Surgical Management of Colorectal Lung

Metastasis
P. James Villeneuve, M.D.1 and R. Sudhir Sundaresan, M.D.1

ABSTRACT

Colon cancer is a systemic disease in 19% of patients and metastasizes most

frequently to the liver and the lung. Survival is enhanced with complete surgical resection
of pulmonary metastases. Comprehensive restaging and verification of preoperative
fitness must precede resection. The operative approach is dictated by the anatomic
location of the metastases, whereas the extent of resection remains a balance between
complete removal of metastatic deposits while preserving as much lung parenchyma as
possible. The presence of metastatic involvement of hilar and mediastinal lymph nodes is
ominous. Multidisciplinary care is highly recommended. An evidence-based algorithm
for the identification assessment and treatment of patients with pulmonary metastases is
proposed.

KEYWORDS: Pulmonary metastases, colorectal cancer, surgical management,

outcomes

Objectives: On completion of this article, the reader should have an appreciation for the role of metastasectomy for pulmonary
metastases from colorectal cancer, understand the importance of restaging and preoperative cardiopulmonary assessment, and apply
the algorithm for identification and referral of patients for consideration of metastasectomy.

METASTATIC COLORECTAL CANCER HISTORICAL ASPECTS AND RATIONALE

Colorectal cancer (CRC) is an extremely prevalent
cancer, with greater than 1 million cases identified in
the world yearly. Of these cases, 19% present with stage
IV disease. Colorectal cancer metastases are most com-
monly found in the liver; lung is the second most
common site. Overall survival with untreated stage IV
disease is 11.3% at 5 years,1 although in a selected
patient population, resection of isolated pulmonary
metastases can increase survival rates up to 40% at
5 years.2,3
FOR PULMONARY METASTASECTOMY
The first reported case of pulmonary metastasectomy
dates back to 1882, when Weinlechner performed pul-
monary resection for two incidental lesions found during
resection of a sarcomatous chest wall lesion.4 This was
followed by a planned resection of pulmonary metastases
by Divis5 in 1927. Long-term survival was observed in
1934, as Edwards6 reported 18-year survival after resec-
tion of metastatic osteogenic sarcoma. Barney and
Churchill7 then reported 23-year survival after resection

1
Division of Thoracic Surgery, The Ottawa Hospital, University of
Ottawa Faculty of Medicine, Ottawa, Ontario, Canada.
Address for correspondence and reprint requests: R. Sudhir
Sundaresan, M.D., Ottawa Hospital–General Campus, 501 Smyth Rd.,
Rm. 6361, Ottawa, Ontario, Canada K1H 8L6 (e-mail: ssundaresan@
ottawahospital.on.ca).
Colorectal Cancer; Guest Editor, Robin P. Boushey, M.D., Ph.D.
Clin Colon Rectal Surg 2009;22:233–241. Copyright # 2009 by
Thieme Medical Publishers, Inc., 333 Seventh Avenue, New York, NY
10001, USA. Tel: +1(212) 584-4662.
DOI 10.1055/s-0029-1242463. ISSN 1531-0043.
233
234 CLINICS IN COLON AND RECTAL SURGERY/VOLUME 22, NUMBER 4 2009

Figure 1 Computed tomographic (CT) and positron emission tomography (PET) images from a 62-year-old man who
underwent resection of a T3N0 sigmoid colon carcinoma 2½ years prior. (A) CT image showing the typical peripheral location
of a pulmonary metastatic lesion in the posterior basal segment of the right lower lobe (arrowhead). (B) Whole body PET scan
shows a solitary focus of uptake in this nodule, confirming the presence of a solitary pulmonary metastasis (arrowhead) without
hilar or mediastinal lymph node involvement. The patient underwent successful right video-assisted thoracoscopy procedure
with wedge resection of this metastasis.

of pulmonary metastases from renal cell cancer. The first
resection of pulmonary colorectal metastases was re-
ported by Blalock8 in 1944. In the intervening years,
multiple series have demonstrated that durable survival
benefits are obtained with surgical resection of meta-
static disease – the current aggregate survival at 5 years
stands at approximately 35% (with variations depending
on the tissue of origin of the primary tumor).9 In the
remainder of this article, the critical issues pertaining to
pulmonary metastasectomy for colorectal metastases will
be presented.
RESTAGING STUDIES AND ASSESSMENT
OF THE METASTATIC BURDEN
Patients treated for colorectal cancer undergo regular
physical examinations, carcinoembryonic antigen (CEA)
serum levels, colonoscopy, and cross-sectional imaging
of the abdomen and pelvis as a part of routine surveil-
lance set out in the National Comprehensive Cancer
Network (NCCN) guidelines.10 If recurrent or meta-
static colorectal carcinoma is suspected, restaging is
indicated. This includes colonoscopy, computed tomog-
raphy (CT) of the thorax/abdomen/pelvis, and the
consideration of a positron emission tomography
(PET) scan if CT imaging and colonoscopy do not
localize the site of recurrence.10 In the case of pulmonary
metastases, a multidetector CT scan is considered a first-
line test. Present CT technology allows for image
acquisition across the entire thorax at 1-mm slice
thickness during a single breath hold. Older generation
(single detector) CT scans were 100% sensitive for
nodules as small as 6 mm, whereas smaller parenchymal
nodules were only accurately characterized in 66% of
cases. Pleural nodules were found to be more difficult to
assess, as only 17% accuracy was achieved for nodules
6 mm or less in size. Increased sensitivity up to 98% can
be obtained using intravenous contrast and objectively
measuring nodular Hounsfield units.11 PET scans are
now the imaging modality of choice for detection of
occult metastases (patients with elevated CEA and no
evidence of disease on imaging), unsuspected pulmonary
or hilar lymph node disease, and for assessing extra-
thoracic disease burden (Fig. 1).12–14
Published estimates suggest that 20% of meta-
static nodules are not detectable preoperatively.15 This
has relevance for the growing enthusiasm for application
of minimally invasive surgical approaches to metastasec-
tomy, in that these approaches do not allow the operat-
ing surgeon to bimanually palpate the lung parenchyma.
Several strategies have therefore been proposed to en-
hance intraoperative identification of smaller nodules.
These include preoperative placement of hookwires,16,17
methylene blue,18 and most recently, metallic coils19
using image-guidance. The published experience has
been small, and the net benefits inconclusive, especially
when one considers periprocedural complications (pleur-
itic pain, pneumothorax, and dislodging of markers).
 SURGICAL MANAGEMENT OF COLORECTAL LUNG METASTASIS/VILLENEUVE, SUNDARESAN
Intraoperative ultrasound,20 image-guided stereotactic
navigation,21 and the use of technetium radiotracer
scintigraphy22 have also been examined. These tech-
niques may have utility in delineating metastatic
burden, but seem to be ideally suited for localizing
solitary pulmonary nodules for video-assisted thoraco-
scopy (VATS) biopsies, rather than for multiple
metastasectomies.
It is our practice to routinely secure preoperative
diagnosis of pulmonary nodules by fine-needle aspiration
biopsy (FNAB), as this facilitates appropriate workup
and operative planning. In patients presenting with
pulmonary nodules after a long disease-free interval
from their primary colorectal cancer resection, and who
have specific risk factors for another primary cancer
(for example, a significant smoking history or asbestos
exposure), it is prudent to determine the tissue of origin.
FNAB samples showing positive immunohistochemical
staining for TTF1 (thyroid transcription factor 1) rep-
resent lung parenchymal origin (91% sensitive, 98%
specific); CDX2 staining (caudal type homeobox tran-
scription factor 2) represents colonic tissue origin (83%
sensitive, 96% specific).23 This distinction is particularly
relevant, as the staging workup and resection of primary
lung cancer is significantly different from that necessary
for colorectal metastases.
PREOPERATIVE ASSESSMENT
OF PULMONARY RESERVE
A detailed assessment of the patient’s medical status
must be undertaken prior to conducting metastasectomy.
In addition to general medical fitness, a close examina-
tion of cardiopulmonary fitness must be assessed by
testing pulmonary function and exercise tolerance.
Fitness criteria24 recommended by the American
College of Chest Physicians are outlined in Table 1.
Smoking status must be determined and smoking cessa-
tion advocated if indicated. Details of prior neo- and
adjuvant treatments must be sought out25 in the history,
as certain chemotherapy regimens are toxic to lung
parenchyma (glycopeptides such as bleomycin), whereas
others are cardiotoxic (anthracyclines such as doxorubi-
cin). Any history of external-beam radiotherapy should
prompt thorough pulmonary function testing. The
Table 1 Fitness Parameters for Pulmonary Resection
Forced expiratory volume (FEV1)
Greater than 2 L suitable for pneumonectomy
Greater than 1.5 L suitable for lobectomy
Carbon monoxide diffusion (DLCO) 80% or greater of predicted
Maximal oxygen consumption (VO2max) should be determined
if FEV1 or DLCO are less than 60% of predicted
Minimum of 15 mL/kg/min
Adapted from Bapoje et al.24
235
Table 2 Selection Criteria for Pulmonary
Metastasectomy
Colorectal primary controlled, or
If present, is considered resectable
Absence of extrathoracic disease, or
If present, is resectable or ablatable
Pulmonary metastases are completely resectable
An R0 resection is the goal
Patient has adequate cardiopulmonary reserve
Adapted from Greelish, Friedberg25 and Pfannschmidt et al.54
severity of functional impairment will dictate the extent
of pulmonary resection that may be considered. Inclusion
of preoperative pulmonary rehabilitation and neuraxial
analgesic strategies26 such as epidural or paravertebral
blocks serve to optimize postoperative recovery of
respiratory function, as do newer surgical approaches
such as VATS and muscle-sparing thoracotomy.27
INDICATIONS FOR PULMONARY
METASTASECTOMY
The goal of resection in metastatic CRC is to achieve a
complete extirpation of intrathoracic disease without
sacrificing excessive amounts of normal lung paren-
chyma. Guiding principles (see Table 2), outlined by
Thomford, Woolner, and Clagett28 in 1965, an exten-
sion of earlier work by Alexander and Haight29 in 1947,
are still considered30 to provide appropriate patient
selection criteria. There should be no doubt that the
ultimate goal is a complete (R0 – no gross or microscopic
residual disease) resection: following complete metasta-
sectomy, the median survival is 35 months, whereas
following incomplete resection, the median survival is
only 15 months.3
CONTROVERSIES IN CHOICE
OF OPERATIVE APPROACH
AND EXTENT OF RESECTION
Choice of Incision and Approach
The surgical approach to R0 resection of pulmonary
metastases is dictated by the size, number and distribu-
tion of individual tumor deposits. The bilateral thora-
costernotomy (‘‘clamshell’’ incision), popularized initially
for lung transplantation and later applied to bilateral
metastasectomies, entails bilateral submammary thora-
cotomies with transverse division of the sternum. This
incision provides excellent exposure to the hilum and all
lobes of the lung, including both lower lobes.31 How-
ever, postoperative complications are significant and
include nonunion and displacement of the transverse
sternotomy, as well as migration or infection of fixation
hardware. Median [midline] sternotomy is commonly
236 CLINICS IN COLON AND RECTAL SURGERY/VOLUME 22, NUMBER 4
used for cardiac surgical procedures and has applicability
in pulmonary surgery. The main advantage is the access
to both lungs (albeit reduced access to the lower lobes,
especially the left), with lower morbidity (decreased
intercostal nerve and muscle injury).32 Anterior and
lateral thoracotomies currently represent the standard
incision for open pulmonary surgery; however, VATS
procedures are rapidly gaining popularity. VATS resec-
tions utilize laparoscopic-style instruments introduced
via trocars, resulting in smaller incisions and reduced
postoperative morbidity.33
Data supporting bilateral resections, via clamshell
or median sternotomy may have been influenced by the
suboptimal imaging modalities of an earlier era (linear
tomography and early CT scan technology). The routine
necessity for bilateral exploration with bimanual palpa-
tion of lung parenchyma has been brought into question
by improvements in current-era imaging modalities such
as helical multidetector CT scans and PET scans. It may
be for these reasons that prior to 1979, lateral thoracot-
omies were performed for metastasectomy; afterwards,
the median sternotomy dominated.34
VATS procedures were reported in the early
1990s and have gained momentum ever since.35 Most
published reports suggest equivalent outcomes with
open and thoracoscopic approaches; VATS appears to
achieve equivalent postoperative and 5-year survival
rates,36,37 with reduced perioperative morbidity. Cancer
recurrence at VATS port sites has not been widely
reported: a single study reports38 four recurrences in
26 cases, with all recurrences occurring within the first
5 postoperative months. A second study39 reports three
port site recurrences in 36 cases. These reports encom-
pass results from early VATS procedures – increasing use
of wound protectors and specimen extraction bags37 has
reduced this risk significantly. The consideration of
minimally invasive operative approaches should be based
on adherence to identified predictors of a successful
VATS approach to pulmonary metastases.15 These pa-
rameters, evaluated by Cerfolio and colleagues, include
the number, size, and location (central versus peripheral;
upper versus lower lobe) of the metastatic deposits, and
are summarized in Table 3.
The choice of operative approach and specifically
the use of minimally invasive approaches will likely be
Table 3 Patterns of Pulmonary Metastatic Spread
and Suggested Operative Approach
Operative Approach
Nodule
Characteristics VATS Thoracotomy
Number (n) 1–3 >3
Size (cm) <1.5 cm >4 cm
Location Peripheral Central
Lobe involved Upper, middle Lower
Adapted from Cerfolio et al. 15
VATS, video-assisted thoracoscopy.
2009
the subject of controversy for some time to come or until
more data are available. However, Roth,34 and more
recently Nakajima36 have published their experiences
showing that the operative approach does not appear
to influence overall outcome.
Extent of Resection
Metastases are most commonly located peripherally in
the lung parenchyma and more frequently in the lower
lobes. This allows for relatively straightforward non-
anatomic resection (Fig. 1), as reflected in the frequen-
cies of this type of resection in larger series, such as the
International Registry of Lung Metastases (IRLM). The
most common pulmonary metastasectomy performed3
was a nonanatomic wedge resection (67% of patients
registered in the IRLM), followed by lobar resections
(21%), segmentectomies (9%), and pneumonectomy
(3%).
Pneumonectomy is rarely performed as the initial
procedure for metastasectomy. This is related to several
factors including a postoperative mortality rate ap-
proaching or exceeding 5%; the lack of conservation of
lung parenchyma; and a 5-year survival rate of only
16%.40 Completion pneumonectomy as a second proce-
dure remains controversial.41 In patients who are not
operative candidates from a pulmonary reserve stand-
point, there is recent evidence that radiofrequency abla-
tion may serve to control metastatic disease,42 although
repeated rounds of ablation are likely required.43
Patients whose disease pattern includes both hep-
atic and pulmonary metastases have been shown to
benefit from either sequential or simultaneous liver and
lung resections, with a 51% 5-year survival rate.44
Factors predictive of good outcome included younger
age, solitary metachronous liver metastases preceding
lung metastases, and a long disease-free interval.45 In
these cases, assessment by a hepatobiliary surgeon in the
context of multidisciplinary cancer care is recommended;
close consultation is required to decide between staged or
concurrent resection strategies (Fig. 2).
OUTCOME FOLLOWING PULMONARY
METASTASECTOMY
The results of several small series of patients undergoing
metastasectomy have been reported – however, we will
focus on data from the largest series from 1991–1995,
and a more contemporary meta-analysis of published
reports from 1995–2006.
The IRLM is a database of pulmonary resections
performed for metastases from all cancer types at 18
thoracic centers worldwide over the years 1991–1995,
representing an accrual of 5206 separate cases.3 This has
generated robust data regarding postoperative outcomes,
survival, and the determination of adverse risk factors.
 SURGICAL MANAGEMENT OF COLORECTAL LUNG METASTASIS/VILLENEUVE, SUNDARESAN 237

Figure 2 Computed tomographic (CT) images of a 56-year-old woman who underwent left colon resection of a T4N1 colon
carcinoma one year prior. (A) Lung windows show a peripheral metastatic deposit in the left lower lobe (arrowhead).
(B) Abdominal CT image showing a metastatic deposit in the left lobe of the liver (arrowhead). The patient underwent
successful surgery for synchronous resection of these metastases, through a left video-assisted thoracoscopy approach
followed by laparotomy.

The disease-free interval strongly affects outcomes, as
patients presenting with early pulmonary metastases
(within the first year) had a median survival of
29 months, whereas those presenting with metastases
3 years or more after their primary treatment had a
median survival of 49 months. Multivariate analysis of
this data allowed for identification of adverse risk factors
and survival grouping. Resectability of metastases, the
disease-free interval, and number of metastases (single
versus multiple) all had significant influence on long-
term outcome, with resectability having the most pro-
found impact (Table 4).
The Heidelberg group2 has published a meta-
analysis of 14 studies of pulmonary metastasectomies for
colorectal cancer, incorporating 1684 patients in series
published from 1995–2006. Perioperative mortality
ranged from 0–2.5%, confirming that metastasectomy
is a safe procedure. The majority of the patients reported
underwent unilateral procedures (n ¼ 886) involving
wedge resections. The overall survival rate in this series
was 48% at 5 years.
In this study, peribronchial and mediastinal
lymph node metastases were observed in 9.8% of cancer
patients with CRC metastases, and had a profound
impact on long-term survival. Although overall 5-year
survival rate was found to be 48%, the survival rate rose
to 60% in the absence of nodal disease. In the presence of
peribronchial/hilar nodes, survival was reduced to 17%.
No patients with mediastinal lymphadenopathy survived
5 years.46 These findings have been corroborated in
another recent meta-analysis.2,30
Preoperative elevation of CEA level (greater than
10 ng/mL47) is also an adverse risk factor. Patients with
normal serum CEA levels preoperatively had a 5-year
survival rate of 60%, whereas those with high CEA levels
had only an 18% survival rate. Other negative prognostic
factors include a tumor doubling time of less than
100 days,48 and the presence of several histopathologic
markers: presence of p53 staining, vascular invasion,
presence of alveolar floating cancer cell clusters, and
positive E-cadherin staining have all been related to
reduced survival.49,50
There are conflicting data supporting the efficacy
of repeat pulmonary metastasectomy for metastatic
CRC. Welter’s group51 reports that the number of
metastases present at the first resection is the most

Table 4 Adverse Risk Factors and Prognostic Grouping for Pulmonary Metastases Based on Multivariate Analysis of
the IRLM Data
Group Resectable? Number of Risk Factors Median Survival (Months)

I Yes 0 61
II Yes 1 34
III Yes 2 24
IV No N/A 14
Risk factors: Disease-free interval less than 36 months, multiple metastases. N/A=not applicable.
Adapted from The International Registry of Lung Metastases (IRLM).3
238 CLINICS IN COLON AND RECTAL SURGERY/VOLUME 22, NUMBER 4
important determinant of overall survival. A Japanese
group52 has reported decreased survival with two or more
resections, suggesting the first pulmonary metastasec-
tomy is the most effective, while Kim and colleagues53
show that 5-year survival is not different between
patients undergoing single or multiple pulmonary
resections.
RECOMMENDATIONS
Pulmonary metastasectomy is currently an accepted
mode of treatment for metastatic colorectal carcinoma
Figure 3 An approach to the patient with suspected pulmonary metastases.
2009
in selected patients. The authors propose an evidence-
based approach applicable in this circumstance (Fig. 3).
Suspicion of pulmonary metastases should
prompt thorough restaging studies, which include CT
of the thorax, abdomen, and pelvis. Consideration
should be given for a PET scan for assessment of intra-
thoracic (hilar or mediastinal) lymphadenopathy as well
as occult recurrence at the primary site or elsewhere in
the abdomen or pelvis. Patients with isolated thoracic
disease should then be further assessed for resection,
with the planned extirpative procedure anticipating an
R0 resection. The extent of pulmonary resection will
 SURGICAL MANAGEMENT OF COLORECTAL LUNG METASTASIS/VILLENEUVE, SUNDARESAN
further guide the magnitude of preoperative workup:
patients requiring a pneumonectomy will necessarily
require a greater level of cardiopulmonary reserve as
compared with patients requiring wedge resection(s)
alone.
For patients whose metastatic disease is unre-
sectable, or whose cardiopulmonary reserve is insuffi-
cient, nonresectional treatments are appropriate.
There is limited experience in ablative techniques
(such as radiofrequency ablation) for lung metastases,
but early results are encouraging.42 The role of che-
moradiotherapy is not yet defined for pulmonary
colorectal metastases because historically, these lesions
did not respond well to adjuvant treatments. The
current era of chemotherapy10 has shown impressive
responses in primary colorectal cancers to such regi-
mens as FOLFOX (fluorouracil, leucovorin and ox-
aliplatin) and FOLFIRI (fluorouracil, leucovorin and
irinotecan), with or without the addition of biologic
agents such as bevacizumab (anti-vascular endothelial
growth factor; VEGF), cetuximab and panitumumab
(anti-epidermal growth factor receptor; EGFR).
These have not yet been studied systematically and
may actually represent more efficacious treatment for
pulmonary metastases. Patients whose functional sta-
tus is poor may be candidates for palliative approaches
to care.
When the metastatic burden and distribution are
amenable to curative resection, and the patient is fit for
pulmonary resection, the next issue is choice of operative
approach. This will be largely dictated by the pattern and
location of metastatic disease.
The operative approach best suited for unilateral
pulmonary disease is based on principles outlined by
Cerfolio and colleagues15 (Table 3), and also on the level
of comfort of the operating surgeon with minimally
invasive thoracic surgical techniques.
Bilateral pulmonary disease can be approached in
a similar manner – the criteria outlined in Table 1 will
determine the suitability of staged VATS resections. If
disease is not amenable to VATS, then staged thor-
acotomies are preferred, followed by median sternot-
omy or a clamshell approach. Arguments in favor of
bilateral access incisions place emphasis on wide
exposure to permit a full manual exploration of the
thoracic cavity and lung parenchyma, with criticism of
the VATS approach being a perceived inability to fully
explore the lung. The authors note in their experience
of VATS metastasectomies, early mobilization of the
inferior pulmonary ligament, coupled with the use of a
‘‘three-finger’’ utility incision (as performed for a thor-
acoscopic lobectomy) allows for a very satisfactory
assessment of the posterior and inferior areas of the
lung.
After pulmonary resection for colorectal metasta-
ses, follow up should include continued surveillance for
239
local and distant recurrence as outlined in the NCCN
guidelines.10 Controlling for pulmonary recurrence and
postoperative complications is most effective with con-
trast enhanced CT scans of the thorax.
CONCLUSION
Pulmonary metastases from colorectal cancer represent
a challenging situation, where metastasectomy carries
genuine benefit in carefully selected patients. Key
factors to consider include adherence to oncologic
principles, technical feasibility of the proposed resec-
tion and the overall fitness of the patient to undergo
pulmonary resection. Although patient selection and
determination of operative fitness must be highly in-
dividualized, an evidence-based algorithm to guide
patient selection, assessment and operative approach
is proposed.
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