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J Thorac Cardiovasc Surg 1995;109:120-129
© 1995 Mosby, Inc.
GENERAL THORACIC SURGERY |
New York, N.Y.
Address for reprints: N. Martini, MD, 1275 York Ave., New York, NY 10021.
Abstract
From 1973 to 1985, 598 patients underwent resection for stage I non-small-cell lung cancer. There were 291 T1 lesions and 307 T2 lesions. The male/female ratio was 1.9:1. The histologic type was squamous carcinoma in 233 and nonsquamous carcinoma in 365. Lobectomy was performed in 511 patients (85%), pneumonectomy in 25 (4%), and wedge resection or segmentectomy in 62 (11%). A mediastinal lymph node dissection was carried out in 560 patients (94%) and no lymph node dissection in 38 (6%). Fourteen postoperative deaths occurred (2.3%). Ninety-nine percent of the patients were observed for a minimum of 5 years or until death with an overall median follow-up of 91 months. The overall 5- and 10-year survivals (Kaplan-Meier) were 75% and 67%, respectively. Survival in patients with T1 N0 tumors was 82% at 5 years and 74% at 10 years compared with 68% at 5 years and 60% at 10 years for patients with T2 tumors (p < 0.0004). The overall incidence of recurrence was 27% (local or regional 7%, systemic 20%) and was not influenced by histologic type. Second primary cancers developed in 206 patients (34%). Of these, 70 (34%) were second primary lung cancers. Despite complete resection, 31 of 62 patients (50%) who had wedge resection or segmentectomy had recurrence. Five- and 10-year survivals after wedge resection or segmentectomy were 59% and 35%, respectively, significantly less than survivals of those undergoing lobectomy (5 years, 77%; 10 years, 70%). The 5- and 10-year survivals in the 38 patients who had no lymph node dissection were reduced to 59% and 32%, respectively. Apart from the favorable prognosis observed in this group of patients, three facts emerge as significant: (1) Systematic lymph node dissection is necessary to ensure that the disease is accurately staged; (2) lesser resections (wedge/segment) result in high recurrence rates and reduced survival regardless of histologic type; and (3) second primary lung cancers are prevalent in long-term survivors. (J THORAC CARDIOVASC SURG 1995;109:120-9)
Stage I non-small-cell lung cancer represents early cancer and is best treated by surgery whenever possible. Despite the expectation of long-term survival after resection without adjuvant therapy, recurrences or new cancers develop in a third of the patients,
1-3 emphasizing the need for continued surveillance. The frequency of recurrences and new primary cancers varies from one report to another. Because of the large number of patients with lung cancer treated by us at various stages of their disease, we have analyzed our experience with the surgical treatment of stage I tumors, focusing on tumor size, histologic type, extent of resection, and the incidence of recurrence and new cancers observed in the course of their follow-up. We here present our results.
PATIENTS AND METHODS
From 1973 to 1985 inclusive, 3145 patients with non-small-cell lung cancer were treated primarily at Memorial Hospital. Those treated elsewhere initially and then referred to us with recurrence or metastases have been excluded. During that period, 598 patients underwent resection for pathologic stage I disease (T1 N0 M0 and T2 N0 M0).
At thoracotomy the extent of intrathoracic disease was carefully assessed with particular reference to regional lymph nodes (N1 or N2). A complete resection of all disease in the lung was carried out, as well as a mediastinal lymph node dissection in the majority of patients. Postoperative pathologic staging was done after the resected specimen was reviewed histologically and all regional nodes were assessed. Histologic type, tumor location, tumor size in centimeters, histologic clearance at bronchial and vascular resection margins, and visceral pleural involvement were recorded. The surgical and pathologic reports of all patients were carefully reviewed to ensure that the resection was complete, that no residual tumor, gross or microscopic, was left behind, and that no involved regional nodes (N1 and N2) were present. Tumor grading, vascular or lymphatic invasion within lung parenchyma, and flow cytometry were not routinely reported. However, several recent reports have suggested that these parameters adversely affect overall survival. 4-9 For that reason, 200 specimens were randomly selected for blinded review by one of us (M.F.Z.). The tumors were categorized into well-differentiated, moderately differentiated, and poorly differentiated grades.
We defined local recurrence as evidence of tumor within the same lung or at the bronchial stump, regional recurrence as clinically or radiologically manifest disease in the mediastinum or in supraclavicular nodes, and distant recurrence as disease in the contralateral lung or outside the hemithorax. The criteria used for the diagnosis of multiple lung cancers are shown in Table I.
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2 test. Significance was defined as p 
0.05.
The patients comprised 392 men and 206 women, a ratio of 19:1. The age range was 19 to 86 years with a median age of 62 years. The tumor was located in the right lung in 359 patients (60%) and in the left lung in 239 (40%) (Table II). Thirteen of the tumors were in the main bronchus beyond 2 cm of the carina, 400 (67%) in the upper lobe, 146 in the lower lobe, and 36 in the right middle lobe.
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There were 291 T1 N0 M0 tumors (49%) and 307 (51%) T2 N0 M0 tumors (51%). Sixty patients had tumors 1 cm or smaller, of which 20 were radiographically occult tumor (TX lesions), 217 had tumors 2 cm or smaller, 351, 3 cm or smaller, 164, larger than 3 cm to 5 cm, and 83, greater than 5 cm. The visceral pleura was involved in 113 patients, 51 of whom had tumors 3 cm or smaller.
Lobectomy was performed in 511 patients (85%), pneumonectomy in 25 (4%), and wedge resection or segmentectomy in 62 (11%) (Table III). Of the latter group, 55 of 62 patients (89%) had T1 tumors. A mediastinal lymph node dissection was carried out in 560 patients (94%) and lymph node sampling and no formal dissection in 38 (6%).
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Ninety-nine percent of the patients were observed for a minimum of 5 years or until death (median follow-up: 91 months). Only seven patients alive and well and one patient alive with disease were observed for less than 5 years from treatment. Fourteen postoperative deaths occurred, an incidence of 2.3%, all in patients with lobectomy. The causes of death included myocardial infarction in six, respiratory failure or pneumonia in six, renal failure in one,and spontaneous esophageal perforation with secondary mediastinitis in one.
Twenty radiologically occult lung cancers were detected on sputum cytology, localized by bronchoscopy, and subsequently resected. Of these, 19 were squamous cell cancers and one was a bronchoalveolar carcinoma. The patient with bronchoalveolar carcinoma died of recurrence 2 years later. One patient with squamous cancer died of liver metastases 61/2 years after initial treatment. The remainder are either alive and free of disease or have died of unrelated causes. The 5- and 10-year survivals of this small group of patients were 95% and 87%, respectively.
The overall 5- and 10-year survivals were 75% and 67% (Fig 1). Survival of patients with T1 tumors was 82% at 5 years and 74% at 10 years, compared with 68% at 5 years and 60% at 10 years for those with T2 tumors (p < 0.0004) (Fig. 2). Because the exact diameter of each resected tumor was recorded, each subset (T1 and T2) was analyzed further by tumor size in centimeters. We found that tumor size in centimeters influenced survival with significant p values between the ranges shown in Fig. 3. Differences in survival were not significant between (1) patients with tumors 2 cm or less in diameter and those with tumors 3 cm or less in diameter (p = 0.63), (2) patients with tumors 1 cm or less in diameter and those with tumors 2 cm or less in diameter (p = 0.24), and (3) patients with tumors 1 to 2 cm in diameter versus 2 to 3 cm in diameter (p = 0.71).
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The retrospective grading of the 200 randomly selected cases did not demonstrate any survival advantage by grade in these patients.
Visceral pleural involvement did not affect overall survival (p = 006) but was a contributing adverse factor in patients with large tumors (Fig. 4).
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Recurrence
During the course of follow-up, recurrence developed in 159 of 598 patients (27%) Of these, 141 (89%) died of their disease, 7 are alive with disease (4%), and 11 (7%) have had successful control of their recurrence; 9 of the 11 are still alive and well and 2 have died of unrelated causes.
In 60% of the patients with recurrent disease, the recurrence developed within the first 2 years after the operation. Although the incidence of recurrence diminished with time, 9% of patients had recurrence 5 or more years after their initial surgical treatment (Table IV). The longest free interval in our series was 12 years in a patient with a solitary brain lesion that was successfully removed.
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Table V. The first sites of recurrences in the overall group of patients were mostly distant (local 20%, regional 8%, and distant 72%). The most common site of distant metastases was the brain, particularly in nonsquamous lung cancers. Local or regional recurrence was slightly more common in patients with squamous carcinoma as compared with those with nonsquamous lung cancers (32% versus 26%).
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The incidence of recurrence was influenced by the T factor and by tumor size in centimeters. The difference was statistically significant between T1 and T2 tumors (p = 0.0004), between tumors 3 cm or smaller and those greater than 3 cm but equal to or less than 5 cm (p = 0.03), and between tumors larger than 3 cm to 5 cm and those greater than 5 cm (p = 0.03).
Multiple primary cancers
A total of 206 patients had second cancers, an overall incidence of 34%. This incidence was similar between histologic types (squamous carcinoma 32%, nonsquamous cancer 36%). The second primary tumors were synchronous in 24 and metachronous in 182 patients (Table VI). One third of the multiple cancers were lung cancers. A total of 69 patients had two primary lung cancers, 14 of which were synchronous and 55 metachronous (10 before, 45 after). Fifteen patients had a third cancer, five of whom had triple lung cancers, four from the metachronous group and one from the synchronous group.
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Table VII).
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DISCUSSION
Few lung cancers are potentially curable. For those patients with stage I non-small-cell carcinoma, however, surgical resection offers a significant chance of cure. 10-16 Radiographically occult carcinomas of the lung detected on sputum cytologic examination represent a very small group of lung cancers, but early removal of these tumors after localization results in cancer cure in the vast majority.
In 1977, we 17 reported our preliminary survival results with the surgical treatment of stage I lung cancer and demonstrated favorable results with complete resection combined with mediastinal lymph node dissection. By 1983, follow-up data were available for at least 5 years on 136 patients treated by lobectomy or pneumonectomy. 12 The 5-year survival was 83% for patients with T1 tumors and 65% for those with T2 tumors, with an overall 5-year survival of 72%. No local recurrence was observed in this group of patients and only three had regional lymph node metastases, emphasizing the need for a complete lymph node dissection to ensure the absence of nodal metastasis and also emphasizing the need to do a lobectomy in patients with stage I lung cancer regardless of the small size of the tumor or its peripheral position.
In our early experience, we had not found vascular or lymphatic invasion or grading to have prognostic significance. As a result, these parameters were not routinely recorded in our pathology reports. Although our current reporting is more standardized and these observations are now noted, we attempted to address grading by reviewing 200 randomly selected cases from our series and found that grading had no predictive value on survival in these patients who had complete resections.
Vascular or lymphatic invasion as a predictor of survival has been controversial. The Veterans Administration Surgical Oncology Study Group had reviewed 865 resections for lung cancer, and the presence or absence of lymphatic or blood vessel invasion was recorded in 90% of the cases. 8 Blood vessel invasion was found to have no predictive value, but lymphatic invasion did in patients with squamous cell cancers. In a more recent publication, blood vessel invasion was reported to be a main predictor of recurrence in T1 N0 M0 disease non-small-cell lung cancer. 4 Of 95 patients treated by resection, 16 had blood vessel invasion and all have died of their cancer. However, the distinction between blood vessel and lymphatics is not always possible even with the use of special stains.
The value of flow cytometry to assess the deoxyribonucleic acid content has also been controversial. 18 Although reports have noted that deoxyribonucleic acid assessment is valuable, 5,9 this was not prognostic in our experience 19 or in that of the Lung Cancer Study Group. 3
A similar controversy exists between advocates of elective segmentectomy or wedge resection 20 and those who recommend a lobectomy as the procedure of choice. In one series, patients with wedge resection did better than those treated by lobectomy or pneumonectomy because median tumor size was smaller. 4 In another series, patients with tumors less than 2 cm in diameter within the T1 N0 group had a survival advantage. 21 It was concluded that deep-seated lesions necessitate a lobectomy, but lesser resections are justified in patients with peripheral tumors less than 2 cm in diameter, because they do better and perhaps should be analyzed separately. These two reports contradict the observations made by the Lung Cancer Study Group 22 and by our current series. Our experience confirms that any resection less extensive than lobectomy places the patient at an increased risk of local recurrence and decreases the chances of long-term survival. Only in those patients with compromised cardiopulmonary function do we recommend a conservative resection such as segmentectomy or wedge resection.
Regardless of the extent of pulmonary resection, systematic mediastinal lymph node dissection should be routinely performed to stage the disease accurately by ascertaining that lymphatic metastases are absent.
Recurrence after initial treatment was identified by radiographic or laboratory evidence and whenever possible by pathologic confirmation. Local and regional recurrences are the result of inadequate initial excision and are considered to represent persistent disease, not a second carcinoma. Recurrences at any site are most commonly detected within the first 2 years after treatment and diminish in occurrence with time. However, inasmuch as these patients live long and overcome their first carcinoma, they remain at risk for second carcinomas. When a complete, potentially curative resection of a primary carcinoma of the lung is performed, when the margins are clear, and when lymph node metastasis is absent, any new lesion, even if in the same lung, may well represent a new and separate primary tumor. Guidelines for acceptance of a carcinoma as a new and separate lung carcinoma were reported by us 23 and are shown in 
Table I. The diagnosis is most convincing when the new lesion is in the contralateral lung and the histologic type of the new tumor is different.
The Lung Cancer Study Group had stated that cancer recurrence represents treatment failure whereas development of new cancers suggests persistent exposure to etiologic risk factors. 24 We concur with this explanation and agree with the need for continued surveillance beyond 5 years. The frequency with which second primary tumors are detected in this group of patients is high and poses a threat to survival despite the potentially curative resection of the initial primary lung cancer.
The emphasis on 5-year survival may be misleading in patients with treated cancers with low recurrence rates. In resected stage I non-small-cell lung cancer, a significant proportion of patients die of other causes and free of cancer. In our series, the incidence of deaths from unrelated causes was 19%. In many studies, patients with prior head and neck, lung, and breast cancers have been excluded, as well as patients with prior cancers treated within 5 years. 24,25 In our series, inclusion of previously treated cancers including head and neck cancers did not adversely affect survival.
The high frequency of the development of second primary lung cancers was also noted in our early report on 136 patients treated by resection for stage I lung cancer (32% second cancers, 34% of which were second primary lung cancers). Our current review notes the same high frequency, namely, a 34% incidence of second cancers, a third of which are second lung cancers.
Because vitamin A and retinoids were found to be strong inhibitors of epithelial cancer progression in experimental carcinogenesis, several randomized studies are currently in progress to assess the merits of retinoids in improving the disease-free interval by preventing secondary aerodigestive cancers or recurrence in patients cured of an early lung cancer. 26,27 The data are still viewed as preliminary and will require several years of follow-up before definitive conclusions can be drawn. At this time, it is recommended that retinoids and vitamin A be offered only in protocol settings.
SUMMARY AND CONCLUSIONS
Appendix: DISCUSSION
Dr. L. Penfield Faber (Chicago, Ill.)
Dr. Martini and the group from Memorial have established another "gold standard" for the surgical treatment of non-small-cell lung cancer. The earlier report by Drs. Martini and Beattie recommended lobectomy as the resection of choice for stage I lung cancer. The projected survival at 5 years for patients with T1 N0 disease after lobectomy was approximately 80%. To me, a gold standard procedure is one to which other variations of resection are compared. Those of us who are reporting results of segmental resections, wedge resections, or resections by video-assisted thoracic surgical techniques must document similar results if these procedures are to become accepted as standard. This exquisitely defined study with exquisitely defined lymph node resection and surgical/pathologic staging sets the standard. It also provides patients with stage I disease a degree of optimism.
I agree that it is important to accomplish a complete lymphadenectomy to assure that these are stage I lesions I concur with Dr. Martini that lymphadenectomy is important for staging and also achieves a more complete resection with an enhanced cure rate.
Dr. Martini, how do you define and differentiate local recurrence from a second primary. A review of the literature of lung cancer shows that second primaries have various definitions, such as the second tumor appearing more than 2 years after the initial resection or the tumor arising in another lobe, having a contralateral location, and being of a different histologic type. Definitions for a second primary do vary, and it can be troublesome to differentiate the development of a second primary from locoregional recurrence.
My second question concerns the recommended approach to solitary metastatic disease in organs other than the brain. What should be done about resection of solitary metastatic tumors in other organs that would include the adrenal gland, the contralateral lung, and the liver?
Dr. Martini
We define local recurrence as disease found in lung in patients who had a lesser resection than a lobectomy or disease found at the bronchial resection margin after a lobectomy or pneumonectomy. We define regional recurrence as development of N2 or N3 disease despite a careful mediastinal lymph node evaluation at the initial operation. All other sites of recurrence are referred to as distant recurrence.
The diagnosis of a new primary tumor is most convincing when the histologic type of the new tumor is different. Also accepted as a new primary is a new lesion in the contralateral lung or different lobe with no carcinoma in lymphatics common to both. We have also accepted as multiple lung primaries, squamous carcinomas in the same lobe when we have clearly identified the origin of each from a carcinoma in situ.
The best treatment for a solitary distant metastasis after adequate control of a primary tumor presumed to be stage I is still an unresolved question. In our opinion, if the solitary area of metastasis is resectable, it should be resected, just as we have done with solitary brain metastasis. We do not have the same experience with the adrenal gland. We have on occasion resected solitary skin metastases or rib metastases with a resultant prolonged survival.
It is important to remember that the treatment for a patient with a solitary lung lesion, be it metastatic or a new primary, ought to be surgical with expectations of prolonged survival.
Dr. John R. Benfield (Sacramento, Calif.)
An important part of your presentation has been that patients who have had lesser resections and lesser lymph node dissections have fared less well than those who have had the more extensive procedures.
Because this was a retrospective study, I am curious to know what selection criteria were used for the patients who had these lesser resections. Is it possible that the lesser survivals among those patients were, at least in part, the result of factors other than the operations that were done?
Dr. Martini
We were heavily influenced from the outset by the fact that the surgical treatment of patients with lung cancer, however small or early, should be no less than a lobectomy. We offered lesser resections only to patients with limited cardiopulmonary reserve caused by chronic obstructive pulmonary disease or prior pulmonary resection for lung cancer and, at times, after a mistaken frozen section diagnosis of metastasis or benign disease. When we did that, we noted a local recurrence rate of 19%. The largest series in this country comes from Rush–Presbyterian–St. Luke's Medical Center reported by Jensik, Faber, Kittle and Warren. In this series elective segmentectomies have resulted in a 12% to 15% incidence of local recurrence.
Because of this fact, we believe very strongly that in a patient with adequate lung reserve who has early lung cancer, there is no justification to do a miniresection and risk local recurrence
Dr. Donald L. Morton (Santa Monica, Calif.)
What pathologic criteria did you use to determine the absence of lymph node metastases? We recently reviewed a series of patients with lung cancer whose mediastinal nodes had no evidence of metastases by standard histopathologic examination with hematoxylin and eosin stains. However, more sensitive immunohistochemical stains revealed micrometastases in 30% of the dissection specimens. I am therefore intrigued by your 30% rate of recurrence in patients without nodal metastases. I put forth the hypothesis that most patients with recurrence have regional node micrometastases that are too small to be detected by routine hematoxylin and eosin staining.
Dr. Nael Martini
Dr. Morton, this is a very interesting piece of information. Our only method of determining that a patient has no regional lymph node metastasis has been the meticulous histologic light microscopic review of any lymph nodes we submitted. Because we were doing lymph node dissections, the approximate number of lymph nodes submitted from the mediastinum varied from 25 to 40. Admittedly, many intraparenchymal and segmental nodes may be overlooked if step sectioning is not done.
Acknowledgments
We gratefully acknowledge Phyllis Byczek for her assistance in collating the data and her tireless efforts in obtaining status follow-up on all patients.
Footnotes
From the Departments of Surgerya and Pathology,b Memorial Sloan-Kettering Cancer Center and Cornell University Medical College, New York, N.Y. 
Read at the Seventy-fourth Annual Meeting of The American Association for Thoracic Surgery, New York, N.Y., April 24-27, 1994.
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W. Sienel, C. Stremmel, A. Kirschbaum, L. Hinterberger, E. Stoelben, J. Hasse, and B. Passlick Frequency of local recurrence following segmentectomy of stage IA non-small cell lung cancer is influenced by segment localisation and width of resection margins -- implications for patient selection for segmentectomy Eur. J. Cardiothorac. Surg., March 1, 2007; 31(3): 522 - 528. [Abstract] [Full Text] [PDF]
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H. Sugimura, F. C. Nichols, P. Yang, M. S. Allen, S. D. Cassivi, C. Deschamps, B. A. Williams, and P. C. Pairolero Survival After Recurrent Nonsmall-Cell Lung Cancer After Complete Pulmonary Resection Ann. Thorac. Surg., February 1, 2007; 83(2): 409 - 418. [Abstract] [Full Text] [PDF]
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W.-H. Hsu, C.-S. Huang, H.-S. Hsu, W.-J. Huang, H.-C. Lee, B.-S. Huang, and M.-H. Huang Preoperative Serum Carcinoembryonic Antigen Level is a Prognostic Factor in Women With Early Non-Small-Cell Lung Cancer Ann. Thorac. Surg., February 1, 2007; 83(2): 419 - 424. [Abstract] [Full Text] [PDF]
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 Y. J. Jeong, C. A. Yi, and K. S. Lee Solitary Pulmonary Nodules: Detection, Characterization, and Guidance for Further Diagnostic Workup and Treatment Am. J. Roentgenol., January 1, 2007; 188(1): 57 - 68. [Abstract] [Full Text] [PDF]
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P. C. Lee, R. J. Korst, J. L. Port, Y. Kerem, A. L. Kansler, and N. K. Altorki Long-term survival and recurrence in patients with resected non-small cell lung cancer 1 cm or less in size J. Thorac. Cardiovasc. Surg., December 1, 2006; 132(6): 1382 - 1388. [Abstract] [Full Text] [PDF]
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The International Early Lung Cancer Action Program Survival of Patients with Stage I Lung Cancer Detected on CT Screening N. Engl. J. Med., October 26, 2006; 355(17): 1763 - 1771. [Abstract] [Full Text] [PDF]
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M. Okada, T. Koike, M. Higashiyama, Y. Yamato, K. Kodama, and N. Tsubota Radical sublobar resection for small-sized non small cell lung cancer: A multicenter study J. Thorac. Cardiovasc. Surg., October 1, 2006; 132(4): 769 - 775. [Abstract] [Full Text] [PDF]
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B. M. Stiles, T. A. Altes, D. R. Jones, K. R. Shen, G. Ailawadi, S. B. Gay, J. Olazagasti, P. K. Rehm, and T. M. Daniel Clinical experience with radiotracer-guided thoracoscopic biopsy of small, indeterminate lung nodules. Ann. Thorac. Surg., October 1, 2006; 82(4): 1191 - 1197. [Abstract] [Full Text] [PDF]
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T. Fukuse, E. Ogawa, F. Chen, H. Sakai, and H. Wada Limited surgery and radiofrequency ablation for recurrent lung cancer. Ann. Thorac. Surg., October 1, 2006; 82(4): 1506 - 1508. [Abstract] [Full Text] [PDF]
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R. J. Korst, A. L. Kansler, J. L. Port, P. C. Lee, and N. K. Altorki Accuracy of surveillance computed tomography in detecting recurrent or new primary lung cancer in patients with completely resected lung cancer. Ann. Thorac. Surg., September 1, 2006; 82(3): 1009 - 1015. [Abstract] [Full Text] [PDF]
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A. El-Sherif, W. E. Gooding, R. Santos, B. Pettiford, P. F. Ferson, H. C. Fernando, S. J. Urda, J. D. Luketich, and R. J. Landreneau Outcomes of Sublobar Resection Versus Lobectomy for Stage I Non-Small Cell Lung Cancer: A 13-Year Analysis Ann. Thorac. Surg., August 1, 2006; 82(2): 408 - 416. [Abstract] [Full Text] [PDF]
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C. L. Nguyen, W. J. Scott, and M. Goldberg Radiofrequency ablation of lung malignancies. Ann. Thorac. Surg., July 1, 2006; 82(1): 365 - 371. [Abstract] [Full Text] [PDF]
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E. O. Machida, M. V. Brock, C. M. Hooker, J. Nakayama, A. Ishida, J. Amano, M. A. Picchi, S. A. Belinsky, J. G. Herman, S. Taniguchi, et al. Hypermethylation of ASC/TMS1 Is a Sputum Marker for Late-Stage Lung Cancer. Cancer Res., June 15, 2006; 66(12): 6210 - 6218. [Abstract] [Full Text] [PDF]
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J. S. Kim, J. W. Kim, J. Han, Y. M. Shim, J. Park, and D.-H. Kim Cohypermethylation of p16 and FHIT Promoters as a Prognostic Factor of Recurrence in Surgically Resected Stage I Non-Small Cell Lung Cancer. Cancer Res., April 15, 2006; 66(8): 4049 - 4054. [Abstract] [Full Text] [PDF]
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H. Sugimura and P. Yang Long-term Survivorship in Lung Cancer: A Review. Chest, April 1, 2006; 129(4): 1088 - 1097. [Abstract] [Full Text] [PDF]
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S. S. Shim, K. S. Lee, M. J. Chung, H. Kim, O J. Kwon, and S. Kim Do hemodynamic studies of stage t1 lung cancer enable the prediction of hilar or mediastinal nodal metastasis? Am. J. Roentgenol., April 1, 2006; 186(4): 981 - 988. [Abstract] [Full Text] [PDF]
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B. A. Williams, H. Sugimura, C. Endo, F. C. Nichols, S. D. Cassivi, M. S. Allen, P. C. Pairolero, C. Deschamps, and P. Yang Predicting Postrecurrence Survival Among Completely Resected Nonsmall-Cell Lung Cancer Patients Ann. Thorac. Surg., March 1, 2006; 81(3): 1021 - 1027. [Abstract] [Full Text] [PDF]
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T. Kawaguchi, A. Matsumura, K. Iuchi, S. Ishikawa, H. Maeda, S. Fukai, H. Komatsu, and M. Kawahara Second Primary Cancers in Patients with Stage III Non-Small Cell Lung Cancer Successfully Treated with Chemo-radiotherapy Jpn. J. Clin. Oncol., January 1, 2006; 36(1): 7 - 11. [Abstract] [Full Text] [PDF]
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C. M. Mery, A. N. Pappas, B. M. Burt, R. Bueno, P. A. Linden, D. J. Sugarbaker, and M. T. Jaklitsch Diameter of Non-small Cell Lung Cancer Correlates With Long-term Survival: Implications for T Stage Chest, November 1, 2005; 128(5): 3255 - 3260. [Abstract] [Full Text] [PDF]
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D. B. Flieder, J. L. Port, R. J. Korst, P. J. Christos, M. A. Levin, D. E. Becker, and N. K. Altorki Tumor Size Is a Determinant of Stage Distribution in T1 Non-Small Cell Lung Cancer Chest, October 1, 2005; 128(4): 2304 - 2308. [Abstract] [Full Text] [PDF]
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V. Sullivan, T. Tran, A. Holmstrom, M. Kuskowski, P. Koh, J. B. Rubins, and R. F. Kelly Advanced Age Does Not Exclude Lobectomy for Non-small Cell Lung Carcinoma Chest, October 1, 2005; 128(4): 2671 - 2676. [Abstract] [Full Text] [PDF]
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D. Lardinois, H. Suter, H. Hakki, V. Rousson, D. Betticher, and H.-B. Ris Morbidity, Survival, and Site of Recurrence After Mediastinal Lymph-Node Dissection Versus Systematic Sampling After Complete Resection for Non-Small Cell Lung Cancer Ann. Thorac. Surg., July 1, 2005; 80(1): 268 - 275. [Abstract] [Full Text] [PDF]
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J. L. Mulshine Clinical Issues in the Management of Early Lung Cancer Clin. Cancer Res., July 1, 2005; 11(13): 4993s - 4998s. [Abstract] [Full Text] [PDF]
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M. Hockel and N. Dornhofer The Hydra Phenomenon of Cancer: Why Tumors Recur Locally after Microscopically Complete Resection Cancer Res., April 15, 2005; 65(8): 2997 - 3002. [Abstract] [Full Text] [PDF]
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S. G. Talbot, C. Estilo, E. Maghami, I. S. Sarkaria, D. K. Pham, P. O-charoenrat, N. D. Socci, I. Ngai, D. Carlson, R. Ghossein, et al. Gene Expression Profiling Allows Distinction between Primary and Metastatic Squamous Cell Carcinomas in the Lung Cancer Res., April 15, 2005; 65(8): 3063 - 3071. [Abstract] [Full Text] [PDF]
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O. Birim, A. P. Kappetein, J. J.M. Takkenberg, R. J. van Klaveren, and A. J.J.C. Bogers Survival After Pathological Stage IA Nonsmall Cell Lung Cancer: Tumor Size Matters Ann. Thorac. Surg., April 1, 2005; 79(4): 1137 - 1141. [Abstract] [Full Text] [PDF]
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H. Uramoto, K. Sugio, T. Oyama, S. Nakata, K. Ono, M. Morita, K. Funa, and K. Yasumoto Expression of {Delta}Np73 Predicts Poor Prognosis in Lung Cancer Clin. Cancer Res., October 15, 2004; 10(20): 6905 - 6911. [Abstract] [Full Text] [PDF]
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J. S. Kim, H. Lee, H. Kim, Y. M. Shim, J. Han, J. Park, and D.-H. Kim Promoter Methylation of Retinoic Acid Receptor Beta 2 and the Development of Second Primary Lung Cancers in Non-Small-Cell Lung Cancer J. Clin. Oncol., September 1, 2004; 22(17): 3443 - 3450. [Abstract] [Full Text] [PDF]
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M. Pellise, A. Castells, A. Gines, R. Agrelo, M. Sole, S. Castellvi-Bel, G. Fernandez-Esparrach, J. Llach, M. Esteller, J. M. Bordas, et al. Detection of Lymph Node Micrometastases by Gene Promoter Hypermethylation in Samples Obtained by Endosonography- Guided Fine-Needle Aspiration Biopsy Clin. Cancer Res., July 1, 2004; 10(13): 4444 - 4449. [Abstract] [Full Text] [PDF]
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T. Iizasa, M. Suzuki, K. Yasufuku, A. Iyoda, M. Otsuji, S. Yoshida, Y. Sekine, K. Shibuya, Y. Saitoh, K. Hiroshima, et al. Preoperative pulmonary function as a prognostic factor for stage I non-small cell lung carcinoma Ann. Thorac. Surg., June 1, 2004; 77(6): 1896 - 1902. [Abstract] [Full Text] [PDF]
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S. Yamada and T. Kohno Video-assisted thoracic surgery for pure ground-glass opacities 2 cm or less in diameter Ann. Thorac. Surg., June 1, 2004; 77(6): 1911 - 1915. [Abstract] [Full Text] [PDF]
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W. J. Scott Metachronous lung cancer: the role of improved postoperative surveillance J. Thorac. Cardiovasc. Surg., March 1, 2004; 127(3): 633 - 635. [Full Text] [PDF]
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R. J. Battafarano, S. D. Force, B. F. Meyers, J. Bell, T. J. Guthrie, J. D. Cooper, and G. A. Patterson Benefits of resection for metachronous lung cancer J. Thorac. Cardiovasc. Surg., March 1, 2004; 127(3): 836 - 842. [Abstract] [Full Text] [PDF]
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N. Sawabata, M. Ohta, A. Matsumura, K. Nakagawa, H. Hirano, H. Maeda, and H. Matsuda Optimal distance of malignant negative margin in excision of nonsmall cell lung cancer: a multicenter prospective study Ann. Thorac. Surg., February 1, 2004; 77(2): 415 - 420. [Abstract] [Full Text] [PDF]
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W. Sienel, C. Varwerk, A. Linder, D. Kaiser, M. Teschner, M. Delire, G. Stamatis, and B. Passlick Melanoma associated antigen (MAGE)-A3 expression in Stages I and II non-small cell lung cancer: results of a multi-center study Eur. J. Cardiothorac. Surg., January 1, 2004; 25(1): 131 - 134. [Abstract] [Full Text] [PDF]
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Y.-C. Wu, C.-F. J. Lin, W.-H. Hsu, B.-S. Huang, M.-H. Huang, and L.-S. Wang Long-term results of pathological stage I non-small cell lung cancer: validation of using the number of totally removed lymph nodes as a staging control Eur. J. Cardiothorac. Surg., December 1, 2003; 24(6): 994 - 1001. [Abstract] [Full Text] [PDF]
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J. L. Port, M. S. Kent, R. J. Korst, D. Libby, M. Pasmantier, and N. K. Altorki Tumor Size Predicts Survival Within Stage IA Non-Small Cell Lung Cancer Chest, November 1, 2003; 124(5): 1828 - 1833. [Abstract] [Full Text] [PDF]
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D. Rice, H.-W. Kim, A. Sabichi, S. Lippman, J. J. Lee, B. Williams, A. Vaporciyan, W. R. Smythe, S. Swisher, G. Walsh, et al. The risk of second primary tumors after resection of Stage I nonsmall cell lung cancer Ann. Thorac. Surg., October 1, 2003; 76(4): 1001 - 1008. [Abstract] [Full Text] [PDF]
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D. R. Jones, B. M. Stiles, C. E. Denlinger, P. Antippa, and T. M. Daniel Pulmonary segmentectomy: results and complications Ann. Thorac. Surg., August 1, 2003; 76(2): 343 - 349. [Abstract] [Full Text] [PDF]
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P. H. Hollaus, P. N. Wurnig, and N. S. Pridun The natural history of recurrence after bronchoplastic procedures for non-small cell lung cancer Ann. Thorac. Surg., August 1, 2003; 76(2): 363 - 369. [Abstract] [Full Text] [PDF]
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M. Okada, W. Nishio, T. Sakamoto, H. Harada, K. Uchino, and N. Tsubota Long-term survival and prognostic factors of five-year survivors with complete resection of non-small cell lung carcinoma J. Thorac. Cardiovasc. Surg., August 1, 2003; 126(2): 558 - 562. [Abstract] [Full Text] [PDF]
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 F. J. Kaye and T. Komiya New Leads Suggest a Clinically Relevant Genotype-Phenotype Relationship for the p53 Gene J Natl Cancer Inst, July 2, 2003; 95(13): 926 - 927. [Full Text] [PDF]
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K. Yasumoto, T. Osaki, Y. Watanabe, H. Kato, and T. Yoshimura Prognostic value of cytokeratin-positive cells in the bone marrow and lymph nodes of patients with resected nonsmall cell lung cancer: a multicenter prospective study Ann. Thorac. Surg., July 1, 2003; 76(1): 194 - 201. [Abstract] [Full Text] [PDF]
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J.-H. Kang, K. D. Kim, and K. Y. Chung Prognostic value of visceral pleura invasion in non-small cell lung cancer Eur. J. Cardiothorac. Surg., June 1, 2003; 23(6): 865 - 869. [Abstract] [Full Text] [PDF]
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C.-H. Chiu, M.-S. Chern, M.-H. Wu, W.-H. Hsu, Y.-C. Wu, M.-H. Huang, and S.-C. Chang Usefulness of low-dose spiral CT of the chest in regular follow-up of postoperative non-small cell lung cancer patients: Preliminary report J. Thorac. Cardiovasc. Surg., June 1, 2003; 125(6): 1300 - 1305. [Abstract] [Full Text] [PDF]
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W. Sienel, S. Dango, U. Woelfle, A. Morresi-Hauf, C. Wagener, J. Brummer, W. Mutschler, B. Passlick, and K. Pantel Elevated Expression of Carcinoembryonic Antigen-related Cell Adhesion Molecule 1 Promotes Progression of Non-Small Cell Lung Cancer Clin. Cancer Res., June 1, 2003; 9(6): 2260 - 2266. [Abstract] [Full Text] [PDF]
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Y. Ichinose, K. Genka, T. Koike, H. Kato, Y. Watanabe, T. Mori, S. Iioka, A. Sakuma, and M. Ohta Randomized Double-Blind Placebo-Controlled Trial of Bestatin in Patients With Resected Stage I Squamous-Cell Lung Carcinoma J Natl Cancer Inst, April 16, 2003; 95(8): 605 - 610. [Abstract] [Full Text] [PDF]
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W. Sienel, R. Seen-Hibler, W. Mutschler, K. Pantel, and B. Passlick Tumour cells in the tumour draining vein of patients with non-small cell lung cancer: detection rate and clinical significance Eur. J. Cardiothorac. Surg., April 1, 2003; 23(4): 451 - 456. [Abstract] [Full Text] [PDF]
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S. V. Harden, Y. Tokumaru, W. H. Westra, S. Goodman, S. A. Ahrendt, S. C. Yang, and D. Sidransky Gene Promoter Hypermethylation in Tumors and Lymph Nodes of Stage I Lung Cancer Patients Clin. Cancer Res., April 1, 2003; 9(4): 1370 - 1375. [Abstract] [Full Text] [PDF]
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T. Sioris, R. Jarvenpaa, P. Kuukasjarvi, H. Helin, S. Saarelainen, and M. Tarkka Comparison of computed tomography and systematic lymph node dissection in determining TNM and stage in non-small cell lung cancer Eur. J. Cardiothorac. Surg., March 1, 2003; 23(3): 403 - 408. [Abstract] [Full Text] [PDF]
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M. Maddaus Safe harbor J. Thorac. Cardiovasc. Surg., March 1, 2003; 125(3): 454 - 455. [Full Text] [PDF]
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N. Kikuchi, H. Satoh, K. Sekizawa, and S. Ishikawa Late recurrence after resection of stage I lung adenocarcinoma Ann. Thorac. Surg., March 1, 2003; 75(3): 1069 - 1070. [Full Text] [PDF]
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 S. J. Swensen, J. R. Jett, T. E. Hartman, D. E. Midthun, J. A. Sloan, A.-M. Sykes, G. L. Aughenbaugh, and M. A. Clemens Lung Cancer Screening with CT: Mayo Clinic Experience Radiology, March 1, 2003; 226(3): 756 - 761. [Abstract] [Full Text] [PDF]
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F. M.A. Melfi, A. Chella, G. F. Menconi, F. Givigliano, G. Boni, G. Mariani, P. Sbragia, and C. A. Angeletti Intraoperative radioguided sentinel lymph node biopsy in non-small cell lung cancer Eur. J. Cardiothorac. Surg., February 1, 2003; 23(2): 214 - 220. [Abstract] [Full Text] [PDF]
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M. Higashiyama, K. Kodama, K. Takami, N. Higaki, T. Nakayama, and H. Yokouchi Intraoperative lavage cytologic analysis of surgical margins in patients undergoing limited surgery for lung cancer J. Thorac. Cardiovasc. Surg., January 1, 2003; 125(1): 101 - 107. [Abstract] [Full Text] [PDF]
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R. L. Quarterman, A. McMillan, M. B. Ratcliffe, and M. I. Block Effect of preoperative delay on prognosis for patients with early stage non-small cell lung cancer J. Thorac. Cardiovasc. Surg., January 1, 2003; 125(1): 108 - 114. [Abstract] [Full Text] [PDF]
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M. S. Brown, J. G. Goldin, R. D. Suh, M. F. McNitt-Gray, J. W. Sayre, and D. R. Aberle Lung Micronodules: Automated Method for Detection at Thin-Section CT--Initial Experience Radiology, January 1, 2003; 226(1): 256 - 262. [Abstract] [Full Text] [PDF]
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N. Sawabata, A. Matsumura, M. Ohota, H. Maeda, H. Hirano, K. Nakagawa, and H. Matsuda Cytologically malignant margins of wedge resected stage I non-small cell lung cancer Ann. Thorac. Surg., December 1, 2002; 74(6): 1953 - 1957. [Abstract] [Full Text] [PDF]
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R. J. Battafarano, B. F. Meyers, T. J. Guthrie, J. D. Cooper, and G. A. Patterson Surgical resection of multifocal non-Small cell lung cancer is associated with prolonged survival Ann. Thorac. Surg., October 1, 2002; 74(4): 988 - 994. [Abstract] [Full Text] [PDF]
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R.-S. Lai, J.-S. Wang, H.-K. Hsu, H.-C. Chang, C.-H. Lin, and M.-H. Lin Prognostic Evaluation of the Expression of p53 and bcl-2 Oncoproteins in Patients with Surgically Resected Non-small Cell Lung Cancer Jpn. J. Clin. Oncol., October 1, 2002; 32(10): 393 - 397. [Abstract] [Full Text] [PDF]
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L. J. Daniels, S. S. Balderson, M. W. Onaitis, and T. A. D'Amico Thoracoscopic lobectomy: a safe and effective strategy for patients with stage i lung cancer Ann. Thorac. Surg., September 1, 2002; 74(3): 860 - 864. [Abstract] [Full Text] [PDF]
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T. Osaki, T. Oyama, C.-D. Gu, T. Yamashita, T. So, M. Takenoyama, K. Sugio, and K. Yasumoto Prognostic Impact of Micrometastatic Tumor Cells in the Lymph Nodes and Bone Marrow of Patients With Completely Resected Stage I Non-Small-Cell Lung Cancer J. Clin. Oncol., July 1, 2002; 20(13): 2930 - 2936. [Abstract] [Full Text] [PDF]
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K. Hiroshima, A. Iyoda, K. Shibuya, T. Toyozaki, Y. Haga, T. Fujisawa, and H. Ohwada Prognostic significance of neuroendocrine differentiation in adenocarcinoma of the lung Ann. Thorac. Surg., June 1, 2002; 73(6): 1732 - 1735. [Abstract] [Full Text] [PDF]
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H. T. Winer-Muram, S. G. Jennings, R. D. Tarver, A. M. Aisen, M. Tann, D. J. Conces, and C. A. Meyer Volumetric Growth Rate of Stage I Lung Cancer prior to Treatment: Serial CT Scanning Radiology, June 1, 2002; 223(3): 798 - 805. [Abstract] [Full Text] [PDF]
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