Copyright #ERS Journals Ltd 2002

Eur Respir J 2002; 19: 722–742 European Respiratory Journal

DOI: 10.1183/09031936.02.00280002 ISSN 0903-1936
Printed in UK – all rights reserved

SERIES 0CONTRIBUTIONS FROM THE EUROPEAN RESPIRATORY MONOGRAPH0

Edited by M. Decramer and A. Rossi
Number 7 in this Series

Diagnostic imaging of lung cancer

N. Hollings, P. Shaw

Diagnostic imaging of lung cancer. N. Hollings, P. Shaw. #ERS Journals Ltd Dept of Radiology, Cecil Fleming
2002. House, University College Hospital,
ABSTRACT: Carcinoma of the bronchus is the most common malignancy in the Grafton Way, London, UK.
Western world. It is also the leading cause of cancer-related death accounting for 32% Correspondence: P. Shaw, Dept of
of all cancer deaths in males and 25% in females [1]. In the USA it causes more deaths Radiology, 2nd Floor, Cecil Fleming
than cancers of the colon, breast and prostate combined [2]. Disappointingly, in a recent House, University College Hospital,
UK survey of improvements in cancer survival [3], carcinoma of the bronchus showed Grafton Way, London, WC1E 6AV,
the smallest percentage reduction in the number of deaths avoided between 1981–1990 UK.
(0.2%). This compares badly with breast (11% reduction) and melanoma (32%). The Fax: 44 2073882147
overall 5-yr survival for lung cancer diagnosed between 1986–1990 was only 5.3% E-mail: [email protected]
(against 66% for breast and 76% for melanoma). It is on this background that the
radiologist remains actively employed in the detection, diagnosis, staging and review of Keywords: Bronchial carcinoma, com-
puted tomography, diagnostic imaging,
this common malignancy. magnetic resonance imaging, positron
Eur Respir J 2002; 19: 722–742. emission tomography, staging

Received: September 11 2001

Accepted September 11 2001

Lung cancer, in theory, should lend itself to in the table is preliminary data from two ongoing
screening. The disease is very common and in its trials in the USA and Germany. These trials show
earliest stages ¡70% of cases can be cured by surgery that CT detects many more lung nodules than chest
[4]. Despite this, lung cancer has an overall prognosis radiography. However, only a small percentage of
so dismal that incidence exceeds prevalence [5]. The these nodules turn out to be lung cancer. In the Mayo
main risk factor, smoking, is easily identifiable and Clinic trial [7] for example, over one-half of all
noninvasive screening tests such as chest radiography patients had at least one nodule. The logistics of
and sputum cytology are widely available. differentiating benign from malignant nodules there-
Why is screening not performed? Three large fore becomes a very real issue and there have been
American screening programmes in the 1970s spon- concerns about the number of biopsies that may need
sored by the National Institute of Health [6–9] and to be performed. However, by assessment of patterns
another in Czechoslovakia in the 1980s [10] screened of calcification at both low-dose and high-resolution
high-risk populations using chest radiography and CT (HRCT) and repeat scanning after an interval,
sputum analysis. All showed increased detection of the Early Lung Cancer Action Project (ELCAP)
early-stage lung cancer, more resectable cancers and group had only one incidence of biopsy performed
improved 5-yr survival rates in the screened versus for a benign, noncalcified nodule [11]. In this study,
control groups. Critically, however, none showed a the cancer detection rate was 2.7% but it was
statistically significant reduction in overall mortality. v0.5% for the two other published studies (table 1).
In the last 5 yrs three nonrandomized trials incor- Although this seems low, it should be remembered
porating low-dose computed tomography (CT) have that breast-cancer screening has a detection rate of
reported prevalence screening data [11–13]. Their only 0.6–0.7% [14].
findings are summarized in (table 1). Also included The importance of rigorous study design cannot

Previous articles in this series: No. 1: Baldacci S, Omenaas E, Oryszcyn MP. Allergy markers in respiratory epidemiology. Eur Respir J 2001;
17: 773–790. No. 2: Antó JM, Vermeire P, Vestbo J, Sunyer J. Epidemiology of chronic obstructive pulmonary disease. Eur Respir J 2001; 17:
982–994. No. 3: Cuvelier A, Muir J-F. Noninvasive ventilation and obstructive lung diseases. Eur Respir J 2001; 17: 1271–1281. No. 4:
Wysocki M, Antonelli M. Noninvasive mechanical ventilation in acute hypoxaemic respiratory failure. Eur Respir J 2001; 18: 209–220. No. 5:
Østerlind K. Chemotherapy in small cell lung cancer. Eur Respir J 2001; 18: 1026–1043. No. 6: Jaakkola MS. Environmental tobacco smoke
and health in the elderly. Eur Respir J 2002; 19: 172–181.
 DIAGNOSTIC IMAGING OF LUNG CANCER 723

Table 1. – Data from low-dose computed tomography a solid mass which grows more rapidly (doubling time
screening trials v1 yr) [20].
Patients Nodules Lung cancer
n % incidence %
Bronchoalveolar carcinoma
#
National Cancer 1369 NA 15 (0.43) This is regarded as a subtype of adenocarcinoma
Centre Hospital and represents 2–10% of all primary lung cancers.
Japan [12]
Shinshu University 3967 220 (5.6) 19 (0.35)
There are three characteristic presentations: most
School of Medicine common is a single pulmonary nodule or mass in
Japan [13] 41%; in 36% there may be multicentric or diffuse
ELCAP USA [11] 1000 233 (23) 27 (2.7) disease; finally, in 22% there is a localized area of
Mayo Clinic USA 1520 782 (51) 15 (1) parenchymal consolidation [21]. Bubble-like areas
University of 919 NA 13 (1.4) of low attenuation within the mass (fig. 1) are a
Münster Germany characteristic finding on CT [22]. Hilar and medi-
Data are presented as n (%) unless otherwise stated. ELCAP:
astinal lymphadenopathy is uncommon [23]. Persis-
Early Lung Cancer Action Project; NA: not available. tent peripheral consolidation with associated nodules
#
: represents percentage figure from 3,457 computed tomo- in the same lobe or in other lobes should raise the
graphy examinations (in 1,369 patients). possibility of bronchoalveolar carcinoma [24].

be overemphasized when assessing the validity of Adenosquamous carcinoma

these large and expensive trials. Although survival
from the time of diagnosis of the disease is com- Adenosquamous carcinoma represents 2% of all
monly reported it is not an appropriate measure of a lung cancers [16]. This cell type is typically identified
diagnostic screening test and may be misleading as as a solitary, peripheral nodule. Over one-half are
it is subject to lead-time bias, length-time bias and 1–3 cm in size and cavitation is seen in 13%. Evidence
overdiagnosis bias. Change in mortality rather than of parenchymal scars or fibrosis in or next to the
survival is necessary to validate such screening tumour is seen in 50% [25].
methods [2]. Although low-dose CT can detect early
stage disease 6–10 times more frequently than chest
radiography [11, 15], there has not as yet been a Squamous cell carcinoma
similar fall in the prevalence of advanced disease [2].
This lack of so-called "stage shift" again questions the Squamous cell carcinoma represents 30% of all lung
ability of low-dose CT screening to decrease overall cancers [16]. These tumours are more often centrally
mortality. Cross-contamination between the screened located within the lung and may grow much larger
and control arms of the study is also a problem in than 4 cm in diameter [17]. Cavitation (fig. 2) is seen
these large trials, especially as the public at large in up to 82% [18]. They commonly cause segmental or
become more aware of health issues. Individuals in the lobar lung collapse due to their central location and
control-arm trials may worry that they are missing out relative frequency [26].
on optimal treatment and manoeuvre their way into
the screened population.
In an attempt to overcome these various difficulties, Small cell lung cancer
groups sponsored by the Medical Research Council
in the UK and the National Cancer Institute in the Small cell lung cancer (SCLC) represents 18% of all
USA are currently piloting prospective, randomized, lung cancers [16]. SCLC often present with bulky hila
controlled trials of 40,000 and 88,000 patients respec- and mediastinal lymph node masses (fig. 3) [27, 28].
tively using low-dose CT. The latter should have the A noncontiguous parenchymal mass can be identified
power to detect a 20% reduction in mortality [2]. in up to 41% at CT [28] that very rarely cavitates [18].
They form the malignant end of a spectrum of neuro-
endocrine lung carcinomas with typical carcinoid
tumours being at the more benign end [27]. A mass
Radiological characteristics by cell type in or adjacent to the hilum is characteristic of SCLC
and the tumour may well show mediastinal invasion
Adenocarcinoma [17].
Adenocarcinoma represents 31% of all lung cancers,
including bronchoalveolar carcinoma [16]. Adeno- Carcinoid tumour
carcinomas are typically peripherally located and
measure v4 cm in diameter [17]; only 4% show Carcinoid tumour represents 1% of all lung cancers
cavitation [18]. Hila or hila and mediastinal involve- [16]. Atypical carcinoid tumours tend to be larger
ment is seen in 51% of cases on chest radiography (typically w2.5 cm at CT) with typical carcinoid
[19] and a recent study describes two characteristic tumours being more often associated with endo-
appearances on CT: either a localized ground glass bronchial growth (fig. 4) and obstructive pneumonia
opacity which grows slowly (doubling time w1 yr) or [27]. Carcinoids tend to be centrally rather than
724 N. HOLLINGS, P. SHAW

a)

Fig. 2. – A 50-yr-old female with irregular cavitating squamous cell

carcinoma in the right upper lobe (arrows).
b)
is diagnosed histologically after exclusion of adeno-
carcinomatous or squamous differentiation [16]. It
may grow extremely rapidly [30] to a large size but
metastasizes early to the mediastinum and brain [31].
It should be noted that there seems to be a change
occurring in the prevalence of the described histologi-
cal subtypes. Two large recent trials have reported
prevalences for adenocarcinoma of 78% and 58%
whilst squamous cell carcinomas accounted for only
4% and 11% respectively [11, 13].

Imaging techniques
Chest radiography
Due to its widespread availability, including to
primary care physicians, the chest radiograph is often
the first imaging modality to suggest the diagnosis of
bronchogenic carcinoma. Lung cancer may present as
a straightforward spiculated mass but its presence
may also be inferred from other appearances such as
Fig. 1. – a) Diffuse alveolar shadowing in the right lower lobe of an unresolving pneumonia or lobar collapse (fig. 5).
a 58-yr-old male presenting as an unresolving pneumonia. b) Air In some situations, no further imaging will be nece-
bronchograms (black arrows) and low attenuation lucencies (open ssary when bulky contralateral mediastinal adenopathy
arrow) in apical "consolidation", later confirmed as broncho- is present or when an obvious bony lesion is identified.
alveolar carcinoma.
However, CT scanning of the chest is often needed
because of the lack of sensitivity of the chest radio-
peripherally located and calcification is seen in graphs in detecting mediastinal lymph node meta-
26–33% [29]. The 5-yr survival for typical carcinoids stases and chest wall and mediastinal invasion [32].
is 95% against 57–66% for atypical carcinoids [29].

Computed tomography
Large cell carcinoma
CT can identify specific features in lung nodules
Large cell carcinoma represents 9% of all lung that are diagnostic, e.g. arteriovenous fistulae, rounded
cancers [16]. Large or giant cell carcinoma is a poorly atelectasis, fungus balls, mucoid impaction and
differentiated nonsmall cell carcinoma (NSCLC) and infarcts. High-resolution scanning further refines this
 DIAGNOSTIC IMAGING OF LUNG CANCER 725

a) a)

b)

b)

Fig. 4. – a) Inspiratory film with asymmetrical vascularity. b)

Expiratory film confirming air trapping due to carcinoid tumour
in the left main bronchus.

data sets enables the technique of virtual broncho-

scopy. An interactive, simulated bronchoscopy can
Fig. 3. – a) A 55-yr-old dyspnoeic female. Chest radiograph
demonstrating widened mediastinum particularly on the right with
be performed with the added benefit of simultaneous
reduced vascularity of the right lung. b) Contrast enhanced information on adjacent mediastinal structures. This
computed tomography showing central mediastinal mass invading technique has far reaching potential both as a teaching
the right pulmonary artery. Small cell carcinoma was confirmed tool and as a means of evaluating patients9 thoracic
on percutaneous biopsy.
and bronchial anatomy prior to interventional proce-
dures and stent placement [38].
diagnostic process [33]. The ability of CT scanning The recent advent of multislice scanners has seen
to evaluate the entire thorax at the time of nodule advances in image resolution with a substantial reduc-
assessment is of further benefit. tion in both tube loading and scanning time as up
Spiral or helical CT is advantageous as small to four slices can be acquired simultaneously [39,
nodules are not missed between slices as may 40]. Both spiral and multislice machines suffer less
happen on older, nonspiral machines. It also increases from respiratory motion artefact due to their shorter
the detection rate of nodules v5 mm in diameter, scanning times.
especially when viewed in cine-format on a work- Spiral CT with a bolus injection of intravenous
station [34, 35]. The acquisition of continuous volume iodinated contrast medium affords "dynamic scan-
data sets permits three-dimensional image reconstruc- ning". A recent study of 84 patients with NSCLC
tion and multiplanar (i.e. nonaxial) reformatting found no difference in radiological stage when non-
(fig. 6). These techniques have been shown to improve contrast enhanced scans were compared with contrast
the detection of pleural invasion by tumour and enhanced scans in 80 patients (95%), recommend-
clarify the origin of peridiaphragmatic tumours ing that nonenhanced CT through the thorax and
respectively [36, 37]. Further manipulation of raw adrenals was sufficient for staging patients with newly
726 N. HOLLINGS, P. SHAW

Fig. 5. – Increased retrocardiac density due to left lower lobe

collapse with inferomedial displacement of the hilum. Fig. 7. – Necrotic mediastinal lymph nodes with irregular enhanc-
ing rims (arrows).

diagnosed NSCLC [41]. However, another study of Magnetic resonance imaging

50 patients comparing both techniques found an 11%
higher detection rate of enlarged mediastinal nodes Magnetic resonance imaging (MRI) is becoming
after contrast enhancement and recommended its more available but pressure on MRI scanning time is
routine administration (figs. 7 and 8) [42]. Many so intense that it is usually used for problem solving
centres perform hepatic and adrenal scans having and where administration of contrast media is contra-
given intravenous contrast. indicated. MRI can be more accurate than CT in
Slice thickness and interval should be ¡10 mm separating stage IIIa (resectable) from IIIb (generally
and extend from the lung apices to the adrenal glands unresectable) tumours in selected patients due to its
[16]. It is now common practice to perform 5-mm ability to detect invasion of major mediastinal struc-
slices through the hila and aortopulmonary regions to tures, i.e. T4 disease [43].
improve delineation of local lymph nodes and the The advantages MRI has over CT include: better
origins of the lobar bronchi. The field of view should soft tissue contrast, multiplanar imaging capability,
include the contiguous chest wall [16]. and therefore useful for superior sulcus tumours and

a) b) c)

Fig. 6. – a) Coronal reformat from multislice computed tomography (CT) demonstrating mediastinal lymph nodes (arrow) and a necrotic
tumour mass within the lung. b) Three-dimensional-reconstruction of a lung tumour with pleural tag (arrow) (images courtesy of
T. McArthur, Dept. of Radiology, University College Hospitals, London). c) Thin slice reconstruction in the axial plane from spiral CT data
permits the correct identification of an inhaled fish bone (arrow), in a different patient, presumed to be a tumour at bronchoscopy.
 DIAGNOSTIC IMAGING OF LUNG CANCER 727

a)

b)

Fig. 9. – Coronal magnetic resonance imaging showing an adeno-

carcinoma in a young male infiltrating the aortopulmonary
window. There is loss of the fat plane against the aorta (arrows)
and invasion of the main pulmonary artery (arrowhead).

[44]. MRI is also poorly tolerated by claustrophobic

patients and is contra-indicated in patients with
indwelling electromagnetic devices and some pro-
sthetic heart valves.
T1-weighted sequences are used for the visualiza-
tion of fat planes and improved spatial resolution.
T2-weighted sequences are useful for detection of
high-signal tumour infiltration. Gadolinium enhance-
ment can further enhance the diagnostic yield [48].

Fig. 8. – a) Mediastinal mass narrowing left lower lobe bronchus

and invading left atrium. b) Distal fluid-filled bronchi (arrows) are
seen in the collapsed lower lobe due to the proximal tumour.
Positron emission tomography

Positron emission tomography (PET) scanning is

evaluation of the aortopulmonary window (fig. 9), a new imaging modality whose role in the assess-
and cardiac gating which enables excellent delineation ment of lung cancer is still being determined. Its
of the heart and great vessels and removes cardiac advantage over other modalities lies in its sensitivity
pulsation artefact [44, 45]. in detecting malignancy and its ability to image the
MRI is also useful in the assessment of mediastinal entire body in one examination.
and chest wall invasion by virtue of its ability to PET is a physiological imaging technique that uses
determine fat-stripe invasion (fig. 10) and involvement radiopharmaceuticals produced by labelling metabolic
of the diaphragm and spinal canal. In addition, it markers such as amino acids or glucose with positron-
has been shown to aid in differentiating lymph nodes emitting radio nuclides such as fluorine-18. The radio-
from hila vessels due to the "flow void" phenomenon marker is then imaged by coincidence detection of two
[46, 47]. 511 KeV photons that are produced by annihilation
MRI has disadvantages compared to CT, being of the emitted positrons. The radiopharmaceutical,
18
slower and more expensive with poorer spatial resolu- F-2-deoxy-D-glucose (FDG) is ideally suited for
tion and providing limited lung parenchyma informa- tumour imaging. PET performed with this agent
tion. MRI can overestimate lymph node size because exploits the differences in glucose metabolism between
of respiratory movement, causing the blurring toge- normal and neoplastic cells, allowing accurate, non-
ther of discrete nodes into a larger, conglomerate mass invasive differentiation of benign versus malignant
728 N. HOLLINGS, P. SHAW

a)

b)

18
Fig. 11. – Avid uptake of F-2-deoxy-D-glucose in left apical
tumour (arrow).

88% and an accuracy of 94% in lesions of o10 mm

[53–58]. However, compared to CT, PET has poorer
spatial resolution, which precludes it from accurate
anatomical assessment of primary tumour status [59].
False-positive PET findings in the lung are seen in
tuberculous infection, histoplasmosis and rheumatoid
lung disease. False negatives are seen with carcinoid
tumours, bronchoalveolar carcinoma and lesions
v10 mm in size [58–61].
PET is more accurate than CT in the detection or
exclusion of mediastinal nodal metastases: sensitivities
Fig. 10. – T1-weighted images demonstrating superior ability of are 67–100% and 50–63% respectively whilst specifi-
magnetic resonance imaging in demonstrating loss of fat plane cities are 81–100% and 59–94% [62–65]. PET has been
(arrow) in a) axial and b) sagittal planes. shown to correctly increase or decrease nodal staging
as initially determined by CT in 21% of presurgical
abnormalities [49]. Uptake of FDG is known to be patients [66]. In a study of 50 patients where PET
proportional to tumour aggressiveness and growth and CT findings were reported jointly, the sensitivity
rates [50]. FDG uptake can be assessed visually on rose to 93%, specificity 97% and accuracy 96% in
PET images (fig. 11) by comparing the activity of the the detection of mediastinal nodal disease [63]. PET
lesion with the background or by semiquantitative has been shown to detect occult extrathoracic meta-
analysis using calculated standardized uptake ratios. stases in 11–14% of patients selected for curative
An uptake ratio of v2.5 is considered indicative of resection and alter management in up to 40% of cases
a benign lesion [51, 52]. [66–68].
PET scanning detects malignancy in focal pulmo- In a recent study of 100 patients comparing
nary opacities with a sensitivity of 96%, specificity of whole body PET with conventional imaging (thoracic
 DIAGNOSTIC IMAGING OF LUNG CANCER 729

CT, bone scintigraphy, and brain CT or MRI) in Benign nodules

staging bronchogenic carcinoma PET accurately
staged NSCLC in 83% of cases when compared with Chest radiography. A number of findings enable a
pathological stage [69]. The figure for conventional nodule to be classed as benign on the basis of chest
imaging was 65%. PET identified nine patients with radiographical findings. 1) Age v35 yrs, no history of
metastases that were missed on conventional imaging cigarette smoking and no history of extrathoracic
whilst 10% of patients suspected of having metastases malignancy [76]. 2) Comparison with old films and
conventionally, were shown not to have by PET. PET establishment of no growth over at least a 2-yr period
was more sensitive and specific than bone scintigraphy [32]. 3) If the nodule contains fat density or a
for the detection of bone metastases and had a 100% benign pattern of calcification such as central nidus-
positive predictive value for the presence of adrenal type, popcorn, laminated or diffuse (fig. 12) [33]. Note
deposits as against 43% for conventional imaging. The should be made that eccentric or stippled calcification
technique faired poorly in the detection of brain is seen in y10% of lung cancers [76]. An appropriate
metastases (60% sensitivity) prompting the authors to history such as fever or chest pain may promote the
recommend the continued use of conventional imag- likelihood of a benign process such as focal pneumonia
ing for routine staging of the brain. However, the or an infarct presenting as an SPN. A repeat radio-
negative predicative value of PET for N3 disease was graph should be performed at 2–6 weeks to assess
identical to that of mediastinoscopy (96%) prompting resolution [76].
the statement that patients with negative mediastinal
PET findings could go directly to surgical resection
of the primary lesion [69]. This approach has been Computed tomography scanning, densitometry and
supported by other authors [59, 68]. Positive PET enhancement. CT scanning can further refine the detec-
findings however warrant nodal biopsy, as guided tion of calcification and fat within nodules. A total
by the areas of increased FDG uptake, in order to 22–38% of noncalcified nodules on chest radiographs
exclude false positives. Causes include infection, appear calcified on CT [76]. Using CT densitometry,
inflammation, hyperplasia and sarcoidosis [59]. a "pixel map" of a nodule can be created with
The main disadvantage for PET is the lack of Hounsfield Unit (HU) values, w200 being indicative
availability and relatively high cost of each examina- of calcification [77, 78]. Only characteristic patterns
tion. However, decision analysis models indicate that of calcification such as central, diffuse, laminar or
combined use of CT and PET imaging for evaluating popcorn are indicative of benignity [33]. The presence
focal pulmonary lesions is the most cost-effective and of fat (-40–-120 HU) or calcification or a combination
useful strategy in determining patient management of the two has been shown to correctly identify 30 of
with a pretest likelihood of having a malignant nodule 47 patients (64%) with hamartomas on 2-mm section
of 0.12–0.69 [70]. CT in one series [79]. However, at least one-third of
PET is more accurate than conventional studies in hamartomas in this series contained neither fat nor
detecting recurrent lung cancer and appears to be sup- calcium leading to an indeterminate assessment.
erior in distinguishing persistent or recurrent tumour
from fibrotic scars [59, 71]. However, false-positive
studies do occur secondary to postirradiation inflam-
matory change and delaying the examination until 4
or 5 weeks postirradiation is recommended [72].
A recent study of 114 patients with solitary
pulmonary nodules, ¡6 cm in diameter, highlighted
the usefulness of single photon emission computed
tomography using the 99mTechnetium-labelled soma-
tostatin analogue, Depreotide [73]. The sensitivity
and specificity for this method in determining benign
from malignant nodules was 97% and 73% respec-
tively. These results are comparable with FDG-PET
imaging and can be performed using a standard
gamma camera.

The solitary pulmonary nodule

Only 20% of carcinomas are resectable at diagnosis

[74] and 50% of "coin lesions" on chest radiography
are malignant: 40% representing primary lung cancers
whilst the other 10% are solitary metastases [75].
However, 20–30% of all cancers present as a solitary
pulmonary nodule (SPN) of which 88% are resectable
with a 5-yr survival rate around 50% [74]. The early
identification and correct assessment of such nodules Fig. 12. – Diffusely calcified, well-defined nodule typical of a
is therefore of the utmost importance. hamartoma.
730 N. HOLLINGS, P. SHAW

Changes in attenuation after intravenous contrast and consolidation of lung beyond the tumour with
administration at CT can also be used to distinguish accompanying volume loss. Air bronchograms may be
benign from malignant parenchymal nodules. In a seen at CT [17].
recent study of 356 nodules (5–40 mm) containing Differentiating central tumours from distal collapse
neither fat nor calcification, enhancement of v15 HU can be difficult but is facilitated by bolus contrast
postcontrast administration was strongly predictive of administration followed by prompt CT scanning
benignity [80]. By retrospectively reducing the cut-off at the level of abnormality (fig. 14). The lung is
threshold to 10 HU it was possible to increase the appreciably enhanced whilst tumour enhancement is
technique9s sensitivity in excluding malignancy from minimal and delayed. The most marked difference
98 to 100%. between the two is seen from 40 s to 2 min after
contrast injection [86].
Differentiating central lung tumours from medi-
Malignant nodules astinal masses can also be problematic. In a study of
A nodule size w3 cm is associated with malignancy
in 93–99% of cases [81]. If the nodule is spiculated
(fig. 13) 88–94% will be malignant [82–84] although a)
11% of malignant nodules do have distinct margins
[74]. The presence of calcification in larger (w3 cm)
and spiculated nodules should not be viewed as
indicative of benignity.

Indeterminate nodules

Small size should not be used as a discriminator

for exclusion of malignancy. One in seven nodules
v1 cm in size have been shown to be malignant [81]
and in a recent study of nodules resected at video-
assisted thoracoscopic surgery, 31% of nodules v1 cm
in size in patients with no known malignancy were
malignant [85]. Cavitation and lobulation are not
helpful discriminators in favour of malignancy as
granulomas and hamartomas can both have these
appearances [74].

Central tumours
Distinct from the SPN, central lung cancers often b)
present radiographically as a hila mass or as collapse

Fig. 14. – a) Collapse of the left lung with mediastinal shift and
a right middle zone nodule (arrow). b) Perihilar low attenuation
adenocarcinoma (arrows) with distal enhancing collapsed lung in
Fig. 13. – Spiculated mass typical of a carcinoma. same patient.
 DIAGNOSTIC IMAGING OF LUNG CANCER 731

pneumonia. 1) The "S" sign of Golden, indicating

a fissure deviated around a central tumour mass
(fig. 15). 2) Pneumonia confined to one lobe (or more
if supplied by a common, obstructed bronchus)
especially if w35-yrs-old and accompanied by volume
loss or mucus filled bronchi with no air bronchograms
present [17]. In an analysis of 50 patients with
segmental or lobar atelectasis, 27 (54%) were caused
by an obstructing tumour, all of which were detected
at CT [88]. 3) Localized pneumonia that persists
for w2 weeks or recurs in the same lobe.
Hila enlargement is a common presenting feature in
patients with lung cancer [17]. In the Mayo Clinic
series, 38% of patients with lung cancer had a hila or
peri-hila mass [89]. More recently, 14 of 25 patients
(56%) with CT performed for an abnormal hilum were
found to have bronchogenic carcinoma [90]. The
presence of a tumour mass or enlarged lymph nodes
will give a dense hilum. Generally speaking the more
lobular the shape the more likely that adenopathy is
present [17].

Staging nonsmall cell lung cancer

Fig. 15. – Central mass with Golden "S" sign of proximal tumour
(arrows) and distal collapse. The revised international system for staging lung
cancer [4] incorporates the tumour, node, metastasis
(TNM) subset system (tables 2 and 3) and shows
90 central lung and mediastinal masses, the single improved survival rates with more accurate staging
most useful CT finding in distinguishing between the and appropriate selection of patients for defini-
two was the "mass-lung interface". Marginal spicula- tive surgical treatment by distinguishing the IIIa
tion, nodularity or irregularity between the mass from the IIIb group (table 4). Percentage survival at
and the surrounding lung almost always indicated 5 yrs by clinical stage for the more advanced stages
the mass had arisen in the lung. A smooth interface remains poor, emphasizing the importance of early
suggested that the mass was mediastinal in location. detection.
A notable exception was Hodgkin9s lymphoma which The overall UK 5-yr survival of only 5.3% serves to
may occasionally cross the pleura, invade the lung and underline the preponderance of advanced-stage disease
result in a poorly marginated mass, mimicking a lung at presentation [3]. Precise tumour (T) and nodal (N)
mass [87]. staging is imperative as it determines subsequent
The following features can be viewed as suspicious treatment, especially when considering neo-adjuvant
for an obstructing neoplasm when associated with a therapy for IIIa and IIIb disease. Only approximately

Table 2. – Tumour, node, metastasis (TNM) classification

Tumour
T1 A tumour ¡3 cm in greatest dimension, surrounded by lung or visceral pleura,
without bronchoscopic evidence of invasion more proximal than the lobar bronchus
T2 A tumour with any of the following features: w3 cm in greatest dimension; involvement
of the main bronchus, o2 cm distal to the carina; invasion of the visceral pleura;
atelectasis or obstructive pneumonia extending to the hilum but not involving the entire lung
T3 A tumour of any size directly invading any of: chest wall (including superior sulcus tumours),
diaphragm, mediastinal pleura or parietal pericardium; or tumour in a main bronchus
within 2 cm of the carina but not involving it; or atelectasis of the entire lung
T4 A tumour of any size invading any of: mediastinum, heart, great vessels, trachea, oesophagus,
vertebral body or carina; or tumour with a malignant pleural or pericardial effusion or with
satellite tumour nodules within the ipsilateral primary-tumour lobe of the lung
Nodes
N0 No regional lymph node metastases
N1 Metastases to ipsilateral peribronchial and/or hilar nodes and direct tumour extension into
intrapulmonary nodes
N2 Metastases to ipsilateral mediastinal and/or subcarinal nodes
N3 Metastases to contralateral mediastinal, contralateral hilar, scalene or supraclavicular nodes
Metastases
M0 No distant metastases
M1 Distant metastases present
732 N. HOLLINGS, P. SHAW

Table 3. – Staging classification

a)
Stage TNM classification

IA T1 N0 M0
IB T2 N0 M0
IIA T1 N1 M0
IIB T2 N1 M0
T3 N0 M0
IIIA T3 N1 M0
T1 N2 M0
T2 N2 M0
T3 N2 M0
IIIB T4 N0 M0
T4 N1 M0
T4 N2 M0
T1 N3 M0
T2 N3 M0
T3 N3 M0
T4 N3 M0
IV Any T Any N M1
TNM: tumour, node, metastasis.

Table 4. – Cumulative percentage survival at 5-yrs post-

treatment by clinical stage
Stage 5-yr survival %
b)
Ia 61
Ib 38
IIa 34
IIb 24
IIIa 13
IIIb 5
IV 1
Modified from [4].

one-half of the TNM stages derived from CT agree

with operative staging, with patients being both under
and over staged [91, 92]. However, quick access to
investigation, high histological confirmation rates
(at bronchoscopic/transthoracic biopsy or at thora-
cotomy), routine CT scanning and review of every
patient by a thoracic surgeon is known to sub-
stantially increase successful surgical resection [93].

Tumour status
The distinction between T3 and T4 tumours is
critical because it separates conventional surgical Fig. 16. – a) Rib erosion (large arrow) due to peripheral tumour
and nonsurgical management [17]. T4 tumours may (small arrows) suggesting at least T3 disease. b) Corresponding
computed tomography showing mass eroding rib and vertebral
be readily identified by virtue of their invasion of body (arrows) confirming T4 status and inoperability.
a vertebral body (fig. 16), obvious invasion of the
mediastinum or heart (fig. 17) or the presence of lung
parenchymal metastases. T3 tumours can however Contact with the mediastinum is not enough to
be more difficult to grade principally because of the diagnose mediastinal invasion [17]. In Glazer9s series
difficulties of distinguishing simple extension of the
of 80 CTs considered indeterminate for direct media-
tumour into the mediastinal pleura or pericardium
stinal invasion, 60% were resectable at thoracotomy
(T3) from actual invasion (T4).
with no evidence of mediastinal invasion, 22% did
invade the mediastinum but were still technically
Mediastinal invasion. Minimal invasion of mediastinal resectable and only 18% were nonresectable [95]. In
fat is considered resectable by many surgeons [94]. fact only one of the 37 masses was not resectable
 DIAGNOSTIC IMAGING OF LUNG CANCER 733

Fig. 18. – Frank chest wall invasion by large peripheral tumour.

Chest wall invasion. CT assessment of tumour chest

wall invasion is variable with quoted sensitivities
Fig. 17. – Large central mass (arrows) narrowing left main
bronchus and encasing left pulmonary artery, indicating T4 status. ranging from 38–87% and specificities from 40–90%
A pleural effusion is noted. [94]. Invasion of the chest wall by a mass results in a
T3 score. This does not mean the mass is irresectable
per se but en bloc resection of the mass and adjacent
provided that the pre-operative CT demonstrated at chest wall is necessary which carries an associated
least one of the following: 1) ¡3 cm contact of the increase in mortality and morbidity [99]. As well as
mass with the mediastinum; 2) v90u contact with the the technique of inducing artificial pneumothoraces
aorta; 3) fat visible between the mass and media- as described earlier, dynamic expiratory multisection
stinal structures. Importantly however, this informa- CT (viewed as a cine loop) has also been evaluated.
tion does not identify inoperable tumours (thus In a study of 15 patients, this was found to be 100%
avoiding unnecessary thoracotomy) because y50% accurate for chest wall and mediastinal fixation at
of the technically resectable tumours had w3 cm of pathological examination [100]. With conventional CT
mediastinal contact or loss of the clear fat plane. imaging, the only reliable criterion for establishing
Artificial pneumothoraces have been used to improve definite invasion is bony destruction with or without
detection of both mediastinal and chest wall inva- tumour mass extending between the ribs and into the
sion by examining whether or not the pleura peels chest wall (fig. 18) [94].
away from the relevant structure. Although one Ultrasound has been cited as an additional tech-
study demonstrated 100% accuracy for chest wall nique for chest wall assessment (fig. 19). In a series of
invasion, its accuracy for mediastinal involvement 120 patients with contiguity between the tumour and
was only 76% [96]. Another study was 100% sensitive the chest wall at CT, 19 patients were judged to have
for mediastinal and chest wall invasion but only invasive tumour on ultrasound with a sensitivity and
80% specific [97]. This again indicated that the tech- specificity of 100% and 98% respectively as compared
nique cannot be categorical about the presence of with operative findings [101].
unresectability. MRI is a useful technique in establishing chest wall
The Radiologic Diagnostic Oncology Group [98] invasion. It relies on the demonstration of infiltration
compared CT and MRI in 170 patients with NSCLC, or disruption of the normal extra pleural fat plane on
90% of whom went on to thoracotomy. There was no T1-weighted images or parietal pleural signal hyper-
significant difference between the sensitivity of the two intensity on T2 weighting. The diagnostic yield is
modalities (63% and 56% respectively) or the specifi- further improved by intravenous gadolinium contrast
city (84% and 80%) for distinguishing between T3–4 medium [48]. Sagittal and coronal MRI better display
and T1–2 tumours, except when receiver operating the anatomical relationships at the lung apex as
characteristic analysis was performed on the statistics. opposed to axial CT (fig. 20). In superior sulcus or
These showed that MRI is better than CT at Pancoast tumours detection of tumour invasion beyond
diagnosing mediastinal invasion. MRI is particularly the lung apex into the brachial plexus, subclavian
useful in determining invasion of the myocardium artery or vertebral body by MRI has been found to be
or tumour extension into the left atrium via the 94% accurate as opposed to 63% for CT [102, 103],
pulmonary veins [76]. although multislice CT with nonaxial reconstruction
734 N. HOLLINGS, P. SHAW

a)

b)

Fig. 20. – Coronal T1-weighted magnetic resonance imaging show-

ing subtle Pancoast tumour (open arrow) with extension into the
superior sulcus and erosion of the adjacent vertebral body
(arrow).

mediastinal lymph node metastases [104] but the

arrival of PET has begun to influence patient manage-
ment in the limited number of centres where it is
available.
The enthusiasm for the usefulness of CT in
assessing nodal status grew throughout the 1980s.
In 1984, LIBSHITZ and MCKENNA [105] demonstrated
CT sensitivity and specificity of 67% and 66%
respectively using a nodal size of 1 cm to distinguish
between benign nodes and those seeded with metas-
Fig. 19. – a) Computed tomography scan suggesting infiltration of tases. In 1988 STAPLES et al. [106] demonstrated 79%
pleural fat (arrows). b) Lack of movement relative to chest wall sensitivity and 65% specificity for CT using a 1-cm
(arrows) confirms invasion. long axis nodal cut-off measurement. A meta-analysis
in 1990 of 42 CT studies assessing mediastinal lymph
may improve this figure. Surface coils and thin node metastases from NSCLC described an overall
sections (5 mm) are advised for MRI of such tumours. sensitivity of 0.79, a specificity of 0.78 and an accuracy
of 0.79 [107]. However, in 1992 MCLOUD et al. [108]
Pleural invasion. Effusions in lung cancer patients using a nodal short axis measurement of 1 cm in
can be benign, especially with a postobstructive 143 patients, returned to less inspiring figures of
pneumonia or malignant due to pleural metastases, 64% sensitivity and 62% specificity, respectively. These
often characterized by pleural nodularity [94]. Such an studies [105, 106, 108] all examined patients with
effusion renders the tumour T4 and irresectable, presumed operable lung cancer in whom complete
though this should be confirmed by thoracocentesis nodal sampling was performed either at mediastino-
or pleural biopsy. scopy or thoracotomy. Both LIBSHITZ and MCKENNA
[105] and MCLOUD et al. [108] observed an increase
in false-positive nodes in patients with obstructive
Nodal status pneumonia. MCLOUD et al. [103] also found that 37%
of nodes, which were 2–3 cm in diameter, did not
The most important predictor of outcome in the contain metastases at thoracotomy. More recently in
majority of patients with lung cancer limited to the a study of hila and mediastinal nodes at CT compared
chest is the presence or absence of involved medi- to pathological examination, sensitivities and specifi-
astinal lymph nodes [17]. N3 nodal disease is not an cities for metastatic involvement were only 48%
option surgically whilst the management of N2 disease and 53% with an overall accuracy of 51% [92]. Despite
is debatable. Mediastinoscopy and CT are recognized these statistics, CT is still recommended as the
to be the most valuable techniques for evaluation of standard strategy for the investigation of lung cancer
 DIAGNOSTIC IMAGING OF LUNG CANCER 735

by the Canadian Lung Oncology Group [109] after Others suggest that a negative nodal CT scan does
the study of 685 patients, CT and mediastinoscopy in not require mediastinoscopy because even if micro-
all patients proving too expensive. They recommended metastases are present, these patients can expect to
that mediastinoscopy and biopsy be reserved for have better survival if treated surgically than those
nodes with a short axis diameter of w1 cm in size denied such treatment [76]. Also N2 disease not
(fig. 21). Further refinements of indications for apparent on CT has been shown to be resectable
mediastinoscopy have been recommended with its with up to 30% 5-yr survival [16, 94].
omission in patients with T1 lesions and negative Hila nodes (N1) can usually be resected from hila
nodes at CT, unless the cell type is adeno- or large vessels. Therefore, although pre-operative detection
cell carcinoma [104]. However, using a CT short axis of hila nodes is useful, it is not generally crucial in
diameter of 1 cm, SEELY et al. [110], whilst examining directing surgical treatment. Moreover, the presence
104 patients with T1 lesions found nodal metastases or absence of hila node metastases is an unreliable
at surgery in 21% of cases of which one-third were indicator of mediastinal nodal metastases (N2 disease)
squamous cell carcinoma. [111, 112].

a) c)

b)

Fig. 21. – Middle-aged-female with a) right hilar mass (arrow) and b) equivocal precarinal lymph node (arrow). c) Positron emission tomo-
graphy (PET) scan shows increased uptake in mediastinal nodes (arrows) and small peripheral nodule (open arrow). Biopsy of hilar mass
confirmed nonsmall cell lung cancer. (PET images courtesy of J. Bomanji, Institute of Nuclear Medicine, University College London).
736 N. HOLLINGS, P. SHAW

CT may help to serve as a road map to guide

fibreoptic bronchoscopy and biopsy and help identify
enlarged nodes that are beyond the reach of the
mediastinoscope [16]. It also alerts the surgeon to
the presence of anatomical anomalies. No significant
difference has been found between the ability of
CT and MRI to detect N2 or N3 mediastinal meta-
stases [98]. The combination of respiratory movement
artefact and poorer spatial resolution [47] inherent
with MRI can mean that small discrete nodes as seen
on CT can appear as a larger, indistinct, single nodal
mass on MRI, leading to the erroneous diagnosis of
nodal enlargement. MRI is also poor at detecting
nodal calcification and may thus misclassify enlarged
benign nodes as malignant [94].

Metastatic status

A meta-analysis of 25 studies evaluating clinical

examination and imaging findings (CT head, abdo-
men or bone scintigraphy), found the risk of meta-
stases detected by imaging to be v3% if clinical
examination is normal [113]. If clinical examination
is positive for metastatic disease then metastases will
be found by imaging in y50% of patients. SIDER
and HOREJS [114], found extrathoracic metastases
in 25% of patients with stage I disease at thoracic
CT, brain 11%, bone 8%, liver 6% and adrenals 6% Fig. 22. – Computed tomography scan of enhancing cerebral meta-
stasis with marked oedema and mass effect.
(some patients having more than one site of metastatic
spread). Clinically occult metastases were present
in only 4% of patients. GRANT et al. [115], found recently however, using a standardized clinical neuro-
distant metastases in patients with no CT evidence of logical examination as opposed to the KARNOFSKY
mediastinal disease spread in three of 114 patients et al. [121] performance scale used in previous studies,
(2.5%). Another meta-analysis of 16 studies found COLICE et al. [122] found that routine CT of the brain
that 113 of 2,426 potentially operable patients (4.7%) was not indicated with a normal clinical examination.
became inoperable as a consequence of findings at Knowledge of the primary tumour cell type may be
CT scanning of the head and abdomen, ultrasound of helpful in reaching a decision. A recent meta-analysis
the abdomen or scintigraphy of the bone and liver [113] has found that adenocarcinoma and SCLC are
[116]. statistically more likely to metastasize to the brain
than squamous cell carcinoma. Finally, in a study
Liver imaging. QUINT et al. [117], found distant using contrast enhanced MRI in patients suspected
metastases in 21% of all NSCLC patients. Relative of having surgically resectable NSCLC, localized to
frequencies were brain 10%, bone 7%, liver 5% and the lung or lung and regional nodes, occult brain
adrenals 3%. Isolated liver metastases were uncommon metastases were identified in 17% of patients with
whilst metastases isolated to the brain were more primary tumours w3 cm [123].
common leading to the recommendation that CT
scanning of the abdomen was not an effective screening Adrenal imaging. In one meta-analysis study up to
method if chest CT is performed. 7% of patients with carcinoma of the bronchus had
Imaging of the liver by CT or ultrasound in the adrenal metastases [113]. However, up to 10% of the
absence of clinical signs, symptoms or laboratory general population have benign adrenal adenomas
abnormalities is controversial and generally not [32]. It has been recommended that CT of the adrenals
recommended [76]. However, if the adrenals are be performed as part of a staging CT of the chest [16].
routinely included on the CT chest scan, as is It involves a minimum amount of extra time, slices
common practice, then the liver is included by default. and dose to the patient, and is the most cost-effective
strategy for evaluating an adrenal mass in a patient
Brain imaging. Two studies have identified 21–64% with newly diagnosed NSCLC [124]. GILLAMS et al.
of brain metastases to be clinically occult prior to [125] found 4% of 546 patients with lung cancer had
CT scanning [118, 119]. KORMAS et al. [120], found solid adrenal tumours. Of these, 23% were proven
metastases in 3% of 158 pre-operative patients after to be due to malignant infiltration. Benign adenomas
negative clinical and laboratory examination. These tended to be v2 cm in size, of low attenuation, well
and other studies [115] recommend CT of the brain defined or to involve only part of the gland. Malignant
routinely in pre-operative patients (fig. 22). More glands tended to be w5 cm and of irregular or mixed
 DIAGNOSTIC IMAGING OF LUNG CANCER 737

Fig. 23. – Massive left adrenal (open arrow) and hepatic metastases
(arrows). M1 disease, stage IV.

attenuation (fig. 23). It was recommended that all

indeterminate glands i.e. 2–3 cm, undergo fine needle
aspiration (FNA) in patients being considered for
surgery. This approach is supported elsewhere [16, 32]
but it should be noted that MRI can provide addi-
tional information via chemical or phase shift-imaging
regarding the possibility of benignity in such adrenal Fig. 25. – Characteristic septal nodular thickening on high-resolution
masses [126, 127]. PET may also have a role to play scans typical of lymphangitis carcinomatosa.
and has been shown to have a sensitivity of 100%
and a specificity of 80% in the detection of metastatic Metastases may also be detected on staging thoracic
adrenal infiltration in a study of patients presenting CTs (fig. 24).
with bronchogenic carcinoma and an adrenal mass
[128].
Lymphangitis carcinomatosa. Malignant infiltration of
the lymphatics and perilymphatic connective tissue
Bone imaging. Most bony metastases are symptomatic is typically asymmetrical and nodular and must be
and bone scintigraphy offers a quick and inexpensive differentiated from left ventricular failure. It is best
survey of all the bones that is sensitive if not very demonstrated on HRCT scanning (fig. 25).
specific [129]. Alternatively, the presence of a patho-
logical fracture, raised serum alkaline phosphatase
and calcium or other nonspecific findings of metastatic Staging small cell lung cancer
disease should similarly prompt a bone scan [16].
SCLC is distinguished from NSCLC by its rapid
tumour doubling time, development of early wide-
spread metastases and almost exclusive occurrence
in smokers [130]. It is divided into two stages: limited
disease, which is confined to the ipsilateral hemitho-
rax within a single, tolerable radiotherapy port and
extensive disease which covers all other disease
including distant metastases. Systemic therapy is
required for all patients with SCLC, even those
with limited disease. Mediastinal radiotherapy is not
always indicated in patients with extensive disease
making the distinction between the two stages
important. To avoid an exhaustive search for exten-
sive disease (e.g. chest, liver, adrenal and cranial CT,
bone scans, marrow aspirates etc.) an alternative
approach is to allow clinical symptoms to direct
imaging, terminating on the discovery of extensive
disease [130]. Given the fact that cranial CT in SCLC
is positive in y15% of patients at diagnosis, one-third
Fig. 24. – Vertebral body metastasis. of whom are asymptomatic and that early treatment
738 N. HOLLINGS, P. SHAW

of brain metastases yields a lower rate of chronic

neurological morbidity, it seems reasonable to begin a)
any extrathoracic staging with brain imaging [32, 130].

Image guided needle biopsy

Transthoracic needle biopsy of a primary lung

tumour is controversial when considering a solitary
nodule or mass. A negative biopsy needs repeating
and the patient will invariably proceed to surgery
unless a positive benign result is obtained. Biopsy is
useful in determining cell type in inoperable disease
to guide further therapy and is essential to confirm
the presence of distant metastatic disease.
Needle biopsy is usually performed under either
ultrasound or CT guidance. Ultrasound guided biopsy
is quick and allows the operator to guide the needle
under direct vision but can only be used with peri-
pheral tumours that abut the pleura or invade the
chest wall. It is then usually possible to obtain a tissue
core using an 18-gauge cutting needle although
FNA may be used. CT guided biopsy takes longer
and systemic analgesia and sedation may be necessary
to maintain patient compliance. b)
CT affords good visualization of all thoracic
structures and CT guided biopsy has an accuracy for
diagnosing malignancy of 80–95% [131, 132]. It is the
procedure of choice for sampling peripheral nodules
(v2 cm in diameter) as the yield for transbronchial
needle biopsy, in the absence of an endobronchial
lesion, falls from 92–95% to 50–80% [132]. FNA is the
preferred sampling method of parenchymal nodules
in order to reduce the incidence of complications
and is known to have a similar sensitivity in detect-
ing malignancy as core biopsy [131]. However, small
tissue fragments for histological evaluation can gen-
erally be obtained with 19–22 gauge needles in 40–75%
of patients [132]. Such evaluation is valuable because
it lends confidence to a cytological diagnosis of
cancer, to cell-type determination and to the reliability
of a negative result [131, 132]. When a cavitatory or
necrotic lesion is encountered, sampling of the wall
is recommended to obtain viable tumour material. A
single negative biopsy does not exclude malignancy
and should prompt a repeat biopsy.
When performing biopsies of mediastinal lesions
it is usually possible to use an 18-gauge cutting needle
after selecting a safe route. This is especially impor-
tant in the diagnosis of lymphomas. Cutting needles Fig. 26. – Versatility of transthoracic needle biopsy with needle tip
are also employed in the biopsy of presumed hepatic in a) mediastinal mass (note safe approach) and b) peripheral
and adrenal metastases although FNA of the latter solitary nodule.
may be necessary with smaller lesions (figs. 26 and
27).
suggests the first diagnosis, but its relative insensitivity
has led to CT scanning being currently evaluated in
Conclusion screening studies.
Currently there is little to choose between CT and
Lung cancer is a common disease that has a poor MRI in staging the disease although CT is more
prognosis. Survival is inversely proportional to the widely available and less expensive. PET imaging
stage, with early detection and diagnosis being the key offers heightened sensitivity for both detection of the
to achieving surgical cure. Cross-sectional imaging primary malignancy and disease spread, although it
is now the main radiological means of assessment. is not 100% accurate and is only available in a few
Chest radiography is still important, and frequently centres. CT scanners are becoming more sophisticated
 DIAGNOSTIC IMAGING OF LUNG CANCER 739

radiologic and cytologic screening in the Johns

a) Hopkins study. Amer Rev Respir Dis 1984; 130: 549–
554.
9. Melamed MR, Flehinger BJ, Zaman MB, Heelan RT,
Perchick WA, Martini N. Screening for early lung
cancer. Results of the Memorial Sloan-Kettering study
in New York. Chest 1984; 86: 44–53.
10. Kubik A, Parkin DM, Khlat M, Erban J, Polak J,
Adamec M. Lack of benefit from semi-annual screen-
ing for cancer of the lung: follow-up report of a
randomized controlled trial on a population of high-
risk males in Czechoslovakia. Int J Cancer 1990;
45: 26–33.
11. Henschke CI, McCauley DI, Yankelevitz DF, et al.
Early Lung Cancer Action Project: overall design and
findings from baseline screening. Lancet 1999; 354:
99–105.
12. Kaneko M, Eguchi K, Ohmatsu H, et al. Peripheral
lung cancer: screening and detection with low-dose
b) spiral CT versus radiography. Radiology 1996; 201:
798–802.
13. Sone S, Takashima S, Li F, et al. Mass screening for
lung cancer with mobile spiral computed tomography
scanner. Lancet 1998; 351: 1242–1245.
14. Wan H, Karesen R, Hervik A, Thoresen SO.
Mammography screening in Norway: results from
the first screening round in four counties and cost-
effectiveness of a modeled nationwide screening.
Cancer Causes Control 2001; 12: 39–45.
15. Sone S, Li F, Yang ZG, et al. Results of three-year
mass screening programme for lung cancer using
mobile low-dose spiral computed tomography scan-
ner. Br J Cancer 2001; 84: 25–32.
16. Pretreatment evaluation of non-small-cell lung cancer.
The American Thoracic Society and The European
Fig. 27. – a) Low attenuation adrenal mass (arrows) with normal Respiratory Society. Amer J Respir Crit Care Med
right adrenal (open arrow) which at biopsy, b) confirmed meta- 1997; 156: 320–332.
static deposits. 17. Armstrong P. Neoplasms of the lungs, airways and
pleura. In: Armstrong P, Wilson AG, Dee P, Hansell
DM, eds. Imaging of Diseases of the Chest. 3rd
in design and versatility and seem likely to remain the edition. London, Mosby (Harcourt), 2000; pp. 305–
principal imaging modality for this disease in the near 401.
future. 18. Chaudhuri MR. Primary pulmonary cavitating carci-
nomas. Thorax 1973; 28: 354–366.
19. Woodring JH, Stelling CB. Adenocarcinoma of the
References lung: a tumor with a changing pleomorphic character.
Am J Roentgenol 1983; 140: 657–664.
1. Landis SH, Murray T, Bolden S, Wingo PA. Cancer stati- 20. Aoki T, Nakata H, Watanabe H, et al. Evolution
stics. Ca: a Cancer Journal for Clinicians 1998; 48: 6–29. of peripheral lung adenocarcinomas: CT findings
2. Patz EF Jr, Goodman PC, Bepler G. Screening for correlated with histology and tumor doubling time.
lung cancer. N Engl J Med 2000; 343: 1627–1633. Am J Roentgenol 2000; 174: 763–768.
3. Richards MA, Stockton D, Babb P, Coleman MP. How 21. Bonomo L, Storto ML, Ciccotosto C, et al. Bronch-
many deaths have been avoided through improve- ioloalveolar carcinoma of the lung. Eur Radiol 1998;
ments in cancer survival? BMJ 2000; 320: 895–898. 8: 996–1001.
4. Mountain CF. Revisions in the International System 22. Zwirewich CV, Vedal S, Miller RR, Muller NL.
for Staging Lung Cancer. Chest 1997; 111: 1710–1717. Solitary pulmonary nodule: high-resolution CT and
5. Smith IE. Screening for lung cancer: time to think radiologic-pathologic correlation. Radiology 1991;
positive. Lancet 1999; 354: 86–87. 179: 469–476.
6. Tockman M. Survival and mortality from lung cancer 23. Clark LR, Stull MA, Twigg HL. Chest case of the
in a screening population: the Johns Hopkins study. day. Bronchoalveolar carcinoma of the lung. Am
Chest 1986; 89: 324S–326S. J Roentgenol 1990; 154: 1318–1319.
7. Fontana RS, Sanderson DR, Woolner LB, Taylor 24. Aquino SL, Chiles C, Halford P. Distinction of
WF, Miller WE, Muhm JR. Lung cancer screening: consolidative bronchioloalveolar carcinoma from
the Mayo program. J Occup Med 1986; 28: 746–750. pneumonia: do CT criteria work? Am J Roentgenol
8. Frost JK, Ball WC Jr, Levin ML, et al. Early lung 1998; 171: 359–363.
cancer detection: results of the initial (prevalence) 25. Kazerooni EA, Bhalla M, Shepard JA, McLoud TC.
740 N. HOLLINGS, P. SHAW

Adenosquamous carcinoma of the lung: radiologic resonance imaging of the thorax. Past, present, and
appearance. Am J Roentgenol 1994; 163: 301–306. future. Clin Chest Med 1999; 20: 775–803.
26. Byrd RB, Miller WE, Carr DT, Payne WS, Woolner 45. Batra P, Brown K, Steckel RJ, Collins JD, Ovenfors
LB. The roentgenographic appearance of squamous CO, Aberle D. MR imaging of the thorax: a
cell carcinoma of the bronchus. Mayo Clinic Proceed- comparison of axial, coronal, and sagittal imaging
ings 1968; 43: 327–332. planes. J Comp Assist Tomogr 1988; 12: 75–81.
27. Forster BB, Muller NL, Miller RR, Nelems B, Evans 46. Aitken K, Armstrong P. Clinical imaging for staging
KG. Neuroendocrine carcinomas of the lung: clinical, lung cancer. Imaging 1992; 4: 15–22.
radiologic, and pathologic correlation. Radiology 47. Webb WR, Jensen BG, Sollitto R, et al. Bronchogenic
1989; 170: 441–445. carcinoma: staging with MR compared with staging
28. Pearlberg JL, Sandler MA, Lewis JW Jr, Beute GH, with CT and surgery. Radiology 1985; 156: 117–124.
Alpern MB. Small-cell bronchogenic carcinoma: CT 48. Padovani B, Mouroux J, Seksik L, et al. Chest wall
evaluation. Am J Roentgenol 1988; 150: 265–268. invasion by bronchogenic carcinoma: evaluation with
29. Dahnert W. Chest Disorders. In: Dahnert W, ed. MR imaging. Radiology 1993; 187: 33–38.
Radiology Review Manual. 3rd edition. Baltimore, 49. Erasmus JJ, Patz EF Jr. Positron emission tomo-
Williams and Wilkins, 1996; pp. 346–346. graphy imaging in the thorax. Clin Chest Med 1999;
30. Fraser RG, Parre JAP. Diagnosis of diseases of the 20: 715–724.
chest. 4th edition. Philadelphia, W.B. Saunders, 1999; 50. Duhaylongsod FG, Lowe VJ, Patz EF Jr, Vaughn AL,
pp. 1142–1143. Coleman RE, Wolfe WG. Lung tumor growth corre-
31. Shin MS, Jackson LK, Shelton RW Jr, Greene RE. lates with glucose metabolism measured by fluoride-18
Giant cell carcinoma of the lung. Clinical and roentgen- fluorodeoxyglucose positron emission tomography.
ographic manifestations. Chest 1986; 89: 366–369. Annals of Thoracic Surgery 1995; 60: 1348–1352.
32. Hyer JD, Silvestri G. Diagnosis and staging of lung 51. Lowe VJ, Fletcher JW, Gobar L, et al. Prospective
cancer. Clin Chest Med 2000; 21: 95–106. investigation of positron emission tomography in lung
33. Webb WR. Radiologic evaluation of the solitary nodules. J Clin Oncol 1998; 16: 1075–1084.
pulmonary nodule. Am J Roentgenol 1990; 154: 701– 52. Lowe VJ, Duhaylongsod FG, Patz EF, et al. Pulmo-
708. nary abnormalities and PET data analysis: a retro-
34. Remy-Jardin M, Remy J, Giraud F, Marquette CH. spective study. Radiology 1997; 202: 435–439.
Pulmonary nodules: detection with thick-section spiral 53. Conti PS, Lilien DL, Hawley K, Keppler J, Grafton
CT versus conventional CT. Radiology 1993; 187: 513– ST, Bading JR. PET and [18F]-FDG in oncology: a
520. clinical update. Nucl Med Biol 1996; 23: 717–735.
35. Tillich M, Kammerhuber F, Reittner P, Riepl T, 54. Gupta NC, Frank AR, Dewan NA, et al. Solitary
pulmonary nodules: detection of malignancy with PET
Stoeffler G, Szolar DH. Detection of pulmonary
with 2-[F-18]-fluoro-2-deoxy-D-glucose. Radiology
nodules with helical CT: comparison of cine and
1992; 184: 441–444.
film-based viewing. Am J Roentgenol 1997; 169: 1611–
55. Gupta NC, Maloof J, Gunel E. Probability of malign-
1614.
ancy in solitary pulmonary nodules using fluorine-18-
36. Brink JA, Heiken JP, Semenkovich J, Teefey SA,
FDG and PET. J Nucl Med 1996; 37: 943–948.
McClennan BL, Sagel SS. Abnormalities of the
56. Hubner KF, Buonocore E, Gould HR, et al. Differ-
diaphragm and adjacent structures: findings on multi- entiating benign from malignant lung lesions using
planar spiral CT scans. Am J Roentgenol 1994; "quantitative" parameters of FDG PET images. Clin
163: 307–310. Nucl Med 1996; 21: 941–949.
37. Kuriyama K, Tateishi R, Kumatani T, et al. Pleural 57. Patz EF Jr, Lowe VJ, Hoffman JM, et al. Focal
invasion by peripheral bronchogenic carcinoma: assess- pulmonary abnormalities: evaluation with F-18 fluor-
ment with three-dimensional helical CT. Radiology odeoxyglucose PET scanning. Radiology 1993; 188:
1994; 191: 365–369. 487–490.
38. Aquino SL, Vining DJ. Virtual bronchoscopy. Clin 58. Scott WJ, Schwabe JL, Gupta NC, Dewan NA,
Chest Med 1999; 20: 725–730. Reeb SD, Sugimoto JT. Positron emission tomo-
39. Ohnesorge B, Flohr T, Schaller S, et al. The technical graphy of lung tumors and mediastinal lymph nodes
bases and uses of multi-slice CT. Radiologe 1999; using [18F]fluorodeoxyglucose. The Members of the
39: 923–931. PET-Lung Tumor Study Group. Annals of Thoracic
40. McCollough CH, Zink FE. Performance evaluation Surgery 1994; 58: 698–703.
of a multi-slice CT system. Med Phys 1999; 26: 2223– 59. Erasmus JJ, McAdams HP, Patz EF Jr. Non-small cell
2230. lung cancer: FDG-PET imaging. J Thorac Imaging
41. Patz EF Jr, Erasmus JJ, McAdams HP, et al. 1999; 14: 247–256.
Lung cancer staging and management: comparison 60. Erasmus JJ, McAdams HP, Patz EF Jr, Coleman
of contrast-enhanced and nonenhanced helical CT of RE, Ahuja V, Goodman PC. Evaluation of primary
the thorax. Radiology 1999; 212: 56–60. pulmonary carcinoid tumors using FDG PET. Am
42. Cascade PN, Gross BH, Kazerooni EA, et al. J Roentgenol 1998; 170: 1369–1373.
Variability in the detection of enlarged mediastinal 61. Jang HJ, Lee KS, Kwon OJ, Rhee CH, Shim YM,
lymph nodes in staging lung cancer: a comparison Han J. Bronchioloalveolar carcinoma: focal area of
of contrast-enhanced and unenhanced CT. Am ground-glass attenuation at thin-section CT as an
J Roentgenol 1998; 170: 927–931. early sign. Radiology 1996; 199: 485–488.
43. Gefter WB. Magnetic resonance imaging in the 62. Steinert HC, Hauser M, Allemann F, et al. Non-small
evaluation of lung cancer. Semin Roentgen 1990; cell lung cancer: nodal staging with FDG PET versus
25: 73–84. CT with correlative lymph node mapping and sampl-
44. Hatabu H, Stock KW, Sher S, et al. Magnetic ing. Radiology 1997; 202: 441–446.
 DIAGNOSTIC IMAGING OF LUNG CANCER 741

63. Vansteenkiste JF, Stroobants SG, De Leyn PR, et al. the pulmonary nodule: a cooperative study. Radiology
Mediastinal lymph node staging with FDG-PET scan 1986; 160: 319–327.
in patients with potentially operable non-small cell 82. Westcott JL. Percutaneous transthoracic needle
lung cancer: a prospective analysis of 50 cases. Leuven biopsy. Radiology 1988; 169: 593–601.
Lung Cancer Group. Chest 1997; 112: 1480–1486. 83. Huston J III, Muhm JR. Solitary pulmonary opacities:
64. Guhlmann A, Storck M, Kotzerke J, Moog F, plain tomography. Radiology 1987; 163: 481–485.
Sunder-Plassmann L, Reske SN. Lymph node staging 84. Zerhouni EA, Boukadoum M, Siddiky MA, et al.
in non-small cell lung cancer: evaluation by [18F]FDG A standard phantom for quantitative CT analysis of
positron emission tomography (PET). Thorax 1997; pulmonary nodules. Radiology 1983; 149: 767–773.
52: 438–441. 85. Ginsberg MS, Griff SK, Go BD, Yoo HH, Schwartz
65. Dwamena BA, Sonnad SS, Angobaldo JO, Wahl RL. LH, Panicek DM. Pulmonary nodules resected at
Metastases from non-small cell lung cancer: medi- video-assisted thoracoscopic surgery: etiology in 426
astinal staging in the 1990s-meta-analytic comparison patients. Radiology 1999; 213: 277–282.
of PET and CT. Radiology 1999; 213: 530–536. 86. Onitsuka H, Tsukuda M, Araki A, Murakami J, Torii Y,
66. Valk PE, Pounds TR, Hopkins DM, et al. Staging Masuda K. Differentiation of central lung tumor from
non-small cell lung cancer by whole-body positron postobstructive lobar collapse by rapid sequence com-
emission tomographic imaging. Ann Thorac Surg puted tomography. J Thorac Imaging 1991; 6: 28–31.
1995; 60: 1573–1581. 87. Woodring JH, Johnson PJ. Computed tomography
67. Lewis P, Griffin S, Marsden P, et al. Whole-body distinction of central thoracic masses. J Thorac
18F-fluorodeoxyglucose positron emission tomo- Imaging 1991; 6: 32–39.
graphy in preoperative evaluation of lung cancer. 88. Woodring JH. Determining the cause of pulmonary
Lancet 1994; 344: 1265–1266. atelectasis: a comparison of plain radiography and
68. Weder W, Schmid RA, Bruchhaus H, Hillinger S, von CT. Am J Roentgenol 1988; 150: 757–763.
Schulthess GK, Steinert HC. Detection of extrathor- 89. Byrd RB, Carr DT, Miller WE, Payne WS, Woolner
acic metastases by positron emission tomography in LB. Radiographic abnormalities in carcinoma of the
lung cancer. Ann Thorac Surg 1998; 66: 886–892. lung as related to histological cell type. Thorax 1969;
69. Marom EM, McAdams HP, Erasmus JJ, et al. Staging 24: 573–575.
non-small cell lung cancer with whole-body PET. 90. Webb WR, Gamsu G, Glazer G. Computed tomo-
graphy of the abnormal pulmonary hilum. J Comput
Radiology 1999; 212: 803–809.
Assist Tomogr 1981; 5: 485–490.
70. Gambhir SS, Shepherd JE, Shah BD, et al. Analytical
91. Lewis JW Jr, Pearlberg JL, Beute GH, et al. Can
decision model for the cost-effective management
computed tomography of the chest stage lung cancer?
of solitary pulmonary nodules. J Clin Oncol 1998;
Yes and no. Ann Thorac Surg 1990; 49: 591–595.
16: 2113–2125.
92. Gdeedo A, Van Schil P, Corthouts B, Van Mieghem
71. Bury T, Corhay JL, Duysinx B, et al. Value of
F, Van Meerbeeck J, Van Marck E. Comparison
FDG-PET in detecting residual or recurrent nonsmall
of imaging TNM [(i)TNM] and pathological TNM
cell lung cancer. Eur Respir J 1999; 14: 1376–1380. [pTNM] in staging of bronchogenic carcinoma. Eur
72. Frank A, Lefkowitz D, Jaeger S, et al. Decision logic J Cardiothoracic Surg 1997; 12: 224–227.
for retreatment of asymptomatic lung cancer recur- 93. Laroche C, Wells F, Coulden R, et al. Improving
rence based on positron emission tomography find- surgical resection rate in lung cancer. Thorax 1998;
ings. Int J Radiat Oncol Bio Phys 1995; 32: 1495–1512. 53: 445–449.
73. Blum J, Handmaker H, Lister-James J, Rinne N. A 94. Quint LE, Francis IR. Radiologic staging of lung
multicenter trial with a somatostatin analog 99mTc cancer. J Thorac Imaging 1999; 14: 235–246.
Depreotide in the evaluation of solitary pulmonary 95. Glazer HS, Kaiser LR, Anderson DJ, et al. Indeter-
nodules. Chest 2000; 117: 1232–1238. minate mediastinal invasion in bronchogenic carci-
74. Viggiano RW, Swensen SJ, Rosenow EC III. Evalua- noma: CT evaluation. Radiology 1989; 173: 37–42.
tion and management of solitary and multiple pulmo- 96. Yokoi K, Mori K, Miyazawa N, Saito Y, Okuyama
nary nodules. Clin Chest Med 1992; 13: 83–95. A, Sasagawa M. Tumor invasion of the chest wall and
75. Webb WR. The solitary pulmonary nodule. In: mediastinum in lung cancer: evaluation with pneumo-
Freundlich IM, Bragg DG, eds. A radiologic thorax CT. Radiology 1991; 181: 147–152.
approach to diseases of the chest. Baltimore, Williams 97. Watanabe A, Shimokata K, Saka H, Nomura F,
and Williams, 1997; pp. 101–108. Sakai S. Chest CT combined with artificial pneumo-
76. McLoud TC, Swenson SJ. Lung carcinoma. Clin thorax: value in determining origin and extent of
Chest Med 1999; 20: 697–713. tumor. Am J Roentgenol 1991; 156: 707–710.
77. Im JG, Gamsu G, Gordon D, et al. CT densitometry 98. Webb WR, Gatsonis C, Zerhouni EA, et al. CT and
of pulmonary nodules in a frozen human thorax. Am MR imaging in staging non-small cell bronchogenic
J Roentgenol 1988; 150: 61–66. carcinoma: report of the Radiologic Diagnostic
78. Siegelman SS, Khouri NF, Scott WW Jr, et al. Oncology Group. Radiology 1991; 178: 705–713.
Pulmonary hamartoma: CT findings. Radiology 1986; 99. Piehler JM, Pairolero PC, Weiland LH, Offord KP,
160: 313–317. Payne WS, Bernatz PE. Bronchogenic carcinoma
79. Siegelman SS, Khouri NF, Leo FP, Fishman EK, with chest wall invasion: factors affecting survival
Braverman RM, Zerhouni EA. Solitary pulmonary following en bloc resection. Ann Thorac Surg 1982;
nodules: CT assessment. Radiology 1986; 160: 307–312. 34: 684–691.
80. Swensen SJ, Viggiano RW, Midthun DE, et al. Lung 100. Murata K, Takahashi M, Mori M, et al. Chest wall
nodule enhancement at CT: multicenter study. Radi- and mediastinal invasion by lung cancer: evaluation
ology 2000; 214: 73–80. with multisection expiratory dynamic CT. Radiology
81. Zerhouni EA, Stitik FP, Siegelman SS, et al. CT of 1994; 191: 251–255.
742 N. HOLLINGS, P. SHAW

101. Suzuki N, Saitoh T, Kitamura S. Tumor invasion of distant metastases from newly diagnosed non-small
of the chest wall in lung cancer: diagnosis with US. cell lung cancer. Ann Thorac Surg 1996; 62: 246–250.
Radiology 1993; 187: 39–42. 118. Ferrigno D, Buccheri G. Cranial computed tomo-
102. Heelan RT, Demas BE, Caravelli JF, et al. Superior graphy as a part of the initial staging procedures for
sulcus tumors: CT and MR imaging. Radiology 1989; patients with non-small-cell lung cancer. Chest 1994;
170: 637–641. 106: 1025–1029.
103. McLoud TC, Filion RB, Edelman RR, Shepard JA. 119. Salvatierra A, Baamonde C, Llamas JM, Cruz F,
MR imaging of superior sulcus carcinoma. J Comput Lopez-Pujol J. Extrathoracic staging of bronchogenic
Assist Tomogr 1989; 13: 233–239. carcinoma. Chest 1990; 97: 1052–1058.
104. Pearson FG. Staging of the mediastinum. Role of 120. Kormas P, Bradshaw JR, Jeyasingham K. Preopera-
mediastinoscopy and computed tomography. Chest tive computed tomography of the brain in non-small cell
1993; 103: 346S–348S. bronchogenic carcinoma. Thorax 1992; 47: 106–108.
105. Libshitz HI, McKenna RJ Jr. Mediastinal lymph node 121. Karnofsky DA, Burchenal JH. The clinical evaluation
size in lung cancer. Am J Roentgenol 1984; 143: 715– of chemotherapeutic agents in cancer. In: Macleod
718. CM, ed. Evaluation of Chemotherapeutic Agents.
106. Staples CA, Muller NL, Miller RR, Evans KG, New York, Columbia University Press, 1949; pp. 199–
Nelems B. Mediastinal nodes in bronchogenic carci- 205.
noma: comparison between CT and mediastinoscopy. 122. Colice GL, Birkmeyer JD, Black WC, Littenberg B,
Radiology 1988; 167: 367–372. Silvestri G. Cost-effectiveness of head CT in patients
107. Dales RE, Stark RM, Raman S. Computed tomo- with lung cancer without clinical evidence of metas-
graphy to stage lung cancer. Approaching a contro- tases. Chest 1995; 108: 1264–1271.
versy using meta-analysis. Amer Rev Respir Dis 1990; 123. Earnest F, Ryu JH, Miller GM, et al. Suspected non-
141: 1096–1101. small cell lung cancer: incidence of occult brain and
108. McLoud TC, Bourgouin PM, Greenberg RW, et al. skeletal metastases and effectiveness of imaging for
Bronchogenic carcinoma: analysis of staging in the detection-pilot study. Radiology 1999; 211: 37–145.
mediastinum with CT by correlative lymph node 124. Remer EM, Obuchowski N, Ellis JD, Rice TW,
mapping and sampling. Radiology 1992; 182: 319–323.
Adelstein DJ, Baker ME. Adrenal mass evaluation
109. Investigation for mediastinal disease in patients with
in patients with lung carcinoma: a cost-effectiveness
apparently operable lung cancer. Canadian Lung
analysis. Am J Roentgenol 2000; 174: 1033–1039.
Oncology Group. Annals of Thoracic Surgery 1995;
125. Gillams A, Roberts CM, Shaw P, Spiro SG, Goldstraw
60: 1382–1389.
P. The value of CT scanning and percutaneous fine
110. Seely JM, Mayo JR, Miller RR, Muller NL. T1 lung
needle aspiration of adrenal masses in biopsy-proven
cancer: prevalence of mediastinal nodal metastases
and diagnostic accuracy of CT. Radiology 1993; 186: lung cancer. Clin Radiol 1992; 46: 18–22.
129–132. 126. Korobkin M, Lombardi TJ, Aisen AM, et al. Char-
111. Kirsh MM, Kahn DR, Gago O, et al. Treatment of acterization of adrenal masses with chemical shift and
bronchogenic carcinoma with mediastinal metastases. gadolinium-enhanced MR imaging. Radiology 1995;
Annals of Thoracic Surgery 1971; 12: 11–21. 197: 411–418.
112. Martini N, Flehinger BJ, Zaman MB, Beattie EJ Jr. 127. Schwartz LH, Panicek DM, Koutcher JA, et al.
Results of resection in non-oat cell carcinoma of the Adrenal masses in patients with malignancy: prospec-
lung with mediastinal lymph node metastases. Annals tive comparison of echo-planar, fast spin-echo, and
of Surgery 1983; 198: 386–397. chemical shift MR imaging. Radiology 1995; 197: 421–
113. Silvestri GA, Littenberg B, Colice GL. The clinical 425.
evaluation for detecting metastatic lung cancer. A 128. Erasmus JJ, Patz EF Jr, McAdams HP, et al.
meta-analysis. Amer J Respir Crit Care Med 1995; Evaluation of adrenal masses in patients with bron-
152: 225–230. chogenic carcinoma using 18F-fluorodeoxyglucose
114. Sider L, Horejs D. Frequency of extrathoracic positron emission tomography. Am J Roentgenol
metastases from bronchogenic carcinoma in patients 1997; 168: 1357–1360.
with normal-sized hilar and mediastinal lymph nodes 129. Shaffer K. Radiologic evaluation in lung cancer:
on CT. Am J Roentgenol 1988; 151: 893–895. diagnosis and staging. Chest 1997; 112: 235S–238S.
115. Grant D, Edwards D, Goldstraw P. Computed 130. Elias AD. Small cell lung cancer: state-of-the-art
tomography of the brain, chest, and abdomen in the therapy in 1996. Chest 1997; 112: 251S–258S.
preoperative assessment of non-small cell lung cancer. 131. Klein JS, Salomon G, Stewart EA. Transthoracic
Thorax 1988; 43: 883–886. needle biopsy with a coaxially placed 20-gauge
116. Hillers TK, Sauve MD, Guyatt GH. Analysis of automated cutting needle: results in 122 patients.
published studies on the detection of extrathoracic Radiology 1996; 198: 715–720.
metastases in patients presumed to have operable 132. Salazar AM, Westcott JL. The role of transthoracic
non-small cell lung cancer. Thorax 1994; 49: 14–19. needle biopsy for the diagnosis and staging of lung
117. Quint LE, Tummala S, Brisson LJ, et al. Distribution cancer. Clin Chest Med 1993; 14: 99–110.