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(Chest. 2000;117:96S-103S.)
© 2000 American College of Chest Physicians

Clinical and Surgical Staging of Non-Small Cell Lung Cancer*

Jean Deslauriers, MD and Jocelyn Grégoire, MD

* From the Centre de pneumologie de l’Hôpital Laval, Sainte-Foy, Quebec, Canada.

Correspondence to: Jean Deslauriers, MD, Centre de pneumologie de l’Hôpital Laval, 2725 chemin Ste-Foy, Sainte-Foy, Quebec, Canada G1V 4G5


   Abstract
TOP
 Abstract
Introduction
 Staging System
 Preoperative Diagnosis
 Clinical Staging of the...
 Clinical Staging of the...
 Clinical Staging of the...
 Intraoperative Staging
 Conclusion
 References
 
The necessity for a compulsive attitude toward preoperative assessment of lung cancer is to be emphasized, since rational treatment and prognosis depend largely on the stage of disease at the time of diagnosis. In the preoperative setting, the techniques used should be sequential, logical, and help to identify patients suitable for treatment with curative intent. With regard to the primary tumor (T status), the accuracy of CT or MRI to predict the need for extended resections is limited. Similarly, all noninvasive methods to determine the nodal status (N) are valuable, but mediastinoscopy has a greater sensitivity and specificity than either CT or MRI. The role of routine organ screening for the detection of distant occult metastasis in the asymptomatic patient is still controversial. Ultimately, the prognosis of the resected patient with lung cancer is based on complete intraoperative staging, which can be done by either systematic node sampling or complete lymphadenectomy. At present, neither of these techniques has been shown to improve the quality of staging or survival.

Key Words: clinical staging • lung cancer • surgical staging


   Introduction
TOP
 Abstract
 Introduction
Staging System
 Preoperative Diagnosis
 Clinical Staging of the...
 Clinical Staging of the...
 Clinical Staging of the...
 Intraoperative Staging
 Conclusion
 References
 
Recognizing that surgical treatment is still the best method of controlling lung cancer, surgeons want an operation to be performed when the benefits clearly outweigh the possible risks, and when it has been determined that cancer resection is the most appropriate course of management. The necessity for a compulsive attitude toward preoperative assessment is therefore to be emphasized, since rational treatment decisions and ultimate prognosis of patients with lung cancer depend largely on the stage of disease at the time of diagnosis.1 2

Staging is the measurement of the extent of tumor that allows rational grouping of patients with similar disease for prognostic, analytic, or therapeutic purposes. In the preoperative setting, staging will define patients most likely to benefit from pulmonary resection, while ensuring that no individual is denied the chance of curative resection based on radiologic or clinical findings alone.3 It will also help the selection of patients eligible for induction therapy programs. If proper pretreatment staging is accomplished, the rate of exploratory thoracotomy or incomplete resection should not exceed 8 to 10%.

In 1997, a consensus panel of the International Association for the Study of Lung Cancer4 made the following recommendations on pretreatment minimal staging for non-small cell lung cancer (NSCLC): (1) any staging protocol should be simple and widely applicable; (2) the staging protocol should be sequential and logical, avoiding unnecessary tests that might prove expensive and invasive; (3) the staging protocol should identify patients suitable for treatment with curative intent; and (4) any staging protocol should be based on the TNM classification. The purpose of this article is to review the role and relative merits of invasive and noninvasive methods utilized in the staging of patients with lung cancer.


   Staging System
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 Abstract
 Introduction
 Staging System
Preoperative Diagnosis
 Clinical Staging of the...
 Clinical Staging of the...
 Clinical Staging of the...
 Intraoperative Staging
 Conclusion
 References
 
The Union Internationale Contre le Cancer and American Joint Committee on Cancer have recently established new criteria for the TNM staging of lung cancer, and the prognosis for the various TNM subsets has also been redefined.5 This staging system uses the TNM classification originally described by Denoix,6 where T indicates site and size of the primary tumor, N relates to nodal involvement according to site, and M indicates the presence or absence of distant metastasis (Table 1 ).


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  		Table 1. TNM Descriptors in Lung Cancer*

 
In this revised classification, the descriptors for the TNM classification have generally remained the same as those described in 1986.7 Tumors classified as T3 are neoplasms that have grown beyond the lung parenchyma to involve structures still amenable to resection, while T4 defines those tumors with extensive extrapulmonary extension, usually precluding curative or complete resection. The T4 descriptor also includes tumors with satellite nodules located within the same lobe.8 Satellite nodules located in the ipsilateral nonprimary tumor lobe(s) of the lung are designated M1.

The problem of nonmalignant pleural effusions has not really been solved, because the use of this descriptor when the effusion is nonbloody and not an exudate is left to clinical judgment.5 It implies that when the effusion is an exudate, as is the case in virtually all paraneoplastic effusions, the tumor should be designated as T4. Patients with cytology-positive malignant effusions are also designated as having T4 tumors.

The issue of site as a descriptor of the T status has been partially addressed. Superficial tumors in which the invasive component is limited to the bronchial submucosa are now classified as T1 tumors, even if they are located within the main bronchus or within 2 cm from the carina. That leaves a number of larger invasive tumors that may be T3 by virtue of their location being proximal to a lobar orifice, but are more likely to behave as T1 or T2 tumors. The new TNM classification still does not establish a difference between T3 tumors invading the parietal pleura and T3 tumors invading the ribs or soft tissues of the chest wall.

The classification of regional lymph node stations has been clarified by Mountain and Dresler,9 who tried to combine the features of the two systems that have been in use for > 30 years, the first one based on the work of Naruke and advocated by the American Joint Committee on Cancer,10 and the second being the nodal map proposed by the American Thoracic Society11 and adopted by the North American Lung Cancer Study Group. In their proposal, all N2 nodes are contained within the mediastinal pleural envelope and are numbered 1 through 9. It is understood, although not clearly stated, that in many cases, the mediastinal pleura reflexion is difficult to identify, even at surgery, so that the distinction between hilar nodes (N1) and low tracheobronchial nodes (N2) may be difficult to make. Anatomically, the pleural envelope begins just proximal to the origin of the upper lobe bronchus, so that all lymph nodes cephalad to this point should be designated as mediastinal.

The issue of Pancoast tumors, where supraclavicular nodes may be involved by direct transpleural seeding through the apical pleura, has not been addressed. If these nodes contain tumor, they are designated as N3 nodes, although they may be the first nodal station involved.

The use of immunohistochemistry to identify micrometastases in lymph nodes and bring improvement in routine tissue staining has not been clearly shown to affect survival.12 13 These procedures may, however, have an impact on the planning of postoperative adjuvant therapies. In one study13 the detection of occult micrometastasis in mediastinal lymph nodes with monoclonal antibody to cytokeratin was used to predict early relapse in patients with stage I NSCLC.

The staging system has also been modified to provide greater specificity for identifying patient groups with similar prognosis and treatment options (Table 2 ).5 Stage I has been divided into I-a and I-b because the difference in survival rate between the two groups is significant (p < 0.01). Since there was little difference between the cumulative 5-year survival rates for patients with T2N1M0 and T3N0M0 disease, these were regrouped in stage II-b. Patients with N2 disease remain in stage III-a, and those with T4 tumors are included in stage III-b disease.


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  		Table 2. Revised Stage Grouping of TNM Subsets*

 
The staging process can be broken down into a clinical stage TNM, determined by pretreatment studies and a pathologic stage TNM, which depends on intraoperative maneuvers by the surgeon and postoperative assessment by the pathologist.


   Preoperative Diagnosis
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 Abstract
 Introduction
 Staging System
 Preoperative Diagnosis
Clinical Staging of the...
 Clinical Staging of the...
 Clinical Staging of the...
 Intraoperative Staging
 Conclusion
 References
 
Although some surgeons continue to advocate thoracotomy without diagnosis because "you are going to operate anyway," adequate treatment planning begins with a proper diagnosis of the underlying disease process. This information allows for a clear discussion with the patient as to what will be done at operation, as well as for streamlining the investigation of the lesion. Further, it avoids the reliance on intraoperative frozen section results, which can at times be misleading.

With improved techniques of biopsy often done under CT guidance, and with refinements in the pathologic interpretation of smaller specimens, the diagnosis of lung cancer can be made preoperatively in virtually all patients. Flexible bronchoscopy is reliable in central tumors, which represent about 30% of all lung neoplasms, while percutaneous fine-needle aspiration biopsy can establish the diagnosis in as many as 90 to 95% of peripheral tumors.14 15 It is important to understand that a negative result does not exclude malignancy, especially if the cytologic findings are reported as unsatisfactory or nonspecific inflammation.14 In these individuals, repeat biopsy may be of some value.


   Clinical Staging of the T Factor
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 Abstract
 Introduction
 Staging System
 Preoperative Diagnosis
 Clinical Staging of the...
Clinical Staging of the...
 Clinical Staging of the...
 Intraoperative Staging
 Conclusion
 References
 
A careful clinical history and physical examination remains a highly cost-effective staging method, especially in higher-stage tumors invading the chest wall, superior sulcus, or mediastinum. Similarly, standard chest radiographs may on occasion provide evidence of chest wall invasion or of pleural effusion. Bronchoscopy should always be done, not only to determine the endobronchial T status of central tumors, but also to rule out synchronous tumors in other parts of the bronchial tree. In addition, bronchoscopy may be helpful to identify possible candidates for sleeve resection of the main bronchus or carina.16 In those patients, the distance of submucosal spread can be estimated by the use of serial biopsies over distances of 1 to 2 cm proximal and distal to the tumor.

In most cases of presumed intrathoracic spread, CT and MRI will improve the preoperative determination of tumor invasion. Even with the use of these imaging modalities, however, the staging of tumors involving the chest wall or mediastinum and that of Pancoast tumors remains difficult.

In patients with lung cancer suspected of direct invasion into the chest wall, one has to try to predict the need for chest wall resection in order to avoid unnecessary extended resections or unneeded violation of tissue planes. In this respect, patients with chest wall pain associated with tumors that abut the pleura, who have a positive isotope bone scan over the tumor area, or who present with a large soft tissue mass are likely to require chest wall resection.

In a prospective study performed in 112 patients to evaluate the diagnostic accuracy of CT criteria in predicting the extent of chest wall invasion by lung cancer, Ratto et al17 showed that obliteration of the extrapleural fat plane and the ratio between tumor-pleura contact and tumor diameter were the only CT variables significantly related to pathologic findings (Table 3 ). In that study, the surgeon was almost certain that an extrapleural dissection would not violate the cancer plane if both criteria were negative (sensitivity, 97%), but if both criteria suggested chest wall invasion, the surgeon was advised against extrapleural dissection (specificity, 89%). In 1991, Yukoi et al18 studied 30 patients with a peripheral lung cancer abutting the chest wall but without CT signs of true parietal invasion. After the induction of a diagnostic pneumothorax, repeated CT was carried out with a diagnostic accuracy of 100% for predicting chest wall invasion. Despite these results, CT is generally considered inaccurate to predict the need for chest wall resection,19 20 although obliteration of the extrapleural fat plane and costal osteolysis are highly predictive signs of chest wall invasion. CT also has great difficulty in differentiating between visceral and parietal pleura invasion, because peritumoral inflammatory adhesions often simulate true invasion. CT and MRI appear to be equivalent in their ability to demonstrate chest wall invasion, as reported by the Radiology Diagnostic Oncology Group.21 In one retrospective study from Japan,22 chest wall invasion was evaluated with ultrasonography in 19 patients and confirmed at thoracotomy. The sensitivity, specificity, and accuracy of ultrasonography was 100, 98, and 98%, respectively.


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  		Table 3. CT Scan Criteria for Chest Wall Invasion*

 
MRI is more accurate than CT to evaluate the local invasiveness of superior sulcus tumors,21 23 particularly their extension to the vertebral body, spinal canal, brachial plexus, and subclavian artery. In a prospective and blinded study of 31 patients with superior sulcus tumors, Heelan et al23 demonstrated that thin-section (5 mm) coronal and sagittal images were more accurate than CT scans (94% accuracy with MRI; 63% with CT) in the evaluation of tumor invasion through the superior sulcus. This information is important, because vertebral body, spinal canal, or upper brachial plexus invasion are contraindications to operation for most surgeons. In that study, the improved accuracy of MRI was interpreted as being related to the ability to image the superior sulcus on thin-section coronal and sagittal images. On occasion, ancillary techniques such as subclavian artery angiography may be indicated to rule out local invasion by superior sulcus tumors. Involvement of the subclavian artery is not considered an absolute contraindication to resection, although invasion of its vertebral branch may make the operation more dangerous. We also suggest that all patients with Pancoast tumors have ultrasonography examination of the ipsilateral scalene area with percutaneous biopsy of nodes > 1 cm in their transverse diameter.

Preoperative documentation of mediastinal invasion is important because it is a major prognostic variable. Tumors that superficially invade the mediastinum (T3 tumors) can be excised, but tumors invading deep into the mediastinum (heart, esophagus, trachea) are T4 tumors that usually preclude surgical resection. Both CT and MRI can depict gross mediastinal invasion, but both studies are quite poor in their ability to distinguish between tumor abutting the mediastinum vs a tumor truly extending into a mediastinal structure. In the Radiology Diagnostic Oncology Group report,21 MRI was statistically significantly more accurate than CT to detect mediastinal invasion. In another report, Glazer et al24 reviewed 80 patients who had indeterminate mediastinal invasion by CT scan. Forty-eight of these masses (60%) were resectable without true invasion of the mediastinum, 18 masses (22%) focally invaded the mediastinum but were still technically resectable, and 14 masses (18%) were unresectable. CT findings considered to be indicative of complete resection included contact of <= 3 cm with the mediastinum, < 90% contact with the aorta, and the presence of mediastinal fat between mass and mediastinal structures.24 Based on these results, one must therefore be very careful before determining that a given tumor is unresectable based on CT criteria alone.

MRI appears to be superior to CT to demonstrate heart and great vessel invasion,25 while tumors invading to the thoracic aorta may be best shown by cine CT.26 In some cases of left atrial involvement, transesophageal ultrasonography may also be useful to determine the depth of invasion. In central tumors invading the main pulmonary artery, it is often impossible to determine preoperatively the exact T status (T3 or T4), so that thoracotomy must be done to ascertain tumor resectability.

The parietal pleura can be involved by a direct extension of the tumor or indirectly through subpleural lymphangitic spread or pleural metastasis. While direct invasion is not a major problem, indirect invasion is always a sign of inoperability that must be documented preoperatively. CT is more accurate than standard radiographs to document the presence of small effusions (< 25 mL), and when fluid is present, it is important to determine its true nature. This can be done by thoracentesis, percutaneous pleural biopsy, or video-assisted thoracoscopic surgery (VATS), which allows direct assessment of the pleural surfaces. By VATS examination, Asamura et al27 were able to demonstrate inoperable factors in 5 of 135 patients with presumed operable lung cancer. Four had a malignant pleural effusion, and one had extensive dissemination without effusion.


   Clinical Staging of the N Factor
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 Abstract
 Introduction
 Staging System
 Preoperative Diagnosis
 Clinical Staging of the...
 Clinical Staging of the...
Clinical Staging of the...
 Intraoperative Staging
 Conclusion
 References
 
The presence of metastases to regional lymph node significantly influences the treatment and prognosis of patients with NSCLC. The presence of N1 nodes, although rarely of crucial importance except perhaps in patients with T3-T4 tumors, means more extensive resection with increased surgical risk and reduced prospects for cure. At present, the techniques used for preoperative documentation of N1 status are imperfect, and CT does not appear to be better than chest radiographs or oblique tomograms, especially in cases where the hilum is of normal size on routine examination. Hilar abnormalities may be easier to detect with MRI because nodes can be more readily distinguished from local vessels by this technique.

The presence of mediastinal lymph node metastasis (N2, N3 disease) is an ominous prognostic sign; stage III-b disease, by virtue of metastatic contralateral lymph nodes in the mediastinum or hilum, is an absolute contraindication to surgical resection. Physical examination can detect enlarged supraclavicular or scalene nodes, but this type of examination is notoriously inaccurate if done by an inexperienced examiner. Careful clinical-history taking and physical examination can also detect evidence of superior vena cava obstruction or left recurrent nerve palsy, both being nearly absolute signs of N2 disease. Enlarged nodes within the mediastinum on standard radiographs are highly specific, if insensitive, signs of N2 disease.

Advanced invasive and noninvasive techniques are currently used to preoperatively determine the status of mediastinal nodes. Imaging modalities such as CT and MRI can demonstrate nodal enlargement but cannot confirm histologic involvement. On the other hand, more invasive procedures such as mediastinoscopy, anterior mediastinotomy, VATS, and ultimately thoracotomy are more specific in assessing lymph nodes but require operative intervention. At present, the choice of techniques to be used continues to be one of the most controversial issues in the staging of lung cancer.

The major contribution of CT is to allow the surgeon to proceed directly to thoracotomy28 if the nodes have a transverse diameter of < 1 cm, where the likelihood of finding metastatic tissue is in the range of 3 to 16%.28 29 30 The accuracy improves if the primary tumor is peripheral or of squamous histology,31 but decreases if the tumor is central or of nonsquamous histology. Lymph nodes that have a diameter of 1 to 2 cm by CT contain metastatic tissue in 70% of cases,30 31 32 while those > 2 cm have an even greater chance of containing tumor tissue. In a meta-analysis of CT accuracy for assessment of mediastinal lymph nodes in lung cancer, the authors reported a sensitivity, specificity, and overall accuracy of 79, 78, and 80%, respectively.33

The predictive value and accuracy of CT in determining mediastinal node involvement is lower in the presence of distal obstructive pneumonitis or old granulomatous disease, and MRI has generally not been shown to be more accurate than CT to evaluate nodal disease.34 For these reasons, there is general agreement that enlarged lymph nodes require histologic confirmation if this finding means inoperability. In other words, suspected inoperability on the basis of abnormal findings from noninvasive procedures should always be confirmed by direct biopsy.

Imaging with whole-body positron emission tomography (PET) appears to be more accurate than CT for the diagnosis of mediastinal node metastasis. In one study carried out in 76 patients,35 mediastinal PET and CT findings were compared with results of surgical staging. Sensitivity and specificity for the diagnosis of N2 disease were 83% and 94% for PET, and 63% and 73% for CT, respectively. PET is also valuable to detect occult adrenal or liver metastases not documented by other means of nonsurgical staging. A recent Technology Evaluation Center of Blue Cross/Blue Shield report36 37 concluded that the literature supported the use of fluorodeoxyglucose-PET for staging lung cancer, even if the technology is currently unavailable in most centers.

Most invasive procedures used to determine the nodal status involve long tubes passed through small holes into highly vascular surroundings.38 Despite this frightening description, these techniques can be carried out with low morbidity if the operator is experienced and familiar with the local anatomy. Perhaps less invasive, needle aspiration biopsy done through a transtracheal or transthoracic approach may be useful to stage patients with inoperable tumors and an enlarged mediastinum on chest radiograph or CT. In 1996, Akamatsu et al39 reported a sensitivity of 88% and specificity of 100% for CT-guided percutaneous cytology of mediastinal lymph nodes. In yet another study, Silvestri et al40 showed that esophageal endoscopic ultrasonography with fine-needle aspiration complemented mediastinoscopy in the assessment of lymph nodes located in the aortopulmonary window or subcarinal space.

As reported by Carlens41 and Pearson et al,42 43 mediastinoscopy involves the inspection, palpation, and biopsy of superior mediastinal lymph nodes. It is a useful and accurate technique that should be used when nodal involvement as determined by CT is unclear (nodes > 1 cm in diameter), or when it is required to have an exact knowledge of mediastinal involvement, such as in higher stage (T2-T3), centrally located, or undifferentiated tumors. In patients where induction treatments are contemplated, mediastinoscopy should be mandatory. Because mediastinoscopy has a greater sensitivity and specificity than CT scanning to document mediastinal node involvement, some centers still recommend its routine use in all presumed operable lung carcinomas.44 45 Ideally, nodes from stations 2, 4, and 10 should be sampled routinely along with the subcarinal (station 7) nodes, as described in the American Thoracic Society staging system.11 Mediastinoscopy may be utilized safely in patients with superior vena cava obstruction and in patients who have had a prior mediastinoscopy. It can be done on an outpatient basis,46 or at the time of thoracotomy.

Lymph nodes located in the aortopulmonary window (station 5) are not accessible by cervical mediastinoscopy, but biopsy can be performed through a left anterior mediastinotomy,47 48 often referred to as a Chamberlain procedure,49 or through an extension of standard cervical mediastinoscopy.50 51 The information gained by these procedures is particularly important for patients with left upper lobe lesions, where survival figures for patients with resectable disease and metastatic subaortic nodes approaches that of patients with N1 disease.52 53 In most centers, these procedures are only done if the aortopulmonary nodes appear to be enlarged on CT scan.

Scalene node biopsy is indicated when they are palpable or in patients who have proven N2 disease prior to undergoing resection. Lee and Ginsberg54 have shown unsuspected microscopic involvement of the scalene nodes in 15% of patients with N2 disease at mediastinoscopy, and in 68% of patients with N3 disease. This information may be relevant in patients for whom an operation is recommended despite N2 disease, or in patients for whom neoadjuvant therapy is considered.

The role of VATS to access mediastinal nodes is unclear,55 56 57 although nodes located in the aortopulmonary window or posterior mediastinum can be readily obtained by this technique. The potential of VATS to disclose hilar disease may be of importance in patients who cannot tolerate pneumonectomy, or in patients in whom N1 disease may need to be documented histologically prior to induction therapy.


   Clinical Staging of the M Factor
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 Abstract
 Introduction
 Staging System
 Preoperative Diagnosis
 Clinical Staging of the...
 Clinical Staging of the...
 Clinical Staging of the...
Intraoperative Staging
 Conclusion
 References
 
The most useful assessment of the M factor is done by complete history and physical examination. While significant weight loss and debility are usually symptoms of metastatic disease, focal symptoms, such as headaches or musculoskeletal pain, or abnormal levels of alkaline phosphatase require further investigation. It is of interest to note that patients with brain or bone metastases are often symptomatic, while patients with liver or adrenal metastasis seldom are symptomatic. Whether routine screening for occult metastatic disease is required for every patient with presumed operable lung cancer remains controversial.58 59 In early-stage asymptomatic tumors, the yield of routine organ screening is in the range of 1 to 4%,60 61 62 and therefore should not be recommended. In one study from the United Kingdom,63 the determination of metastatic disease by CT scanning was addressed in 114 consecutive patients with NSCLC who, on the basis of history, clinical examination, chest radiography, and bronchoscopy, had been considered potentially operable. CT of the abdomen and brain detected occult metastasis in 15 patients (13%), but the extrathoracic abnormality proved to be the only contraindication to surgery in only 3 patients. In potentially operable asymptomatic patients with mediastinal node involvement or with tumors of nonsquamous histology,64 routine multiorgan screening yields a greater number of extrathoracic metastases,61 and may therefore be recommended.65 66

Common sites of distant metastases from lung cancer are the brain (10%), bone (7%), liver (5%), and adrenal glands (3%).67 Focal metastatic nodules in the liver can be detected by contrast-enhanced CT or sonography, with sensitivities in the range of 80%.28 68 69 Histologic confirmation by percutaneous biopsy is often required, since many of these liver nodules represent hepatic cysts or hemangiomas.

Contrast-enhanced CT and MRI have replaced radionuclide scans to detect brain metastasis,70 71 with MRI being reserved for patients with high suspicion despite negative CT. Gadolinium-enhanced T1-weighted MRI scans are more sensitive than contrast CT for detecting brain metastasis.72 In one study,73 it was concluded that because of expense and lack of positive findings, neither MRI nor CT were indicated in the asymptomatic patient.

Metastatic disease to the adrenals is usually discovered by routine CT scanning of the upper abdomen. A biopsy should be done of unilaterally enlarged glands, because in about 80% of cases, these masses will be benign. Metastatic disease is more likely if the adrenal mass is > 3 cm in diameter, or if the mass alters the usual concave border of the gland.74 MRI imaging offers no significant advantage over CT,75 but in one study, the chemical-shift MRI technique was shown to be highly accurate for distinguishing benign from malignant adrenal masses.76

Technetium 99m methylene bone scintigraphy is the method of choice to demonstrate skeletal metastasis. Multiple areas of increased uptake has a specificity of 80 to 90% for metastasis.77 If the presence of metastatic disease remains in question with a positive scan, correlative radiographs or CT should be obtained and, in some cases, CT or sonography-guided percutaneous biopsies should also be done. One of the main values of bone scanning is to provide a baseline, should the patient present with musculoskeletal pain sometime after his operation.


   Intraoperative Staging
TOP
 Abstract
 Introduction
 Staging System
 Preoperative Diagnosis
 Clinical Staging of the...
 Clinical Staging of the...
 Clinical Staging of the...
 Intraoperative Staging
Conclusion
 References
 
The ultimate stage of the resected patient depends on accurate intraoperative staging, which can either be done by nonsystematic or systematic lymph node sampling or by complete mediastinal node dissection.

Lymph node sampling in a nonsystematic fashion is inadequate for accurate staging. In an interesting study, Gaer and Goldstraw78 reviewed 100 thoracotomies done for lung cancer, and compared the naked-eye assessment of nodal staging with the ultimate histologic diagnosis. False-positive assessment was made at 14 node stations (11 patients), and false-negative assessments were made at 10 lymph node stations (9 patients). In that study, the sensitivity, specificity, and overall accuracy of naked-eye assessment was 71.4, 94.4, and 91.6%, respectively.78

Whether complete mediastinal node dissection improves the quality of staging and length of survival over systematic sampling remains controversial, even if lower stage tumors are known to have a high incidence of mediastinal node metastases.79 80 In a retrospective study of 337 patients with T1 tumors who had undergone pulmonary resection with complete lymphadenectomy, Asamura et al79 showed that 88 patients (26.1%) had lymph node involvement: 32 (9.5%) at N1 nodes, 55 (16.3%) at N2 nodes, and 1 at N3 nodes. The authors concluded that complete hilar mediastinal lymphadenectomy should be routinely done. Ishida et al80 (Table 4 ) and Martini et al81 also concurred that it is important to do a complete mediastinal lymphadenectomy. Ishida et al80 further documented that for patients with N1 or N2 disease, "skip metastases" are present in > 25% of cases.


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  		Table 4. Nodal Status of 221 Patients With Lung Tumor <= 3 cm in Diameter*

 
Despite these data, most surgeons, including surgeons involved in Lung Cancer Study Group clinical trials,82 prefer the technique of systematic node sampling, which consists of lymph node biopsy at multiple predetermined levels within the mediastinum and bronchopulmonary areas. This technique is simple, faster, and may involve less morbidity than complete lymphadenectomy. It may, in addition, be just as accurate if mediastinoscopy has been done preoperatively. If the patient is found to have N1 or N2 disease, systematic nodal dissection should be performed.

Two studies compared systematic sampling to mediastinal lymphadenectomy in terms of their ability to stage the mediastinum intraoperatively.83 84 In a retrospective study, Bollen et al83 concluded that the discovery ratio for N2 disease in the mediastinal node dissection and systematic sampling groups were similar, and both were better than nonsystematic sampling. The second study is that of Izbicki et al,84 who directly compared mediastinal lymph node dissection with systematic sampling in a prospective randomized trial involving 201 patients. These investigators showed that, regardless of the type of lymphadenectomy performed, the percentage of pathologic N1 or N2 disease was very similar in both groups (sampling, 23%, n = 23; lymphadenectomy, 26.8%, n = 22). Lymphadenectomy resulted in a more detailed staging, with detection of significantly more patients with multiple levels of involvement. The role of bilateral mediastinal node dissection remains unclear,85 although it is unlikely to have a major impact on techniques of resection.


   Conclusion
TOP
 Abstract
 Introduction
 Staging System
 Preoperative Diagnosis
 Clinical Staging of the...
 Clinical Staging of the...
 Clinical Staging of the...
 Intraoperative Staging
 Conclusion
References
 
Because decision making in managing lung cancer depends more on the clinical stage than on histology of the tumor, the importance of complete preoperative evaluation cannot be overemphasized. This is even more important in the context of pulmonary resection, where morbidity is related to cardiopulmonary events, most of which can also be identified and prevented prior to surgery. Pathologic staging that depends on complete intraoperative sampling not only reflects the ultimate stage of the resected patient but is also indicative of its prognosis.


   Footnotes
 
Abbreviations: NSCLC = non-small cell lung cancer; PET = position emission tomography; VATS = video-assisted thoracoscopic surgery


   References
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 Abstract
 Introduction
 Staging System
 Preoperative Diagnosis
 Clinical Staging of the...
 Clinical Staging of the...
 Clinical Staging of the...
 Intraoperative Staging
 Conclusion
 References
 

  1. Miller, JA, Gorenstein, LA, Patterson, GA (1992) Staging: the key to rational management of lung cancer. Ann Thorac Surg 53,170-178[Abstract]
  2. Sugarbaker, DJ, Strauss, GM (1993) Advances in surgical staging and therapy of non-small cell lung cancer. Semin Oncol 20,163-172[ISI][Medline]
  3. Karmy-Jones, R, Hyland, RH, Lewis, JW, Jr, et al (1997) Staging lung cancer: current controversies and strategies. Can Respir J 4,297-305
  4. Feld, R, Abratt, R, Graziano, S, et al (1997) Pretreatment minimal staging and prognostic factors for non-small cell lung cancer. Lung Cancer 17(suppl),S3-S10
  5. Mountain, CF (1997) Revisions in the international system for staging lung cancer. Chest 111,1710-1717[Abstract/Free Full Text]
  6. Denoix, PF (1946) Enquête permanente dans les centers anticancéreux. Bull Int Natl Hyg 1,70-75
  7. Mountain, CF (1986) A new international staging system for lung cancer. Chest 89(suppl),225S-233S[Free Full Text]
  8. Deslauriers, J, Brisson, J, Cartier, R, et al (1989) Evaluation of satellite nodules as a factor influencing prognosis after resection. J Thorac Cardiovasc Surg 97,504-512[Abstract]
  9. Mountain, CF, Dresler, CM (1997) Regional lymph node classification for lung cancer staging. Chest 111,1718-1723[Abstract/Free Full Text]
  10. American Joint Committee on Cancer Lung. In: Beahrs OH, Hensen DE, Hutter RVP, et al, eds. Manual for staging cancer. 4th ed. Philadelphia, PA: Lippincott, 1992; 115–121
  11. . American Thoracic Society. (1983) Clinical staging of primary lung cancer. Am Rev Respir Dis 127,1-6[ISI][Medline]
  12. Nicholson, AG, Graham, ANJ, Pezzella, F, et al (1997) Does the use of immunohistochemistry to identify micrometastases provide useful information in the staging of node-negative non-small cell lung carcinoma? Lung Cancer 18,231-240[ISI][Medline]
  13. Maruyama, R, Sugio, K, Mitsudomi, T, et al (1997) Relationship between early recurrence and micrometastases in the lymph nodes of patients with stage I non-small cell lung cancer. J Thorac Cardiovasc Surg 114,535-543[Abstract/Free Full Text]
  14. Weisbrod, GL (1993) Transthoracic needle biopsy. World J Surg 17,705-711[CrossRef][ISI][Medline]
  15. Todd, TRJ, Weisbrod, G, Tao, LC, et al (1981) Aspiration needle biopsy of thoracic lesions. Ann Thorac Surg 32,154-161[Abstract]
  16. Deslauriers, J, Mehran, RJ, Guimont, C, et al (1993) Staging and management of lung cancer: sleeve resection. World J Surg 17,712-719[CrossRef][ISI][Medline]
  17. Ratto, GB, Piacenza, G, Frola, C, et al (1991) Chest wall involvement by lung cancer: computed tomographic detection and results of operation. Ann Thorac Surg 51,182-188[Abstract]
  18. Yokoi, K, Mori, K, Miyazawa, N, et al (1991) Tumor invasion of the chest wall and mediastinum in lung cancer: evaluation with pneumothorax CT. Radiology 181,147-152[Abstract/Free Full Text]
  19. Pennes, DR, Glazer, GM, Wimbish, KJ, et al (1985) Chest wall invasion by lung cancer: limitations of CT evaluation. AJR Am J Roentgenol 144,507-511[Abstract/Free Full Text]
  20. Glazer, HS, Duncan-Meyer, J, Aronberg, DJ, et al (1985) Pleural and chest wall invasion in bronchogenic carcinoma: CT evaluation. Radiology 157,191-194[Abstract/Free Full Text]
  21. Webb, WR, Gatsonis, C, Zerhouni, EA, et al (1991) CT and MR imaging in staging non-small cell bronchogenic carcinoma: report of the Radiologic Diagnostic Oncology Group. Radiology 178,705-713[Abstract/Free Full Text]
  22. Susuki, N, Saitoh, T, Kitamura, S (1993) Tumor invasion of the chest wall in lung cancer: diagnosis with US. Radiology 187,37-42
  23. Heelan, RT, Demas, BE, Caravelli, JF, et al (1989) Superior sulcus tumors: CT and MR imaging. Radiology 170,637-641[Abstract/Free Full Text]
  24. Glazer, HS, Kaiser, LR, Anderson, DJ, et al (1989) Indeterminate mediastinal invasion in bronchogenic carcinoma: CT evaluation. Radiology 173,37-42[Abstract/Free Full Text]
  25. Kameda, K, Adachi, S, Kono, M (1988) Detection of the T factor in lung cancer using magnetic resonance imaging and computed tomography. J Thorac Imaging 3,73-80
  26. Ohtsuka, T, Minami, M, Nakajima, J, et al (1996) Cine computed tomography for evaluation of tumors invasive to the thoracic aorta: seven clinical experiences. J Thorac Cardiovasc Surg 112,190-192[Free Full Text]
  27. Asamura, H, Nakajima, H, Kondo, H, et al (1997) Thoracoscopic evaluation of histologically/cytologically proven or suspected lung cancer: a VATS exploration. Lung Cancer 16,183-190[CrossRef][ISI][Medline]
  28. Whittlesey, D (1988) Prospective computed tomographic scanning in the staging of bronchogenic cancer. J Thorac Cardiovasc Surg 95,876-882[Abstract]
  29. Gross, BH, Glazer, GM, Orringer, MB, et al (1988) Bronchogenic carcinoma metastatic to normal-sized lymph nodes: frequency and significance. Radiology 166,71-74[Abstract/Free Full Text]
  30. Libshitz, HI (1990) Computed tomography in bronchogenic carcinoma. Semin Roentgenol 25,64-72[CrossRef][ISI][Medline]
  31. Staples, CE, Muller, NL, Miller, RR, et al (1988) Mediastinal nodes in bronchogenic carcinoma: comparison between CT and mediastinoscopy. Radiology 167,367-372[Abstract/Free Full Text]
  32. McLoud, TC, Bourgouin, PM, Greenberg, RW, et al (1992) Bronchogenic carcinoma: analysis of staging in the mediastinum with CT by correlative lymph node mapping and sampling. Radiology 182,319-323[Abstract/Free Full Text]
  33. Dales, RE, Stark, RM, Raman, S (1990) Computed tomography to stage lung cancers: approaching a controversy using meta-analysis. Am Rev Respir Dis 141,1096-1101[ISI][Medline]
  34. Martini, N, Heelan, R, Westcott, J, et al (1989) Comparative merits of conventional, computed tomographic, and magnetic resonance imaging in assessing mediastinal involvement in surgically confirmed lung carcinomas. J Thorac Cardiovasc Surg 90,639-648[Abstract]
  35. Valk, PE, Pounds, TR, Hopkins, DM, et al (1995) Staging non-small cell lung cancer by whole-body positron emission tomographic imaging. Ann Thorac Surg 60,1573-1582[Abstract/Free Full Text]
  36. FDG positron emission tomography for non-CNS cancers. Chicago, IL: Blue Cross/Blue Shield TEC Assessment Program, 1997; 5
  37. Coleman RE, Tesar RD. Clinical PET: are we ready? J Nucl Med 1997; 38:16N, 24N
  38. Johnston, MR (1993) Invasive staging of the mediastinum. World J Surg 17,700-704[CrossRef][ISI][Medline]
  39. Akamatsu, H, Terashima, M, Koike, T, et al (1996) Staging of primary lung cancer by computed tomography-guided percutaneous needle cytology of mediastinal lymph nodes. Ann Thorac Surg 62,352-355[Abstract/Free Full Text]
  40. Silvestri, GA, Hoffman, BJ, Bhutani, MS, et al (1996) Endoscopic ultrasound with fine-needle aspiration in the diagnosis and staging of lung cancer. Ann Thorac Surg 61,1441-1446[Abstract/Free Full Text]
  41. Carlens, E (1959) Mediastinoscopy: a method of inspection and palpation in the superior mediastinum. Dis Chest 36,343-352[ISI][Medline]
  42. Pearson, FG, Nelems, JM, Henderson, RD, et al (1972) The role of mediastinoscopy in the selection of treatment for bronchial carcinoma with involvement of superior mediastinal nodes. J Thorac Cardiovasc Surg 64,382-390[ISI][Medline]
  43. Pearson, FG, Delarue, NC, Ilves, R, et al (1982) Significance of positive superior mediastinal nodes identified at mediastinoscopy in patients with resectable cancer of the lung. J Thorac Cardiovasc Surg 83,1-11[ISI][Medline]
  44. Coughlin, M, Deslauriers, J, Beaulieu, M, et al (1985) Role of mediastinoscopy in pretreatment staging of patients with primary lung cancer. Ann Thorac Surg 40,556-560[Abstract]
  45. Luke, WP, Pearson, FG, Todd, TR, et al (1986) Prospective evaluation of mediastinoscopy for assessment of carcinoma of the lung. J Thorac Cardiovasc Surg 91,53-56[Abstract]
  46. Vallières, E, Pagé, A, Verdant, A (1991) Ambulatory mediastinoscopy and anterior mediastinoscopy. Ann Thorac Surg 52,1122-1126[Abstract]
  47. Schreinemakers, H, Joosten, H, Mravunac, M, et al (1988) Parasternal mediastinoscopy: assessment of operability in left upper lobe lung cancer; a prospective analysis. J Thorac Cardiovasc Surg 95,298-302[Abstract]
  48. Pagé, A, Mercier, C, Verdant, A, et al (1980) Parasternal mediastinoscopy in bronchial carcinoma of the left upper lobe. Can J Surg 23,171-173[ISI][Medline]
  49. McNeill, TM, Chamberlain, JM (1966) Diagnostic anterior mediastinotomy. Ann Thorac Surg 2,532-539[Medline]
  50. Deslauriers, J, Beaulieu, M, Dufour, C, et al (1976) Mediastino-pleuroscopy: a new approach to the diagnosis of intrathoracic diseases. Ann Thorac Surg 22,265-269[Abstract]
  51. Ginsberg, RJ, Rice, T, Goldberg, M, et al (1987) Extended cervical mediastinoscopy. J Thorac Cardiovasc Surg 94,673-678[Abstract]
  52. Patterson, GA, Piazza, D, Pearson, FG, et al (1987) Significance of metastatic disease in subaortic lymph nodes. Ann Thorac Surg 43,155-159[Abstract]
  53. Ginsberg, RJ (1994) The role of preoperative staging in left upper lobe tumors. Ann Thorac Surg 57,526-527[ISI][Medline]
  54. Lee, JD, Ginsberg, RJ (1996) Lung cancer staging: the value of ipsilateral scalene lymph node biopsy performed at mediastinoscopy. Ann Thorac Surg 62,338-341[Abstract/Free Full Text]
  55. Naruke, T, Asamura, H, Kando, H, et al (1993) Thoracoscopy for staging of lung cancer. Ann Thorac Surg 56,661-663[Abstract]
  56. Wain, JC (1993) Video-assisted thoracoscopy and the staging of lung cancer. Ann Thorac Surg 56,776-778[Abstract]
  57. Roviaro, GC, Varoli, F, Rebuffat, C, et al (1995) Videothoracoscopic staging and treatment of lung cancer. Ann Thorac Surg 59,971-974[Abstract/Free Full Text]
  58. Winton, TL (1993) Staging for M disease. World J Surg 17,690-693[CrossRef][ISI][Medline]
  59. Hillers, TK, Sauvé, MD, Guyatt, GH (1994) Analysis of published studies on the detection of extrathoracic metastases in patients presumed to have operable non-small cell lung cancer. Thorax 49,14-19[Abstract]
  60. Ramsdell, J, Peters, RM, Taylor, AA, et al (1977) Multi-organ scans for staging lung cancer: correlation with clinical evaluation. J Thorac Cardiovasc Surg 73,653-659[Abstract]
  61. Quinn, DL, Ostrow, LB, Porter, DK, et al (1986) Staging of non-small cell bronchogenic carcinoma: relationship of the clinical evaluation to organ scans. Chest 89,270-275[Abstract/Free Full Text]
  62. Ichinose, Y, Hara, N, Ohata, M (1989) Preoperative examination to detect distant metastasis is not advocated for asymptomatic patients with stages I and II non-small cell lung cancer. Chest 96,1104-1109[Abstract/Free Full Text]
  63. Grant, D, Edwards, D, Goldstraw, P (1988) Computed tomography of the brain, chest, and abdomen in the preoperative assessment of non-small cell lung cancer. Thorax 43,883-886[Abstract]
  64. Salbeck, R, Grau, HC, Artman, H (1990) Cerebral tumor staging in patients with bronchial carcinoma by computer tomography. Cancer 66,2007-2011[CrossRef][ISI][Medline]
  65. Salvatierra, A, Baamonde, C, Llamas, JM, et al (1990) Extrathoracic staging of bronchogenic carcinoma. Chest 97,1052-1058[Abstract/Free Full Text]
  66. Sider, L, Horejs, D (1988) Frequency of extrathoracic metastases from bronchogenic carcinoma in patients with normal sized hilar and mediastinal lymph nodes on CT. AJR Am J Roentgenol 15,893-895
  67. Quint, LE, Tummala, S, Brisson, LJ, et al (1996) Distribution of distant metastases from newly diagnosed non-small cell lung cancer. Ann Thorac Surg 62,246-250[Abstract/Free Full Text]
  68. Chapman, GS, Kumar, D, Redmond, J, III, et al (1984) Upper abdominal computerized tomography scanning in staging non-small cell lung carcinoma. Cancer 54,1541-1543[CrossRef][ISI][Medline]
  69. Doyle, PT, Weir, J, Robertson, EM, et al (1986) Role of computed tomography in assessing "operability" of bronchial carcinoma. BMJ 292,231-233
  70. Kormas, P, Bradshaw, JR, Jeyasingham, K (1992) Prospective computer tomography of the brain in non-small bronchial carcinoma. Thorax 47,106-108[Abstract]
  71. Tarver, RD, Richmond, BD, Klatte, EC (1984) Cerebral metastases from lung carcinoma: neurologic and CT correlation. Radiology 153,689-692[Abstract/Free Full Text]
  72. Edelman, RR, Warach, S (1993) Magnetic resonance imaging. N Engl J Med 328,708-716[Free Full Text]
  73. Cole, FH, Thomas, JE, Wilcox, B, et al (1994) Cerebral imaging in the asymptomatic preoperative bronchogenic carcinoma patient: is it worthwhile? Ann Thorac Surg 57,838-840[Abstract]
  74. Nielsen, ME, Heaston, DK, Dunnick, NR, et al (1982) Preoperative CT evaluation of adrenal glands in non-small cell bronchogenic carcinoma. Am J Radiol 139,317-320[Abstract/Free Full Text]
  75. Burt, M, Heelan, RT, Coit, D, et al (1994) Prospective evaluation of unilateral masses in patients with operable non-small cell lung cancer. J Thorac Cardiothorac Surg 107,584-589
  76. Mitchell, DR, Crovello, M, Matteuci, T, et al (1992) Benign adrenocortical masses: diagnosis with chemical shift MR imaging. Radiology 185,345-351[Abstract/Free Full Text]
  77. Jacobson, AF, Cronin, EB, Stomper, PC, et al (1990) Bone scans with one or two abnormalities in cancer patients with no known metastases: frequency and serial scintigraphic behavior of benign and malignant lesions. Radiology 175,229-232[Abstract/Free Full Text]
  78. Gaer, JAR, Goldstraw, P (1990) Intraoperative assessment of nodal staging at thoracotomy for carcinoma of the bronchus. Eur J Cardiothoracic Surg 4,207-210[Abstract]
  79. Asamura, H, Nakayama, H, Kondo, H, et al (1996) Lymph node involvement, recurrence, and prognosis in resected small, peripheral, non-small cell lung carcinomas: are these carcinomas candidates for video-assisted lobectomy? J Thorac Cardiovasc Surg 111,1125-1134[Abstract/Free Full Text]
  80. Ishida, T, Yano, T, Maeda, K, et al (1990) Strategy for lymphadenectomy in lung cancers three centimeters or less in diameter. Ann Thorac Surg 50,708-713[Abstract]
  81. Martini, N, Bains, MS, Burt, ME, et al (1995) Incidence of local recurrence and second primary tumors in resected stage I lung cancer. J Thorac Cardiovasc Surg 109,120-129[Abstract/Free Full Text]
  82. Thomas, P, Rubinstein, L (1990) Cancer recurrence after resection: T1N0 non-small cell lung cancer. Ann Thorac Surg 49,242-247[Abstract]
  83. Bollen, ECM, van Duin, CJ, Theunissen, PHMH, et al (1993) Mediastinal lymph node dissection in resected lung cancer: morbidity and accuracy of staging. Ann Thorac Surg 55,961-966[Abstract]
  84. Izbicki, JR, Passlick, B, Karg, O, et al (1995) Impact of radical systematic mediastinal lymphadenectomy on tumor staging in lung cancer. Ann Thorac Surg 59,209-214[Abstract/Free Full Text]
  85. Nakahara, K, Fujii, Y, Matsumura, A, et al (1993) Role of systematic mediastinal dissection in N2 non-small cell lung cancer patients. Ann Thorac Surg 56,331-336[Abstract]



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