained. The 3 year survival rate was 17.3%
in patients who had no surgical procedure and 35%
in patients operated with negative margins. Independent prognostic co-variates were the number of
metastatic sites, the type of metastatic burden and
the extent of resection of the primary tumor. This
large data set adds strength to the hypothesis that
local therapy is valuable, even in the presence of distant disease.
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Furthermore, Babiera and colleagues reviewed the
records of 224 primary metastatic breast cancer patients, treated between 1997 and 2002. Eighty-two
patients (37%) underwent surgical treatment (52%
total mastectomy, 48% partial mastectomy) and 142
patients (63%) were treated without surgery.16 The
median follow-up in this study was 32.1 months.
On multivariate analysis, surgery was associated
with a trend towards improved overall survival (p=
0.12) and a significant improvement in metastatic
progression-free survival (p= 0.0007).
Rapiti and colleagues reported a retrospective study
of 300 metastatic breast cancer patients recorded
at the Geneva Cancer Registry between 1977 and
1996.17 Overall, 173 patients (58%) did not receive
any kind of surgery of the primary tumor, whereas
127 (42%) underwent either mastectomy (N= 87)
or partial mastectomy (N= 40). They concluded that
women who had a complete excision of the primary
tumor with negative surgical margins had a 40% reduced risk of death as a result of breast cancer compared with women who did not have surgery (multiadjusted HR= 0.6). This effect was even greater in
the subgroup of women who had bone metastases
only at the time diagnosis (HR= 0.2). However, the
survival rate did not differ between women who underwent surgery with positive surgical margins and
women who did not have surgery. The results of this
study also provided some evidence of an additional
beneficial effect of axillary lymph node dissection
when performed together with removal of the primary tumor.
Gnerlich and colleagues conducted a retrospective
population based cohort study of 9,734 patients in
the SEER database (Surveillance, Epidemiology and
End Results program data).18 Data were collected between 1988 and 2003. Overall, 5,156 patients (53%)
did not receive a surgical treatment whereas 4,578
(47%) underwent breast cancer surgery. In this
study, the median survival was longer for women
who had surgery than for women who did not. After controlling for demographic and clinical factors
associated with survival, patients who underwent
surgery were 37% less likely to die during the study
period than women who did not undergo surgery.
Furthermore, Ruiterkamp and colleagues performed
a retrospective study on 728 stage IV breast cancer patients diagnosed between 1993 and 2004.19
A total of 40% of these patients underwent breast
surgery. The median survival was 31 months in
women who had surgery compared with 14 months
in women who did not. Removal of the tumor was
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associated with a reduction of the mortality risk of
around 40%.
In a retrospective single institution study reported
by Shien et al including 344 patients who had stage
IV breast cancer at diagnosis of which 47% had
surgery of the primary tumor, the overall survival
improved with surgery but also with young age and
bone or soft tissue metastasis.20
Bafford et al conducted a retrospective review of 147
patients who presented with stage IV breast cancer.
A total of 41% of the patients underwent surgery in
this study.21 The mean overall survival, adjusted for
age, number of sites of metastasis, systemic therapy,
ER and HER2 status was 4.13 years in the surgery
group versus 2.36 years in the non-surgery group
(HR= 0.47, p= 0.003).
In summary, all these clinical studies provide additional evidence that women with stage IV breast
cancer have a significantly improved survival when
the primary tumor is removed with negative margins,
especially in patients with solitary bone metastasis.
Selection of patients with stage IV breast
cancer for resection of the primary tumor
Mastectomy in stage IV breast cancer patients is conventionally the treatment of choice in case of ulceration, infection or bleeding. The treatment is palliative with the intention to have an optimal symptom
control and to enhance the quality of life. In view
of the recent clinical studies, there is emerging evidence that removal of the primary tumor and axillary
lymph nodes in patients with stage IV breast cancer is
also associated with improved metastatic progressionfree survival. Determining which patients will definitely benefit from surgery is now the key question.
Based on the available data, the major benefit is noticed in young patients with only one site of metastasis, a good response to systemic therapy and in whom
negative margins at the primary site can be obtained.
Optimal timing of surgery in these patients appears
to be 3-9 months after diagnosis.22
These findings may serve as the basis for designing a
prospective randomized controlled trial.
The role of surgery in the treatment of single or multiple metastatic lesions restricted
to one site in stage IV breast cancer patients
Rationale for resection of metastatic lesions
A similar debate could be held on the treatment of
the metastasis in patients with metastatic disease
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limited to a solitary lesion or multiple lesions at a
single organ. Only a few reports of breast cancer
patients treated with aggressive local therapy to the
metastatic site combined with systemic therapy have
been reported. At the MD Anderson Cancer Center,
80 patients with solitary metastases were treated
with surgery with or without radiation therapy followed by systemic therapy. Nearly 25% of patients
were alive without disease 15 years after treatment.23
A recent study by Nieto and colleagues included 60
patients who were treated with surgical resection
and radiation therapy when possible, followed by
systemic chemotherapy.24 After a median followup of 62 months, more than half (51.6%) of these
patients were disease-free.
Other reports concerning gastric carcinoma or
colorectal cancer confirm this trend, obliging us
to reconsider the importance of surgery in patients
with stage IV breast cancer.13,14 It has been suggested that the total tumor burden plays a central
role in survival and that the primary tumor could
be viewed as another metastatic site.
Indications for resection of the metastatic
lesions
Urgencies which require regional radiotherapy
(RT), surgery or interventional procedures prior to,
or along with systemic therapy are: brain metastasis,
cord compression, choroid disease, pleural effusion,
pericardial effusion, pending/pathologic fracture
and obstruction of the biliary tree, the ureters, the
trachea, the bowel or the esophagus.
Singletary and colleagues determined which patients
with metastatic disease limited to a solitary lesion
or to multiple lesions at a single organ site are the
best candidates for surgery by reviewing the literature from 1992 until 2002 on each organ site.25
Several kinds of bias might influence these results,
however the data are suggestive. Again the need for
prospective randomized controlled trials in search
for guidelines is emphasized. An overview of the
available literature is summarized below.
Across the four sites (lung, liver, brain, bone) better
patient outcome after surgery was associated with
good performance status, long disease free interval
after treatment of the primary tumor, complete resection of the tumor and restriction of metastasis to
single tumors or to multiple tumors at single site.25
Liver
Isolated liver metastases are found in 5-25% of patients with metastatic breast cancer. The presence
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of liver metastases implies poor prognosis with
a reported median survival of 19 to 22 months.
Singletary et al reviewed 6 small retrospective studies
which indicated that there is evidence that surgery
can significantly increase survival.25 The median
survival times ranged from 22 to 44 months and
the 5 years survival rates ranged from 22 to 38%
with one study showing a 4-years survival rate of
46%. These results were confirmed in 5 more recent
studies.26-30 Elias et al suggest to propose resection of
the liver metastases when the three following conditions are absolutely confirmed: (1) a low operative
risk, (2) liver metastases completely resectable and
(3) no extra hepatic disease (except for rare bone
metastases).30 Parameters that negatively influence
survival are a short interval between breast surgery
and the appearance of liver metastasis and a negative hormone receptor status.
The role of radiofrequency ablation remains unclear.
Several studies are currently ongoing and the first
results seem promising.31,32 At this time, radiofrequency ablation should be reserved for patients unfit
for surgery or used as an adjuvant to resection.
Lung
Of all women with breast cancer 3% will develop a
solitary pulmonary lesion, of which 33% will be a
breast metastasis.33,34 The remaining two thirds will
consist of other tumortypes. In order to determine
the optimal treatment strategies for these patients,
early identification of the type of lesion is an additional reason for recommending surgical resection.
In a study performed in 467 patients with lung metastases from breast cancer, a complete metastatic
resection was obtained in 84% of patients, with a
5-year survival rate of 38%.35 A positive survival outcome after surgery was associated with a longer disease free interval after excision of the primary tumor
and a positive hormone receptor status. These findings are in line with most of the published studies.
Brain
Off all women with breast cancer, 10% will develop
brain metastases and in only one third of these patients the brain is the only site of metastasis.25 Conventionally, palliation of neurological symptoms
is obtained by steroids and whole brain radiation
therapy. Only 5 small studies considered the possible increase of survival by surgical excision added
to whole brain radiation therapy. The median survival ranged from 15 to 37 months, with 5 years
survival rates ranging from 7 to 38%. Good can-
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Key messages for clinical practice
1. Concepts of cancer biology and treatment are evolving.
2.There is emerging evidence of a potential survival benefit of loco-regional surgery in young
patients with only one site of metastasis, a good response to systemic therapy and in whom
negative margins at the primary site can be obtained. Optimal timing of surgery in these patients appears to be 3-9 months after diagnosis.
3.Candidates for surgery of metastases might be patients with a good response to systemic
treatment, a long disease free interval and a single site of metastasis or multiple metastases
confined to one organ, provided that a complete excision of all metastases can be obtained.
didates for surgical therapy are patients who have
a single operable brain lesion and well-controlled
systemic disease. Leptomeningeal disease has a very
poor prognosis and is a contra-indication for surgical excision Stereotactic radiation therapy is an
alternative for surgical excision in those cases were
the metastasis is located in an inaccessible site or is
inoperable, though larger lesions may not respond.
Bone
Bone is the most common site of breast cancer metastasis, mainly in patients with receptor positive
tumors, and is usually treated with systemic therapy. Surgery has been reserved for the treatment of
lesions that are not responsive to systemic therapy
in order to enhance the quality of life (pain relief),
reduce fracture risk and treat spinal or nerve compression. Surgery as a curative treatment option for
bone metastasis has only been considered in case
of isolated sternal metastases. Data concerning patient selection are scarce, in the 1980s Noguchi et al
suggested that surgical resection of solitary sternal
metastases may have led to significantly better survival.36 The largest study is from Incarbone and colleagues.37 They reviewed 19 patients with local recurrences or metastases of breast tumors, the 5-year
survival rate was 49% in patients with direct extension to the chest wall and 60% in patients with distant bone metastasis. However, an isolated sternal
metastasis should be regarded with caution as Kwai
et al demonstrated that 54% of patients with breast
cancer and a solitary sternal metastasis developed
other foci of distant disease within 20 months.38
Conclusion
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As the concepts of cancer biology and treatment continue to evolve, so does the definition of “cure”. By
changing the focus from complete eradication of all
tumor cells as the goal of therapy to that of rendering
the disease stable, selected patients with metastatic
breast cancer might be candidates for surgery.
There is emerging evidence of a potential survival benefit of loco-regional surgery in young patients with
single site metastasis and a good response to systemic
treatment, provided a complete loco-regional treatment is obtained (negative margins + axilla + RT).
Candidates for surgery of metastasis might be patients with a good response to systemic treatment, a
long disease free interval and a single site of metastasis or multiple metastases confined to one organ,
provided that a complete excision of all metastases
can be obtained.
However, prospective studies are needed to validate
these results.
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Correspondence address
Authors: A. Steyaert, A. Smeets, I. Cadron,
H. Wildiers, M.R. Christiaens.
Multidisciplinary Breast Centre, University Hospitals
Leuven.
Please send all correspondence to:
Dr. A. Smeets
Multidisciplinary Breast Centre
University Hospitals Leuven
Herestraat 49
B-3000 Leuven
Belgium
Tel 0032 (0)16 34 68 32
Fax 0032 (0)16 34 68 34
[email protected]
Conflicts of interest: The authors have nothing to
disclose and indicate no potential conflicts of interest.
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are looking forward to receiving any comments
you might have to develop this journal in future.
The Editorial Board and Ariez Medical Publishing Ltd.
O N C O L O G Y vol.
3
issue
5 - 2009
190