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European Journal of Cardio-thoracic Surgery 39 (2011) 955—962

www.elsevier.com/locate/ejcts

Review

Current status of pulmonary metastasectomy


Kåre Hornbech *, Jesper Ravn, Daniel Andreas Steinbrüchel
Department of Cardiothoracic Surgery, Rigshospitalet, University Hospital of Copenhagen, Copenhagen, Denmark

Received 27 April 2010; received in revised form 24 September 2010; accepted 6 October 2010; Available online 27 November 2010

Summary

Malignant disease’s ability to metastasize remains one of the major obstacles when treating patients with cancer. The change from loco-
regional to systemic disease usually renders the patient beyond surgical treatment, as local treatment with surgery in a systemic disease is usually
considered without benefit. However, numerous retrospective studies have demonstrated that resection of metastases limited to the lungs may
be associated with prolonged survival. No prospective, randomized studies have been published, and most series compare highly selected
patients with historical data for unresected patients. In this article, we discuss the current status on pulmonary metastasectomy. Preoperative
assessment and selection of surgical candidates is covered. The different surgical strategies including surgical approach, unilateral versus
bilateral exploration, lymph node dissection, and repeat surgery are discussed. Finally, we review some of the common tumors that metastasize
to the lungs, the role of metastasectomy in their treatment and the prognostic factors with impact on survival.
# 2010 European Association for Cardio-Thoracic Surgery. Published by Elsevier B.V. All rights reserved.

Keywords: Pulmonary metastasectomy; Resection; Surgery; Lung metastases; Cancer; Surgical approach; Thoracoscopic; Preoperative assessment; Survival

1. Introduction tolerable. Since then, numerous studies have demonstrated 5-


year survival rates of 30—50% for a large variety of primary
Malignant disease’s ability to metastasize remains one of tumors in highly selected patients. These survival rates are far
the major obstacles when treating patients with cancer. The superior to any other treatment. The landmark study of the
lungs are one of the most common organs to which cancer International Registry of Lung Metastases accrued 5206
metastasizes, and approximately 30% of all cancer patients patients with different primary tumor histologies treated
will develop lung metastases at some point [1]. with pulmonary metastasectomy from 18 thoracic surgical
The change from loco-regional to systemic disease usually departments in Europe, the USA and Canada. Survival after
renders the patient beyond surgical treatment, as local complete metastasectomy at 5, 10, and 15 years was 36%, 26%,
treatment with surgery in a systemic disease is usually and 22%, respectively, whereas survival after incomplete
considered without benefit. When systemic disease is metastasectomy was 13% and 7% at 5 and 10 years,
present, chemotherapy is the mainstay of treatment and respectively. The discriminatory power of this study confirmed
radiation and/or surgery is reserved for palliative measures that pulmonary metastasectomy is potentially curative.
only. However, that is not always the case. Furthermore, multivariate analysis showed that disease-free
Pulmonary metastasectomy has been performed for interval (DFI) <36 months and more than one metastasis were
decades; Alexander and Haight [2] published the first series independent risk factors. Numerous subsequent studies have
of pulmonary metastasectomies in 1947, and proposed the first supported these findings. No prospective, randomized studies
set of selection criteria for surgery. Thomford [3] revised these have been published and most series compare highly selected
in 1965 and, with minor changes, they remain relevant today. patients with historical data for unresected patients.
They are: (1) primary tumor is controlled, (2) no extrathoracic In this article, we discuss the current status on pulmonary
lesions are present (with the exception of hepatic lesions in metastasectomy. Preoperative assessment of these patients
which it is possible to completely remove both hepatic and and different surgical strategies are covered. Finally, we
pulmonary metastases), (3) the metastases seem technically review some of the common tumors that metastasize to the
resectable, and (4) the general and functional risks are lungs, the prognostic factors with impact on survival and the
role of metastasectomy in their treatment.

2. Method and search strategy


* Corresponding author. Address: Department of Cardiothoracic Surgery,
2152, Rigshospitalet, Blegdamsvej 9, 2100 Copenhagen East, Denmark.
Tel.: +45 39 77 25 07. Studies and articles were identified using online
E-mail address: khornbech@hotmail.com (K. Hornbech). searches of The U.S. National Library of Medicine via
1010-7940/$ — see front matter # 2010 European Association for Cardio-Thoracic Surgery. Published by Elsevier B.V. All rights reserved.
doi:10.1016/j.ejcts.2010.10.001

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www.Pubmed.com, regarding the topic of pulmonary only 29.6%. The sensitivity also varied with primary tumor
metastasectomy. Several searches were conducted to histology, as only 44% of sarcoma metastases were positive
retrieve all potentially relevant articles; the searches in contrast to 93% for squamous cell carcinomas. The
were performed between October 2009 and January 2010. authors conclude that PET scan cannot stand alone in the
Terms and keywords associated with pulmonary metasta- detection of pulmonary metastases, but it can be useful as
sectomy were used and included, for example, ‘pulmonary an adjunct to the CT scan and also to exclude extrathoracic
metastases’, ‘pulmonary resection’, ‘thoracoscopy’, and disease in the selection of patients for surgery.
‘colorectal and pulmonary metastasectomy’. None of the
retrieved studies were specifically excluded from this
4. Lymph node status
review. However, due to the advancement in surgical and
anesthesiological techniques, we disregarded studies
The question of lymph node sampling and/or involvement
published before 1980 unless they were of historic value.
remains controversial. The performance of lymph node
All studies identified were retrospective case series and,
dissection during pulmonary metastasectomy is infrequent
thus, no randomized trial has been published.
and varies between institutions. Of all the patients in The
International Registry of Lung Metastases, only 4.6% under-
3. Diagnosis and preoperative imaging
went lymph node dissection. In a recent survey by Internullo
and colleagues [8] amongst the members of the European
A pulmonary lesion in a patient with a history of cancer
Society of Thoracic Surgeons, 55% perform mediastinal lymph
could represent metastatic disease. It should always be
node sampling whereas 33% perform no nodal sampling at all.
further investigated, as it also could represent a new lung
The rate of lymph node involvement varies between primary
primary and, thus, a different treatment strategy.
tumors. Pfannschmidt and colleagues [9] performed systemic
In the preoperative assessment of a patient with a
lymph node dissection in concurrence with pulmonary
pulmonary lesion suspected to be a lung metastasis,
metastasectomy in 245 patients with metastases from
computed tomography (CT) has become the standard.
colorectal carcinoma, renal cell carcinoma and sarcoma.
With the invention of fast high-resolution CT (HRCT), the
Nodal involvement was more frequent in renal cell carcinoma
size of pulmonary nodules detected may be as small as
(42.4%) and colorectal carcinoma (31.3%) than sarcomas
3 mm, although the sensitivity at this size diminishes.
(20.3%). Several studies have found the presence of positive
Margaritora and colleagues [4] evaluated accuracy with
intrathoracic lymph nodes an ominous prognostic factor.
conventional CT or HRCT, and found a sensitivity of 100%
Ercan and colleagues [10] found a 3-year survival of 69% for
for nodules measuring 10 mm for both types of scans.
patients without lymph node involvement versus 38% in
However, the sensitivity for nodules measuring less than
patients with positive lymph nodes. Saito and colleagues [11]
6 mm dropped to 62% with conventional CT and to 48% with
reported a 5-year survival of 53.6 for patients without hilar or
HRCT. The overall sensitivity for pulmonary metastases
mediastinal node involvement versus 6.2% at 4 years for
was 82.1%.
patients with positive nodes.
Diederich and colleagues [5] reported a sensitivity of 69%
In remains unclear whether the removal of these lymph
for nodules smaller than 6 mm with helical CT and 5-mm slice
nodes is associated with a survival benefit or merely allows
thickness. For nodules larger than 6 mm, the sensitivity was
for a more accurate postoperative staging and guidance for
95%. Pfannschmidt and colleagues [6] evaluated the slice
additional oncological treatment. The above-mentioned
thickness of helical CT. They found that reducing the slice
authors proposed the latter.
thickness from 5 to 3 mm resulted in statistically more lesions
found during preoperative imaging compared with surgically
resected lesions with an overall sensitivity of 88.8% for 3-mm 4.1. Surgical approach
slices and 83.7% for 5-mm slices. The sensitivity in the
detection of nodules measuring 1—4 mm was 74.7% for 3-mm The original surgical approach to pulmonary metasta-
slices and 64.0% for 5-mm slices. sectomy was simultaneous bilateral thoracotomy or staged
With the improvement in scanning techniques, the need surgery. Posterolateral thoracotomy provides excellent
for perioperative bimanual palpation of the lung has been exposure of the entire lung, and allows total bimanual
questioned. However, with the diminishing sensitivity with palpation of the lung for undetected pulmonary lesions
nodule size, bimanual palpation of the lung during surgery missed by preoperative imaging. The disadvantage is post-
may still detect small lesions missed by preoperative operative muscle pain and respiratory problems. The midline
imaging. sternotomy used in cardiac surgery can provide access to
The positron emission tomography (PET) scan is now both lungs while sparing the patient from some of the
widely used in the evaluation of cancer patients because of postoperative morbidity associated with thoracotomy. How-
its ability to detect malignant disease. The uptake of the ever, access to the posterior parts of the lung is limited,
18
F-labeled glucose analog is increased in cells with high especially the left lower lobe, and, thus, lesions in these
metabolic turnover and is, thus, concentrated in malignant areas can be technically difficult to resect. The clamshell
cells compared with normal tissue. A study by Fortes and incision, which involves bilateral simultaneous thoraco-
colleagues [7] found an overall sensitivity of 67.5% for the tomies and a sternal split, has also been used in pulmonary
PET scan in the detection of pulmonary metastases. If the metastasectomy. While providing excellent exposure to both
lesion was greater than 10 mm, the sensitivity increased to hemithoraces, it combines the worst of thoracotomy and
87.8%. For lesions smaller than 10 mm, the sensitivity was sternotomy with regard to postoperative morbidity.

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The need for bilateral exploration of the lungs is based CT scan were included in this study. Another study by
upon the assumption that pulmonary metastases represent a Mutsaerts and colleagues [18] with VATS followed by
systemic disease with a great probability of bilateral spread, confirmatory thoracotomy found that in patients with only
even though metastases are not detectable by preoperative one lesion detected on preoperative CT, no further lesions
imaging. Thus, unilateral exploration would result in were found by confirmatory thoracotomy. Gossot and
incomplete resection due to undetected contralateral colleagues [19] investigated the VATS approach in patients
lesions. This was successfully challenged by Roth and with two or less pulmonary metastases from sarcoma and
colleagues [12] when they found that bilateral exploration found a 5-year survival rate of 52.5%.
by sternotomy provided no survival benefit when compared There is no doubt that open surgical exploration can
with unilateral exploration by thoracotomy. In a more recent detect lesions missed by preoperative imaging. However,
study, Younes and colleagues [13] investigated the need for evidence of prolonged survival with the removal of micro-
bilateral exploration in patients with unilateral disease from nodules with a size of 1—2 mm, missed by CT scan and
various primary tumors. They performed 179 unilateral detected by bimanual palpation, does not exit. The
thoracotomies in patients with unilateral disease and 88 assumption of this would be that removal of a 1—2-mm
bilateral thoracotomies for bilateral disease, and followed lesion results in survival benefit whereas overlooking a 0.5-
the patients for contralateral disease-free survival and mm lesion has no influence of survival. A lesion of that size
overall survival. They found no significant difference in would also be missed preoperatively, even with modern CT.
survival in patients with unilateral disease with recurrence in Another advantage of VATS is the preservation of the
the contralateral lung when compared with the patients, who ability to perform repeat operations. VATS results in fewer
had undergone bilateral thoracotomy. The authors concluded pleural adhesions than thoracotomy, and does not complicate
that delaying contralateral thoracotomy until disease a potential repeat operation by thoracotomy [20].
becomes radiologically evident does not affect survival To date, no randomized studies regarding VATS versus
and that bilateral exploration for unilateral disease is not open surgery have been published. At present, it seems that
indicated. VATS can be considered for diagnosis and for pulmonary
The newest surgical approach to pulmonary metastasect- metastasectomy in the presence of few, peripherally located
omy is by video-assisted thoracoscopic surgery (VATS). This lesions. In case of discrepancy between preoperative imaging
minimally invasive approach provides excellent exposure of and perioperative findings or inability to achieve radical
the lung surface, reduces surgical trauma, minimizes post- surgical margins, conversion to open surgery should be
operative pain, provides earlier patient mobilization and mandatory.
decreases hospital length of stay. Pulmonary metastases are
often small nodules located in the periphery of the lung, well
suited for wedge resection by stapler and the VATS approach. 4.2. Recurrence of disease and repeat surgery
The disadvantage is the loss of tactile sensation and the
ability to bimanually palpate the entire lung and, hence, miss The recurrence of disease after pulmonary metastasect-
lesions undetected by imaging. Thus, the quality of the omy is not uncommon. In the International Registry of Lung
preoperative imaging becomes critical to success with VATS Metastases [21], the rate of recurrence of disease was 53% for
surgery. all patients, who underwent complete resection. The rate of
McCormack and colleagues [14] have addressed this issue. recurrence varied amongst the different primary tumors,
They retrospectively reviewed 72 patients, who underwent with sarcomas and melanoma being more frequent (64%) than
pulmonary metastasectomy by thoracotomy. When the epithelial tumors (46%). The site of recurrence also differed
number of metastases removed during surgery was compared with sarcoma (66%) being the most frequent as regards
with preoperative imaging, they found a 42% error rate and intrathoracic relapse in contrast to melanoma where 73%
that CT scan underreported the number of lesions in 25% of relapsed extrathoracically. The 5-year survival for all
patients. In another study, they prospectively compared CT patients with repeat surgery was 44%.
scan results, VATS and confirmatory open thoracotomy with Several later studies have analyzed the impact on survival
bimanual palpation and found a 56% failure rate of CT and after recurrence of disease and repeated pulmonary
VATS to detect all lesions [15]. The study was ended pre- metastasectomy, and have confirmed these findings. In
emptively due to the failure rate, and they concluded that patients with recurrence of colorectal metastases, studies
VATS should be reserved for solely diagnostic purposes. by Pfannschmidt [22], Welter [23], and Ogata [24] have
However, these studies are confounded by the use of older CT reported a 5-year survival of 54.6%, 46%, and 33%,
scanners. respectively. For sarcomas, studies by Briccoli [25], Harting
More recent studies have demonstrated equal survival [26], and Rehders [27] have reported 5-year survival rates of
outcomes with VATS surgery as compared with open 32%, 22,6%, and 36%, respectively.
thoracotomy. Landreneau and colleagues [16] performed Jaklitsch and colleagues [28] investigated the value of
80 VATS procedures and reported a 5-year survival of 30.8% sequential pulmonary metastasectomy from various primary
for patients with colorectal pulmonary metastases resected. tumors. As many as 54 patients underwent at least two
Mutsaerts and colleagues [17] found no significant difference metastasectomies and up till six. They found that 5-year
in survival in patients who underwent VATS compared with survival was stable (>33%) until the 5th or subsequent
patients who underwent VATS followed by confirmatory procedure. With the loss of local control due to unresectable
thoracotomy. Only patients with a single, peripherally tumor in the thorax, further survival dropped to a 2-year
located lesion, and <3 cm, preoperatively detected by a survival of 19%. The authors concluded that repeated

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metastasectomy was well justified as long as local control disease is an established treatment [33]. If control of liver
within the thorax was feasible. metastases can be achieved, combined resection for liver and
None of the above-mentioned studies have found repeat lung metastases does not have an adverse effect on survival
surgery to be an ominous prognostic factor. Thus, if a patient [34,35].
fulfils the initial criteria for pulmonary metastasectomy, Shiono and colleagues [36] investigated the prognostic
repeat surgery does not have an adverse effect on survival. A effect of histopathological variables such as the presence of
possible explanation for this could be that these patients aerogenous spread with floating cancer-cell clusters within
represent an even further-selected subgroup of less malig- the alveoli (ASFCs) and bronchial, vascular, lymphatic or
nant tumors. Further, the patients must be in good condition pleural invasion. They investigated 136 metastatic lesions
to undergo a second operation and, thus, only good from 89 patients. Patients without any of these features had a
candidates for surgery are selected. remarkable 5-year survival of 93.3% while in patients positive
It remains unclear whether resection of all metastases at for both AFSC and vascular invasion it was 24.7%. The
one time is critically important in terms of survival. Naturally, influence of tumor biology on survival seems emphasized by
during each surgery, all malignant disease should be this study.
removed. Lesions undetected by preoperative imaging or
during surgery, but detected during follow-up, may not alter 4.4. Renal cell carcinoma
survival as long as they are resected before they become
unresectable. Approximately 25—30% of patients with renal cell
The current status and recent results of pulmonary carcinoma will have metastatic disease at diagnosis and a
metastasectomy from various primary tumors are discussed further 30% of patients will eventually develop metastases,
in the following sections. with the lungs being the most common organ [37]. Previous
studies have demonstrated 5-year survival rates between 31%
4.3. Colorectal cancer and 53% from renal cell carcinoma, after pulmonary
metastasectomy [38—40].
Approximately 10—20% of patients with colorectal cancer Of the studied prognostic factors, completeness of
will develop pulmonary metastatic disease [29]. Isolated resection was found to be a significant prognosticator of
pulmonary metastases without extrathoracic disease are, survival in all studies. The number and size of metastases also
however, rare and account for as little as 2% of patients with influenced survival, with few and small metastases having a
metastatic colorectal carcinoma [30]. In a recent article, positive effect on postoperative survival. Further, with a
Pfannschmidt and colleagues [31] evaluated the current longer DFI, a better survival was reported compared with
status of surgical resection of pulmonary metastases from short DFI. However, the latter prognostic factors could only
colorectal carcinoma and prognostic factors significant in be verified in some of the above-mentioned studies.
patient selection. Inclusion criteria included studies pub-
lished between 1995 and 2006, more than 40 patients and
patients included in the studies should be no later than 1980. 5. Malignant melanoma
Twenty studies were included.
The overall 5-year survival after pulmonary metasta- Surgical treatment of lung metastases from melanoma is
sectomy ranged between 38.3% and 63.7% with a median of controversial, as the expected outcome is much poorer than
52.5%. They suggested that achieving R0 resection is most for other primary tumors. The ability of malignant
critical for postoperative survival. In their article, two melanoma to disseminate widely causes the number of
studies confirmed this and three studies could not. More than patients eligible for pulmonary metastasectomy to be very
50% of the patients included presented with a single small, as patients with isolated pulmonary metastases are
metastasis and seven studies demonstrated a significantly rare. Once malignant melanoma has spread to a distant site,
better survival with a single lesion versus multiple lesions. the median survival is 8 months, and the 5-year survival is
Thus, patients with a single lesion seem to benefit more from less than 5% [41]. Previous studies with pulmonary metas-
pulmonary metastasectomy than patients with multiple tasectomy from malignant melanoma have demonstrated 5-
metastases. An elevated level of prethoracotomy carci- year survival rates between 22% and 33% [42—44]. This is,
noembryonic antigen (CEA) had an adverse effect on survival however, far superior to medical treatment alone. Of the
in the majority of studies. However, patients with an prognostic factors investigated, completeness of resection
elevated level of CEA still fared better than unresected seems to be the strongest, as patients without R0 resection
patients, and they concluded that even though an elevated have a survival similar to non-resected patients. Further,
level of CEA is an ominous prognostic factor, these patients presence of only a single metastasis and long DFI seem
should not be excluded from pulmonary metastasectomy. associated with a positive effect on survival. Given the grim
The DFI, one of four different prognostic factors in the prognosis for patients with metastatic melanoma, pulmon-
International Registry of Lung Metastases, was only sig- ary resection is a reasonable option in carefully selected
nificant in two studies and, in the majority of studies, DFI did patients.
not influence survival.
Approximately 15% of patients resected for colorectal 5.1. Head and neck cancer
carcinomas can be expected to have hepatic metastases at
the time of exploration [32]. As many as 50% will eventually Head and neck cancer is comprised of a heterogeneous
develop liver metastases, and liver resection for metastatic group of carcinomas such as squamous cell carcinoma of the

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larynx, pharynx and oral cavity, and glandular and adenoid 5.3. Testicular cancer
cystic carcinomas. They usually metastasize to regional
lymph nodes and then to more distant organs, with the Non-seminomatous germ cell tumors are characterized by
lungs being the most frequent [45]. Ferlito and colleagues a wide dissemination, with the lungs being the most frequent
reported an incidence of metastases of 4.2—23.8% in organ and a high sensitivity to cisplatin-based chemotherapy.
squamous cell carcinomas and 37.7—58.8% in adenoid The cure rate has greatly improved to a range of 59—82% over
cystic carcinomas. The number of reports evaluating the the past decades [55,58,59]. Metastectomy is performed
benefit of pulmonary metastasectomy in head and neck after completion of cisplatin-based chemotherapy. Surgery is
cancers is limited. Studies by Mazer [46], Wedman [47], Liu directed at removing residual lung disease to determine
[48], Chen [49], and Winter [50] have reported 5-year further treatment. Therefore, aggressive resection of all
survival ranging from 20.9% to 59%. Survival varies with suspicious lesions is required for prognostic assessment. In
primary tumor histology with best survival reported for case of necrosis/fibrosis or teratoma, no further treatment is
adenoid cystic carcinoma followed by glandular and required in contrast to detection of viable cancer cells, which
squamous carcinoma (84%, 64%, and 34%, respectively in require additional chemotherapy. The presence of multiple
the study by Liu). Reported prognostic factors with metastases, elevated tumor marker levels of human
significant influence on survival were completeness of chorionic gonadotropin (hCG) or alpha fetoprotein (AFP) or
resection and long DFI. Due to the small number of studies, the presence of viable tumor cells in the resected nodules
the benefit of pulmonary metastasectomy in head and neck have been demonstrated to be associated with an adverse
carcinomas is still unclear. Most authors, however, effect on survival [60—62].
advocate resection if the patient fulfils the standard
criteria for pulmonary metastasectomy. 5.4. Osteosarcoma

5.2. Breast cancer Osteosarcoma patients are particularly prone to develop


pulmonary metastases. A total of 10—20% of patients will
The role of pulmonary metastasectomy in metastatic have detectable pulmonary lesions at initial diagnosis and up
breast cancer is unclear. Several studies have shown decent till 70% of patients will develop pulmonary metastases [63—
5-year survival ranging from 30% to 54% [51—53]. However, it 65]. Failure to control thoracic disease is the cause of death
is doubtful whether these survival rates are better than those of nearly all patients with metastatic osteosarcoma [66]. As
achieved by modern, systemic oncological treatment with discussed previously, sarcoma predominantly relapses in the
chemotherapy and/hormone therapy. In a study by Rahman lungs. Therefore, several studies have shown a possible
and colleagues [54] with 1581 patients treated with survival benefit in patients with metastatic osteosarcoma
chemotherapy, a response rate of 65%, including 16.6% when pulmonary resection is performed aggressively and
complete responders, could be demonstrated. The overall repetitively. Studies by Tsuchiya [67], Kager [68], and Suzuki
median survival was 21.3 months and 41.8 months for [69] have shown 5-year survival rates between 29% and 43%.
complete responders. The median survival for resected In almost all reports, the radicality of resection is a strong
patients is not superior to patients treated with modern prognostic factor, as patients without R0 resection have a
chemotherapy. very poor prognosis. Conflicting data have been reported
Planchard and colleagues [55] and Welter and with regard to DFI, number of metastases, size of metastases
colleagues [56] found no difference in survival between and laterality, and the prognostic importance of these factors
complete and incomplete resection, which certainly remains unclear.
questions the impact of surgery on survival. McDonald Surgery remains the mainstay of treatment in the case of
and colleagues [57] even found a better 5-year survival for disseminated osteosarcoma to the lungs, and in non-
patients with incomplete resection (41.1%) versus com- metastatic disease, chemotherapy also plays an important
plete resection (35.6%). However, the difference was not role in prolonging survival [65]. The addition of neo-adjuvant
significant. chemotherapy before pulmonary resection has also been
Of prognostic factors associated with longer survival in demonstrated to be associated with a positive effect on
patients with resectable pulmonary disease, a long DFI and survival, in particular when histologic response to che-
single metastasis have been demonstrated as positive motherapy can be demonstrated. However, patients treated
prognosticators. only with chemotherapy have a very poor prognosis [70], and
The recent study by Welter [56] also investigated hormone surgical resection of metastatic disease to the lungs remains
receptor status of the resected nodules and found the the most efficient therapy.
presence of positive estrogen receptor or Her2-neu receptor
status to have a positive impact on survival. 5.5. Soft tissue sarcoma
At present, it seems that the value of pulmonary
metastasectomy in patients with breast cancer is of Soft tissue sarcoma (STS) is a heterogeneous group of
diagnostic purpose. However, the value of histological malignant tumors with more than 50 histological subtypes
examination of pulmonary lesions cannot be underestimated [71]. In metastatic STS, the lungs are the most frequent organ
to find and resect a possible new lung primary, or, in case of affected and is seen in 20% of patients [72], less than with
confirmed breast cancer metastases, direct further treat- osteosarcoma. Several studies on pulmonary metastasect-
ment with regard to grading, estrogen receptor, and Her2- omy for STS have been published and the 5-year survival
neu receptor status. ranges from 25% to 43% [73—76]. All these studies showed

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that complete surgical resection of pulmonary metastases is randomized, multicenter study is clear. The recently opened
a significant prognostic factor of STS. There is less Pulmonary Metastasectomy in Colorectal Cancer (PulMiCC)
concordance in terms of other prognostic factors such as trial [80], a multicenter and randomized trial, may provide
number, size, and laterality of metastases. However, in most some answers.
studies, a short DFI was associated with a worse prognosis. Furthermore, the Lung Metastasectomy Working Group, a
Usually, the many different histologies of STS are grouped working group under the European Society of Thoracic
together and reported as a whole. However, studies by Surgeons established in 2006, is working towards evaluating
Billingsley [74], and Casson [77] have demonstrated histology the evidence and to generate guidance for the future in
of the primary STS to be a significant prognostic factor of pulmonary metastasectomy [81].
postoperative survival. Malignant fibrous histiocytoma,
rhabdomyosarcoma, and synovial sarcoma are regarded as
more favorable while liposarcoma or peripheral nerve References
sarcomas have a worse prognosis. In general, metastatic
STS is less sensitive to chemotherapy than osteogenic [1] Davidson RS, Nwogu CE, Brentjens MJ, Anderson TM. The surgical
sarcoma, and the response and survival data with che- management of pulmonary metastasis: current concepts. Surg Oncol
motherapy remain disappointing. Therefore, surgical treat- 2001;10:35—42.
ment of metastatic pulmonary STS is the best hope for cure in [2] Alexander J, Haight C. Pulmonary resection for solitary metastatic
sarcomas and carcinomas. Surg Gynecol Obstet 1947;85:129—46.
selected patients. [3] Thomford NR, Woolner LB, Clagett OT. The surgical treament of meta-
static tumors in the lungs. J Thorac Cardiovasc Surg 1965;49:357—63.
[4] Margaritora S, Porziella V, D’Andrilli A, Cesario A, Galetta D, Macis G,
6. Conclusion Granone P. Pulmonary metastases: can accurate radiological evaluation
avoid thoracotomic approach? Eur J Cardiothorac Surg 2002;21:1111—4.
[5] Diederich S, Semik M, Lentschig MG, Winter F, Scheld HH, Roos N,
Patients with untreated metastatic disease have a 5-year Bongartz G. Helical CT of pulmonary nodules in patients with extrathor-
survival rate of less than 5—10% and, for a patient with acic malignancy: CT-surgical correlation. AJR Am J Roentgenol
isolated metastatic disease to the lungs, pulmonary metas- 1999;172:353—60.
tasectomy is often the best hope for cure. It is a safe and [6] Pfannschmidt J, Bischoff M, Muley T, Kunz J, Zamecnik P, Schnabel PA,
Hoffmann H, Dienemann H, Heussel CP. Diagnosis of pulmonary metasta-
effective treatment that leads to possible cure in selected ses with helical CT: the effect of imaging techniques. Thorac Cardiovasc
patients. Regardless of primary tumor, completeness of Surg 2008;56:471—5.
resection is the key to improved survival. Low morbidity and [7] Fortes DL, Allen MS, Lowe VJ, Shen KH, Wigle DA, Cassivi SD, Nichols FC,
mortality rates, in contrast with the lack of any other Deschamps C. The sensitivity of 18F-fluorodeoxyglucose positron emission
tomography in the evaluation of metastatic pulmonary nodules. Eur J
effective systemic oncological treatment, justify the aggres-
Cardiothorac Surg 2008;34:1223—7.
sive approach of surgery. Thoracoscopic resection is a valid [8] Internullo E, Cassivi SD, Van RD, Friedel G, Treasure T. Pulmonary
option in selected patients with few, peripherally located metastasectomy: a survey of current practice amongst members of the
metastases. In case of recurrence of pulmonary disease, and European Society of Thoracic Surgeons. J Thorac Oncol 2008;3:1257—66.
if the patient fulfils the initial criteria for pulmonary [9] Pfannschmidt J, Klode J, Muley T, Dienemann H, Hoffmann H. Nodal
involvement at the time of pulmonary metastasectomy: experiences in
metastasectomy, repeat surgery should be performed. 245 patients. Ann Thorac Surg 2006;81:448—54.
Aggressive postoperative follow-up is warranted. The [10] Ercan S, Nichols III FC, Trastek VF, Deschamps C, Allen MS, Miller DL,
patients should be treated in close collaboration between Schleck CD, Pairolero PC. Prognostic significance of lymph node metas-
the medical oncologist, diagnostic radiologist and thoracic tasis found during pulmonary metastasectomy for extrapulmonary carci-
noma. Ann Thorac Surg 2004;77:1786—91.
surgeon.
[11] Saito Y, Omiya H, Kohno K, Kobayashi T, Itoi K, Teramachi M, Sasaki M,
However, despite numerous studies and decades of Suzuki H, Takao H, Nakade M. Pulmonary metastasectomy for 165 patients
metastasectomies, the lack of randomized studies continues with colorectal carcinoma: a prognostic assessment. J Thorac Cardiovasc
to make the effect of pulmonary metastasectomy question- Surg 2002;124:1007—13.
able. Most studies have been retrospective and the biases are [12] Roth JA, Pass HI, Wesley MN, White D, Putnam JB, Seipp C. Comparison of
median sternotomy and thoracotomy for resection of pulmonary metas-
many: possibly, only patients in good physical condition are tases in patients with adult soft-tissue sarcomas. Ann Thorac Surg
referred; possibly only patients with slow-growing tumors are 1986;42:134—8.
referred (time-length bias) or, possibly, earlier detection [13] Younes RN, Gross JL, Deheinzelin D. Surgical resection of unilateral lung
through more aggressive follow-up leads to earlier surgery metastases: is bilateral thoracotomy necessary? World J Surg
2002;26:1112—6.
with a seemingly longer period of survival. Most reports
[14] McCormack PM, Ginsberg KB, Bains MS, Burt ME, Martini N, Rusch VW,
recommend pulmonary metastasectomy for a properly Ginsberg RJ. Accuracy of lung imaging in metastases with implications for
selected group of patients. However, the case-mix from the role of thoracoscopy. Ann Thorac Surg 1993;56:863—5.
which patients are selected for surgery is rarely described. [15] McCormack PM, Bains MS, Begg CB, Burt ME, Downey RJ, Panicek DM,
Whether the survival of these patients is based on Rusch VW, Zakowski M, Ginsberg RJ. Role of video-assisted thoracic
surgery in the treatment of pulmonary metastases: results of a prospec-
selection rather than surgery is still not clear. As argued tive trial. Ann Thorac Surg 1996;62:213—6.
by Treasure and colleagues [78,79], amongst others, it [16] Landreneau RJ, De GT, Mack MJ, Hazelrigg SR, Ferson PF, Keenan RJ,
remains ‘a common practice based on weak evidence.’ Luketich JD, Yim AP, Coloni GF. Therapeutic video-assisted thoracoscopic
Further, prognostic factors that determine which patients surgical resection of colorectal pulmonary metastases. Eur J Cardi-
othorac Surg 2000;18:671—6.
will benefit from surgery are still not clearly established. To
[17] Mutsaerts EL, Zoetmulder FA, Meijer S, Baas P, Hart AA, Rutgers EJ. Long
determine how to select surgical candidates for pulmonary term survival of thoracoscopic metastasectomy vs metastasectomy by
metastasectomy more precisely, further analysis of prog- thoracotomy in patients with a solitary pulmonary lesion. Eur J Surg Oncol
nostic factors is evident and the need for a prospective, 2002;28:864—8.

Downloaded from https://academic.oup.com/ejcts/article-abstract/39/6/955/379434


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on 03 April 2018
K. Hornbech et al. / European Journal of Cardio-thoracic Surgery 39 (2011) 955—962 961

[18] Mutsaerts EL, Zoetmulder FA, Meijer S, Baas P, Hart AA, Rutgers EJ. [41] Lee ML, Tomsu K, Von Eschen KB. Duration of survival for disseminated
Outcome of thoracoscopic pulmonary metastasectomy evaluated by malignant melanoma: results of a meta-analysis. Melanoma Res
confirmatory thoracotomy. Ann Thorac Surg 2001;72:230—3. 2000;10:81—92.
[19] Gossot D, Radu C, Girard P, Le Cesne A, Bonvalot S, Boudaya MS, Validire P, [42] Leo F, Cagini L, Rocmans P, Cappello M, Geel AN, Maggi G, Goldstraw P,
Magdeleinat P. Resection of pulmonary metastases from sarcoma: can Pastorino U. Lung metastases from melanoma: when is surgical treatment
some patients benefit from a less invasive approach? Ann Thorac Surg warranted? Br J Cancer 2000;83:569—72.
2009;87:238—43. [43] Neuman HB, Patel A, Hanlon C, Wolchok JD, Houghton AN, Coit DG. Stage-
[20] Ludwig C, Cerinza J, Passlick B, Stoelben E. Comparison of the number of IV melanoma and pulmonary metastases: factors predictive of survival.
pre-, intra- and postoperative lung metastases. Eur J Cardiothorac Surg Ann Surg Oncol 2007;14:2847—53.
2008;33:470—2. [44] Andrews S, Robinson L, Cantor A, DeConti RC. Survival after surgical
[21] Long-term results of lung metastasectomy: prognostic analyses based on resection of isolated pulmonary metastases from malignant melanoma.
5206 cases. The International Registry of Lung Metastases. J Thorac Cancer Control 2006;13:218—23.
Cardiovasc Surg 1997;113:37—49. [45] Calhoun KH, Fulmer P, Weiss R, Hokanson JA. Distant metastases from
[22] Pfannschmidt J, Muley T, Hoffmann H, Dienemann H. Prognostic factors head and neck squamous cell carcinomas. Laryngoscope 1994;104:1199—
and survival after complete resection of pulmonary metastases from 205.
colorectal carcinoma: experiences in 167 patients. J Thorac Cardiovasc [46] Mazer TM, Robbins KT, McMurtrey MJ, Byers RM. Resection of pulmonary
Surg 2003;126:732—9. metastases from squamous carcinoma of the head and neck. Am J Surg
[23] Welter S, Jacobs J, Krbek T, Krebs B, Stamatis G. Long-term survival after 1988;156:238—42.
repeated resection of pulmonary metastases from colorectal cancer. Ann [47] Wedman J, Balm AJ, Hart AA, Loftus BM, Hilgers FJ, Gregor RT, van
Thorac Surg 2007;84:203—10. Zandwijk N, Zoetmulder FA. Value of resection of pulmonary metastases
[24] Ogata Y, Matono K, Hayashi A, Takamor S, Miwa K, Sasatomi T, Ishibashi N, in head and neck cancer patients. Head Neck 1996;18:311—6.
Shida S, Shirouzu K. Repeat pulmonary resection for isolated recurrent [48] Liu D, Labow DM, Dang N, Martini N, Bains M, Burt M, Downey Jr R, Rusch
lung metastases yields results comparable to those after first pulmonary V, Shah J, Ginsberg RJ. Pulmonary metastasectomy for head and neck
resection in colorectal cancer. World J Surg 2005;29:363—8. cancers. Ann Surg Oncol 1999;6:572—8.
[25] Briccoli A, Rocca M, Salone M, Bacci G, Ferrari S, Balladelli A, Mercuri M. [49] Chen F, Sonobe M, Sato K, Fujinaga T, Shoji T, Sakai H, Miyahara R, Bando
Resection of recurrent pulmonary metastases in patients with osteosar- T, Okubo K, Hirata T, Date H. Pulmonary resection for metastatic head and
coma. Cancer 2005;104:1721—5. neck cancer. World J Surg 2008;32:1657—62.
[26] Harting MT, Blakely ML, Jaffe N, Cox Jr CS, Hayes-Jordan A, Benjamin RS, [50] Winter H, Meimarakis G, Hoffmann G, Hummel M, Rüttinger D, Zilbauer A,
Raymond AK, Andrassy RJ, Lally KP. Long-term survival after aggressive Stelter K, Spelsberg F, Jauch KW, Hatz R, Löhe F. Does surgical resection of
resection of pulmonary metastases among children and adolescents with pulmonary metastases of head and neck cancer improve survival? Ann
osteosarcoma. J Pediatr Surg 2006;41:194—9. Surg Oncol 2008;15:2915—26.
[27] Rehders A, Hosch SB, Scheunemann P, Stoecklein NH, Knoefel WT, Peiper [51] Tanaka F, Li M, Hanaoka N, Bando T, Fukuse T, Hasegawa S, Wada H.
M. Benefit of surgical treatment of lung metastasis in soft tissue sarcoma. Surgery for pulmonary nodules in breast cancer patients. Ann Thorac Surg
Arch Surg 2007;142:70—5. 2005;79:1711—4.
[28] Jaklitsch MT, Mery CM, Lukanich JM, Richards WG, Bueno R, Swanson SJ, [52] Rena O, Papalia E, Ruffini E, Filosso PL, Oliaro A, Maggi G, Casadio C. The
Mentzer SJ, Davis BD, Allred EN, Sugarbaker DJ. Sequential thoracic role of surgery in the management of solitary pulmonary nodule in breast
metastasectomy prolongs survival by re-establishing local control within cancer patients. Eur J Surg Oncol 2007;33:546—50.
the chest. J Thorac Cardiovasc Surg 2001;121:657—67. [53] Yoshimoto M, Tada K, Nishimura S, Makita M, Iwase T, Kasumi F, Okumura
[29] August DA, Ottow RT, Sugarbaker PH. Clinical perspective of human S, Sato Y, Nakagawa K. Favourable long-term results after surgical
colorectal cancer metastasis. Cancer Metastasis Rev 1984;3:303—24. removal of lung metastases of breast cancer. Breast Cancer Res Treat
[30] McCormack PM, Burt ME, Bains MS, Martini N, Rusch VW, Ginsberg RJ. Lung 2008;110:485—91.
resection for colorectal metastases. 10-year results. Arch Surg [54] Rahman ZU, Frye DK, Smith TL, Asmar L, Theriault RL, Buzdar AU,
1992;127:1403—6. Hortobagyi GN. Results and long term follow-up for 1581 patients with
[31] Pfannschmidt J, Dienemann H, Hoffmann H. Surgical resection of pulmo- metastatic breast carcinoma treated with standard dose doxorubicin-
nary metastases from colorectal cancer: a systematic review of published containing chemotherapy: a reference. Cancer 1999;85:104—11.
series. Ann Thorac Surg 2007;84:324—38. [55] Planchard D, Soria JC, Michiels S, Grunenwald D, Validire P, Caliandro R,
[32] Manfredi S, Lepage C, Hatem C, Coatmeur O, Faivre J, Bouvier AM. Girard P, Le Chevalier T. Uncertain benefit from surgery in patients with
Epidemiology and management of liver metastases from colorectal can- lung metastases from breast carcinoma. Cancer 2004;100:28—35.
cer. Ann Surg 2006;244:254—9. [56] Welter S, Jacobs J, Krbek T, Totsch M, Stamatis G. Pulmonary metastases
[33] Geoghegan JG, Scheele J. Treatment of colorectal liver metastases. Br J of breast cancer. When is resection indicated? Eur J Cardiothorac Surg
Surg 1999;86:158—69. 2008;34:1228—34.
[34] Kobayashi K, Kawamura M, Ishihara T. Surgical treatment for both pul- [57] McDonald ML, Deschamps C, Ilstrup DM, Allen MS, Trastek VF, Pairolero PC.
monary and hepatic metastases from colorectal cancer. J Thorac Cardi- Pulmonary resection for metastatic breast cancer. Ann Thorac Surg
ovasc Surg 1999;118:1090—6. 1994;58:1599—602.
[35] Headrick JR, Miller DL, Nagorney DM, Allen MS, Deschamps C, Trastek VF, [58] Anyanwu E, Krysa S, Buelzebruck H, Vogt-Moykopf I. Pulmonary metas-
Pairolero PC. Surgical treatment of hepatic and pulmonary metastases tasectomy as secondary treatment for testicular tumors. Ann Thorac Surg
from colon cancer. Ann Thorac Surg 2001;71:975—9. 1994;57:1222—8.
[36] Shiono S, Ishii G, Nagai K, Yoshida J, Nishimura M, Murata Y, Tsuta K, [59] Gels ME, Hoekstra HJ, Sleijfer DT, Nijboer AP, Molenaar WM, Ebels T,
Nishiwaki Y, Kodama T, Ochiai A. Histopathologic prognostic factors in Schraffordt Koops H. Thoracotomy for postchemotherapy resection of
resected colorectal lung metastases. Ann Thorac Surg 2005;79:278—82. pulmonary residual tumor mass in patients with nonseminomatous tes-
[37] Hofmann HS, Neef H, Krohe K, Andreev P, Silber RE. Prognostic factors and ticular germ cell tumors: aggressive surgical resection is justified. Chest
survival after pulmonary resection of metastatic renal cell carcinoma. 1997;112:967—73.
Eur Urol 2005;48:77—81. [60] Pfannschmidt J, Zabeck H, Muley T, Dienemann H, Hoffmann H. Pulmo-
[38] Piltz S, Meimarakis G, Wichmann MW, Hatz R, Schildberg FW, Fuerst H. nary metastasectomy following chemotherapy in patients with testicular
Long-term results after pulmonary resection of renal cell carcinoma tumors: experience in 52 patients. Thorac Cardiovasc Surg 2006;54:484—
metastases. Ann Thorac Surg 2002;73:1082—7. 8.
[39] Murthy SC, Kim K, Rice TW, Rajeswaran J, Bukowski R, DeCamp MM, [61] Bajorin DF, Herr H, Motzer RJ, Bosl GJ. Current perspectives on the role of
Blackstone EH. Can we predict long-term survival after pulmonary adjunctive surgery in combined modality treatment for patients with
metastasectomy for renal cell carcinoma? Ann Thorac Surg germ cell tumors. Semin Oncol 1992;19:148—58.
2005;79:996—1003. [62] Steyerberg EW, Keizer HJ, Zwartendijk J, Van Rijk GL, Van Groeningen CJ,
[40] Marulli G, Sartori F, Bassi PF, dal MF, Gino FA, Rea F. Long-term results of Habbema JD, Stoter G. Prognosis after resection of residual masses
surgical management of pulmonary metastases from renal cell carcino- following chemotherapy for metastatic nonseminomatous testicular can-
ma. Thorac Cardiovasc Surg 2006;54:544—7. cer: a multivariate analysis. Br J Cancer 1993;68:195—200.

Downloaded from https://academic.oup.com/ejcts/article-abstract/39/6/955/379434


by guest
on 03 April 2018
962 K. Hornbech et al. / European Journal of Cardio-thoracic Surgery 39 (2011) 955—962

[63] Goorin AM, Shuster JJ, Baker A, Horowitz ME, Meyer WH, Link MP. Cancer-Soft Tissue and Bone Sarcoma Group study of 255 patients. Cancer
Changing pattern of pulmonary metastases with adjuvant chemotherapy 1996;77:675—82.
in patients with osteosarcoma: results from the multiinstitutional osteo- [73] van Geel AN, van CF, Blankensteijn JD, Hoekstra HJ, Schuurman B,
sarcoma study. J Clin Oncol 1991;9:600—5. Bruggink ED, Taat CW, Theunissen EB. Surgical treatment of pulmonary
[64] Huth JF, Eilber FR. Patterns of recurrence after resection of osteosarcoma metastases from soft tissue sarcomas: a retrospective study in The
of the extremity. Strategies for treatment of metastases. Arch Surg Netherlands. J Surg Oncol 1994;56:172—7.
1989;124:122—6. [74] Billingsley KG, Burt ME, Jara E, Ginsberg RJ, Woodruff JM, Leung DH,
[65] Meyers PA, Heller G, Healey JH, Huvos A, Applewhite A, Sun M, LaQuaglia Brennan MF. Pulmonary metastases from soft tissue sarcoma: analysis of
M. Osteogenic sarcoma with clinically detectable metastasis at initial patterns of diseases and postmetastasis survival. Ann Surg 1999;229:602—
presentation. J Clin Oncol 1993;11:449—53. 10.
[66] Sternberg DI, Sonett JR. Surgical therapy of lung metastases. Semin Oncol [75] Chen F, Fujinaga T, Sato K, Sonobe M, Shoji T, Sakai H, Miyahara R, Bando
2007;34:186—96. T, Okubo K, Hirata T, Date H. Significance of tumor recurrence before
[67] Tsuchiya H, Kanazawa Y, Abdel-Wanis ME, Asada N, Abe S, Isu K, Sugita T, pulmonary metastasis in pulmonary metastasectomy for soft tissue sar-
Tomita K. Effect of timing of pulmonary metastases identification on coma. Eur J Surg Oncol 2009;35:660—5.
prognosis of patients with osteosarcoma: the Japanese Musculoskeletal [76] Pfannschmidt J, Klode J, Muley T, Dienemann H, Hoffmann H. Pulmonary
Oncology Group study. J Clin Oncol 2002;20:3470—7. metastasectomy in patients with soft tissue sarcomas: experiences in 50
[68] Kager L, Zoubek A, Potschger U, Kastner U, Flege S, Kempf-Bielack B, patients. Thorac Cardiovasc Surg 2006;54:489—92.
Branscheid D, Kotz R, Salzer-Kuntschik M, Winkelmann W, Jundt G, [77] Casson AG, Putnam JB, Natarajan G, Johnston DA, Mountain C, McMurtrey
Kabisch H, Reichardt P, Jürgens H, Gadner H, Bielack SS. Primary meta- M, Roth JA. Five-year survival after pulmonary metastasectomy for adult
static osteosarcoma: presentation and outcome of patients treated on soft tissue sarcoma. Cancer 1992;69:662—8.
neoadjuvant Cooperative Osteosarcoma Study Group protocols. J Clin [78] Treasure T. Pulmonary metastasectomy: a common practice based on
Oncol 2003;21:2011—8. weak evidence. Ann R Coll Surg Engl 2007;89:744—8.
[69] Suzuki M, Iwata T, Ando S, Iida T, Nakajima T, Ishii T, Yonemoto T, Tatezaki [79] Treasure T, Fallowfield L, Farewell V, Ferry D, Lees B, Leonard P, Macbeth
S, Fujisawa T, Kimura H. Predictors of long-term survival with pulmonary F, Utley M. Pulmonary metastasectomy in colorectal cancer: time for a
metastasectomy for osteosarcomas and soft tissue sarcomas. J Cardio- trial. Eur J Surg Oncol 2009;35:686—9.
vasc Surg (Torino) 2006;47:603—8. [80] Treasure T, Fallowfield L, Lees B. Pulmonary metastasectomy in colorec-
[70] Bacci G, Briccoli A, Longhi A, Ferrari S, Mercuri M, Faggioli F, Versari M, tal cancer: the PulMiCC trial. J Thorac Oncol 2010;5:S203—6.
Picci P. Treatment and outcome of recurrent osteosarcoma: experience at [81] Anile M, Bis B, Bruna MC, Cassivi S, Detterbeck F, Detterbeck FC,
Rizzoli in 235 patients initially treated with neoadjuvant chemotherapy. Dienemann H, Fallowfield L, Filosso PL, Fiorentino F, Friedel G, Furrer
Acta Oncol 2005;44:748—55. M, Garcı́a-Yuste M, Gebitekin C, Gleeson F, Grodzki T, Hensens A, Hoff-
[71] van VM, Kliffen M, Krestin GP, van Dijke CF. Soft tissue sarcomas at a mann H, Jakovic R, Klepetko W, Lees B, Martucci N, Migliore M, Molnar T,
glance: clinical, histological, and MR imaging features of malignant Mossetti C, Oliaro A, Paleru C, Pass HI, Pastorino U, Pfannschmidt J,
extremity soft tissue tumors. Eur Radiol 2009;19:1499—511. Robert JH, Rocco G, Rolle A, Ruffini E, Rusch V, Treasure T, Turna A, Utley
[72] van Geel AN, Pastorino U, Jauch KW, Judson IR, van Coevorden F, Buesa M, van Raemdonck D, Van Schil PE, Venuta F. Pulmonary Metastasectomy
JM, Nielsen OS, Boudinet A, Tursz T, Schmitz PI. Surgical treatment of lung 2010 Working Group Report and Invited Papers The European Society of
metastases: The European Organization for Research and Treatment of Thoracic Surgeons. J Thorac Oncol 2010;5(June Suppl. 2):127—203.

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