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Ann Thorac Surg 1999;68:1154-1158
© 1999 The Society of Thoracic Surgeons

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Original Articles

Prospective comparison of radiologic, thoracoscopic, and pathologic staging in patients with early non-small cell lung cancer

^a Section of Surgical SciencesVanderbilt University Hospital, Nashville, Tennessee, USA
^b Department of Cardiac and Thoracic Surgery, Vanderbilt University Hospital, Nashville, Tennessee, USA
^c Department of Radiology, Vanderbilt University Hospital, Nashville, Tennessee, USA

Address reprint requests to Dr Roberts, Department of Cardiac and Thoracic Surgery, 2986 The Vanderbilt Clinic, Vanderbilt University Hospital, Nashville, TN 37232
e-mail: bob.roberts{at}mcmail.vanderbilt.edu

Presented at the Forty-fifth Annual Meeting of the Southern Thoracic Surgical Association, Orlando, FL, Nov 12–14, 1998.

	Abstract

Top Abstract Introduction Material and methods Results Comment References

 
Background. More accurate staging at the time of initial presentation could improve design of clinical trials and avoid inappropriate surgical decisions in individual patients. Preresection staging of patients with non-small cell lung cancer (NSCLC) is not straightforward, especially in patients with negative mediastinal nodes. The purpose of this study was to compare the results of radiologic, thoracoscopic, and pathologic staging in patients with NSCLC and negative mediastinoscopy.

Methods. All patients with NSCLC underwent computed tomographic (CT) scanning before surgical staging with mediastinoscopy. Patients with negative mediastinoscopy then underwent thoracoscopic staging with examination of pleural surfaces, and identification of T (visceral and parietal pleural invasion, sampling of pleural fluid, and pleural lavage) and N (intraparenchymal and inferior mediastinal nodal sampling, if possible) stage descriptors before resection.

Results. Thoracoscopy was more accurate than CT scanning in the staging of 50 patients with early lung cancer (stages IA, IB, IIA, and IIB), especially as regards T stage. Further, thoracoscopic examination ruled out malignant pleural effusions in 7 (14%) patients with radiologically obvious effusions, and identified radiologically silent malignant pleural effusions in 3 (6%) patients. Chest wall invasion was accurately identified at thoracoscopy in most patients. Finally, 3 patients with T1 lower lobe lesions and negative mediastinoscopy were found to have involvement of inferior mediastinal nodes (level 8 or 9) at thoracoscopy. However, thoracoscopy did not allow sampling of aortopulmonary window nodes in some patients with bulky left upper lobe lesions.

Conclusions. Errors in thoracoscopic staging resulted in no inappropriate operations. However, errors in CT staging would have resulted in operations unlikely to help the patients, or would have inappropriately excluded patients from surgery. Thoracoscopic staging was more accurate than CT staging in this cohort of patients with NSCLC and negative mediastinoscopy.

	Introduction

Top Abstract Introduction Material and methods Results Comment References

 
Surgical resection remains the mainstay of therapy of lung cancer, especially for earlier stage malignancy. However, the 5-year survival for patients with any, but the earliest stage of malignancy remains poor. Mountain found that resected clinically staged IA tumors (T1N0M0) had a 61% 5-year survival, while clinically staged IB tumors (T2N0M0) had only 38% survival [1]. The survival for pathologically staged tumors was significantly better (pT1N0M0 = 67% at 5 years and pT2N0M0 = 57% at 5 years), indicating the significant inherent inaccuracy in clinical staging, which in this series was generally based on CT scanning. These results were reflected in Japanese studies [2]. Naruke and associates found that clinical stage I tumors had 50.1% 5-year survival, while pathological stage I tumors had 65.0% survival. Similarly, clinical stage II tumors had 31.2% 5-year survival, while pathologic stage II tumors had 42.9% survival. The data for all large series are consistent; striking differences between clinical and pathologic staging indicate inaccurate clinical staging.

Most research in preoperative clinical staging has been directed toward determining the status of mediastinal nodes (or the N descriptor), whether diagnosed by mediastinoscopy, computed tomographic (CT) scanning, or positron emission tomography (PET) scanning. There has been little evaluation of the relative accuracy of staging of the T descriptor. We undertook this study to determine whether another surgical staging method, thoracoscopy, would be more accurate than CT scanning in the staging of early stage non-small cell lung cancer (NSCLC). We postulate that this increased accuracy would allow better selection of patients likely to benefit from surgery and better stratification of patients enrolled in future clinical trials.

	Material and methods

Top Abstract Introduction Material and methods Results Comment References

 
All patients (n = 50, 35 men and 15 women) with NSCLC and negative mediastinoscopy referred between October 1, 1997 and September 1, 1998 were included in this prospective study. Our routine is to perform mediastinoscopy on all patients with proven NSCLC. A single surgeon performed surgical staging and resection. All patients were staged preoperatively with CT scanning of the chest and upper abdomen. Patients with symptoms of headache underwent head CT scanning, and patients with any symptoms that could be considered bone pain underwent bone scanning.

If there was no evidence of metastatic disease, patients underwent mediastinoscopy with sampling of bilateral paratracheal and subcarinal nodes. Patients with left upper lobe cancers underwent either anterior mediastinoscopy or thoracoscopic sampling of the aortopulmonary (AP) nodes. Positive AP window nodes eliminated the patient from the study, as these nodes were considered mediastinal nodes. If all nodes were benign, patients subsequently underwent thoracoscopic staging.

Thoracoscopic staging was performed by examination through a port in the anterior axillary line in the seventh intercostal space. The pleura was carefully examined for lesions, any significant pleural fluid aspirated for cytology, and pleural lavage performed with 200 cc normal saline with 10,000 U of heparin. Immediate cytology results were available; if positive or suspicious, the surgery was aborted or delayed, respectively. For lower lobe lesions, inferior mediastinal nodes (levels 8 and 9) were always sampled. Intraparenchymal or fissure nodes were sampled when possible, but could only be identified in a minority of patients. Paratracheal and subcarinal nodes were not sampled unless they appeared pathologic at thoracoscopy.

Large masses were carefully examined to determine whether chest wall invasion was found, whether mediastinal invasion was demonstrated, and, if so, whether mediastinal fat or pericardium were involved (lesions generally completely resectable), or whether aorta, esophagus, or vertebrae were involved (lesions generally not completely resectable). All patients with previously identified pleural effusions underwent thoracentesis before surgery.

Patients without N2 disease or malignant effusions underwent complete resection and lymphadenectomy. A range of procedures was necessary for complete resection, including video-assisted segmentectomy or lobectomy, open lobectomy, sleeve lobectomy, lobectomy and pericardiectomy, lobectomy and chest wall resection, and pneumonectomy.

Data are presented as patients who were understaged, accurately staged, or overstaged by CT and thoracoscopy, respectively. For the purposes of statistical analysis, the proportions of patients correctly and incorrectly staged were compared using ² analysis.

	Results

Top Abstract Introduction Material and methods Results Comment References

 
Fifty patients (within 12 months at Vanderbilt University Hospital) had negative mediastinoscopy and complete CT scanning of chest and upper abdomen before thoracoscopic staging. Their mean age was 66.9 ± 11.1 years, and ranged from 45 to 90 years. Thirty patients underwent lobectomy, 2 had segmentectomy, 3 had pneumonectomy, 4 had lobectomy and pericardiectomy, 4 had lobectomy and chest wall resection, and 4 had sleeve lobectomies. Three patients underwent staging procedures only, either because they were found to have malignant pleural effusions or involvement of inferior mediastinal nodes. Three patients developed pneumonia. There were no complications directly attributed to thoracoscopic staging. The 30-day mortality was zero, though 1 patient died of an Aspergillus empyema at 85 days.

The percentage of patients understaged, correctly staged, and overstaged by CT scanning were 30%, 42%, and 28%, respectively, and for thoracoscopic examination were 14%, 86%, and 0%, respectively, with pathologic stage as the benchmark. The difference in the percentage of correctly staged patients (by ² analysis) was highly significant (p = 0.00000458). In those patients found to have radiographically silent malignant pleural effusions (stage IIIB) or involvement of inferior mediastinal nodes (IIIA), the stage determined by thoracoscopy was considered the final stage. Thoracoscopic examination was found to be more accurate than CT scanning in terms of agreement with final pathologic staging when ² analysis was used to compare the proportions of correct and incorrect staging.

Figure 1 depicts the types of errors found with each technique. A total of six pathologic stage I tumors were overstaged by CT: four tumors with bulky mediastinal nodes on CT found to be stage I tumors; one large pleural effusion that was reactive; and one tumor read to have chest wall invasion that did not. Thirteen patients with pathologic stage II lesions were inaccurately staged: 7 read as stage I lesions on CT; 2 as having mediastinal node involvement that did not; 3 as having malignant pleural effusions, and 1 as having an intraparenchymal met. Two patients with pathologic stage II lesions were incorrectly assigned to stage I at thoracoscopy, both with involved hilar nodes.

View larger version (26K): [in this window] [in a new window]   Fig 1. Errors in staging: the number of patients (out of a total of 50) who were inaccurately staged by CT or thoracoscopy are shown. The inaccurate clinical stage is presented on the left, and the accurate pathologic stage on the right.

T status
The percentage of patients understaged, correctly staged, and overstaged for T status by thoracoscopy was 0%, 96%, and 4%, respectively, and for CT scanning was 24%, 56%, and 20%, respectively, compared with pathologic staging. The difference in the percentage of correctively staged patients (by ² analysis) was highly significant (p = 0.00000283). Thoracoscopy was extremely accurate in identifying the appropriate final pathologic T stage. Of the 50 patients, only 2 were inaccurately T-staged by thoracoscopy: one lesion read as a T3 at thoracoscopy was found to be a T2 at pathology, and one lesion read as a T2 at thoracoscopy was ultimately read as a T1 at pathology (Fig 1). Neither of these errors changed therapy. In contrast, CT scanning both understaged and overstaged tumors in terms of T status, with any inaccurate stage as likely to be overstaged as understaged. The difference in the accuracy of staging between thoracoscopy and CT scanning was highly significant (p = 2.83 x 10^-6 by ² analysis when proportions of accurate T stage were compared with proportions of inaccurate T stage).

Further, dependence upon CT scanning alone would have resulted either in unnecessary surgery (in the 3 patients who were found to have malignant pleural effusions) or in denying surgery to patients that would benefit (in the 3 patients who were described on CT scanning to have malignant effusions and the 6 other patients who were described as having unresectable mediastinal invasion). In total, 12 of 50 patients (24%) had major changes in operative decision making (whether or not surgery was possible) that depended upon thoracoscopy. Several others had minor changes in operative decision making (whether posterolateral thoracotomy or muscle-sparing thoracotomy) that depended upon thoracoscopy.

Thoracoscopic lavage was successfully completed in 38 of 50 patients. Six were positive, while 32 were negative. Because there are no clear guidelines for the treatment of patients with positive pleural lavage, and positive lavage does not figure into the staging, these data were collected, but patients were treated without regard to it.

N status
At thoracoscopy, lymphadenectomy was not done, but inferior mediastinal nodes (levels 8 and 9) were always sampled for lower lobes and a search was made for N1 nodes for all lesions. While not as accurate as T staging, thoracoscopy was more accurate than CT scanning for nodal disease. The percentage of patients understaged, correctly staged, and overstaged for N status by CT scan was 26%, 50%, and 24%, respectively, and by thoracoscopy + mediastinoscopy was 26%, 74%, and 0%, respectively. The difference in the percentage of correctly staged patients (by ² analysis) was significant (p = 0.013), though less so than for T staging. Two patients with lower lobe lesions and negative subcarinal nodes at mediastinoscopy were found to have involvement of inferior mediastinal nodes. Both were started on chemotherapy; one subsequently developed distant metastases and the second is completing chemotherapy before planned resection. Several other patients had enlarged nodes on CT that proved to be benign at resection. These patients were also correctly staged by thoracoscopy.

Problems with thoracoscopic staging
Though the AP window can usually be easily sampled via thoracoscopy, 2 patients presented with bulky left upper lobe lesions that did not allow access to the AP window. They subsequently had anterior mediastinotomy to stage the AP window.

	Comment

Top Abstract Introduction Material and methods Results Comment References

 
Controversy about radiographic versus surgical staging of lung cancer is not new. CT scans are obtained routinely by most chest surgeons to plan their resections, and a striking number still use a 1-cm nodal size as the threshold for likely involvement with malignancy. Nonetheless, the topic has been studied extensively, and radiologic staging has generally been found to be considerably less accurate than mediastinoscopy at staging the mediastinum, and the 1-cm threshold misleading, at best.

Patterson and associates performed a prospective evaluation of magnetic resonance imaging (MRI), CT, and mediastinoscopy in the preoperative assessment of mediastinal node status in bronchogenic carcinoma, and found both MRI and CT to be less accurate than mediastinoscopy [3]. Izbicki and associates studied 108 patients and found that CT scans predicted the final pathologic stage accurately only in 58% of patients, because adenocarcinomas tended to have normal-sized tumor-positive nodes and squamous carcinomas tended to have enlarged tumor-free nodes [4]. White and associates found that CT scanning could not reliably differentiate between stage I/II and stage III tumors, whether for nodal involvement or parietal pleural involvement, and stated that "Patients should not be denied the opportunity for curative surgery on the basis of equivocal CT signs" [5]. Fernando and Goldstraw found that CT scans accurately predicted nodal involvement in 55.3% and the final stage in only 46.6% [6]. Nonetheless, surprising numbers of oncologists, thoracic surgeons included, continue to use CT scans as the bottom line for nodal involvement.

PET scanning, combined with CT scanning, has been extensively evaluated in the staging of mediastinal nodal disease and the identification of distant metastases. PET scanning can neither identify chest wall invasion nor visceral pleural invasion, and so is useless in determining the T descriptor. Nonetheless, it seems to be more accurate, when combined with CT scans, than CT alone in the staging of mediastinal nodes. Scott and associates compared PET and CT and found an accuracy of 99% [7]. Others have found somewhat less accuracy, but in general, the combination of CT and PET scanning has been found to be accurate in 90% to 93% of patients [8].

CT scanning is only marginally better in diagnosing chest wall or mediastinal invasion. White and associates found that only 19 of 45 stage III tumors were correctly identified as being stage III and resectable or unresectable [5]. By combining two separate criteria of chest wall invasion (obliteration of the extrapleural fat plane and the ratio of tumor/pleura contact and tumor diameter), Ratto and associates were able to get 86% accuracy in the prediction of actual chest wall invasion from CT scans [9]. Any of four criteria analyzed separately only gave an accuracy of 67% to 86%. Finally, Herman and associates evaluated mediastinal involvement in 90 patients who underwent thoracotomy and determined that CT scanning was insensitive in detection of mediastinal invasion by primary bronchogenic carcinoma [10].

Thoracoscopic staging has been demonstrated to be effective in identifying thoracic lymph node involvement in patients with esophageal carcinoma [11]. Champion and McKernan found that thoracoscopy was equivalent to open thoracotomy for the purposes of staging NSCLC in 17 patients who had thoracoscopy and subsequently thoracotomy [12]. Others have found that thoracoscopy can easily clarify whether effusions identified on CT scan are malignant or benign, and whether lesions abutting the mediastinum are invading it [13]. Because of these and other data, some authors have recommended routine video assisted thoracic surgery (VATS) exploration before resection of intrathoracic malignancy [14].

Our data confirm that thoracoscopy can be safely done and can clarify mediastinal invasion and sample pleural effusions previously identified on CT scan. We further found that thoracoscopy can identify malignant pleural effusions too small to be seen on CT, that chest wall invasion can be reliably determined, and that inferior mediastinal nodes (levels 8 and 9) can be sampled, and that patients with negative mediastinoscopy may nonetheless have involvement of mediastinal nodes. Our 3 patients with malignant pleural effusions avoided unnecessary surgery, and appropriate incisions were chosen for those patients with chest wall involvement. Our patients who had CT scans suspicious for mediastinal invasion were resected, and our patients with involvement of inferior mediastinal nodes received chemotherapy rather than surgery.

Preresectional staging is important because postoperative adjuvant therapy has resulted in no improvement in survival. In the 1970s, the use of postoperative alkylating agents was found to have a detrimental effect on the survival of patients with resected lung cancer [15]. Many large randomized studies in the 1970s and 1980s evaluated the benefits of postoperative cisplatin-based chemotherapy on patients with resected NSCLC. Some studies showed a slight improvement in disease-free or recurrence-free survival [16–18], but no improvement in 5-year survival. Other analyses of postoperative cisplatin-based chemotherapy showed no benefit in terms of disease-free nor long-term survival [19, 20]. Rare studies have found increased 5-year survival with postoperative chemotherapy, but these have clearly been in the minority [21, 22]. Taken together, these studies have been taken to indicate, depending upon one’s bias about chemotherapy, either that there is no benefit to postoperative chemotherapy or that there may be a 5% improvement in 5-year survival, as found by the meta-analysis [16].

Disappointing results in adjuvant studies prompted at least two significant neoadjuvant studies, with strikingly different results. Rosell and associates found a 30% improvement in 5-year survival when patients with stage IIIA disease were treated with neoadjuvant chemotherapy compared with surgery alone [23]. Roth and associates found improvement in 5-year survival from 20% to 56% when patients with stage IIIA NSCLC were treated with neoadjuvant chemotherapy [24]. Finally, Elias and the CALGB randomized 30 patients to each arm (surgery alone versus chemotherapy followed by surgery) and found no difference in survival [26].

The improved results with neoadjuvant therapy in stage IIIA patients combined with the relatively poor results with surgical resection alone in earlier stage patients have led to study of neoadjuvant therapy and resection in stages IB, IIA, and IIB by a group of 10 hospitals (the Bimodality Lung Oncology Team or BLOT trial) in an effort to determine if neoadjuvant therapy will be efficacious in this group. The BLOT study has relied upon radiologic staging, which has been shown to be inaccurate in the staging of mediastinal nodes [25]. If future therapies require neoadjuvant therapy of certain stages, but immediate resection of others, thoracoscopic techniques will be necessary to adequately stage these earlier cancers.

In summary, thoracoscopic staging should be used at least in those patients with lower lobe cancers, with pleural effusions, and with bulky tumors potentially invading unresectable structures to better determine the appropriateness and timing of surgical intervention. We now routinely perform thoracoscopic staging before all resections for NSCLC.

	Acknowledgments

 
This work was supported by the Vanderbilt-Ingram Cancer Center. Manuscript preparation assistance was provided by Debbie Poteet.

	References

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