- Email: [email protected]
Bronchoscopy and surgical staging procedures and their correlation with imaging
European Journal of Radiology 45 (2003) 39 /48 www.elsevier.com/locate/ejrad
Bronchoscopy and surgical staging procedures and their correlation with imaging Z.C. Traill, F.V. Gleeson Radiology Department, Churchill Hospital, Old Road, Headington, Oxford OX3 7LJ, UK Received 17 September 2002; received in revised form 18 September 2002; accepted 19 September 2002
Abstract Bronchoscopy, computed tomography (CT) and surgical staging procedures are complimentary methods of investigating patients with lung cancer. CT has been shown to be of value prior to bronchoscopy in the investigation of haemoptysis and malignancy, with excellent correlation between the detection of disease within the large airways on CT and direct visualisation at bronchoscopy. The utility of CT has been further increased by the development of multislice scanners with the generation of volumetric data enabling multiplanar image acquisition. Additionally the advent of CT co-registered with positron emission tomography will play an important role in guiding the choice of surgical staging procedures The increasing use of multidisciplinary medical care requires radiologists to have a greater understanding of the abilities and limitations of both bronchoscopy and surgical staging procedures in evaluating disease demonstrated on imaging. # 2002 Published by Elsevier Science Ireland Ltd. Keywords: Lung cancer; Bronchoscopy; Staging; Surgery
1. Introduction The majority of bronchoscopies are performed in patients with suspected lung cancer; either with a suspicious clinical history such as haemoptysis, or radiographic abnormality such as lobar collapse or a pulmonary mass. Increasingly computed tomography (CT) is performed in this patient group prior to bronchoscopy, in an attempt to increase the diagnostic yield [1 /4]. Most patients presenting with lung cancer have advanced disease, stage IIIB or IV [4,5]. As such it is critically important to accurately stage the patient to allow correct treatment selection and avoid unnecessary thoracotomy. In the current climate of spiralling health care costs it is also important to enable a timely and cost-effective tissue diagnosis. CT, bronchoscopy and surgical staging procedures such as mediastinoscopy, and anterior mediastinotomy are mutually complimen Corresponding author. Tel.: /44-1865-225945; fax: /44-1865225946 E-mail address: [email protected] (F.V. Gleeson).
tary, allowing appropriate investigative and treatment decisions to be made with this in mind [6 /12]. It is imperative that when reporting staging CT scans in patients with either suspected or proven lung cancer that the radiologist is aware of the likelihood of bronchoscopy providing a tissue diagnosis; and correctly identifies local tumour operability, nodal disease and disease elsewhere when advising on the necessity for surgical staging procedures. More recently, positron emission tomography (PET) has been shown to play a key role in determining the need for surgical staging prior to attempted curative surgery [13 /22]. Magnetic resonance imaging (MRI) [23 /26] and ultrasound [27,28] both have limited but important roles in staging lung cancer. Patients with small cell lung cancer rarely present at a stage when surgery can be contemplated, but both bronchoscopy and surgical staging procedures may play an important role in diagnosis. This article reviews thoracic CT and its correlation with bronchoscopy and surgical staging predominantly in patients with lung cancer, and briefly describes the role of other imaging modalities and the techniques of the non-imaging procedures.
0720-048X/02/$ - see front matter # 2002 Published by Elsevier Science Ireland Ltd. PII: S 0 7 2 0 - 0 4 8 X ( 0 2 ) 0 0 2 9 8 - X
40
Z.C. Traill, F.V. Gleeson / European Journal of Radiology 45 (2003) 39 /48
2. Bronchoscopy Diagnostic bronchoscopy enables direct visualisation of the bronchial mucosa to the level of the segmental and proximal subsegmental bronchi [5]. At these levels direct visually guided biopsy is possible. Bronchoscopy also enables endobrochial brushing and lavage of disease beyond direct visualisation. Transbronchial needle aspiration biopsy may also be performed of adjacent non-visualised masses or lymphadenopathy identified on CT [5]. 2.1. Correlation with chest radiographs (CXR) Bronchoscopy is very likely to be diagnostic in patients with suspected malignancy and a CXR demonstrating a central localising abnormality [2,4,5,29 /32], including those producing lobar or lung collapse. It is less likely to be diagnostic in patients with a more peripheral abnormality [4,5]. In patients with haemoptysis, bronchoscopy is abnormal in the majority with an abnormal CXR [31,32]. However, even when bronchoscopy is abnormal a definitive diagnosis or localisation of the bleeding source may not be possible [31]. It appears of less value in patients with a normal or nonlocalising CXR and haemoptysis, and between 4 and 6% of patients investigated in these circumstances have a bronchogenic carcinoma on bronchoscopy [32 /35]. 2.2. Correlation with CT There have been numerous reports on the ability of CT to evaluate the airways in comparison to direct visualisation at bronchoscopy [1,2,4,36/44]. Studies were initially performed on conventional non-spiral CT scanners, with the later addition of thin sections to aid diagnosis [1,4,32,36/42]. More recently, the development of multislice CT scanners enabling volumetric scanning has generated increased interest in their potential to evaluate the airways [43 /47]: a review of all the applications in this regard are beyond the scope of this article, which will be limited to assessing the role of CT in patients with suspected malignancy and, or haemoptysis. In patients with lobar collapse the diagnostic value of bronchoscopy is sufficiently great, /80% sensitivity for malignancy, that bronchoscopy is the diagnostic procedure of choice, and the majority of chest physicians would perform bronchoscopy without prior imaging other than a CXR [3,5]. However, even in this patient group CT can demonstrate the cause of the collapse (Fig. 1) and may provide additional information, e.g. lymphadenopathy suitable for Transbronchial needle aspiration biopsy or metastatic disease elsewhere [3]. In patients without lobar collapse, initial reports using non-spiral CT demonstrated excellent sensitivities of /
Fig. 1. Endobronchial extension of tumour into the right main bronchus, in a patient with right upper lobe collapse.
80% in detecting bronchial abnormalities, but revealed an inability to determine whether a lesion was endobronchial, submucosal or peribronchial [1,4,36,37]. In addition CT failed to detect some patients with submucosal disease (Fig. 2) [37,41], and despite initial optimism on the use on data reconstruction to produce virtual bronchoscopy this continues to be a limitation using spiral CT [44] (Fig. 3). More recent reports suggest that the use of multiplanar reformatting and 3D volume rendering allowing visualisation of different tissue types enables greater correlation with bronchoscopy [47], although this remains largely unsubstantiated. Reformatted images are of value in the planning and followup of stent placement [47]. The presence of an endobronchial abnormality detected on CT has a high positive predictive value, 70/
Fig. 2. Large perihilar tumour adjacent to the left upper lobe bronchus. The tumour abuts lobar, segmental and subsegmental bronchi, and occludes the left apical basal segmental bronchus. No definite endobronchial disease is seen on CT within the left upper lobe but there was extensive mucosal disease at bronchoscopy.
Z.C. Traill, F.V. Gleeson / European Journal of Radiology 45 (2003) 39 /48
Fig. 3. (a) Conventional axial CT image demonstrating almost complete occlusion of the right main bronchus. (b) Virtual bronchoscopy reconstruction of the same CT data. Note the apparent smooth mucosa created by reconstruction.
90%, of abnormality at bronchoscopy (Fig. 4) and is significantly associated with a positive tissue diagnosis from bronchoscopy, P B/0.001 in one series [4]. CT may also be used to triage patients into those in whom bronchoscopy is likely to produce a tissue diagnosis and those in whom an alternative means of obtaining a diagnosis (ie percutaneous needle biopsy) should be performed [1 /4]. A segmental or larger airway leading to a mass seen on CT, proximity to the nearest lobar bronchus ( B/4 cm), and poorly defined margins have a high positive predictive value, 70/90%, of obtaining a tissue diagnosis at bronchoscopy (Fig. 5) [4]. In addition to detecting airway abnormalities, CT is able to confirm that extrinsic compression seen at bronchoscopy is due to lymphadenopathy or tumour and that transbronchial needle aspiration biopsy may be safely performed (Fig. 11) [1,4,6]. In reported series assessing CT in patients with haemoptysis, it has been shown to detect nearly all
41
Fig. 4. (a) Bronchial adenoma in left upper lobe bronchus in a patient with haemoptysis and a normal CXR; (b) endobronchial disease clearly seen in right main bronchus, confirmed at bronchoscopy.
malignancies, and enable diagnoses not made at bronchoscopy such as bronchiectasis to be made [36,41,42,48]. The proven ability of CT to evaluate the airways, and provide additional diagnostic information has led some authors to suggest that CT be performed as the initial investigation in patients with haemoptysis and a normal or non-localizing CXR, and in all patients prior to bronchoscopy for suspected malignancy [1 /4].
3. Surgical staging procedures The majority of surgical staging procedures in patients with lung cancer are performed to evaluate nodal disease [49 /51]. A minority of procedures are performed to evaluate chest wall or mediastinal invasion by tumour and less commonly to evaluate pulmonary nodules coincidentally identified on a staging CT scan
Z.C. Traill, F.V. Gleeson / European Journal of Radiology 45 (2003) 39 /48
42
Table 2 Stage grouping /TNM subsets Stage
TNM Subset
0
Carcinoma in situ
IA IB
T1N0M0 T2N0M0
IIA IIB
T1N1M0 T2N1M0 T3N0M0
IIIA
T3N1M0 T1N2M0 T2N2M0 T3N2M0
IIIB
T4N0M0 T4N1M0 T4N2M0 T1N3M0 T2N3M0 T3N3M0 T4N3M0
IV
Any T Any N M1
Fig. 5. Tumour within the superior segment of the lingula, demonstrating proximity to the hilum, and airway into the mass.
distant from the primary tumour [50] i.e. in a separate lobe from the primary tumour. The overall tumour staging should be as per the revised TNM subsets (T, primary tumour; N, regional lymph nodes; M, distant metastasis) from the International System for Staging Lung Cancer [52] (Tables 1 and 2).
Local tumour staging, T-staging, takes into consideration the size of the tumour, its proximity to the carina and its potential extension into adjacent structures, i.e. the mediastinum or chest wall. Patients with T3 disease
Table 1 TNM descriptors Primary tumour (T) TX Primary tumour cannot be assessed, or tumour proven by the presence of malignant cells in sputum or bronchial washings but not visualised by imaging or bronchoscopy TO No evidence of primary tumour Tis Carcinoma in situ T1 Tumour B 3 cm in greatest dimension, surrounded by lung or visceral pleura, without bronchoscopic evidence of invasion more proximal than the lobar bronchus (i.e. not in the main bronchus) T2 Tumour with any of the following features of size or extent: 3 cm in greatest dimension Involves main bronchus, 2 cm distal to the carina Invades the visceral pleura Associated with atelectasis or obstructive pneumonitis that extends to the hilar region but does not involve the entire lung T3 Tumour of any size that directly invades any of the following: chest wall (including superior sulcus tumours), diaphragm, mediastinal pleura, parietal pericardium; or tumour in the main bronchus B 2 cm distal to the carina, but without involvement of the carina: or associated atelectasis or obstructive pneumonitis of the entire lung T4 Tumour of any size that invades any of the following: mediastinum, heart, great vessels, trachea, oesophagus, vertebral body, carina; or tumour with a malignant pleural or pericardial effusion, or with satellite tumour nodule(s) within the ipsilateral primary-tumour lobe of the lung Regional lymph nodes (N) NX Regional lymph nodes cannot be assessed N0 No regional lymph node metastasis N1 Metastasis to ipsilateral peribronchial and/or ipsilateral hilar lymph nodes, and intrapulmonary nodes involved by direct extension of the primary tumour N2 Metastasis to ipsilateral mediastinal and/or subcarinal lymph node(s) N3 Metastasis to contralateral mediastinal, contralateral hilar, ipsilateral or contralateral scalene or supraclavicular lymph node(s) Distant metastasis (M) MX Presence of distant metastasis cannot be assessed M0 No distant metastasis M1 Distant metastasis presenta a
Separate metastatic tumour nodule(s) in the ipsilateral nonprimary-tumour lobe(s) of the lung are also classified M1.
Z.C. Traill, F.V. Gleeson / European Journal of Radiology 45 (2003) 39 /48
may be potentially operable provided there is no mediastinal nodal involvement or distant metastatic spread [53 /57]. Patients with T4 tumours are regarded for the most part as inoperable. Unfortunately imaging is not always accurate in distinguishing T3 from T4 tumours [58 /61]. Unless there is evidence of new phrenic nerve palsy, with elevation of the ipsilateral hemidiaphragm, the CXR is insensitive in the detection of mediastinal invasion. Both CT and MRI are also insensitive in the detection of mediastinal invasion [25,26]. Criteria used to determine mediastinal invasion include extensive contact between tumour and mediastinum, loss of adjacent fat planes, mass effect on adjacent mediastinal structures and pleural or pericardial thickening [60] (Figs. 6 and 7). The accuracy of both techniques is good when mediastinal disease is gross, but in cases of diagnostic doubt i.e. when there is tumour contiguity with mediastinal structures without obvious invasion either VATS or thoracotomy should be performed. Similarly chest wall invasion may be difficult to assess accurately [62,63]. Signs traditionally used to indicate chest wall invasion such as an obtuse angle between the tumour and the pleural surface, obliteration of the adjacent extrapleural fat plane (Fig. 8) and pleural thickening adjacent to the tumour are neither sensitive nor specific in identifying parietal pleural involvement [62,63]. Only a mass within the chest wall or rib destruction are reliable signs of chest wall involvement on CT. Attempts to increase diagnostic accuracy by using artificially induced pneumothorax have not proved popular [64]. Non-movement on dynamic (cine) CT only confirms fixity and not invasion [65,66]. Disruption of the pleura, extension through the chest
Fig. 6. Tumour within the left lower lobe, extending into the middle and posterior mediastinum, with extensive contact between the tumor and mediastinum, and loss of the adjacent fat planes. There are multiple calcified pleural plaques demonstrated bilaterally.
43
Fig. 7. (a) T1-weighted; and (b) T2-weighted sequences, demonstrating a mass within the left upper lobe and apical basal segment of the left lower lobe. The tumour abuts the mediastinal and posterior chest wall pleural surfaces. There is extensive contact and loss of adjacent fat planes, despite this the tumour had not invaded the mediastinum or chest wall at surgery.
Fig. 8. Right lower lobe tumour abutting the pleural surface, demonstrating an obtuse angle to the chest wall and obliteration of the extrapleural fat. There was no evidence of chest wall invasion at surgery.
44
Z.C. Traill, F.V. Gleeson / European Journal of Radiology 45 (2003) 39 /48
Fig. 9. Bronchogenic carcinoma on ultrasound; seen to disrupt the pleura (arrows show the nomal pleural stripe), extend into the chest wall and was fixed on dynamic scanning. The tumour was confirmed to have invaded the chest wall at surgery, but was successfully resected.
wall and fixity on respiration (Fig. 9) have been shown to be reliable indicators of chest wall invasion on US when two out of three of these signs are present [27]. Spiral CT and 3D reformatting also appears of little value [67]. Metastatic nodal disease in patients with lung cancer is classified as N1, N2, or N3 based on the position of the nodes in relation to the primary tumour. Nodal stations are identified and recorded as per Mountain and Dressler [68,69], (Table 3 and Figs. 12 and 13). N1 is local enlargement of intrapulmonary peribronchial and ipsilateral hilar nodes. N2 disease includes ipsilateral mediastinal and midline prevascular, retrotracheal, and subcarinal nodal enlargement. N3 disease is spread to contralateral mediastinal or hilar nodes, or to supraclavicular nodes (Fig. 10a/c). Most radiologists perform dynamic contrast enhanced CT to stage patients with lung cancer. However, it has been shown, that if carefully reported, nonenhanced CT reliably demonstrates mediastinal lymphadenopathy [70,71] (Fig. 11). Nodal enlargement on CT or MRI is commonly defined as enlargement greater than 1 cm in short axis-diameter [72 /74]. Both CT and MRI suffer from the same limitation in detecting mediastinal nodal involvement; that the main criterion used to diagnose nodal metastatic disease is size. Patients with mediastinal nodal enlargement who do not have a tissue diagnosis or who would be a surgical candidate should undergo nodal sampling via mediastinoscopy, mediastinotomy or transbronchial needle biopsy. PET has been shown to be extremely sensitive in the detection of mediastinal nodal metastases and is now often used to determine the need for nodal sampling and direct the surgeon to the appropriate nodal group [13 /22]. Recently US has been shown to be of value in detecting impalpable supraclavicular lymphadenopathy
Fig. 12. Frontal diagrammatic illustration of nodal stations according to Mountain and Dressler. Nodal stations 1, 2 and 4 can be sampled at mediastinoscopy, 7, 8 and 9 at VATS.
and directing biopsy of these nodes [28]. Fultz et al. [28] recommend including the lower neck on all lung cancer CT staging scans followed by US guided biopsy of enlarged supraclavicular nodes.
Fig. 13. Diagramatic illustration of nodal stations 5, 6 and 7. These cannot be reached by mediastinoscopy and require anterior mediastinotomy or VATS to be sampled.
Z.C. Traill, F.V. Gleeson / European Journal of Radiology 45 (2003) 39 /48
45
Table 3 Lymph node map definition Nodal station
Anatomic landmarks
N2 nodes */All N2 nodes lie within the mediastinal pleural envelope 1. Highest mediastinal nodes Nodes lying above a horizontal line at the upper rim of the bracheocephalic (left innominate) vein where it ascends to the left, crossing in front of the trachea at its midline 2. Upper paratracheal nodes Nodes lying above a horizontal line drawn tangential to the upper margin of the aortic arch and below the inferior boundary of No. 1 nodes 3. Prevascular and retrotracheal nodes Prevascular and retrotracheal nodes may be designated 3A and 3P; midline nodes are considered to be ipsilateral 4. Lower paratracheal nodes The lower paratracheal nodes on the right lie to the right of the midline of the trachea between a horizontal line drawn tangential to the upper margin of the aortic arch and a line extending across the right main bronchus at the upper margin of the upper lobe bronchus, and contained within the mediastinal pleural envelope; the lower paratracheal nodes on the left lie to the left of the midline of the trachea between a horizontal line drawn tangential to the upper margin of the aortic arch and a line extending across the left main bronchus at the level of the upper margin of the upper lobe bronchus, medial to the ligamentum arteriosum and contained within the mediastinal pleural envelope 5. Subaortic (aortopulmonary window) Subaortic nodes are lateral to the ligamentum arteriosum or the aorta or left pulmonary artery and proximal to the first branch of the left pulmonary artery and lie within the mediastinal pleural envelope 6. Para-aortic nodes (ascending aorta Nodes lying anterior and lateral to the ascending aorta and the aortic arch or the innominate artery, or phrenic) beneath a line tangential to the upper margin of the aortic arch 7. Subcarinal nodes Nodes lying caudal to the carina of the trachea, but not associated with the lower lobe bronchi or arteries within the lung 8. Paraoesophageal nodes (below car- Nodes lying adjacent to the wall of the oesophagus and to the right or left of the midline, excluding ina) subcarinal nodes 9. Pulmonary ligament nodes Nodes lying within the pulmonary ligament, including those in the posterior wall and lower part of the inferior pulmonary vein N1 */All nodes lie distal to the mediastinal pleural reflection and within the visceral pleura 10. Hilar nodes The proximal lobar nodes, distal to the mediastinal pleural reflection and the nodes adjacent to the bronchus intermedius on the right; radiographically, the hilar shadow may be created by the enlargement of both hilar and interlobar nodes 11. Interlobar nodes Nodes lying between the lobar bronchi 12. Lobar nodes Nodes adjacent to the distal lobar bronchi 13. Segmental nodes Nodes adjacent to the segmental bronchi 14. Subsegmental nodes Nodes around the subsegmental bronchi
3.1. Mediastinoscopy Mediastinoscopy was initially described by Carlens in 1959 [75], and is now routinely used to assess mediastinal nodal enlargement seen on CT staging for lung carcinoma. It is performed under general anaesthesia, with the patient positioned supine and the neck extended. A 2/3 cm transverse incision is made between the thyroid cartilage and the suprasternal notch. The trachea is then exposed by dividing the platysma, the strap muscles and the pretracheal fascia below the isthmus of the thyroid gland. A plane anterior to the trachea is then developed by blunt dissection and the mediastinoscope passed into this plane and manoeuvred inferiorly towards the carina [76 /78]. In this manner the high and low paratracheal nodes, nodes at stations; 1, 2 and 4 can be visualised and biopsied. Only the most proximal hilar lymph nodes and the most superior/
anterior of subcarinal lymphadenopathy, nodal station 7, can be visualised and biopsied [76,77]. 3.2. Anterior mediastinotomy Anterior mediastinotomy was originally reported by McNeill and Chamberlain in 1966 [78], although the technique has been subsequently modified to stage lung cancer [77,79]. It is performed under general anaesthetic. A 5 /7 cm transverse incision is made over the second costal cartilage on either side of the sternum. The internal mammary vessels are identified and avoided. From a right sided approach it is possible to assess and biopsy lymphadenopathy: in the anterior mediastinum, nodal station 6; the anterior aspect of the right hilum; and lymphadenopathy anterior and/or lateral to the superior vena cava and azygos vein. From a left sided approach it is possible to biopsy lymphadenopathy: in the anterior mediastinum, and the region of the aortic
46
Z.C. Traill, F.V. Gleeson / European Journal of Radiology 45 (2003) 39 /48
Fig. 11. Unenhanced CT demonstrating subcarinal lymphadenopathy.
arch, nodal station 6, and the aortopulmonary window (subaortic fossa), nodal station 5.
3.3. Video-assisted thoracic surgery (VATS)
Fig. 10. (a) Lymphadenopathy adjacent to the great vessels, nodal station 2, arrow; (b) lymphadenopathy in the right paratracheal region, nodal station 4, large arrow; with sub 1 cm nodes in nodal station 6 */ anterior to the superior vena cava and aortic arch, small arrows; (c) lymphadenopathy in the aortopulmonary window, nodal station 5, arrowed.
Thoracoscopy was first performed by Jacobaeus in 1910 using a modified cystoscope [80]. For a long time following this it was only performed by physicians to assess and biopsy the pleura. More recently the introduction of laparoscopic video-assisted procedures has resulted in its use in the chest and the term/technique VATS introduced [9 /11,50,51]. It is performed under general anaesthetic using a double lumen endotracheal tube and single lung inflation. A thoracoscope, videomonitor and camera are used. Usually access sites are positioned in the third and fifth intercostal space with the thoracoscope introduced through the fifth interspace. The para-aortic, aortopulmonary, inferior mediastinal and hilar lymph nodes are all accessible by VATS; nodal stations: 3 if right sided approach, 4, 5, 6 if left sided approach, 7, 8, 9 and 10. An additional benefit of VATS is its use in confirming or excluding mediastinal or chest wall invasion by adjacent tumour when there is doubt at CT or MRI [9 /11,50]. In addition VATS may be performed to biopsy small pulmonary nodules demonstrated on lung cancer staging CT scans [50,81,82]. In these cases accurate CT identification of the position of the nodule when reporting the scan is extremely important. On some occasions it may be necessary to help identify the nodule at surgery by placing a guidewire into or adjacent to the nodule, or injecting methylene blue dye adjacent to it under CT guidance [83].
Z.C. Traill, F.V. Gleeson / European Journal of Radiology 45 (2003) 39 /48
4. Conclusion For patients with suspected malignancy and/or haemoptysis, CT scanning is able to accurately detect the presence of an abnormality and if a bronchogenic carcinoma is detected is able to determine the likelihood of obtaining a tissue diagnosis at bronchoscopy. CT, MRI and US all play an important role in detecting chest wall and mediastinal invasion, but radiologists need to be aware of their limitations, in order not to deny patients potentially curative surgery. Knowledge of nodal stations in patients undergoing a staging CT scan for lung cancer enables appropriate advice to be given by radiologists in the choice of surgical staging procedures and also for potential transbronchial needle biopsy if lymphadenopathy is identified. Most recently PET scanning has been shown to be very sensitive in the detection of nodal mediastinal and extrathoracic metastases.
References [1] Naidich DP, Harkin TJ. Airways and lung: correlation of CT with fiberoptic bronchoscopy. Radiology 1995;197:1 /12. [2] Marshall TJ, Flower CDR, Jackson JE. The role of radiology in the investigation and management of patients with haemoptysis. Clin Radiol 1996;51:391 /400. [3] Laroche C, Fairburn I, Moss H, Pepke-Zaba J, Sharples L, Flower C, Coulden R. Role of computed tomographic scanning of the thorax prior to bronchoscopy in the investigation of suspected lung cancer. Thorax 2000;55:359 /63. [4] Bungay HK, Pal CR, Davies CWH, Davies RJO, Gleeson FV. An evaluation of computed tomography as an aid to diagnosis in patients undergoing bronchoscopy for suspected bronchial carcinoma. Clin Radiol 2000;55:554 /60. [5] Savage C, Morrison RJ, Zwischenberger JB. Bronchoscopic diagnosis and staging of lung cancer. Chest Surg Clin North Am 2001;11(4):701 /21. [6] Pearson FG. Staging of the mediastinum. Role of mediastinoscopy and computed tomography. Chest 1993;103(4):346S /8S. [7] The Canadian Lung Oncology Group. Investigation for mediastinal disease in patients with apparently operable lung cancer. Ann Thorac Surg 1995;60:1382 /9. [8] Shaffer K. Radiologic evaluation in lung cancer. diagnosis and staging. Chest 1997;112(4):S235 /8. [9] Lau CL, Harpole DH, Patz E. Staging techniques for lung cancer. Chest Surg Clin North Am 2000;10(4):781 /801. [10] Hyer JD, Silvestri G. Diagnosis and staging of lung cancer. Clin Chest Med 2000;21(1):95 /106. [11] Bogot NR, Shaham D. Semi-invasive and invasive procedures for the diagnosis and staging of lung cancer II. Bronchoscophic and Surgical Procedures. Lung Cancer 2000;38(3):535 /44. [12] Gurses A, Turna A, Bedirhan MA, et al. The value of mediastinoscopy in preoperative evaluation of mediastinal involvement in non-small cell lung cancer patients with clinical NO disease. Thorac Cardiov Surg 2002;50:174 /7. [13] Steinert HC, Hauser M, Allemann F, et al. Non-small cell lung cancer: nodal staging with FDG PET versus CT with correlative lymph node mapping and sampling. Radiology 1997;202:441 /6. [14] Coleman RE. PET in lung cancer. J Nucl Med 1999;40(5):814 /9.
47
[15] Farrell MA, McAdams HP, Herndon JE, Patz EF. Non-small cell lung cancer: FDG-PET for nodal staging in patients with stage I disease. Radiology 2000;215:886 /90. [16] Goldsmith SJ, Kostakoglu L. Nuclear medicine imaging of lung cancer. Radiol Clin North Am 2000;38(3):511 /23. [17] Pieterman RM, van Putten JWG, Meuzelaar JJ, et al. Preoperative staging of non-small cell lung cancer with 18-fluorodeoxyglucose positron emission tomography. N Engl J Med 2000;343:254 /61. [18] Laking G, Price P. 18-Fluorodeoxyglucose positron emission tomography (FDG-PET) and the staging of early lung cancer. Thorax 2001;56(Suppl. II):ii38 /44. [19] Coleman RE. PET in lung cancer staging. Q J Nucl Med 2001;45:231 /4. [20] Haberkorn U, Schoenberg SO. Imaging of lung cancer with CT, MRT and PET. Lung Cancer 2001;34:S13 /23. [21] van Tinteran H, Hoekstra OS, Smit EF, et al. Effectiveness of positron emission tomography in the preoperative assessment of patients with suspected non-small-cell lung cancer: the PLUS multicentre randomised trial. Lancet 2002;359:1361 /2. [22] Vansteenkiste JF. Imaging in lung cancer: positron emission tomography scan. Eur Respir J Suppl 2002;35:49s /60s. [23] Heelan RT, Demas BE, Caravelli JE, et al. Superior sulcus tumours: CT and MR imaging. Radiology 1989;170:637 /41. [24] Webb R, Gatsonis C, Zerhouni EA, et al. CT and MR imaging in staging non-small cell bronchoscopic carcinoma: report of the radiologic diagnostic oncology group. Radiology 1991;178:705 / 13. [25] Padovani B, Mouroux J, Seksik L, Chanalet S, et al. Chest wall invasion by bronchogenic carcinoma: evaluation with MR imaging. Radiology 1993;187:33 /8. [26] Bonomo L, Ciccotosto C, Guidotti A, Storto ML. Lung cancer staging: the role of computed tomography and magnetic resonance imaging. Eur J Radiol 1996;23:35 /45. [27] Suzuki N, Saitoh T, Kitamura S. Tumour invasion of the chest wall in lung cancer: diagnosis with US. Radiology 1993;187:39 / 42. [28] Fultz PJ, Feins RH, Strang JG, et al. Detection and diagnosis of nonpalpable supraclavicular lymph nodes in lung cancer at CT and US. Radiology 2002;222:245 /51. [29] Weaver LJ, Solliday N, Cugell DW. Selection of patients with hemoptysis for fiberoptic bronchoscopy. Chest 1979;76(1):7 /10. [30] Hirshberg B, Biran I, Glazer M, Kramer MR. Hemoptysis: etiology, evaluation, and outcome in tertiary referral hospital. Chest 1997;112:440 /4. [31] Gong H, Salvatierra C. Clinical efficacy of early and delayed fibreoptic bronchoscopy in patients with hemoptysis. Am Rev Respir Dis 1981;124:221 /5. [32] Naidich DP, Funt S, Ettenger NA, Arranda C. Hemoptysis: CTbronchoscopic correlations in 58 cases. Radiology 1990;177:357 / 62. [33] Jackson CV, Savage PJ, Quinn DL. Role of fiberoptic bronchoscopy in patients with hemoptysis and a normal chest roentgenogram. Chest 1985;87(2):142 /4. [34] Poe RH, Israel RH, Marin MG. Utility of fiberoptic bronchoscoy in patients with hemoptysis and a nonlocalizing chest roentgenogram. Chest 1988;92(1):70 /5. [35] Lederle FA, Nichol KL, Parenti CM. Bronchoscopy to evaluate hemoptysis in older men with nonsuspicious chest roentgenograms. Chest 1989;95(5):1043 /7. [36] Colice GL, Chappel GJ, Frenchman SM, Solomon DA. Comparisonof computerized tomography with fiberoptic bronchoscopy in identifying abnormalities in patients with known or suspected lung cancer. Am Rev Respir Dis 1985;131:397 /400. [37] Naidich DP, Lee J, Garay SM, McCauley DI, Aranda CP, Boyd AD. Comparison of CT and fiberoptic bronchoscopy in the evaluation of bronchial disease. Am J Roentgenol 1987;148:1 /7.
48
Z.C. Traill, F.V. Gleeson / European Journal of Radiology 45 (2003) 39 /48
[38] Henschke CI, Davis SD, Auh Y. Detection of bronchial abnormalities: comparison of CT and bronchoscopy. J Comp Assist Tomogr 1987;11(3):432 /5. [39] Naidich DP, Zinn WI, Ettenger NA, McCauley DI, Garay SM. Basilar segmental bronchi: thin-section CT evaluation. Radiology 1988;169:11 /6. [40] Mayr B, Ingrisch H, Haussinger K, Huber RM, Sunder-Plassmann L. Tumors of the bronchi: role of evaluation with CT. Radiology 1989;172:647 /52. [41] Set PAK, Flower CDR, Smith IE, Cahn AP, Twentyman OP, Shneerson JM. Hemoptysis: comparative study of the role of CT and fiberoptic bronchoscopy. Radiology 1993;189:677 /80. [42] McGuinness Georgeann, Beacher Jon R, Harkin Timothy J, et al. Hemoptysis: prospective high-resolution CT/bronchoscopic correlation. Chest 1994;105:1155 /62. [43] Kauczor HU, Wolcke B, Fischer B, et al. Three-dimensional helical CT of the tracheobronchial tree: evaluation of imaging protocols and assessment of suspected stenoses with bronchoscopic correlation. Am J Roentgenol 1996;167:419 /24. [44] Lee KS, Yoon JH, Kim TK, et al. Evaluation of tracheobronchial disease with helical CT with multiplanar and three-dimensional reconstruction: correlation with bronchoscopy. Radiographics 1997;17:555 /67. [45] Remy-Jardin M, Remy J, Artaud D, Friburg M, Duhamel A. Volume rendering of the tracheobronchial tree: clinical evaluation of bronchographic images. Radiology 1998;208:761 /70. [46] Haponik EF, Aquino SL, Vining DJ. Virtual bronchoscopy. Clin Chest Med 1999;20(1):201 /16. [47] Lawler LP, Fishman EK. Multi-detector row CT of thoracic disease with emphasis on 3D volume rendering and CT angiography. Radiographics 2001;21:1257 /73. [48] Millar AB, Boothroyd AE, Edwards D, Hetzel MR. The role of computed tomography (CT) in the investigation of unexplained haemoptysis. Respir Med 1992;86:39 /44. [49] Ginsberg RJ. Evaluation of the mediastinum by invasive techniques. Surg Clin North Am 1987;67(5):1025 /35. [50] Van Schil P. Role of Video-Assisted Thoracic Surgery (VATS) in staging, diagnosis and treatment of lung cancer. Acta Chir Belg 1998;98:103 /8. [51] Hoffman H. Invasive staging of lung cancer by mediastinoscopy and video-assisted thoracoscopy. Lung Cancer 2001;34:S3 /5. [52] Mountain CF. Revisions in the international system for staging lung cancer. Chest 1997;111:1710 /7. [53] McCaughan BC, Martini N, Bains M, McCormack PM. Chest wall invasion in carcinoma of the lung. Therapeutic and prognostic implications. J Thorac Cardiovasc Surg 1985;89:836 /41. [54] Allen MS, Mathisen DJ, Grillo HC, et al. Bronchogenic carcinoma with chest wall invasion. Ann Thorac Surg 1991;51:948 /51. [55] Van Raemdonck DE, Schneider A, Ginsberg RJ. Surgical treatment for higher stage non-small cell lung cancer. Ann Thorac Surg 1992;54:999 /1013. [56] Mountain CF. Surgery for stage IIIa-N2 non-small cell lung cancer. Cancer 1994;73:2589 /98. [57] Shah SS, Goldstraw P. Combined pulmonary and thoracic wall resection for stage III lung cancer. Thorax 1995;50:782 /4. [58] McLoud TM. CT of bronchogenic carcinoma: indeterminate mediastinal invasion. Radiology 1989;173:15 /6. [59] Glazer HS, Kaiser LR, Anderson DJ, et al. Indeterminate mediastinal invasion in bronchogenic carcinoma: CT evaluation. Radiology 1989;173:37 /43. [60] Herman SJ, Winton TL, Weisbrod GL, Towers MJ, Mentzer SJ. Mediastinal invasion by bronchoscopic carcinoma: CT signs. Radiology 1994;190:841 /6. [61] White PG, Adams H, Crane MD, Buchart EG. Preoperative staging of carcinoma of the bronchus: can computed tomographic
[62]
[63]
[64]
[65]
[66]
[67]
[68] [69]
[70]
[71]
[72]
[73]
[74]
[75] [76]
[77] [78] [79] [80] [81]
[82]
[83]
scanning reliably identify stage III tumour? Thorax 1994;49:951 / 7. Pennes DR, Glazer GM, Wimbish KJ, Gross BH, Long RW, Orringer MB. Chest wall invasion by lung cancer: limitations of CT evaluation. Am J Roentgenol 1985;144:507 /11. Glazer HS, Duncan-Meyer J, Aronberg DJ, Moran JF, Levitt RG, Sagel SS. Pleural and chest wall invasion in bronchogenic carcinoma: CT evaluation. Radiology 1985;157:191 /4. Yokoi K, Mori K, Miyazawa N, et al. Tumour invasion of the chest wall and mediastinum in lung cancer: evaluation with pneumothorax CT. Radiology 1991;181:147 /52. Murata K, Takahashi M, Mori M, et al. Chest wall and mediastinum invasion by lung cancer: evaluation with multisection expiratory dynamic CT. Radiology 1994;191:251 /5. Shirakawa T, Fukuda K, Miyamoto Y, et al. Parietal pleural invasion of lung masses: evaluation with CT performed during deep inspiration and expiration. Radiology 1994;192:809 /11. Kuriyama K, Tateishi R, Kumatani T. Pleural invasion by peripheral bronchogenic carcinoma: assessment with three-dimensional helical CT. Radiology 1994;191:365 /9. Mountain CF, Carolyn Dresler M. Regional lymph node classification for lung cancer staging. Chest 1997;111:1718 /23. Ko JP, Drucker EA, Shepard JO, Mountain CF, et al. CT depiction of regional nodal stations for lung cancer staging. Am J Roentgenol 2000;174:775 /82. Cascade P, Gross B, Kazerooni E, et al. Variability in the detection of enlarged mediastinal lymph nodes in staging lung cancer: a comparison of contrast-enhanced and unenhanced CT. Am J Roentgenol 1998;170:927 /31. Patz EJ, Erasmus JJ, McAdams HP. Lung cancer staging and management: comparison of contrast-enhanced and non-enhanced helical CT of the thorax. Radiology 1999;212:56 /60. McLoud T, Bourgouin PM, Greenberg RW, et al. Bronchogenic carcinoma: analysis of staging in the mediastinum with CT by correlative lymph node mapping and sampling. Radiology 1992;182:319 /23. Poon P, Bronskill MJ, Henkelman RM, et al. Mediastinal lymph node metastases from bronchogenic carcinoma: detection with MR imaging and CT. Radiology 1987;162:651 /6. Boiselle PM. MR imaging of thoracic lymph nodes. A comparison of computed tomography and positron emission tomography. MRI Clin North Am 2000;8(1):33 /41. Carlens E. Mediastinoscopy: a method for inspection and tissue biopsy in the superior mediastinum. Dis Chest 1959;36:343 /7. Foster ED, Munro DD, Dobell ARC. Mediastinoscopy. A review of anatomical relationships and complications. Annals Thorac Surg 1972;13(3):273 /86. Goldstraw P. Mediastinal exploration by mediastinoscopy and mediastinotomy. Br J Dis Chest 1988;82:111 /20. McNeill TM, Chamberlain JM. Diagnostic anterior mediastinoscopy. Ann Thorac Surg 1966;2(4):532 /9. Evans DS, Hall JH, Harrison GK. Anterior mediastinoscopy. Thorax 1973;28:444 /7. Jacobeus HC. Possibility of the use of cystoscope for investigation of serous cavities. Munch Med Wochenschr 1910;57:2090 /2. Allen MS, Deschamps C, Lee RE, et al. Video-assisted thoracoscopic stapled wedge excision for indeterminate pulmonary nodules. J Thorac Cardiovasc Surg 1993;106(6):1048 /52. Ginsberg MS, Griff SK, Go BD, et al. Pulmonary nodules resected at video-assisted thoracoscopic surgery: etiology in 426 patients. Radiology 1999;213:277 /82. Choi BG, Kim HH, Kim B, et al. Pulmonary nodules: CT-guided contrast material localization for thoracoscopic resection. Radiology 1998;208:399 /401.
Bronchoscopy and surgical staging procedures and their correlation with imaging Z.C. Traill, F.V. Gleeson Radiology Department, Churchill Hospital, Old Road, Headington, Oxford OX3 7LJ, UK Received 17 September 2002; received in revised form 18 September 2002; accepted 19 September 2002
Abstract Bronchoscopy, computed tomography (CT) and surgical staging procedures are complimentary methods of investigating patients with lung cancer. CT has been shown to be of value prior to bronchoscopy in the investigation of haemoptysis and malignancy, with excellent correlation between the detection of disease within the large airways on CT and direct visualisation at bronchoscopy. The utility of CT has been further increased by the development of multislice scanners with the generation of volumetric data enabling multiplanar image acquisition. Additionally the advent of CT co-registered with positron emission tomography will play an important role in guiding the choice of surgical staging procedures The increasing use of multidisciplinary medical care requires radiologists to have a greater understanding of the abilities and limitations of both bronchoscopy and surgical staging procedures in evaluating disease demonstrated on imaging. # 2002 Published by Elsevier Science Ireland Ltd. Keywords: Lung cancer; Bronchoscopy; Staging; Surgery
1. Introduction The majority of bronchoscopies are performed in patients with suspected lung cancer; either with a suspicious clinical history such as haemoptysis, or radiographic abnormality such as lobar collapse or a pulmonary mass. Increasingly computed tomography (CT) is performed in this patient group prior to bronchoscopy, in an attempt to increase the diagnostic yield [1 /4]. Most patients presenting with lung cancer have advanced disease, stage IIIB or IV [4,5]. As such it is critically important to accurately stage the patient to allow correct treatment selection and avoid unnecessary thoracotomy. In the current climate of spiralling health care costs it is also important to enable a timely and cost-effective tissue diagnosis. CT, bronchoscopy and surgical staging procedures such as mediastinoscopy, and anterior mediastinotomy are mutually complimen Corresponding author. Tel.: /44-1865-225945; fax: /44-1865225946 E-mail address: [email protected] (F.V. Gleeson).
tary, allowing appropriate investigative and treatment decisions to be made with this in mind [6 /12]. It is imperative that when reporting staging CT scans in patients with either suspected or proven lung cancer that the radiologist is aware of the likelihood of bronchoscopy providing a tissue diagnosis; and correctly identifies local tumour operability, nodal disease and disease elsewhere when advising on the necessity for surgical staging procedures. More recently, positron emission tomography (PET) has been shown to play a key role in determining the need for surgical staging prior to attempted curative surgery [13 /22]. Magnetic resonance imaging (MRI) [23 /26] and ultrasound [27,28] both have limited but important roles in staging lung cancer. Patients with small cell lung cancer rarely present at a stage when surgery can be contemplated, but both bronchoscopy and surgical staging procedures may play an important role in diagnosis. This article reviews thoracic CT and its correlation with bronchoscopy and surgical staging predominantly in patients with lung cancer, and briefly describes the role of other imaging modalities and the techniques of the non-imaging procedures.
0720-048X/02/$ - see front matter # 2002 Published by Elsevier Science Ireland Ltd. PII: S 0 7 2 0 - 0 4 8 X ( 0 2 ) 0 0 2 9 8 - X
40
Z.C. Traill, F.V. Gleeson / European Journal of Radiology 45 (2003) 39 /48
2. Bronchoscopy Diagnostic bronchoscopy enables direct visualisation of the bronchial mucosa to the level of the segmental and proximal subsegmental bronchi [5]. At these levels direct visually guided biopsy is possible. Bronchoscopy also enables endobrochial brushing and lavage of disease beyond direct visualisation. Transbronchial needle aspiration biopsy may also be performed of adjacent non-visualised masses or lymphadenopathy identified on CT [5]. 2.1. Correlation with chest radiographs (CXR) Bronchoscopy is very likely to be diagnostic in patients with suspected malignancy and a CXR demonstrating a central localising abnormality [2,4,5,29 /32], including those producing lobar or lung collapse. It is less likely to be diagnostic in patients with a more peripheral abnormality [4,5]. In patients with haemoptysis, bronchoscopy is abnormal in the majority with an abnormal CXR [31,32]. However, even when bronchoscopy is abnormal a definitive diagnosis or localisation of the bleeding source may not be possible [31]. It appears of less value in patients with a normal or nonlocalising CXR and haemoptysis, and between 4 and 6% of patients investigated in these circumstances have a bronchogenic carcinoma on bronchoscopy [32 /35]. 2.2. Correlation with CT There have been numerous reports on the ability of CT to evaluate the airways in comparison to direct visualisation at bronchoscopy [1,2,4,36/44]. Studies were initially performed on conventional non-spiral CT scanners, with the later addition of thin sections to aid diagnosis [1,4,32,36/42]. More recently, the development of multislice CT scanners enabling volumetric scanning has generated increased interest in their potential to evaluate the airways [43 /47]: a review of all the applications in this regard are beyond the scope of this article, which will be limited to assessing the role of CT in patients with suspected malignancy and, or haemoptysis. In patients with lobar collapse the diagnostic value of bronchoscopy is sufficiently great, /80% sensitivity for malignancy, that bronchoscopy is the diagnostic procedure of choice, and the majority of chest physicians would perform bronchoscopy without prior imaging other than a CXR [3,5]. However, even in this patient group CT can demonstrate the cause of the collapse (Fig. 1) and may provide additional information, e.g. lymphadenopathy suitable for Transbronchial needle aspiration biopsy or metastatic disease elsewhere [3]. In patients without lobar collapse, initial reports using non-spiral CT demonstrated excellent sensitivities of /
Fig. 1. Endobronchial extension of tumour into the right main bronchus, in a patient with right upper lobe collapse.
80% in detecting bronchial abnormalities, but revealed an inability to determine whether a lesion was endobronchial, submucosal or peribronchial [1,4,36,37]. In addition CT failed to detect some patients with submucosal disease (Fig. 2) [37,41], and despite initial optimism on the use on data reconstruction to produce virtual bronchoscopy this continues to be a limitation using spiral CT [44] (Fig. 3). More recent reports suggest that the use of multiplanar reformatting and 3D volume rendering allowing visualisation of different tissue types enables greater correlation with bronchoscopy [47], although this remains largely unsubstantiated. Reformatted images are of value in the planning and followup of stent placement [47]. The presence of an endobronchial abnormality detected on CT has a high positive predictive value, 70/
Fig. 2. Large perihilar tumour adjacent to the left upper lobe bronchus. The tumour abuts lobar, segmental and subsegmental bronchi, and occludes the left apical basal segmental bronchus. No definite endobronchial disease is seen on CT within the left upper lobe but there was extensive mucosal disease at bronchoscopy.
Z.C. Traill, F.V. Gleeson / European Journal of Radiology 45 (2003) 39 /48
Fig. 3. (a) Conventional axial CT image demonstrating almost complete occlusion of the right main bronchus. (b) Virtual bronchoscopy reconstruction of the same CT data. Note the apparent smooth mucosa created by reconstruction.
90%, of abnormality at bronchoscopy (Fig. 4) and is significantly associated with a positive tissue diagnosis from bronchoscopy, P B/0.001 in one series [4]. CT may also be used to triage patients into those in whom bronchoscopy is likely to produce a tissue diagnosis and those in whom an alternative means of obtaining a diagnosis (ie percutaneous needle biopsy) should be performed [1 /4]. A segmental or larger airway leading to a mass seen on CT, proximity to the nearest lobar bronchus ( B/4 cm), and poorly defined margins have a high positive predictive value, 70/90%, of obtaining a tissue diagnosis at bronchoscopy (Fig. 5) [4]. In addition to detecting airway abnormalities, CT is able to confirm that extrinsic compression seen at bronchoscopy is due to lymphadenopathy or tumour and that transbronchial needle aspiration biopsy may be safely performed (Fig. 11) [1,4,6]. In reported series assessing CT in patients with haemoptysis, it has been shown to detect nearly all
41
Fig. 4. (a) Bronchial adenoma in left upper lobe bronchus in a patient with haemoptysis and a normal CXR; (b) endobronchial disease clearly seen in right main bronchus, confirmed at bronchoscopy.
malignancies, and enable diagnoses not made at bronchoscopy such as bronchiectasis to be made [36,41,42,48]. The proven ability of CT to evaluate the airways, and provide additional diagnostic information has led some authors to suggest that CT be performed as the initial investigation in patients with haemoptysis and a normal or non-localizing CXR, and in all patients prior to bronchoscopy for suspected malignancy [1 /4].
3. Surgical staging procedures The majority of surgical staging procedures in patients with lung cancer are performed to evaluate nodal disease [49 /51]. A minority of procedures are performed to evaluate chest wall or mediastinal invasion by tumour and less commonly to evaluate pulmonary nodules coincidentally identified on a staging CT scan
Z.C. Traill, F.V. Gleeson / European Journal of Radiology 45 (2003) 39 /48
42
Table 2 Stage grouping /TNM subsets Stage
TNM Subset
0
Carcinoma in situ
IA IB
T1N0M0 T2N0M0
IIA IIB
T1N1M0 T2N1M0 T3N0M0
IIIA
T3N1M0 T1N2M0 T2N2M0 T3N2M0
IIIB
T4N0M0 T4N1M0 T4N2M0 T1N3M0 T2N3M0 T3N3M0 T4N3M0
IV
Any T Any N M1
Fig. 5. Tumour within the superior segment of the lingula, demonstrating proximity to the hilum, and airway into the mass.
distant from the primary tumour [50] i.e. in a separate lobe from the primary tumour. The overall tumour staging should be as per the revised TNM subsets (T, primary tumour; N, regional lymph nodes; M, distant metastasis) from the International System for Staging Lung Cancer [52] (Tables 1 and 2).
Local tumour staging, T-staging, takes into consideration the size of the tumour, its proximity to the carina and its potential extension into adjacent structures, i.e. the mediastinum or chest wall. Patients with T3 disease
Table 1 TNM descriptors Primary tumour (T) TX Primary tumour cannot be assessed, or tumour proven by the presence of malignant cells in sputum or bronchial washings but not visualised by imaging or bronchoscopy TO No evidence of primary tumour Tis Carcinoma in situ T1 Tumour B 3 cm in greatest dimension, surrounded by lung or visceral pleura, without bronchoscopic evidence of invasion more proximal than the lobar bronchus (i.e. not in the main bronchus) T2 Tumour with any of the following features of size or extent: 3 cm in greatest dimension Involves main bronchus, 2 cm distal to the carina Invades the visceral pleura Associated with atelectasis or obstructive pneumonitis that extends to the hilar region but does not involve the entire lung T3 Tumour of any size that directly invades any of the following: chest wall (including superior sulcus tumours), diaphragm, mediastinal pleura, parietal pericardium; or tumour in the main bronchus B 2 cm distal to the carina, but without involvement of the carina: or associated atelectasis or obstructive pneumonitis of the entire lung T4 Tumour of any size that invades any of the following: mediastinum, heart, great vessels, trachea, oesophagus, vertebral body, carina; or tumour with a malignant pleural or pericardial effusion, or with satellite tumour nodule(s) within the ipsilateral primary-tumour lobe of the lung Regional lymph nodes (N) NX Regional lymph nodes cannot be assessed N0 No regional lymph node metastasis N1 Metastasis to ipsilateral peribronchial and/or ipsilateral hilar lymph nodes, and intrapulmonary nodes involved by direct extension of the primary tumour N2 Metastasis to ipsilateral mediastinal and/or subcarinal lymph node(s) N3 Metastasis to contralateral mediastinal, contralateral hilar, ipsilateral or contralateral scalene or supraclavicular lymph node(s) Distant metastasis (M) MX Presence of distant metastasis cannot be assessed M0 No distant metastasis M1 Distant metastasis presenta a
Separate metastatic tumour nodule(s) in the ipsilateral nonprimary-tumour lobe(s) of the lung are also classified M1.
Z.C. Traill, F.V. Gleeson / European Journal of Radiology 45 (2003) 39 /48
may be potentially operable provided there is no mediastinal nodal involvement or distant metastatic spread [53 /57]. Patients with T4 tumours are regarded for the most part as inoperable. Unfortunately imaging is not always accurate in distinguishing T3 from T4 tumours [58 /61]. Unless there is evidence of new phrenic nerve palsy, with elevation of the ipsilateral hemidiaphragm, the CXR is insensitive in the detection of mediastinal invasion. Both CT and MRI are also insensitive in the detection of mediastinal invasion [25,26]. Criteria used to determine mediastinal invasion include extensive contact between tumour and mediastinum, loss of adjacent fat planes, mass effect on adjacent mediastinal structures and pleural or pericardial thickening [60] (Figs. 6 and 7). The accuracy of both techniques is good when mediastinal disease is gross, but in cases of diagnostic doubt i.e. when there is tumour contiguity with mediastinal structures without obvious invasion either VATS or thoracotomy should be performed. Similarly chest wall invasion may be difficult to assess accurately [62,63]. Signs traditionally used to indicate chest wall invasion such as an obtuse angle between the tumour and the pleural surface, obliteration of the adjacent extrapleural fat plane (Fig. 8) and pleural thickening adjacent to the tumour are neither sensitive nor specific in identifying parietal pleural involvement [62,63]. Only a mass within the chest wall or rib destruction are reliable signs of chest wall involvement on CT. Attempts to increase diagnostic accuracy by using artificially induced pneumothorax have not proved popular [64]. Non-movement on dynamic (cine) CT only confirms fixity and not invasion [65,66]. Disruption of the pleura, extension through the chest
Fig. 6. Tumour within the left lower lobe, extending into the middle and posterior mediastinum, with extensive contact between the tumor and mediastinum, and loss of the adjacent fat planes. There are multiple calcified pleural plaques demonstrated bilaterally.
43
Fig. 7. (a) T1-weighted; and (b) T2-weighted sequences, demonstrating a mass within the left upper lobe and apical basal segment of the left lower lobe. The tumour abuts the mediastinal and posterior chest wall pleural surfaces. There is extensive contact and loss of adjacent fat planes, despite this the tumour had not invaded the mediastinum or chest wall at surgery.
Fig. 8. Right lower lobe tumour abutting the pleural surface, demonstrating an obtuse angle to the chest wall and obliteration of the extrapleural fat. There was no evidence of chest wall invasion at surgery.
44
Z.C. Traill, F.V. Gleeson / European Journal of Radiology 45 (2003) 39 /48
Fig. 9. Bronchogenic carcinoma on ultrasound; seen to disrupt the pleura (arrows show the nomal pleural stripe), extend into the chest wall and was fixed on dynamic scanning. The tumour was confirmed to have invaded the chest wall at surgery, but was successfully resected.
wall and fixity on respiration (Fig. 9) have been shown to be reliable indicators of chest wall invasion on US when two out of three of these signs are present [27]. Spiral CT and 3D reformatting also appears of little value [67]. Metastatic nodal disease in patients with lung cancer is classified as N1, N2, or N3 based on the position of the nodes in relation to the primary tumour. Nodal stations are identified and recorded as per Mountain and Dressler [68,69], (Table 3 and Figs. 12 and 13). N1 is local enlargement of intrapulmonary peribronchial and ipsilateral hilar nodes. N2 disease includes ipsilateral mediastinal and midline prevascular, retrotracheal, and subcarinal nodal enlargement. N3 disease is spread to contralateral mediastinal or hilar nodes, or to supraclavicular nodes (Fig. 10a/c). Most radiologists perform dynamic contrast enhanced CT to stage patients with lung cancer. However, it has been shown, that if carefully reported, nonenhanced CT reliably demonstrates mediastinal lymphadenopathy [70,71] (Fig. 11). Nodal enlargement on CT or MRI is commonly defined as enlargement greater than 1 cm in short axis-diameter [72 /74]. Both CT and MRI suffer from the same limitation in detecting mediastinal nodal involvement; that the main criterion used to diagnose nodal metastatic disease is size. Patients with mediastinal nodal enlargement who do not have a tissue diagnosis or who would be a surgical candidate should undergo nodal sampling via mediastinoscopy, mediastinotomy or transbronchial needle biopsy. PET has been shown to be extremely sensitive in the detection of mediastinal nodal metastases and is now often used to determine the need for nodal sampling and direct the surgeon to the appropriate nodal group [13 /22]. Recently US has been shown to be of value in detecting impalpable supraclavicular lymphadenopathy
Fig. 12. Frontal diagrammatic illustration of nodal stations according to Mountain and Dressler. Nodal stations 1, 2 and 4 can be sampled at mediastinoscopy, 7, 8 and 9 at VATS.
and directing biopsy of these nodes [28]. Fultz et al. [28] recommend including the lower neck on all lung cancer CT staging scans followed by US guided biopsy of enlarged supraclavicular nodes.
Fig. 13. Diagramatic illustration of nodal stations 5, 6 and 7. These cannot be reached by mediastinoscopy and require anterior mediastinotomy or VATS to be sampled.
Z.C. Traill, F.V. Gleeson / European Journal of Radiology 45 (2003) 39 /48
45
Table 3 Lymph node map definition Nodal station
Anatomic landmarks
N2 nodes */All N2 nodes lie within the mediastinal pleural envelope 1. Highest mediastinal nodes Nodes lying above a horizontal line at the upper rim of the bracheocephalic (left innominate) vein where it ascends to the left, crossing in front of the trachea at its midline 2. Upper paratracheal nodes Nodes lying above a horizontal line drawn tangential to the upper margin of the aortic arch and below the inferior boundary of No. 1 nodes 3. Prevascular and retrotracheal nodes Prevascular and retrotracheal nodes may be designated 3A and 3P; midline nodes are considered to be ipsilateral 4. Lower paratracheal nodes The lower paratracheal nodes on the right lie to the right of the midline of the trachea between a horizontal line drawn tangential to the upper margin of the aortic arch and a line extending across the right main bronchus at the upper margin of the upper lobe bronchus, and contained within the mediastinal pleural envelope; the lower paratracheal nodes on the left lie to the left of the midline of the trachea between a horizontal line drawn tangential to the upper margin of the aortic arch and a line extending across the left main bronchus at the level of the upper margin of the upper lobe bronchus, medial to the ligamentum arteriosum and contained within the mediastinal pleural envelope 5. Subaortic (aortopulmonary window) Subaortic nodes are lateral to the ligamentum arteriosum or the aorta or left pulmonary artery and proximal to the first branch of the left pulmonary artery and lie within the mediastinal pleural envelope 6. Para-aortic nodes (ascending aorta Nodes lying anterior and lateral to the ascending aorta and the aortic arch or the innominate artery, or phrenic) beneath a line tangential to the upper margin of the aortic arch 7. Subcarinal nodes Nodes lying caudal to the carina of the trachea, but not associated with the lower lobe bronchi or arteries within the lung 8. Paraoesophageal nodes (below car- Nodes lying adjacent to the wall of the oesophagus and to the right or left of the midline, excluding ina) subcarinal nodes 9. Pulmonary ligament nodes Nodes lying within the pulmonary ligament, including those in the posterior wall and lower part of the inferior pulmonary vein N1 */All nodes lie distal to the mediastinal pleural reflection and within the visceral pleura 10. Hilar nodes The proximal lobar nodes, distal to the mediastinal pleural reflection and the nodes adjacent to the bronchus intermedius on the right; radiographically, the hilar shadow may be created by the enlargement of both hilar and interlobar nodes 11. Interlobar nodes Nodes lying between the lobar bronchi 12. Lobar nodes Nodes adjacent to the distal lobar bronchi 13. Segmental nodes Nodes adjacent to the segmental bronchi 14. Subsegmental nodes Nodes around the subsegmental bronchi
3.1. Mediastinoscopy Mediastinoscopy was initially described by Carlens in 1959 [75], and is now routinely used to assess mediastinal nodal enlargement seen on CT staging for lung carcinoma. It is performed under general anaesthesia, with the patient positioned supine and the neck extended. A 2/3 cm transverse incision is made between the thyroid cartilage and the suprasternal notch. The trachea is then exposed by dividing the platysma, the strap muscles and the pretracheal fascia below the isthmus of the thyroid gland. A plane anterior to the trachea is then developed by blunt dissection and the mediastinoscope passed into this plane and manoeuvred inferiorly towards the carina [76 /78]. In this manner the high and low paratracheal nodes, nodes at stations; 1, 2 and 4 can be visualised and biopsied. Only the most proximal hilar lymph nodes and the most superior/
anterior of subcarinal lymphadenopathy, nodal station 7, can be visualised and biopsied [76,77]. 3.2. Anterior mediastinotomy Anterior mediastinotomy was originally reported by McNeill and Chamberlain in 1966 [78], although the technique has been subsequently modified to stage lung cancer [77,79]. It is performed under general anaesthetic. A 5 /7 cm transverse incision is made over the second costal cartilage on either side of the sternum. The internal mammary vessels are identified and avoided. From a right sided approach it is possible to assess and biopsy lymphadenopathy: in the anterior mediastinum, nodal station 6; the anterior aspect of the right hilum; and lymphadenopathy anterior and/or lateral to the superior vena cava and azygos vein. From a left sided approach it is possible to biopsy lymphadenopathy: in the anterior mediastinum, and the region of the aortic
46
Z.C. Traill, F.V. Gleeson / European Journal of Radiology 45 (2003) 39 /48
Fig. 11. Unenhanced CT demonstrating subcarinal lymphadenopathy.
arch, nodal station 6, and the aortopulmonary window (subaortic fossa), nodal station 5.
3.3. Video-assisted thoracic surgery (VATS)
Fig. 10. (a) Lymphadenopathy adjacent to the great vessels, nodal station 2, arrow; (b) lymphadenopathy in the right paratracheal region, nodal station 4, large arrow; with sub 1 cm nodes in nodal station 6 */ anterior to the superior vena cava and aortic arch, small arrows; (c) lymphadenopathy in the aortopulmonary window, nodal station 5, arrowed.
Thoracoscopy was first performed by Jacobaeus in 1910 using a modified cystoscope [80]. For a long time following this it was only performed by physicians to assess and biopsy the pleura. More recently the introduction of laparoscopic video-assisted procedures has resulted in its use in the chest and the term/technique VATS introduced [9 /11,50,51]. It is performed under general anaesthetic using a double lumen endotracheal tube and single lung inflation. A thoracoscope, videomonitor and camera are used. Usually access sites are positioned in the third and fifth intercostal space with the thoracoscope introduced through the fifth interspace. The para-aortic, aortopulmonary, inferior mediastinal and hilar lymph nodes are all accessible by VATS; nodal stations: 3 if right sided approach, 4, 5, 6 if left sided approach, 7, 8, 9 and 10. An additional benefit of VATS is its use in confirming or excluding mediastinal or chest wall invasion by adjacent tumour when there is doubt at CT or MRI [9 /11,50]. In addition VATS may be performed to biopsy small pulmonary nodules demonstrated on lung cancer staging CT scans [50,81,82]. In these cases accurate CT identification of the position of the nodule when reporting the scan is extremely important. On some occasions it may be necessary to help identify the nodule at surgery by placing a guidewire into or adjacent to the nodule, or injecting methylene blue dye adjacent to it under CT guidance [83].
Z.C. Traill, F.V. Gleeson / European Journal of Radiology 45 (2003) 39 /48
4. Conclusion For patients with suspected malignancy and/or haemoptysis, CT scanning is able to accurately detect the presence of an abnormality and if a bronchogenic carcinoma is detected is able to determine the likelihood of obtaining a tissue diagnosis at bronchoscopy. CT, MRI and US all play an important role in detecting chest wall and mediastinal invasion, but radiologists need to be aware of their limitations, in order not to deny patients potentially curative surgery. Knowledge of nodal stations in patients undergoing a staging CT scan for lung cancer enables appropriate advice to be given by radiologists in the choice of surgical staging procedures and also for potential transbronchial needle biopsy if lymphadenopathy is identified. Most recently PET scanning has been shown to be very sensitive in the detection of nodal mediastinal and extrathoracic metastases.
References [1] Naidich DP, Harkin TJ. Airways and lung: correlation of CT with fiberoptic bronchoscopy. Radiology 1995;197:1 /12. [2] Marshall TJ, Flower CDR, Jackson JE. The role of radiology in the investigation and management of patients with haemoptysis. Clin Radiol 1996;51:391 /400. [3] Laroche C, Fairburn I, Moss H, Pepke-Zaba J, Sharples L, Flower C, Coulden R. Role of computed tomographic scanning of the thorax prior to bronchoscopy in the investigation of suspected lung cancer. Thorax 2000;55:359 /63. [4] Bungay HK, Pal CR, Davies CWH, Davies RJO, Gleeson FV. An evaluation of computed tomography as an aid to diagnosis in patients undergoing bronchoscopy for suspected bronchial carcinoma. Clin Radiol 2000;55:554 /60. [5] Savage C, Morrison RJ, Zwischenberger JB. Bronchoscopic diagnosis and staging of lung cancer. Chest Surg Clin North Am 2001;11(4):701 /21. [6] Pearson FG. Staging of the mediastinum. Role of mediastinoscopy and computed tomography. Chest 1993;103(4):346S /8S. [7] The Canadian Lung Oncology Group. Investigation for mediastinal disease in patients with apparently operable lung cancer. Ann Thorac Surg 1995;60:1382 /9. [8] Shaffer K. Radiologic evaluation in lung cancer. diagnosis and staging. Chest 1997;112(4):S235 /8. [9] Lau CL, Harpole DH, Patz E. Staging techniques for lung cancer. Chest Surg Clin North Am 2000;10(4):781 /801. [10] Hyer JD, Silvestri G. Diagnosis and staging of lung cancer. Clin Chest Med 2000;21(1):95 /106. [11] Bogot NR, Shaham D. Semi-invasive and invasive procedures for the diagnosis and staging of lung cancer II. Bronchoscophic and Surgical Procedures. Lung Cancer 2000;38(3):535 /44. [12] Gurses A, Turna A, Bedirhan MA, et al. The value of mediastinoscopy in preoperative evaluation of mediastinal involvement in non-small cell lung cancer patients with clinical NO disease. Thorac Cardiov Surg 2002;50:174 /7. [13] Steinert HC, Hauser M, Allemann F, et al. Non-small cell lung cancer: nodal staging with FDG PET versus CT with correlative lymph node mapping and sampling. Radiology 1997;202:441 /6. [14] Coleman RE. PET in lung cancer. J Nucl Med 1999;40(5):814 /9.
47
[15] Farrell MA, McAdams HP, Herndon JE, Patz EF. Non-small cell lung cancer: FDG-PET for nodal staging in patients with stage I disease. Radiology 2000;215:886 /90. [16] Goldsmith SJ, Kostakoglu L. Nuclear medicine imaging of lung cancer. Radiol Clin North Am 2000;38(3):511 /23. [17] Pieterman RM, van Putten JWG, Meuzelaar JJ, et al. Preoperative staging of non-small cell lung cancer with 18-fluorodeoxyglucose positron emission tomography. N Engl J Med 2000;343:254 /61. [18] Laking G, Price P. 18-Fluorodeoxyglucose positron emission tomography (FDG-PET) and the staging of early lung cancer. Thorax 2001;56(Suppl. II):ii38 /44. [19] Coleman RE. PET in lung cancer staging. Q J Nucl Med 2001;45:231 /4. [20] Haberkorn U, Schoenberg SO. Imaging of lung cancer with CT, MRT and PET. Lung Cancer 2001;34:S13 /23. [21] van Tinteran H, Hoekstra OS, Smit EF, et al. Effectiveness of positron emission tomography in the preoperative assessment of patients with suspected non-small-cell lung cancer: the PLUS multicentre randomised trial. Lancet 2002;359:1361 /2. [22] Vansteenkiste JF. Imaging in lung cancer: positron emission tomography scan. Eur Respir J Suppl 2002;35:49s /60s. [23] Heelan RT, Demas BE, Caravelli JE, et al. Superior sulcus tumours: CT and MR imaging. Radiology 1989;170:637 /41. [24] Webb R, Gatsonis C, Zerhouni EA, et al. CT and MR imaging in staging non-small cell bronchoscopic carcinoma: report of the radiologic diagnostic oncology group. Radiology 1991;178:705 / 13. [25] Padovani B, Mouroux J, Seksik L, Chanalet S, et al. Chest wall invasion by bronchogenic carcinoma: evaluation with MR imaging. Radiology 1993;187:33 /8. [26] Bonomo L, Ciccotosto C, Guidotti A, Storto ML. Lung cancer staging: the role of computed tomography and magnetic resonance imaging. Eur J Radiol 1996;23:35 /45. [27] Suzuki N, Saitoh T, Kitamura S. Tumour invasion of the chest wall in lung cancer: diagnosis with US. Radiology 1993;187:39 / 42. [28] Fultz PJ, Feins RH, Strang JG, et al. Detection and diagnosis of nonpalpable supraclavicular lymph nodes in lung cancer at CT and US. Radiology 2002;222:245 /51. [29] Weaver LJ, Solliday N, Cugell DW. Selection of patients with hemoptysis for fiberoptic bronchoscopy. Chest 1979;76(1):7 /10. [30] Hirshberg B, Biran I, Glazer M, Kramer MR. Hemoptysis: etiology, evaluation, and outcome in tertiary referral hospital. Chest 1997;112:440 /4. [31] Gong H, Salvatierra C. Clinical efficacy of early and delayed fibreoptic bronchoscopy in patients with hemoptysis. Am Rev Respir Dis 1981;124:221 /5. [32] Naidich DP, Funt S, Ettenger NA, Arranda C. Hemoptysis: CTbronchoscopic correlations in 58 cases. Radiology 1990;177:357 / 62. [33] Jackson CV, Savage PJ, Quinn DL. Role of fiberoptic bronchoscopy in patients with hemoptysis and a normal chest roentgenogram. Chest 1985;87(2):142 /4. [34] Poe RH, Israel RH, Marin MG. Utility of fiberoptic bronchoscoy in patients with hemoptysis and a nonlocalizing chest roentgenogram. Chest 1988;92(1):70 /5. [35] Lederle FA, Nichol KL, Parenti CM. Bronchoscopy to evaluate hemoptysis in older men with nonsuspicious chest roentgenograms. Chest 1989;95(5):1043 /7. [36] Colice GL, Chappel GJ, Frenchman SM, Solomon DA. Comparisonof computerized tomography with fiberoptic bronchoscopy in identifying abnormalities in patients with known or suspected lung cancer. Am Rev Respir Dis 1985;131:397 /400. [37] Naidich DP, Lee J, Garay SM, McCauley DI, Aranda CP, Boyd AD. Comparison of CT and fiberoptic bronchoscopy in the evaluation of bronchial disease. Am J Roentgenol 1987;148:1 /7.
48
Z.C. Traill, F.V. Gleeson / European Journal of Radiology 45 (2003) 39 /48
[38] Henschke CI, Davis SD, Auh Y. Detection of bronchial abnormalities: comparison of CT and bronchoscopy. J Comp Assist Tomogr 1987;11(3):432 /5. [39] Naidich DP, Zinn WI, Ettenger NA, McCauley DI, Garay SM. Basilar segmental bronchi: thin-section CT evaluation. Radiology 1988;169:11 /6. [40] Mayr B, Ingrisch H, Haussinger K, Huber RM, Sunder-Plassmann L. Tumors of the bronchi: role of evaluation with CT. Radiology 1989;172:647 /52. [41] Set PAK, Flower CDR, Smith IE, Cahn AP, Twentyman OP, Shneerson JM. Hemoptysis: comparative study of the role of CT and fiberoptic bronchoscopy. Radiology 1993;189:677 /80. [42] McGuinness Georgeann, Beacher Jon R, Harkin Timothy J, et al. Hemoptysis: prospective high-resolution CT/bronchoscopic correlation. Chest 1994;105:1155 /62. [43] Kauczor HU, Wolcke B, Fischer B, et al. Three-dimensional helical CT of the tracheobronchial tree: evaluation of imaging protocols and assessment of suspected stenoses with bronchoscopic correlation. Am J Roentgenol 1996;167:419 /24. [44] Lee KS, Yoon JH, Kim TK, et al. Evaluation of tracheobronchial disease with helical CT with multiplanar and three-dimensional reconstruction: correlation with bronchoscopy. Radiographics 1997;17:555 /67. [45] Remy-Jardin M, Remy J, Artaud D, Friburg M, Duhamel A. Volume rendering of the tracheobronchial tree: clinical evaluation of bronchographic images. Radiology 1998;208:761 /70. [46] Haponik EF, Aquino SL, Vining DJ. Virtual bronchoscopy. Clin Chest Med 1999;20(1):201 /16. [47] Lawler LP, Fishman EK. Multi-detector row CT of thoracic disease with emphasis on 3D volume rendering and CT angiography. Radiographics 2001;21:1257 /73. [48] Millar AB, Boothroyd AE, Edwards D, Hetzel MR. The role of computed tomography (CT) in the investigation of unexplained haemoptysis. Respir Med 1992;86:39 /44. [49] Ginsberg RJ. Evaluation of the mediastinum by invasive techniques. Surg Clin North Am 1987;67(5):1025 /35. [50] Van Schil P. Role of Video-Assisted Thoracic Surgery (VATS) in staging, diagnosis and treatment of lung cancer. Acta Chir Belg 1998;98:103 /8. [51] Hoffman H. Invasive staging of lung cancer by mediastinoscopy and video-assisted thoracoscopy. Lung Cancer 2001;34:S3 /5. [52] Mountain CF. Revisions in the international system for staging lung cancer. Chest 1997;111:1710 /7. [53] McCaughan BC, Martini N, Bains M, McCormack PM. Chest wall invasion in carcinoma of the lung. Therapeutic and prognostic implications. J Thorac Cardiovasc Surg 1985;89:836 /41. [54] Allen MS, Mathisen DJ, Grillo HC, et al. Bronchogenic carcinoma with chest wall invasion. Ann Thorac Surg 1991;51:948 /51. [55] Van Raemdonck DE, Schneider A, Ginsberg RJ. Surgical treatment for higher stage non-small cell lung cancer. Ann Thorac Surg 1992;54:999 /1013. [56] Mountain CF. Surgery for stage IIIa-N2 non-small cell lung cancer. Cancer 1994;73:2589 /98. [57] Shah SS, Goldstraw P. Combined pulmonary and thoracic wall resection for stage III lung cancer. Thorax 1995;50:782 /4. [58] McLoud TM. CT of bronchogenic carcinoma: indeterminate mediastinal invasion. Radiology 1989;173:15 /6. [59] Glazer HS, Kaiser LR, Anderson DJ, et al. Indeterminate mediastinal invasion in bronchogenic carcinoma: CT evaluation. Radiology 1989;173:37 /43. [60] Herman SJ, Winton TL, Weisbrod GL, Towers MJ, Mentzer SJ. Mediastinal invasion by bronchoscopic carcinoma: CT signs. Radiology 1994;190:841 /6. [61] White PG, Adams H, Crane MD, Buchart EG. Preoperative staging of carcinoma of the bronchus: can computed tomographic
[62]
[63]
[64]
[65]
[66]
[67]
[68] [69]
[70]
[71]
[72]
[73]
[74]
[75] [76]
[77] [78] [79] [80] [81]
[82]
[83]
scanning reliably identify stage III tumour? Thorax 1994;49:951 / 7. Pennes DR, Glazer GM, Wimbish KJ, Gross BH, Long RW, Orringer MB. Chest wall invasion by lung cancer: limitations of CT evaluation. Am J Roentgenol 1985;144:507 /11. Glazer HS, Duncan-Meyer J, Aronberg DJ, Moran JF, Levitt RG, Sagel SS. Pleural and chest wall invasion in bronchogenic carcinoma: CT evaluation. Radiology 1985;157:191 /4. Yokoi K, Mori K, Miyazawa N, et al. Tumour invasion of the chest wall and mediastinum in lung cancer: evaluation with pneumothorax CT. Radiology 1991;181:147 /52. Murata K, Takahashi M, Mori M, et al. Chest wall and mediastinum invasion by lung cancer: evaluation with multisection expiratory dynamic CT. Radiology 1994;191:251 /5. Shirakawa T, Fukuda K, Miyamoto Y, et al. Parietal pleural invasion of lung masses: evaluation with CT performed during deep inspiration and expiration. Radiology 1994;192:809 /11. Kuriyama K, Tateishi R, Kumatani T. Pleural invasion by peripheral bronchogenic carcinoma: assessment with three-dimensional helical CT. Radiology 1994;191:365 /9. Mountain CF, Carolyn Dresler M. Regional lymph node classification for lung cancer staging. Chest 1997;111:1718 /23. Ko JP, Drucker EA, Shepard JO, Mountain CF, et al. CT depiction of regional nodal stations for lung cancer staging. Am J Roentgenol 2000;174:775 /82. Cascade P, Gross B, Kazerooni E, et al. Variability in the detection of enlarged mediastinal lymph nodes in staging lung cancer: a comparison of contrast-enhanced and unenhanced CT. Am J Roentgenol 1998;170:927 /31. Patz EJ, Erasmus JJ, McAdams HP. Lung cancer staging and management: comparison of contrast-enhanced and non-enhanced helical CT of the thorax. Radiology 1999;212:56 /60. McLoud T, Bourgouin PM, Greenberg RW, et al. Bronchogenic carcinoma: analysis of staging in the mediastinum with CT by correlative lymph node mapping and sampling. Radiology 1992;182:319 /23. Poon P, Bronskill MJ, Henkelman RM, et al. Mediastinal lymph node metastases from bronchogenic carcinoma: detection with MR imaging and CT. Radiology 1987;162:651 /6. Boiselle PM. MR imaging of thoracic lymph nodes. A comparison of computed tomography and positron emission tomography. MRI Clin North Am 2000;8(1):33 /41. Carlens E. Mediastinoscopy: a method for inspection and tissue biopsy in the superior mediastinum. Dis Chest 1959;36:343 /7. Foster ED, Munro DD, Dobell ARC. Mediastinoscopy. A review of anatomical relationships and complications. Annals Thorac Surg 1972;13(3):273 /86. Goldstraw P. Mediastinal exploration by mediastinoscopy and mediastinotomy. Br J Dis Chest 1988;82:111 /20. McNeill TM, Chamberlain JM. Diagnostic anterior mediastinoscopy. Ann Thorac Surg 1966;2(4):532 /9. Evans DS, Hall JH, Harrison GK. Anterior mediastinoscopy. Thorax 1973;28:444 /7. Jacobeus HC. Possibility of the use of cystoscope for investigation of serous cavities. Munch Med Wochenschr 1910;57:2090 /2. Allen MS, Deschamps C, Lee RE, et al. Video-assisted thoracoscopic stapled wedge excision for indeterminate pulmonary nodules. J Thorac Cardiovasc Surg 1993;106(6):1048 /52. Ginsberg MS, Griff SK, Go BD, et al. Pulmonary nodules resected at video-assisted thoracoscopic surgery: etiology in 426 patients. Radiology 1999;213:277 /82. Choi BG, Kim HH, Kim B, et al. Pulmonary nodules: CT-guided contrast material localization for thoracoscopic resection. Radiology 1998;208:399 /401.