The Role of VATS for Staging and Diagnosis

in Patients with Non-Small Cell Lung Cancer

John A. Howington, MD, FACS

Video-assisted thoracoscopic surgery is an effective and versatile tool for the diagnosis
and staging of patients with lung cancer. Despite advances in imaging technology, includ-
ing integrated positron emission tomography/computed tomography scans, the clinical
staging of patients with lung cancer remains inaccurate. Tissue confirmation is critical for
accurate staging and treatment of patients with lung cancer. Thoracoscopy is an excellent and
often preferred approach to the biopsy of inferior mediastinal, anteroposterior window, and
para-aortic lymph nodes, and has the added advantage of allowing simultaneous assessment
of the pleural space, satellite lung nodules, and T status of the tumor. Thoracoscopic wedge
resection is the preferred technique for diagnosing indeterminate solitary pulmonary nod-
ules. In the era of computed tomography screening, most indeterminate lung nodules are
less than 1 cm in size and pose unique challenges in determining malignant potential and
obtaining a tissue diagnosis. Several techniques have been adopted to allow successful
thoracoscopic biopsy of these subcentimeter lung nodules.
Semin Thorac Cardiovasc Surg 19:212-216 © 2007 Elsevier Inc. All rights reserved.

KEYWORDS lung cancer, staging, thoracoscopy, VATS, video-assisted thoracic surgery,

thoracoscopic staging

T horacoscopy was first described by Hans Christian Jaco-

baeus in 1910 for the management of a pleural effusion
with a cystoscope.1 During the first half of the 20th century,
thoracoscopy was used almost exclusively for the manage-
ment of pleural effusions and pulmonary tuberculosis. With
the development of video imaging capabilities and high-op-
tical– quality thoracoscopes in the late 1970s and 1980s, the
utility and applicability of thoracoscopy grew dramatically.
Thoracoscopy is now the current standard approach to pleu-
ral space disorders, spontaneous pneumothorax, sympathec-
tomy, and wedge resection of peripheral solitary pulmonary
nodules.
Today, the technology continues to advance at a more
rapid pace with high-definition video monitors, robot-as-
sisted technology, specialized thoracoscopic surgical instru-
ments, and endomechanical stapling devices designed spe-
cifically for minimally invasive thoracoscopic procedures.
Recently, several large surgical series have reported on the
Division of Thoracic Surgery, Department of Surgery, Evanston Northwest-
ern Healthcare, Northwestern University, Feinberg School of Medicine,
Evanston, Illinois.
Address reprint requests to John A. Howington, MD, FACS, Department of
Surgery, Evanston Northwestern Healthcare, Northwestern University,
Feinberg School of Medicine, 2650 Ridge Avenue, 3507 Walgreen Bldg,
Evanston, IL 60201. E-mail: jhowington@enh.org
safety, efficacy, and outcomes of minimally invasive thoraco-
scopic lobectomy for the treatment of early-stage lung can-
cer.2-4 This article will focus on the role of thoracoscopy in
staging patients with known or suspected lung cancer and its
role in the diagnosis of lung cancer.
The Role of
Thoracoscopy in Staging Patients
with Non-Small Cell Lung Cancer
Video-assisted thoracoscopic surgical staging is complemen-
tary to other minimally invasive approaches to mediastinal
staging, provides ready access to nodes at levels 5, 6, 7, 8, and
9, and is the only minimally invasive modality capable of
providing complete visualization of the pleural space. Video-
assisted thoracoscopic surgery (VATS) provides the opportu-
nity to assess for mediastinal or chest wall invasion by the
primary tumor, biopsy satellite lung nodules, evaluate pleural
effusions, and perform pleurodesis if indicated all at the time of
mediastinal staging. Patients cleared of unresectable tumors or
mediastinal lymph node metastasis can proceed immediately to
surgical resection and thoracic lymphadenectomy.
Despite advances in imaging technology and sophisticated
techniques, including integrated positron emission tomogra-

212 1043-0679/07/$-see front matter © 2007 Elsevier Inc. All rights reserved.
doi:10.1053/j.semtcvs.2007.07.007
Role of VATS in patients with non-small cell lung cancer
phy (PET)/computed tomography (CT) scans, clinical stag-
ing of non-small cell lung cancer remains inaccurate.5-10 In-
vasive staging continues to play an essential role in the
preoperative or pretreatment management of the patient with
non-small cell lung cancer.
Cerfolio and colleagues5 performed a prospective review of
383 patients with primary non-small cell lung cancer. All
patients were clinically staged with CT scans of the chest and
integrated PET/CT scans. Patients with suspicious N2 or N3
lymph nodes had invasive mediastinal staging with cervical
mediastinoscopy and/or endoscopic ultrasound with fine-
needle aspiration (EUS FNA) before surgical resection. If
there was no evidence of N2 or higher disease, patients were
treated with thoracotomy, pulmonary resection, and a tho-
racic lymphadenectomy. PET/CT and CT scan clinical staging
suggested N2 disease in 184 of 383 patients (48%). Ninety-
seven (53%) of these patients were found to be false positives
after invasive mediastinal staging and surgical resection with
thoracic lymphadenectomy. False positives were not uncom-
mon, even with very high maxSUV (⬎12 at station 4R). This
study and others confirm that tissue confirmation of any
suspicious mediastinal lymph node is mandatory, and treat-
ment decisions cannot be made based on findings of 2-de-
oxy-2[(18)F]fluoro-D-glucose-PET/CT scans alone. The au-
thors noted a 14% incidence of unsuspected N2 disease
(false-negative PET/CT), with the most common site being
the subcarinal and aorto-pulmonary lymph nodes. Both of
these sites are readily accessible by thoracoscopy.
Thoracoscopy in the
Clinically Negative Mediastinum
Thoracoscopy is highly accurate in staging patients with clin-
ically negative mediastinal lymph nodes. Roberts and col-
leagues11 reported on a prospective comparison of clinical CT
staging, thoracoscopic staging, and pathologic staging in 50
patients with early-stage lung cancer. All the patients had a
complete CT scanning of the chest and upper abdomen and
negative cervical mediastinoscopy before thoracoscopic stag-
ing. For lower lobe lesions, inferior mediastinal nodes (levels
8 and 9) were always sampled. Patients in this study did not
have routine sampling of the subcarinal location with thora-
coscopy. Paratracheal and subcarinal nodes were not sam-
pled unless they appeared pathologic at thoracoscopy. Pa-
tients without N2 disease or malignant pleural effusion had a
complete pulmonary resection of the primary tumor and tho-
racic lymphadenectomy. CT scan staging understaged 30%
of patients and overstaged 28% of patients while only cor-
rectly staging 42%. In comparison, thoracoscopic staging
correctly staged 86% of patients and understaged 14% with
pathologic staging as the benchmark. Two patients (4%) with
pathologic stage II cancers based on involved hilar lymph
nodes were incorrectly staged by thoracoscopy as stage I.
However, this would not have changed the approach to treat-
ment in these patients because the current standard for pa-
tients with stage II disease is complete surgical resection fol-
lowed by adjuvant chemotherapy. Five patients (10%) with
negative invasive mediastinal staging by cervical mediasti-
213
noscopy and thoracoscopy were found to have single-station
N2 disease in the subcarinal location on pathologic staging of
the surgical lymphadenectomy. This high false negative rate
highlights the importance of systematic lymph node sam-
pling and the inaccuracy of visual inspection of lymph nodes
which was used during thoracoscopy for lymph nodes in the
subcarinal location in this trial. Cervical mediastinoscopy
most often allows sampling of the highest subcarinal lymph
node and misses the lower and more posterior subcarinal
lymph nodes, which may be the sentinel node in lower lobe
tumors.
Cerfolio and colleagues,9 in a prospective trial of 153 pa-
tients who were clinically N2 negative by integrated PET/CT,
performed routine cervical mediastinoscopy and EUS FNA in
all patients even if 1 test yielded N2 disease. At mediastinos-
copy, stations 2R, 4R, 2L, 4L, and 7 were investigated and if
lymph nodes were identified, biopsies were performed irre-
spective of the node appearance. EUS FNA was performed on
all patients, and biopsies at levels 7, 8, and 9 were performed
in all patients. In this study, only 6 patients (4%) staged as
negative for N2 or N3 disease by cervical mediastinoscopy
and EUS FNA had pathologic N2 disease after surgical resec-
tion and lymphadenectomy. Of note, all 6 patients were
staged as clinical N0 by integrated PET/CT. The authors also
noted a significant incidence of positive N2 disease (17.6% at
mediastinoscopy and 23.4% with EUS FNA) in patients
staged as clinical N1 disease by integrated PET/CT, which
highlights the need for routine invasive mediastinal staging in
patients with clinical N1 disease.
Thoracoscopy also proved effective in evaluating patients
for malignant pleural disease in the study by Roberts and
colleagues.11 Four patients with moderate to large pleural
effusion read as malignant on CT scanning were proven re-
active by thoracoscopy, and 3 patients had small pleural ef-
fusions not seen on CT scan that proved to be malignant.
Thoracoscopy in the
Clinically Positive Mediastinum
Thoracoscopy is also an effective and minimally invasive ap-
proach to patients with clinically positive mediastinal lymph
nodes. Massone and colleagues12 reported on their experi-
ence with a video-assisted thoracoscopic approach to the
diagnosis of clinical lymphadenopathy in the mediastinum.
Patients were deemed clinical N2 if they had a lymph node
⬎1 cm in diameter on CT scan or had increased metabolic
activity in a mediastinal lymph node on PET scan. Patients
with bilateral superior mediastinal lymph node enlargement
or suspected disease at the 2R or 4R location were ap-
proached with cervical mediastinoscopy and excluded from
this study. Eighty-five patients with clinical N2 disease un-
derwent VATS biopsies. Two patients had pleural nodules
not seen preoperatively and had pleural biopsy confirming
malignancy. This further illustrates the advantage of detailed
assessment of the pleural space obtained during thoraco-
scopic staging. Lymph node biopsies were performed in the
remaining 83 patients at stations 5, 6, 7, or 8. Fifty-five pa-
tients with suspected primary lung cancer and clinical N2
214
disease had VATS biopsies performed. The false-positive rate
for clinical staging in this series was 36%. Twenty patients
with lung cancer found negative for N2 disease on frozen
section at the time of thoracoscopic staging had surgical re-
section and lymphadenectomy, confirming the absence of
mediastinal lymph node metastasis. The false-negative rate of
VATS staging in this series was 0.
The Role of
Thoracoscopy in the Diagnosis
of Non-Small Cell Lung Cancer
The modern thoracic surgeon has many choices in the
approach to solitary pulmonary nodules and ground glass
opacities.13,14 Thoracoscopy as a diagnostic tool for indeter-
minate pulmonary nodules has many advantages over open
thoracotomy. VATS has been proven to be highly sensitive,
specific, and accurate in the diagnosis of indeterminate soli-
tary lung nodules.
Santambrogio and colleagues15 performed a randomized
trial comparing a VATS approach to diagnosis of solitary
pulmonary nodule with a muscle-sparing lateral thoracot-
omy in 44 patients treated between January 1991 and May
1994. The 22 patients in each arm of the trial were similar in
age, comorbid conditions, and symptoms. All patients in
each group had a final diagnosis made with no nondiagnostic
results. The hospital stay was significantly shorter at 4.6 ⫾
1.08 days in the VATS group compared with 7.8 ⫾ 0.89 days
in the lateral thoracotomy group (P ⬍0.01). The visual ana-
log pain score on postoperative day 6 was significantly less at
26.5 ⫾ 11.6 in the VATS group compared with 48.3 ⫾ 12.8
in the lateral thoracotomy group (P ⬍0.05). Swanson and
colleagues16 confirmed the sensitivity and specificity of tho-
racoscopic resection of solitary pulmonary nodules ap-
proaches 100% in their report on a prospective series of 65
patients.
Jiménez17 and fellow members of the Spanish Video-As-
sisted Thoracic Surgery Study Group reported on the pro-
spective study of 209 cases of VATS resection of pulmonary
nodules at 17 member hospitals between January 1996 and
January 1998. The mean age was 57 years (standard devia-
tion, 14.11; median, 60; range, 15-87 years). The majority of
the patients (79.4%) had a solitary nodule, with 93.8% of
nodules located in the periphery of the lung. The size of the
nodules ranged from 3 mm to 5 cm, with a mean of 1.9 cm
(standard deviation, 0.9; median, 2 cm). Localization of the
nodule was visual in 49% of cases, by palpation in 39.2%,
and by some form of preoperative localization in 4.8% (10
cases). Complications occurred in 17 patients (9.6%) includ-
ing 9 cases of prolonged air leak and 2 cases of infection.
Malignancy risk in the study was related to age ⬎60 years,
smoking history, size ⬎2 cm, central location, growth, and
history of previous malignancy.
Chang and colleagues18 reported on 62 ambulatory pa-
tients with indeterminate pulmonary nodules or interstitial
lung disease approached with thoracoscopic lung biopsy be-
tween June 2000 and June 2001. Forty-five patients (72.5%)
J.A. Howington
were discharged home within 8 hours of their operation.
Fourteen patients (22.5%) were discharged within 23 hours
of their operation. Only 3 patients (5%) required admission
for prolonged air leak2 or conversion to a thoracotomy.1 One
patient required readmission for a pneumothorax. There was
no operative mortality in the study group. Outpatient thora-
coscopic lung biopsy has become their procedure of choice
for diagnosis of interstitial or focal lung disease.
Cardillo and colleagues19 reported on the results of VATS
biopsy for a solitary pulmonary nodule in 429 patients
treated at a single institution from 1992 to 2001. No intra-
operative complications were detected, and there were no
perioperative deaths. Morbidity was low and included pro-
longed air leak (⬎5 days) in 13 patients (3%), 3 cases (0.6%)
of subcutaneous emphysema, and 2 cases (0.4%) of bloody
pleural effusion requiring thoracentesis to resolve. No wound
infections were reported. The mean chest tube duration was
3.5 days, and the mean hospital stay was 4.6 days. Ninety-
two percent of patients were able to return to work within 3
weeks after surgery. Multivariate analysis of the group re-
vealed age ⬎55 (odds ratio [OR] 4.9), diameter ⬎2 cm (OR
4.7), smoking history (OR 1.9), and history of previous can-
cer (OR 17.7) to be statistically significant risk factors for
malignancy in a solitary pulmonary nodule. These studies
add to the body of evidence confirming VATS as a safe and
effective approach to the diagnosis of pulmonary nodules.
Based on this evidence, thoracoscopy is the preferred surgical
approach to diagnosis of solitary pulmonary nodules in most
thoracic surgery programs.
Thoracoscopy for
Small (<1 cm) Lung Nodules
Today, many patients have subcentimeter lung nodules iden-
tified on screening CT scans of the chest, chest CT scans
performed for cancer surveillance and as incidental findings
on CT pulmonary angiograms, and, most recently, CT coro-
nary angiography. Thoracic surgeons are often called on to
assist in the management of these indeterminate lung nod-
ules. These small lung nodules pose unique challenges be-
cause of their size. They are typically below the resolution for
accurate clinical staging with PET and, outside of specialized
centers, are not ready targets for transthoracic needle biopsy.
Bronchoscopy in these subcentimeter lung nodules has very
low yield.
Several centers have reported on the high success rate and
diagnostic yield of preoperative localization of small (⬍1 cm)
lung nodules with a variety of techniques.20-23 Burdine and
colleagues20 reported on the results of a prospective study of
a preoperative localization technique for small pulmonary
nodules in 17 patients with newly diagnosed malignancy6 or
a prior history of malignancy11 between March 2000 and
January 2001. Using CT scan localization, 105-␮Ci techne-
tium sulfur colloid was injected into the area of the small
nodule, and methylene blue was injected near the visceral
pleural surface. During VATS, a sterile gamma probe was
used to identify the area of radioactivity and plan place-
ment of staple lines with an endomechanical stapling in-
Role of VATS in patients with non-small cell lung cancer
strument. The mean nodule size was 9.2 ⫾ 3.6 mm, and the
mean depth was 9.4 ⫾ 5.2 mm. All lesions were successfully
resected on the first try. The nodules were distributed in 10
separate segments and all lobes. Fourteen of the 17 nodules
(82.4%) could not be seen or felt with standard VATS tech-
niques. Five of the 17 nodules (29.4%) were malignant in-
cluding metastatic disease in 4 patients and a new primary
lung cancer in 1 patient. The remaining 12 nodules revealed
benign diagnoses including 2 carcinoid tumors, 2 inflamma-
tory pseudotumors, 1 acid-fast bacillus infection, and an ad-
ditional 7 granulomas. The median length of stay was 2 days.
Only 1 patient had a complication (a delayed pneumotho-
rax), and there were no deaths. This study demonstrated that
excisional VATS biopsy of small pulmonary nodules could be
performed safely and reliably after localization with techne-
tium sulfur colloid.
Finley and associates21 reported on the use of a CT-guided
percutaneous microcoil nodule localization procedure in 18
patients. With CT guidance and a percutaneously placed
Chiba needle, 1 end of the microcoil was placed deep to the
lesion and the other end was placed at the pleural surface.
The pleural end of the microcoil and lung surface were
grasped together during VATS and elevated. Fluoroscopy
was used to visualize the deep end of the coil and to guide the
placement of the endomechanical staple lines. One patient
was excluded because the nodule was located too close to the
inferior pulmonary vein to allow safe wedge excision. All of
the remaining 17 patients had successful fluoroscopically
guided VATS resections of the lung nodules. The mean nod-
ule size was 11.6 mm (range, 6-18 mm), and the mean depth
was 29 mm (range, 10-54 mm). The mean fluoroscopy and
operative times for resection were 3.2 and 56 minutes, re-
spectively. The authors reported 1 case of symptomatic
pneumothorax requiring chest tube placement before oper-
ation and 1 dislodged coil. In the patients treated with VATS
excision only, there were no postoperative complications and
the hospital stay was 2.6 ⫾ 0.6 days.
Stiles and colleagues23 reported on their experience with a
technique of percutaneous transthoracic radiotracer localization
of small, indeterminate lung nodules before thoracoscopic
lung resection in an initial cohort of 46 patients. Under CT
guidance, 0.1 mL of technetium Tc 99m macro-aggregated
albumin was injected into or adjacent to the lung nodule.
They routinely performed an immediate postprocedure scin-
tigram to confirm an intraparenchymal location of the radio-
tracer. The median nodule size was 9.0 mm (range, 3-22
mm), and the median depth was 5 mm (range, 0-50 mm).
Three patients developed a pneumothorax after injection,
but no patient required a chest tube.
Localization of the radiotracer and thoracoscopic excision
of the nodule was possible in 44 of 46 patients (96%). The 2
failures were related to radiotracer spillage in the pleural
space. Both nodules were successfully located with digital
palpation after conversion to open thoracotomy. Forty-six
percent (21 of 46) of the resected nodules were malignant,
with primary lung cancer (71%) being the most common
diagnosis. The median length of stay was only 1 day for
patients who underwent the thoracoscopic localization and
215
excision only. One patient developed urinary retention, but
no other complications were reported.
A common theme in these articles has been the direct
correlation between the size of a lung nodule and the poten-
tial risk of malignancy. Ginsberg and colleagues24 reported
on the pathology results of pulmonary nodules resected with
a VATS approach at Memorial Sloan Kettering between Jan-
uary 1995 and July 1997. In this study, nodules larger than 1
cm were more likely to be malignant (P ⬍0.002). In patients
with known malignancy, nodules ⬍5 mm were more likely
benign, whereas nodules greater than 5 mm but smaller than
1 cm were more likely malignant (P ⬍0.001). Henschke and
colleagues25 have reported on the natural history of small
pulmonary nodules identified on baseline CT chest scans in
the ongoing Early Lung Cancer Action Program screening
trials. The frequency of cancer when the largest noncalcified
nodule was less than 5.0 mm in diameter on baseline screen-
ing was 0 of 378 cases. The frequency of cancer when the
largest noncalcified nodule was 5.0 mm to 9.0 mm in diam-
eter was 14 of 238 cases. Thus, detected solid, noncalcified
nodules smaller than 5.0 mm in diameter in patients who are
asymptomatic with no prior cancer history have a very low
risk for malignancy and require no immediate workup but
only annual repeat CT scans of the chest to determine
whether interim growth of the nodule has occurred. Re-
searchers in the Early Lung Cancer Action Program study26
noted nonsolid nodules 5.0 to 9.0 mm in diameter possess a
very low risk of malignancy and recommend repeat scanning
in 1 year in these cases as well.
Conclusion
VATS is an effective and versatile tool for the diagnosis and
staging of patients with lung cancer. VATS is complimentary
to other invasive staging approaches in patients with non-
small cell lung cancer and is the preferred approach to pleural
space and T-stage assessment. Small (less than 5 mm) pul-
monary nodules identified by CT scan have a low risk for
malignancy, do not require immediate testing or biopsy, and
can be safely followed with annual scans. Growth in a nodule
suggests malignancy, and many of these small nodules can be
safely and successfully approached by VATS with or without
preoperative localization techniques.
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