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J Thorac Cardiovasc Surg 2006;131:988-993
© 2006 The American Association for Thoracic Surgery

General Thoracic Surgery

Clinicopathologic study of resected, peripheral, small-sized, non–small cell lung cancer tumors of 2 cm or less in diameter: Pleural invasion and increase of serum carcinoembryonic antigen level as predictors of nodal involvement

Masayoshi Inoue, MD * , Masato Minami, MD, Hiroyuki Shiono, MD, Noriyoshi Sawabata, MD, Kan Ideguchi, MD, Meinoshin Okumura, MD

Division of General Thoracic Surgery, Department of Surgery (E1), Osaka University Graduate School of Medicine, Osaka, Japan

Received for publication October 12, 2005; revisions received December 11, 2005; accepted for publication December 16, 2005.

* Address for reprints: Masayoshi Inoue, MD, PhD, 2-2 Yamadaoka Suita-city, Osaka 565-0871, Japan (Email: masa{at}surg1.med.osaka-u.ac.jp).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Discussion
 References
 
OBJECTIVE: The number of surgical interventions for small-sized lung cancer has increased with the development of computed tomography. We attempted to identify clinicopathologic characteristics of peripheral, small-sized, non–small cell lung cancer to show the limitation of partial resection or segmentectomy.

METHODS: A retrospective analysis of 143 patients who underwent a complete resection for a peripheral non–small cell lung cancer of 2 cm or less in diameter was performed. The relationships between nodal involvement and other clinical factors were also assessed in patients who underwent a lobectomy plus node dissection.

RESULTS: The overall 5-year survival rate was 88.1%. The 5-year survival rate was 100% for patients with a tumor of 1.5 cm or less. Survival for patients with adenocarcinoma histology was significantly better than for those with nonadenocarcinoma histology (P = .03). The 5-year survival rate for patients without lymph node metastases was 91.6%, whereas it was 62.5% for those with nodal involvement (P < .01). Increase of prethoracotomy serum carcinoembryonic antigen level was an independent predictor of a poor prognosis. Lymph node metastasis was significantly increased in those with pleural invasion by the primary lesion and increased serum carcinoembryonic antigen level. Fourteen (16.9%) of 83 patients with a tumor diameter of larger than 1.5 cm had nodal metastasis.

CONCLUSIONS: Nodal involvement should be considered in patients with non–small cell lung cancer of 2 cm or less in diameter who show pleural invasion or an increased carcinoembryonic antigen level. A lobectomy with node dissection is recommended for patients with a tumor larger than 1.5 cm, suspected pleural invasion, or prethoracotomy carcinoembryonic antigen level increase.

Abbreviations and Acronyms BAC = bronchioloalveolar carcinoma; CEA = carcinoembryonic antigen; CT = computed tomography; GGO = ground-glass opacity


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Discussion
 References
 
With the development of high-resolution computed tomography (CT), small-sized peripheral lung cancer has been more frequently encountered. At our institute, the ratio of resected cases with peripheral lung cancer tumors sized 2 cm in diameter or less has increased from 17.1% of all lung cancer cases in the period from 1992 through 1995 to more than 34.3% from 1996 through 1999 and 42.6% from 2000 through 2003. In addition, several reports have suggested the feasibility of a limited operation for stage I early lung cancer. 1,2 Go

Recently, bronchioloalveolar carcinoma (BAC) showing ground-glass opacity (GGO) on chest CT images was identified as an independent entity among well-differentiated adenocarcinomas. 3 Go Patients with BAC with a GGO appearance, which has been clarified to be less invasive, seldom have lymph node metastasis and usually have better outcomes compared with patients with typical adenocarcinoma. 4-6 Go Thus patients with BAC detected as a peripheral small-sized nodule could be good candidates for a limited resection. Lymph node metastasis is detected in a proportion of patients with small-sized peripheral lung cancer, even when the tumor size is smaller than 2 cm in diameter, and the risks of limited resection for these patients have been documented. 7,8 Go An inappropriate limited resection can lead to an incomplete resection or misdiagnosis of nodal staging, and such patients might miss a chance to be cured or to receive adjuvant chemotherapy, which has been shown to be effective for those with completely resected non–small cell lung cancer (NSCLC). 9 Go Thus it is important to identify the characteristics of small-sized lung cancer, including GGO lesions, to determine the appropriate operative mode for each patient.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Discussion
 References
 
Patients
The records of 565 patients with NSCLC who underwent a thoracotomy between 1992 and 2003 at Osaka University Hospital were reviewed. Of those, we analyzed 143 patients with a small-sized peripheral lesion of 2 cm or less in diameter who underwent a complete resection (Table 1). Patients treated with induction therapy or those with multiple primary lesions were excluded. Follow-up was completed in 133 of the patients, and the mean follow-up time for all was 52.1 months. We performed a lobectomy with systematic hilar and mediastinal lymph node dissection in principle. A limited resection was indicated not only for high-risk cases, including patients with low pulmonary function, cardiovascular comorbidity, advanced age, and severe diabetes mellitus, but also for patients with GGO or a peripheral lesion smaller than 1.5 cm in diameter. There were 15 compromised cases, and an intentional limited resection as a curative operation was performed in 20 patients, including 12 lesions with a GGO appearance. Preoperative staging was done with chest and abdominal CT scanning, brain magnetic resonance imaging, and bone scintigraphy. Lymph nodes larger than 1 cm in the short axis on chest CT images were defined as clinical N factor positive. Transbronchial lung biopsy or CT-guided needle biopsy was performed to obtain a histologic diagnosis. A proportion of patients with node swelling have been evaluated with fluorodeoxyglucose positron emission tomography since 1997. Postoperative staging was performed according to the TNM classification. 10 Go We defined a GGO lesion as a tumor occupied mainly by ground-glass shadows in at least two thirds of the area on thin-section CT scans and noted as a GGO lesion by the attending radiologist. Otherwise, tumors with a partial ground-glass area were included in the solid tumor category. Variables used for evaluation were age, sex, tumor size, histology, tumor density, operation mode, lymph node metastases, pleural invasion, and prethoracotomy serum carcinoembryonic antigen (CEA) level.


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  		TABLE 1. Characteristics of 143 patients with resected non–small cell lung cancer of 2 cm or less in diameter
 
Statistical Analyses
The probability of survival was calculated by using the Kaplan-Meier method. 11 Go The prognostic influence of variables on survival was analyzed with a Wilcoxon test and Cox regression. 12 Go A {chi}2 test was used to compare the ratio between 2 groups.


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Discussion
 References
 
A preoperative histologic diagnosis of lung cancer was obtained in 95 patients on the basis of results of CT-guided needle biopsy in 61 patients and transbronchial lung biopsy in 34 patients. We performed fluorodeoxyglucose positron emission tomography in 16 cases. Among those cases, 14 primary tumors showed positive uptake, and 2 were negative. Positive uptake in lymph nodes was observed in 3 cases (2 with node metastases, and 1 false-positive result), whereas negative results were shown in the remaining 13 patients (12 with no metastasis, and 1 false-negative result).

The overall 5-year survival rate for patients with peripheral NSCLC tumors of 2 cm or less in diameter was 88.1%, whereas that for patients with tumors of 1.5 cm or less was 100% and that for patients with tumors of 1.6 to 2 cm was 84% (Figure 1). Patients with a tumor of 1.5 cm or less in diameter survived longer than those with a tumor from 1.6 to 2 cm in diameter. No patient with a tumor smaller than 1 cm showed recurrence over a mean follow-up period of 43.7 months.


Figure 1
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  		Figure 1. Probability of survival for patients with peripheral non–small cell lung cancer who underwent a complete resection according to tumor size. Survival for those with tumors of 1.5 cm or less in diameter was better than for those with tumors of 1.6 to 2.0 cm in diameter.

 
According to histologic type, the 5-year survival rate for patients with adenocarcinoma was 89.8%, which was significantly better than that for patients with nonadenocarcinoma histology (P = .03, Figure 2). Patients with nonadenocarcinoma histology consisted of 14 with squamous cell carcinoma and 2 others. The 5-year survival rate for patients with a GGO lesion was 96.3%, whereas that for patients with a solid lesion was 85.1% (statistically not significant). We did not observe recurrence in any of the patients with a GGO lesion, although 1 died of respiratory failure associated with chronic constructive pericarditis. When excluding patients with GGO from the adenocarcinoma group, patients with an adenocarcinoma still showed a better survival than those with nonadenocarcinoma histology (P = .05).


Figure 2
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  		Figure 2. Probability of survival for patients with peripheral, small-sized, non–small cell lung cancer who underwent a complete resection according to histology of the primary lesion. Survival for those with adenocarcinoma histology (Ad) was significantly better than for those with nonadenocarcinoma histology (Non-Ad). Fourteen of the 16 nonadenocarcinoma cases showed squamous cell carcinoma histology.

 
There was no significant difference in survival rates between the 108 patients treated with a lobectomy and the 35 patients treated with a segmentectomy or partial resection according to operation mode. Among the 35 patients, hilar node sampling was preformed in 18 patients, and both hilar and mediastinal node dissection or sampling was performed in 5 patients, whereas the remaining 12 patients received no lymph node assessment. No metastasis was found in any of these resected nodes. The 5-year survival rate was 88.0% for patients treated with a lobectomy and 87.0% for those treated with a limited resection.

The 5-year survival rate for patients without lymph node metastasis was 91.6%, which was significantly better than for those with nodal involvement, who had a survival rate of 62.5% (P < .01, Figure 3). Pleural invasion was pathologically determined in 12 patients. The 5-year survival rate for patients without pleural involvement was 89.6%, whereas it was 75.8% for those with pleural invasion diagnosed pathologically (statistically not significant).


Figure 3
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  		Figure 3. Probability of survival for patients with peripheral, small-sized, non–small cell lung cancer who underwent a complete resection according to nodal involvement. Survival for those without lymph node metastases was significantly better than for those with nodal involvement.

 
Twenty-nine (21.8%) of 133 patients showed an increase of preoperative serum CEA levels, and their 5-year survival rate was 77.6%, which was significantly worse than the rate of 92.1% for those with a normal CEA level (P < .01, Figure 4). Multivariate analyses using tumor size, histology, CT finding (solid or GGO), lymph node metastasis, pleural invasion, and prethoracotomy serum CEA level as variables identified only CEA level as an independent prognostic factor (Table 2).


Figure 4
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  		Figure 4. Probability of survival for patients with peripheral, small-sized, non–small cell lung cancer who underwent a complete resection according to preoperative serum carcinoembryonic antigen (CEA) level. Survival for those with CEA level increase (≥5 ng/mL) was significantly worse than for those with a normal CEA level.

 

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  		TABLE 2. Multivariate analyses of potential prognostic factors in patients with resected non–small cell lung cancer of 2 cm or less in diameter
 
In addition, we analyzed the frequency of lymph node metastasis by small-sized NSCLC in 108 patients treated with a lobectomy plus systematic hilar and mediastinal node dissection. Regarding the accuracy of preoperative nodal evaluation with CT scanning, sensitivity, specificity, accuracy, positive predictive value, and negative predictive value were 18.8%, 95.6%, 84.3%, 87.1%, and 42.9%, respectively. The relationships between nodal metastasis and clinical factors are summarized in Table 3.


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  		TABLE 3. Relationship between clinical factors and lymph node metastasis in patients with small-sized non–small cell lung cancer
 
Lymph node metastasis was found in 1 (9.1%) of 11 and 1 (6.7%) of 15 patients with tumors sized less than 1 cm and from 1.1 to 1.5 cm in diameter, respectively, whereas 14 (17%) of 82 patients with a tumor larger than 1.5 cm in diameter had nodal involvement (statistically not significant). Eight patients were associated with pathologic pleural invasion, of whom 4 (50%) had nodal metastases. The ratio of metastasis-positive lymph nodes was significantly higher in patients with pleural involvement (P = .05). In addition, patients with an increased prethoracotomy serum CEA level had lymph node metastasis more frequently than those with a normal CEA level. Nodal involvement was found in 8 (10.3%) of 78 patients with normal CEA levels, whereas 7 (29.2%) of 24 with increased CEA levels had nodal metastases (P = .02). Notably, nodal involvement was observed in 6 (60%) of 10 patients with a CEA level greater than the 2-fold cutoff. We found no lymph node metastasis in patients with a GGO lesion.


   Discussion
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Discussion
References
 
In the present study we focused on patients who underwent resection of a peripheral, small-sized NSCLC tumor of 2 cm or less in diameter and identified 3 prognostic factors, adenocarcinoma histology, pathologic nodal metastases, and preoperative serum CEA level, with the latter shown to be the only independent prognostic predictor by means of multivariate analysis. We also identified pleural invasion and prethoracotomy serum CEA level increase as clinical factors related to lymph node metastasis in an analysis of patients treated with a lobectomy plus systematic node dissection. In addition, preoperative nodal staging with CT imaging for small-sized NSCLCs revealed a high specificity and positive predictive value, whereas sensitivity and negative predictive value were quite low.

Tumor size has been reported to be related to the survival of patients with stage IA NSCLC and a nodule size of less than 2 cm in diameter and has also been identified as a prognostic factor. 13 Go Survival analyses based on tumor size in patients with stage I NSCLC have shown statistically significant differences among those with tumors sized from 5 to 15 mm, 16 to 25 mm, and 26 to 36 mm. 14 Go Another report showed that tumor size was an independent prognostic factor in pN0 resected cases. 15 Go In the present study we found node metastases in one sixth of our patients with a tumor larger than 1.5 cm in diameter compared with previous studies that found lymph node metastasis in 28% of patients with tumors smaller than 2 cm, 7 Go 15% of patients with subcentimeter-sized solid tumors, 8 Go and 7% of patients with subcentimeter-sized tumors. 16 Go Thus a limited resection or omission of nodal clearance requires careful assessment of node status. For tumors larger than 1.5 cm in diameter, we recommend that a lobectomy with systematic node dissection be chosen as a general practice. These results could be part of the basic data to promote the prospective trial regarding sublobar resection for small-sized lung cancer.

Nodal staging with CT imaging was reported to show a sensitivity ranging from 50% to 81%, specificity from 56% to 94%, and accuracy from 59% to 85% in studies published in the last decade. 17-21 Go However, the accuracy of nodal staging focused on small-sized lung cancer has not been clarified. The present results revealed a high specificity and positive predictive value for evaluation of metastatic nodes by using CT scanning for small-sized NSCLC tumors compared with those for all tumors because there were few false-positive results in preoperative nodal evaluations. Thus lymph node swelling associated with small-sized NSCLCs should be considered as a sign of metastasis.

High-resolution CT scanning can sometimes detect GGO lesions. The proportion of GGO area and tumor shadow disappearance rate, calculated by using mediastinal and lung windows in the CT images, have been shown to have a correlation with patient outcome. 4,6 Go Another study reported that most pure GGO tumors smaller than 1 cm in diameter were BAC or atypical adenomatous hyperplasia, which are suitable candidates for thoracoscopic limited resection. 22 Go Furthermore, a recent prospective study concluded that limited resection procedures with intraoperative histologic diagnosis for pulmonary nodules of 2 cm or smaller were satisfactory, showed accurate diagnoses corresponding with those of frozen sections, and demonstrated no recurrence. 23 Go Because patients with GGO lesions did not show nodal involvement or postoperative recurrence in the present study, we can propose a limited resection for patients with NSCLC with GGO lesions of 2 cm or less in diameter.

Prethoracotomy serum CEA level has been reported to be a good predictor of poor prognosis for patients with stage I NSCLC 24-26 Go and was the only independent prognostic predictor in the present study of small-sized NSCLC. It is considered that a combination of CEA level and CT or histologic findings might be more valuable to identify a patient group with poor outcome. 27,28 Go We also found a correlation between CEA level and nodal involvement in small-sized peripheral NSCLC. Interestingly, more than half of our patients with serum CEA levels that increased to greater than the 2-fold cutoff had node metastasis. Because the slight increase of CEA level could be caused by smoking or other pulmonary disorders, we also analyzed the frequency of node metastases for patients with CEA levels higher than 2-fold cutoff. These results indicate that a limited resection should be avoided in patients with CEA level increase. Therefore we propose that measurement of CEA level is useful to select patients with advanced disease among those with peripheral, small-sized NSCLC.

Pleural invasion was frequently found in patients with lymph node metastases, and several other studies have shown pleural involvement to be a prognostic factor and noted its clinical importance. 29,30 Go However, a preoperative accurate evaluation of pleural factors is difficult to obtain by means of CT or magnetic resonance imaging, and macroscopic findings during surgical intervention are unreliable. It was recently reported that a unique CT finding, the so-called pitfall sign, was able to predict pleural invasion. 30 Go Thus we consider that peripheral lung cancer with suspected pleural involvement on CT or intraoperative findings should be treated with a lobectomy plus node dissection, even if the tumor is smaller than 2 cm in diameter.


   Acknowledgments
 
We thank Professor Y. Ohno from the Department of Mathematical Health Science, Osaka University Medical School, for help with statistical analyses.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Discussion
 References
 

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