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(Chest. 2004;125:1424-1430.)
© 2004 American College of Chest Physicians

Association Between Lower Lobe Location and Upstaging for Early-Stage Non-small Cell Lung Cancer*

Ana T. Rocha, MD, MHS; Meg McCormack, PA-C; Gustavo Montana, MD and Gilbert Schreiber, MD, PhD

* From the Division of Pulmonary Medicine (Dr. Rocha and Ms. McCormack), Department of Radiation Oncology (Dr. Montana), Duke University Medical Center, Durham, NC; and Division of Pulmonary Medicine (Dr. Schreiber), University of Utah Health Sciences Center, Salt Lake City, UT.

Correspondence to: Gilbert Schreiber, MD, PhD, FCCP, Associate Professor of Medicine, University of Utah Health Sciences Center, Division of Pulmonary Medicine, 26 North 1900 East, Salt Lake City, UT 84132-4701; e-mail: Gilbert.Schreiber{at}hsc.utah.edu


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Study objective: To identify factors associated with a misclassification of the true disease stage by comparing the differences between the clinical and pathologic stage of patients with early-stage non-small cell lung cancer (NSCLC).

Design: A prospective cohort study.

Setting: A multidisciplinary thoracic oncology clinic at a university-affiliated Veterans Affairs medical center.

Patient population: One hundred nine male veterans with clinical stage I/II NSCLC who had undergone thoracotomy with systematic lymph node dissection.

Methods: Prospective data were collected on all patients between September 1997 and April 2002. Logistic regression analysis was used to establish the odds ratio (OR) for predictors of changes in stage.

Results: A stage misclassification was found in 35.8% of patients (39 of 109 patients) after thoracotomy with lymph node dissection, and all but one patient were upstaged. Unsuspected nodal involvement (N stage) resulted in the upstaging of 16.5% of the patients, a change in tumor stage (T stage) resulted in the upstaging of 13.8% of the patients, a change in both stages resulted in the upstaging of 2.7% of patients, and the designation of metastatic disease resulted in the upstaging of 1.9% of the patients. The rate of unsuspected mediastinal lymph node involvement (pathologic stage N2) was 8.3% (9 of 109 patients), despite negative mediastinoscopy findings. Complete anatomic resection was performed in all patients. Advanced disease was found in 8.3% of the patients (9 of 109 patients) [stage IIIB or IV]. Having the primary tumor in a lower lobe location was the only statistically significant factor associated with upstaging (OR, 3.56; 95% confidence interval, 1.4 to 9.1). The effect of location was robust after controlling for tumor size and the prior performance of mediastinoscopy. Patient age, smoking history, weight loss, tumor size, and tumor histology were all found not to be associated with upstaging.

Conclusion: A lower lobe tumor location in patients with early-stage NSCLC appears to be associated with upstaging after surgery. We conclude that a tumor location in a lower lobe deserves special attention.

Key Words: interdisciplinary communication • lung neoplasm • mediastinoscopy • neoplasm staging • prospective studies • risk factors • tomography


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Non-small cell lung cancer (NSCLC) is the most common histologic type of lung cancer and accounts for approximately 75 to 85% of all newly diagnosed lung neoplasms.1 Once the tissue diagnosis has been established, the workup focuses on the most accurate assessment of the extent of the disease.2 This is because surgical resection offers a promise for cure in those patients with early-stage lung cancer who do not show involvement of the mediastinal lymph nodes or distant disease. Even though the combined surgical and pathologic stage using the TNM system (pTNM) defines the disease most accurately, ascertaining the clinical stage using the TNM system (cTNM) is a crucial step in the decision to recommend that the patient undergo a potentially curative resection. The cTNM combines the interpretation of the patient’s history, physical examination findings, laboratory data, chest radiograph findings, and the chest CT scan findings, including imaging of the adrenal glands. Additional imaging studies (eg, brain CT scan, bone scan, and positron emission tomography [PET] imaging) may be warranted on the basis of clinical findings to delineate the nature of distant disease.2

The clinical evaluation of the stage largely depends on the interpretation of the chest CT scan images. Chest CT imaging is the most widely available noninvasive staging modality for lung cancer and often guides the choice of additional, more invasive steps. However, CT imaging for the clinical staging of lung cancer has limitations with respect to its test performance characteristics. The accuracy of CT imaging for metastatic disease in the thorax has been evaluated extensively, from the standpoints both of selecting the patient and of using the nodal station as the unit of analysis.34567 Despite improvements in chest CT scan resolution over the last decade, its accuracy for the evaluation of nodal disease in the mediastinum has not improved (sensitivity, 57%; specificity, 82%).8 In addition, chest CT scanning lacks reliability for the prediction of direct tumor invasion into the chest wall or into mediastinal structures (T3 and T4 involvement), with a false-negative rate of 18% and a false-positive rate of 32%.9

Our prospective, cohort study focused on the identification of factors associated with a misclassification of the true stage by comparing the cTNM with the pTNM of veterans with early-stage NSCLC (cN0, cN1) who were evaluated in a large multidisciplinary thoracic oncology clinic (MTOC).


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Patients and Data Collection
Prospective clinical data were collected on all patients referred to the MTOC at the Durham Veterans Affairs Medical Center from September 1997 to April 2002. The study included only patients with early, clinical stage I/II (cN0, cN1) NSCLC who were deemed to be candidates for surgical resection. Patients with radiographic evidence of cN2 disease were excluded from this analysis. Also excluded were patients with early-stage, clinical NSCLC whose lung function or comorbidities precluded surgical resection or who declined surgery because of personal preferences.

Demographic information, imaging findings, diagnostic study findings, pulmonary function test results, clinical and pathologic staging, types of treatments, lead times to diagnosis and therapy, and follow-up information were prospectively collected. Information on the tumor size and its location was based on the interpretation of the last chest CT scan obtained immediately before undergoing thoracotomy. Survival information was obtained through the medical records system and/or from the National Death Registry at the end of the observation period. All data were purged of personal identifiers before analysis. The data collection was approved by the local institutional review board.

Determination of Clinical Stage and Treatment Triage
The MTOC physicians determined the cTNM using thorough patient history information, physical examination findings, baseline laboratory test results (ie, CBC count, chemistry studies, liver function tests, and lactate dehydrogenase and serum calcium measurements), chest radiograph studies, and the findings of chest CT scans that included imaging of the adrenal glands. A short-axis transverse lymph node diameter of > 1 cm on the chest CT scan was used as the threshold for defining abnormal lymph node enlargement.10

The MTOC team included a pulmonologist, a radiation oncologist, a medical oncologist, and a radiologist. Treatment decisions were made in the presence of the thoracic surgeon after a review of the imaging studies and tissue diagnosis with the radiologist and the lung pathologist. All involved members reached a consensus regarding further diagnostic workups and therapeutic interventions. All patients underwent surgical exploration and systematic lymph node dissection, and had pTNM ascertained. Their final stage was determined through a careful review of the operative findings and the pathology report. The cTNM was directly compared with the pTNM to determine possible disparities.

Statistical Analysis
Continuous variables were analyzed using the Student t test, and categoric variables were analyzed by {chi}2 test. The Karnofsky performance status was split into the following two performance categories: normal to mildly reduced (80 to 100%); and moderately to severely reduced (<= 70%).11 Logistic regression was used to define the odds ratio (OR) for predictors of upstaging or downstaging after surgical exploration and to control for confounders. The survival time was calculated as the time from the date of diagnosis to the date of death or to the end of the observation period. Survival was evaluated only as the proportion of patients who were alive at the end of the observation period and were compared using a {chi}2 test because of the variable length of follow-up and the small number of patients in some stage groups.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
One hundred nine male patients with early, clinical stage (I/II) NSCLC were identified. All patients had pTNM determined at the time of thoracotomy.

The patients’ characteristics are outlined in Table 1 . Twenty-five patients (22.9%) were African-American and 84 (77.1%) were white. The mean (± SD) smoking history was 68.4 ± 40.2 pack-years. As expected for surgical candidates, the patient cohort had a good performance status (Karnofsky status, 100 to 80% [93.6%]) and adequate airway mechanics (mean FEV1, 61 ± 18% of predicted) to tolerate surgical resection. The predominant tumor location was in the upper lobes (78.0%). The breakdown of the group by tumor histology was as follows: adenocarcinoma, 42 patients (38.5%); squamous cell carcinoma, 51 patients (46.8%); large cell carcinoma, 11 patients (10.1%); and NSCLC not subtyped, 5 patients (4.6%) [Table 1].


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  		Table 1. Characteristics of All Patients With Clinical Early-Stage NSCLC Who Underwent Systematic Lymph Node Dissection at Thoracotomy*

 
In 64.2% of the patients (70 of 109 patients), the cTNM corresponded with the pTNM. Only one patient (0.9%) was downstaged, and 38 patients (34.9%) were upstaged. For the statistical analysis the single downstaged patient was grouped together with those patients without stage alterations and compared to the patients who required upstaging after surgery. Table 2 compares the characteristics of patients without stage disparities with those patients who were upstaged at the time of thoracotomy. Of the 38 patients whose disease was upstaged, unsuspected nodal involvement (N stage) was responsible for upstaging in 16.5% of the patients (18 of 109 patients), and more extensive tumor stage (T stage) was responsible for upstaging in 13.8% of the patients (15 of 109 patients). Changes in both T stage and N stage were responsible for upstaging in two patients with cTNM IA and in one patient with cTNM IB. Two patients with cTNM IA were identified by PET imaging as having potential metastatic spread of tumor to a different lung lobe. However, synchronous disease was confirmed through surgical exploration. None of the patients with clinically suspected N stage (stages IIA/IIB) were upstaged, and one patient with cTNM IIB disease was downstaged to stage IIA. An average of 4.4 nodes per patient (range, 2 to 8 nodes) were sampled in those patients whose disease was upstaged because of an underestimated T stage, whereas an average of 3.3 nodes (range, 1 to 6 nodes) were sampled in those with unsuspected N stage.


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  		Table 2. Clinical Characteristics of Same Stage vs Upstaged Patients*

 
Although lung tumors were found, as expected, more frequently in the upper lobes (78.0%), tumors in the lower lobes were significantly more likely to be upstaged after surgery than were upper lobe tumors (58.3% vs 28.2%, respectively; p < 0.006) [Fig 1 ]. The effect of location was robust after controlling for the size of the lesion and for the performance of mediastinoscopy before the thoracotomy (OR, 3.56; 95% confidence interval, 1.4 to 9.1; p < 0.01). The patient age, smoking history, weight loss, tumor histology, and tumor size were not associated with upstaging (Table 3 ). An increase in T stage was responsible for upstaging in 64.3% of lower lobe tumors and in 36.0% of upper lobe tumors, whereas nodal disease resulted in upstaging of 35.7% of lower lobe tumors and 64.0% of upper lobe tumors, but the difference was not statistically significant. A central tumor location was found in 16.7% of T-stage misclassifications (3 of 18 patients) and 23.8% of N-stage misclassifications (5 of 21 patients). In the nine patients with lower lobe tumors and T-stage alterations, six tumors were peripheral (underestimation in tumor size [T1 to T2], one tumor; invaded the visceral pleura [T2], two tumors; invaded the chest wall [T3], three tumors; and central invasion, three tumors [two involved the carina/trachea (T40), and one invaded the mediastinum (T4)]). Of the 38 patients whose disease was upstaged, 5 ultimately were found to have stage IB, 2 to have stage IIA, 13 to have stage IIB, 9 to have stage IIIA, 7 to have stage IIIB, and 2 to have stage IV (Table 4 ). Overall, 23.7% of patients whose disease was upstaged (9 of 38 patients), or 8.3% of all patients (9 of 109 patients) had unresectable tumors (stages IIIB or IV).



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  		Figure 1. Percentage of upstaged patients with lower lobe and upper lobe tumors.

 

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  		Table 3. Factors Related to Upstaging After Thoracotomy*

 

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  		Table 4. Reasons for Upstaging After Thoracotomy With Lymph Node Dissection*

 
Survival for the short follow-up interval available was not significantly different between patients without changes in stage and those whose disease was upstaged. Seventy-six percent of the patients whose disease was upstaged and 71% of patients without a change in stage were alive at the end of this analysis (Table 2).


   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
Accurate staging for patients with NSCLC is essential not only to allow potentially curative resection whenever possible but also to avoid unnecessary surgery in patients who will not benefit from it. We found a stage misclassification in 35.8% of patients with clinical, early-stage NSCLC (cN0, cN1), and most of those (94.7%) were upstaged at the time of surgery. We suspected that N stage would be responsible for upstaging in the majority of patients with early-stage NSCLC. Indeed, 16.5% of patients were upstaged because of unsuspected N stage, but 13.8% were upstaged solely because of a change in the T stage. As expected, over two thirds of lung cancers originated in the upper lobes, but lower lobe tumors were significantly more likely to be upstaged than were upper lobe tumors (58.3% vs 28.2%, respectively; p < 0.006). This observation was independent of both the tumor size and the performance of mediastinoscopy before surgery. Lower lobe tumors were more often upstaged because of a more advanced T stage than because of unsuspected N stage. The explanation for this observation was radiographically unapparent pleural or chest wall invasion of peripherally located tumors, or unsuspected involvement of the central airway or mediastinal structures (Fig 2 ). These findings emphasize the fact that current chest CT imaging technologies are not satisfactory for the evaluation of involvement of the pleura, chest wall, or mediastinum.9 MRI has not shown any advantage over chest CT imaging in detecting chest wall or mediastinal tumor invasion, except for the prediction of vascular and brachial plexus involvement by Pancoast tumors.5121314 Similarly, PET imaging does not offer added benefit in this situation because of its poor spatial resolution.



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  		Figure 2. Distribution of stage and tumor location in patients with clinical stage I/II NSCLC after pathologic staging (pTNM).

 
The presence of unsuspected stage N1 disease has no immediate clinical relevance for surgical management, although it ultimately affects local recurrence rates and 5-year survival rates.1516 Patients with stage N1 disease remain surgical candidates. The potential benefit of neoadjuvant therapy in this setting is at this time speculative and subject to ongoing trials in the United States and Europe.

The accurate diagnosis of nodal disease in the mediastinum (stage N2 or N3 disease) is more relevant from a management perspective because of the impact on surgical resectability. The appropriate staging modality for patients without radiographic evidence of mediastinal lymph node enlargement, as documented in our patient cohort (cN0, cN1), remains controversial. The current practice differs widely from the routine performance of mediastinoscopy before thoracotomy to no prior mediastinoscopy, regardless of the size and location of the primary tumor. PET imaging has emerged as a functional noninvasive staging modality with higher sensitivity (84%) and specificity (89%) than chest CT scanning (57% and 82%, respectively) for the diagnosis of mediastinal involvement.817 However, the technology is hampered by its lack of spatial resolution, its false-positive rate due to reactive nodal disease, and its inability to reliably detect early, small-size tumor foci. A recent prospective study18 on the role of PET imaging for mediastinal staging of NSCLC demonstrated false-negative PET results in 5.5% of patients (22 of 400 patients). More importantly, the false-negative results were found almost exclusively at the level of the subcarina (level 7) and the aortopulmonary window (level 5/6), two crucial stations.18 High PET uptake may be helpful in directing nodal biopsies but requires tissue confirmation, most often through mediastinoscopy.19

Even surgical staging through cervical mediastinoscopy, which is considered to be the "gold standard" for the evaluation of the mediastinum, has limited sensitivity. Although mediastinoscopy allows the inspection and biopsy of nodes of the superior mediastinum with a sensitivity ranging from 88 to 94%,202122 some poorly accessible areas, including the subcarinal nodes, the paraesophageal nodes, and the nodes of the inferior ligament, are responsible for false-negative results. Nodes that are not accessible by mediastinoscopy account for half of all false-negative results.20232425 Lower lobe tumors show more frequent spread to the subcarinal station than upper lobe disease, and the sampling of subcarinal nodes as "sentinel" stations has been strongly advocated in patients with early-stage lower lobe disease.2627 Unfortunately, mediastinoscopy can only sample the anterior portion of the subcarinal level adequately, resulting in a limited sensitivity for this crucial station. The yield is even lower for nodes with negative CT scan findings when the tumor burden is small. Endoscopic esophageal ultrasound with fine-needle aspiration may be a helpful diagnostic adjunct in these situations, given its access to posterior subcarinal and aortopulmonary nodes.8 However, the test performance characteristics of endoscopic esophageal ultrasound with fine-needle aspiration have not been defined for nonenlarged nodes with negative CT scan findings.

The average rate of unsuspected pathologic stage N2 involvement in patients with a radiographically negative mediastinum has been reported to be 14% (range, 7 to 24%), irrespective of the different strategies toward the performance of mediastinoscopy.25282930313233 Using an aggressive approach to invasive surgical staging, our data showed a low 8.3% rate (9 of 109 patients) of unsuspected stage N2 disease at the time of surgery. If their disease had been accurately staged prior to surgical resection, these patients would have undergone neoadjuvant treatment. Most notably, all of these patients had a false-negative mediastinoscopy finding prior to surgery. The false-negative rate is explained by the sampling error as a result of the small tumor burden in nodes with negative CT scan findings. Therefore, it is not surprising that a complete anatomic resection was technically feasible in all cases.

PET imaging was performed in only 22.9% of our patients (25 of 109 patients). The use of PET imaging in this study was restricted because of the prohibitive costs, the inherent lack of anatomic resolution, and the unclear reliability for small nodes with negative CT scan findings. Patients who underwent PET imaging in our study were either part of a separate Veterans Affairs Cooperative Studies Program (ie, CSP 27) on the evaluation of single pulmonary nodules or required special diagnostic considerations (ie, the presence of an additional, indeterminate nodule in a different lobe). Thirty-six percent of patients (9 of 25 patients) with PET imaging studies were ultimately upstaged. PET imaging suggested a spread to additional lung lobes in the two patients who ultimately proved to have synchronous disease and who were still considered to be suitable candidates for surgical resection.

Overall, 8.3% of our patients (9 of 109 patients) were unresectable at the time of thoracotomy (stage IIIB disease, 7 patients; stage IV disease, 2 patients). Most patients had tumor invasion in the mediastinum or central airway that was not apparent.

There are limitations to this study. First, the study population consisted exclusively of male veterans and did not reflect the rising trend toward lung cancer in women. The male predominance in our study is also responsible for the high rate of squamous cell carcinoma as histologic subtype. Second, we limited our study to patients with radiographic early-stage NSCLC (cN0, cN1). We therefore cannot comment on the false-positive rate of lymph node involvement seen on chest CT imaging. Third, this study does not address the potential value of PET imaging prior to invasive staging for radiographically negative mediastinal nodes. But because of its dependence on both, the intensity of tracer uptake and the size of the lesion, PET imaging has obvious limitations in detecting very small tumor foci. Fourth, our observation of an association between lower lobe location and underestimation of the true disease stage deserves confirmation in larger series of patients with early-stage lung cancer. Finally, because of the short follow-up time and the small number of patients in some staging groups, we could not make inferences about the effects of clinical misclassification on the long-term survival of our cohort.

In summary, we found that, despite an aggressive approach to invasive surgical staging, over one third of patients with clinical, early-stage NSCLC (cN0, cN1) required upstaging after surgery. The rate of unsuspected pathologic stage N2 involvement was 8.3%, despite negative mediastinoscopy findings. Inoperable, advanced stage disease was found in an additional 8.3% of patients, which was mostly related to more extensive local tumor invasion. Patients with a lower lobe location of their cancer had a higher chance of being upstaged than those with a tumor location in an upper lobe. The effect of location was robust after controlling for tumor size and performance of mediastinoscopy before surgery. We conclude that a tumor location in a lower lobe deserves caution. A confirmation of these findings in a larger group of patients would be desirable.


   Footnotes
 
Abbreviations: cTNM = clinical stage using the TNM system; MTOC = multidisciplinary thoracic oncology clinic; N stage = nodal involvement; NSCLC = non-small cell lung cancer; OR = odds ratio; PET = positron emission tomography; pTNM = pathologic stage using the TNM system; T stage = tumor stage

Received for publication April 17, 2003. Accepted for publication November 11, 2003.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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