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Ann Thorac Surg 1995;60:615-622
© 1995 The Society of Thoracic Surgeons
Abstract
Background. It has been reported that limited resection (segment or wedge) is equivalent to lobectomy in the management of early stage (T1-2 N0) non-small cell lung cancer.
Methods. A prospective, multiinstitutional randomized trial was instituted comparing limited resection with lobectomy for patients with peripheral T1 N0 non-small cell lung cancer documented at operation. Analysis included locoregional and distant recurrence rates, 5-year survival rates, perioperative morbidity and mortality, and late pulmonary function assessment.
Results. There were 276 patients randomized, with 247 patients eligible for analysis. There were no significant differences for all stratification variables, selected prognostic factors, perioperative morbidity, mortality, or late pulmonary function. In patients undergoing limited resection, there was an observed 75% increase in recurrence rates (p = 0.02, one-sided) attributable to an observed tripling of the local recurrence rate (p = 0.008 two-sided), an observed 30% increase in overall death rate (p = 0.08, one-sided), and an observed 50% increase in death with cancer rate (p = 0.09, one-sided) compared to patients undergoing lobectomy (p = 0.10, one-sided was the predefined threshold for statistical significance for this equivalency study).
Conclusions. Compared with lobectomy, limited pulmonary resection does not confer improved perioperative morbidity, mortality, or late postoperative pulmonary function. Because of the higher death rate and locoregional recurrence rate associated with limited resection, lobectomy still must be considered the surgical procedure of choice for patients with peripheral T1 N0 non-small cell lung cancer.
See also page 622 and page 623.
Lung Cancer Study Group (Prepared by Robert J. Ginsberg, MD, and Lawrence V. Rubinstein, PhD)
Non-small cell lung cancer (NSCLC) affects more than 140,000 people in the United States annually. An estimated 14% of these patients will be cured of their disease, most curable patients presenting with early stage (I or II) disease [1]. For the past 40 years, the standard surgical treatment for early stage lung cancer has been lobectomy whenever possible [2]. After lobectomy, patients with T1 N0 NSCLC experience up to an 80% 5-year cancer-free survival [3]. In an attempt to preserve pulmonary function, in 1973 Jensik and colleagues [4] were the first to suggest that a lesser resection (segmentectomy) might be an adequate operation for this stage of disease. Many other investigators have subsequently reported results using lesser resections (wedge or segmental resection) for stage I disease, but these were viewed by most surgeons as a ``compromise'' procedure for patients having limited pulmonary function [5–9]. However, recently some centers have advocated lesser resections as appropriate treatment for patients with T1 N0 NSCLC [10–12]. The theoretical advantages of such a procedure include preservation of pulmonary function, decreased perioperative mortality and morbidity, and the ability of the patient to undergo further resections in the future if a second primary lung cancer should develop [13, 14]. The theoretical disadvantage would be the potential for an increased local recurrence rate and, ultimately, a poorer cure rate for this deadly disease.
In 1982, the North American Lung Cancer Study Group initiated a prospective, randomized trial comparing limited resection (segmentectomy or adequate wedge resection) with lobectomy for the treatment of patients with T1 N0 NSCLC. Accrual to the study was concluded in November, 1988. After a minimum follow-up of 4.5 years, we report the results of this trial.
Material and Methods
Patient Eligibility
All patients had suspected lung cancer discovered on chest roentgenogram. Patients were screened preoperatively and ``registered'' for entry into the study if they had a clinical T1 N0 peripheral tumor (3 cm or less in all dimensions on posteroanterior and lateral chest roentgenogram), suspected or proven to be a lung cancer that was not visible on flexible bronchoscopy. All patients were able to tolerate a lobectomy as assessed by cardiopulmonary function. Patients were ineligible if they had a history of previously treated cancer other than basal or squamous cell carcinoma of the skin. In addition, before registration, there had to be no evidence of metastatic disease as determined by history, physical examination, and blood chemistry analysis including a normal alkaline phosphatase and serum glutamic-oxaloacetic transaminase. Abnormalities in any of these parameters required a metastatic survey including computed tomography or ultrasonography of the liver and a radionuclide bone scan. Routine computed tomographic examination of the brain, lung, liver, and adrenal glands to detect occult metastases was not required.
Randomization Procedure
After preoperative registration, at the time of thoracotomy and before randomization, if not previously proven, the tumor was confirmed by the pathologist to be a NSCLC, and by the surgeon to be T1 by intraoperative assessment of size. Frozen section analysis of sampled segmental, lobar, hilar, and mediastinal lymph nodes from the drainage area of the tumor confirmed the N0 status. A minimum sample of one node from each area was required. As well, an assessment was made by the surgeon as to the appropriateness of a limited resection for curative treatment and whether the intended limited procedure would be an adequate large wedge or a segmental resection. Middle lobe tumors were excluded because of the small size of the lobe involved. At this point, randomization occurred intraoperatively by telephone communication to the Operations Office (Information Management Services, Rockville, MD). Eligible patients were randomly assigned to one of two treatment groups, lobectomy or limited resection, and stratified according to age, pulmonary function, and whether the intended limited resection would be a wedge or a segment.
The study design and informed consent procedures were reviewed and approved by the Institutional Review Board for the protection of human subjects at each participating North American Lung Cancer Study Group institution. Each patient, before registration and operation, gave written informed consent.
Surgical Technique
The technique of segmental resection required isolation, division, and suture of the appropriate segmental bronchus, artery, and vein. In this protocol, portions of up to two adjacent segments could be removed as part of a limited resection. Surgeons were allowed latitude of technique in methods of division of pulmonary tissue. This included segmental stripping, ``cut-and-sew'' technique, or the use of surgical staplers.
Large adequate wedge resections could also be used as a limited resection treatment when considered appropriate. At least 2 cm of normal lung tissue was required to be resected beyond the tumor. As with segmental resection, surgeons were allowed latitude in surgical technique for division of pulmonary tissue.
After completion of the resection, the surgeon had to confirm that clinically the tumor had been completely resected and all required lymph node stations had been sampled and, by frozen section analysis, confirmed to be negative for metastatic disease. If resection was incomplete or the tumor was found to be greater than T1 or N0 by immediate pathologic analysis, the protocol specified that the surgeon complete the lobectomy.
Postoperatively, the surgeon was required to complete a detailed surgical form to ensure standardized surgical quality control.
Pathologic Assessment
At the time of operation, frozen section analysis was required of all bronchopulmonary, hilar, and mediastinal lymph nodes submitted by the surgeon. Once the tumor was resected, the pathologist was required to measure immediately the tumor and assess the lack of pleural invasion to confirm its T1 status, perform a frozen section analysis of the primary tumor to confirm its non-small cell carcinoma status, and ensure that all resection margins including pulmonary tissue margins indicated a complete resection. The pathologist was required to inform the surgeon if any of these variables did not conform with the study intent of a T1 N0 NSCLC completely resected.
Patient Follow-up
Postoperatively, all minor and major postoperative complications, mortality, and length of hospital stay were recorded. Patients were then followed at 3-month intervals for the first 2 years, and 6-month intervals for the subsequent 3 years, and yearly thereafter. Follow-up evaluation included history and physical examination, routine hematologic and biochemical analysis, and chest roentgenograms were monitored for evidence of recurrent disease. Pulmonary function tests were administered preoperatively, and at 6-month intervals postoperatively for the first 18 months. These included 1 second forced expiratory volume, forced volume capacity, maximum midexpiratory flow rate, and maximum voluntary ventilation.
Statistical Methods
Trial size and duration was originally determined by the number of patients and follow-up necessary for approximately 80 deaths and 70 recurrences (exclusive of second primaries) to occur, which yields a power of 0.9 to detect a 1.8-fold difference in median survival or a 1.85-fold difference in median time to recurrence, both treatment effects in favor of lobectomy, with a one-sided log rank test of size 0.10. This original design (in particular, the use of 
= 0.10, one-sided) had as its purpose to maximize the power of this equivalency study to detect a medically significant advantage for lobectomy, should it exist, given the practical constraints on accrual time and subsequent follow-up time. In conformance with this original design, we report the one-sided p values associated with the log rank tests of potential over-all survival and recurrence advantage differences in favor of lobectomy, and we declare as statistically significant those that are less than 0.10. Analyses of potential survival and recurrence differences within subgroups, and analyses of potential prognostic factors, are reported with two-sided p values and for these comparisons, 0.05 is the threshold for statistical significance.
In the analysis of the data, sites of relapse were categorized as ``local only'' (ipsilateral lung or mediastinum) versus ``nonlocal'' (distant sites as well as simultaneous local and distant sites). The Pearson 
2 test was used for contingency table analyses, with Yates continuity correction in the case of two-by-two tables [15]. Survival curves were estimated as in the Kaplan-Meier method [16], and significance tests were based on log rank statistics as given by Mantel but without continuity correction [17]. Adjusted survival analyses for stratification variables and for other important covariates were obtained from the Cox model [18] or from a stratified log rank score statistic. Variables were screened for prognostic value for death with a score statistic based on the proportional hazards model with stratification for treatment.
A number of definitions were used for the end points of the study. Disease-free interval was the number of days from randomization to proven detection of recurrence or metastases (locoregional, distant, or second primary). Recurrent disease was defined as the discovery of any new lesion considered to be recurrence of the original lung cancer and required pathologic proof. Locoregional recurrence included recurrence at or near the primary site or in lymphatic drainage areas, either bronchopulmonary or mediastinal. Second primary tumors in the lung were considered only if the lesion met accepted criteria [19]. Survival time was the number of days from randomization to death. All randomized patients were followed until death or study termination, unless lost to follow-up.
Results
Patient Population
The study was activated in February 1982 and was closed in November 1988 when 276 patients had been entered. An additional 495 patients were ``registered'' and appeared to eligible for the study before operation, but for various reasons were found to be ineligible at operation. Approximately 40% of these were found to have benign disease, 25% (because of tumor location or configuration) required more than a limited resection for adequate treatment, and 25% had greater than T1 N0 tumors or other than non-small cell histologies (Table 1
).
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Stratification and Prognostic Variables
There were no significant differences between the lobectomy patients and the limited resection patients for all stratification variables and selected prognostic factors (Table 2).
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Survival Differences
A total of 86 patients have died among the 247 eligible patients, 38 in the lobectomy group and 48 in the limited resection group. Of these 86 patients, 51 died with cancer at the time of death (21 in the lobectomy group and 30 in the limited resection group) and 35 died cancer-free. Both the death rates and the death with cancer rates were lower after lobectomy than after limited resection, although the observed differences were of borderline statistical significance (Table 3 and Fig 1). Limited resection was associated with a 30% increase in the overall death rate and a 50% increase in the observed death with cancer rate. These observed survival differences are reduced when the entire population of 276 patients is considered (to approximately 20% and 30%, respectively) and lose statistical significance.
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). There were statistically significant (p = 0.02 two-sided) increases in the death rates of patients older than 60 years and in patients with Karnofsky performance status less than 10 (hazard ratios equal to 1.8 and 1.6, respectively).
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and Fig 2). This observed increase in recurrence rate is 50% when the entire population of 276 randomized patients is considered but it maintains statistical significance (p = 0.06, one-sided). The approximate doubling of the recurrence rate, among eligible patients, associated with the limited resection arm appears to apply regardless of whether the intended resection was wedge or segmental (p < 0.10 more than two-sided, with or without inclusion of second primaries).
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). This effect appears to apply regardless of whether the histology was squamous or nonsquamous or whether the intended resection was wedge or segmental. The locoregional recurrence rate per person/year was 0.022 for lobectomy, 0.044 for segmental resection, and 0.086 for wedge resection.
Preservation of Pulmonary Function
Pulmonary function testing was performed preoperatively and postoperatively, but pulmonary function follow-up and reporting was judged to be not totally reliable after funding for the Lung Cancer Study Group was terminated in 1989. We report the results of the pulmonary function testing that were available as of July 1989. Of the eligible patients with at least 9 months follow-up at that time, only 60% received a 6-month pulmonary function examination. Compliance on the 12- to 18-month examination was only 66%. On the 6-month examination, the changes from baseline for all pulmonary function tests except the maximum midexpiratory flow rate are significantly better for patients receiving limited resection, but these treatment differences decrease and (excepting 1 second forced expiratory volume) lose statistical significance when we compare the 12- to 18-month pulmonary function tests (Table 5).
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).
Second Primary Cancer
Second primary cancers developed in 13 of the 247 eligible patients, a rate of 0.017 per person/year. Among these second primary tumors, nine occurred in the lobectomy group and four in the limited resection group. There were five second pulmonary malignancies (four in the lobectomy group and one in the limited resection group) and eight new primary malignancies in other sites.
Comment
Although this trial was designed to prove that a lesser resection would afford a similar chance of cancer-free survival and a no greater chance of local recurrence, unfortunately, the study proves that limited resection carries a significantly increased risk of local recurrence and a lesser chance of overall survival and disease-free survival. It should be noted, however, that the observed treatment differences for survival (time to death and time to death with cancer) are of borderline statistical significance for the analysis of eligible patients (p = 0.09, one-sided for both comparisons). Because this trial was an equivalency study, we were particularly concerned about failing to detect a potential benefit for lobectomy. In trials that involve testing a conservative experimental therapy against a more aggressive standard therapy, one is more concerned about failing to detect a potential benefit associated with the more aggressive therapy than if that therapy were the experimental therapy. To maximize the power of detecting a potential benefit for lobectomy, we set the significance level at 0.10, one-sided, in accord with common statistical practice reflected by the statement by Makruch and Simon [20] that in equivalency trials ``it will often be necessary to use a significance level of 0.10 or 0.20 rather than the usual 0.05 to avoid the more dangerous false negative conclusion.'' In contrast with the observed treatment differences for survival, the observed treatment difference for recurrence, excluding second primary, is quite substantial. Longer follow-up would be necessary for a final assessment of survival differences. For the above reasons, we cannot recommend less than a lobectomy for the treatment of even peripheral T1 N0 NSCLC when the patient can tolerate a lobectomy without significantly adverse effects on pulmonary function.
The original reports by Jensik and colleagues [4] from Rush-Presbyterian were extremely optimistic, suggesting that segmental resection was equivalent to lobectomy both in survival and freedom from recurrence for these early stage tumors. However, a recent analysis by the Rush-Presbyterian group, comparing, in a nonrandomized retrospective fashion, their recent results of segmental resection and lobectomy in these early stage patients corroborates our findings in this report of a higher local recurrence rate for patients treated by segmental resection [21].
Other reports have suggested that the addition of postoperative radiotherapy may decrease the local recurrence rate in patients undergoing wedge resection as definitive treatment, especially those with squamous cell carcinoma [8, 9]. Although there is no documented evidence, there is concern that postoperative radiotherapy to the surrounding pulmonary tissue confers at least as much pulmonary function loss as one would expect from a lobectomy. As well, the economic costs related to such additional therapy would be considerable.
This trial has important implications for the standard care of lung cancer patients. In North America of the 14% of patients who ultimately survive their lung cancer each year, it is estimated that at least 75% have stage I NSCLC tumors, about half of whom are T1 N0 [22]. The increased deaths conferred by the use of limited resection (versus lobectomy) would be substantial when one considers the worldwide lung cancer population.
In our study, there were no observed late functional advantages or decreased perioperative morbidity for limited resection. With the very gross methods of pulmonary function assessment performed in this trial, we could not demonstrate a prolonged benefit for limited resection, there being no significant difference in the two groups in ultimate pulmonary function as measured by us in the 12- to 18-month follow-up (except a modest benefit in 1 second forced expiratory volume). Other studies have demonstrated impaired pulmonary function after lobectomy but did not extend measurements beyond 6 months [13, 23, 24]. Our limited assessment suggests no medically significant difference at 12 to 18 months postoperatively. Similarly, the perioperative morbidity and mortality of limited resection was no different than that of lobectomy, save the 5% of patients requiring prolonged ventilation in the lobectomy group.
Many investigators, including proponents of video-assisted thoracoscopic techniques, have suggested the use of wedge resection for the definitive treatment of very small peripheral primary lung tumors [11, 12, 25]. The results of this study suggest that this frequently will not be adequate therapy. This is extremely relevant when using video-assisted techniques in cancer operations where lymph node staging may be less than complete and the temptation to perform a large wedge resection as definitive therapy is greatest. In such circumstances, it would be anticipated that a large number of patients would undergo less than adequate operation, leaving tumor behind at resection margins, in lymphatic channels, and lymph nodes. This would almost certainly result in even higher local recurrences and cancer death rates than in our study because of failure of adequate staging and resections.
The locoregional recurrence rates in this trial demonstrated a threefold increase with wedge resection and 2.4-fold increase with segmental resection compared to lobectomy. Although impossible to assess, it is believed that this increased locoregional recurrence with limited resection is most likely due to two factors: inadequate resection of the primary tumor or failure to identify and resect intrapulmonary microscopic and lymphatic spread of the tumor [26–32]. Occult intrapulmonary lymphatic and nodal disease almost certainly was present in limited resection patients accounting for the higher locoregional recurrence rate. It would be impossible for any pathologist to identify all microscopic lymphatic spread beyond the tumor but within the lobe.
It has been suggested that tumors less than 1 cm rarely contain lymphatic metastases and have a smaller risk of locoregional recurrence and greater chance of survival [11, 12, 25]. When we assessed this variable by estimating initial tumor volume (less than 3, 9, 27 cm3) we found no significant difference in locoregional recurrence or cancer death rates per person/year. Treatment of T1 N0 NSCLC, no matter the size, appears to be adversely affected by limited resection.
The importance of accurate intraoperative staging including lymph node sampling is demonstrated by the fact that more than 25% of patients with lung cancer (122 of 427) deemed to be clinically T1 N0 were found to have a higher stage of disease after the intraoperative maneuvers of primary tumor and lymph node assessment (Table 1).
There are certain instances where lobectomy cannot be the procedure of choice for patients with early stage lung cancer including patients with insufficient pulmonary reserve to tolerate a lobectomy, especially those patients where a previous contralateral pneumonectomy has been performed [33]. In such instances, a lesser resection is appropriate treatment with segmental resection affording in lesser risk of locoregional recurrence than wedge resection.
This study has failed to demonstrate the equivalence of wedge or segmental resection to lobectomy for those patients with lung cancer deemed to have a peripheral NSCLC T1 N0 tumor. Lobectomy with systematic hilar and mediastinal lymph node sampling or dissection should remain the standard surgical treatment for such individuals.
Appendix 1. Participating Institutions
Principal investigators of institutions participating in this study include E. Carmack Holmes (Lung Cancer Study Group Chairman, University of California, Los Angeles, CA); John C. Ruckdeschel (Albany Medical College, Albany, NY); Michael Johnston (University of Colorado, Denver, CO); Paul A. Thomas, Jr (Illinois Cancer Council, Chicago, IL); Jean Deslauriers (Hospital Laval, Quebec, Canada); Frederick L. Grover (University of Texas Health Science Center, San Antonio, TX); Lucius D. Hill (Fred Hutchinson Cancer Research Center, Seattle, WA); Ronald Feld, Robert J. Ginsberg (University of Toronto, Toronto, Ont, Canada); and Clifton F. Mountain (University of Texas Reference Center for Anatomic and Pathologic Classification, Houston, TX). Members of the Lung Cancer Study Group participating in this study included John C. Ruckdeschel, Stanley Dzuiban, Maureen Kiely, Martin F. McKneally, Darroch W. O. Moores, Carmella Ramnes, Henry Wagner, Jr (Albany Medical College, Albany, NY); Michael Johnston, Paul Bunn, Henry Chu, David Dienhart, Mark Hazuka, Jeannie Kinzie, Julie Sorensen, Virginia Vance (University of Colorado Health Sciences Center, Denver, CO); Thomas Braun, Alan Hopeman, Madeline Kane, Paul Russ, Glen J.R. Whitman (Veterans Administration Medical Center, Denver, CO); Stephen M. Fall, Dana P. Hansen, Randal H. Henderson, Christian L. Moncrief, Fred Pauling, Jerry Sims, Dan Tell, Sandra Wisely-Carr (Fitzsimmons Army Medical Center, Aurora, CO); Charles M. Abernathy, Douglas A. Clark, Brian McCroskey, George Moore, Fred Moore, Adam Myers, Madeline White (Denver General Hospital, Denver, CO); Robert J. Brooks, Malcolm Bull, F. Bing Johnson, Margaret Neimyr, Fred R. Paquette, Geno Saccomanno (St. Mary's Hospital & Medical Center, Grand Junction, CO); Paul A. Thomas, Jr, Thomas Lad, Karen Hermansen, Edwin Liebner, William P. McGuire III (University of Illinois/West Side Medical Center, Chicago, IL); Willard Fry, Barbara Stempelfeld, John C. Alexander, Jr, Janet Beck, Rafael M. Garces, Joseph P. Imperato, Janu Kahandekar, Richard Knop, Gershon Locker, Douglas E. Merkel, Joseph S. Panella, David Rochester, Thomas A. Victor (Evanston Hospital, Veterans Hospital, Hines, IL); Carole Johnson (Illinois Cancer Council, Chicago, IL); Axel W. Joob, P. Robinson, S. Rosen, T. Shields (Lakeside Veterans Administration Medical Center, San Antonio, TX); Suzette Dooley, Fermin O. Tio, Carol Holland (Audie Murphy Veterans Administration Hospital, San Antonio, TX); Robert L. Treasure, Brigida Gottfried (San Antonio Chest Hospital, San Antonio, TX); George Beddingfield, Jeffrey Bower, David Cheng, Mary B. Daly, William A. Ladd, Christopher Leach, Kim Murphy, Ronald Quinton, Vernon C. Smith, Mary E. Young (Wilford Hall Medical Center, Lackland Air Force Base, Ft Sam Houston, TX); Mack Blanton, Richard Briggs, Brent A. Grishkin, Robert Helsel, Douglas Jackson, Michael E. Jackson, Richard Young, Arlene Zaloznik (Brook Army Medical Center, Ft Sam Houston, TX); Lucius D. Hill, Kathleen Block, David H. Dail, David Dreis, Steven W. Guyton, M. Hafermann, Samuel P. Hammar, Philip C. Jolly, E. Morgan, Steven Springmeyer, Eric W. Taylor, Paul W. Weiden (Virginia Mason Medical Center, Seattle, WA); Nancy Knudsen (Fred Hutchinson Cancer Center, Seattle, WA); Robert B. Livingston, Valerie W. Rusch (University Hospital Medical Center, Seattle, WA); Clive Grafton, Jean LeRiche, Nevin Murray, Ruth Page (Cancer Control Agency of British Columbia, Vancouver, BC); Gary E. Goodman, Ralph W. Aye (Swedish Medical Center, Seattle, WA); Kenneth G. Evans, Roberta R. Miller, Bill Nelems (Vancouver General Hospital, Vancouver, BC); Celestia Higano (Veterans Administration Medical Center, Seattle, WA); Ronald Feld, Daniel Bergsagel, Thomas C. Brown, John Curtis, David Payne, Jack F. Pringle, Ian Quirt, Lesley Steward, David Warr, Lim Yeoh (The Princess Margaret Hospital, Toronto, Canada); Ronald Burkes, Noel Cooter, Melvyn Goldberg, Brendan Mullen, Barbara Schmocker (Mount Sinai Hospital, Toronto, Canada); Fred Harris, Riivo Ilves, James M. Sinclair, Ernest Spratt (St. Joseph's Health Center, Toronto, Canada); Michael Baker, Dean W. Chamberlain, Joel D. Cooper, Diane DeSantis, William K. Evans, G. Alexander Patterson, F. Griffith Pearson, Alexander C. Ritchie, Frances A. Shepherd, Diane Taylor, Thomas R. J. Todd, Jan Webster, Timothy L. Winton (Toronto General Hospital, Toronto, Canada); Thomas J. Kirby, Michael Lipa, Sandra French, David Sutton, Ellen Warner, Paul F. Waters (Toronto Western Hospital, Toronto, Canada); Donald Jones (Wellesley Hospital, Toronto, Canada); E. Carmack Holmes, Robert A. Selch, Josephine Shiplacoff (University of California at Los Angeles School of Medicine, Los Angeles, CA); Patricia Ganz, Barry Silverman (Sepulveda Veterans Administration Hospital, Sepulveda, CA); Charles Haskell, Ahmad Sadeghi, Adrian Williams, Jerome Wollman (Wadsworth Veterans Administration Hospital, Los Angeles, CA); Jack H. Bloch, Michael P. Corder (Kern Medical Center, Los Angeles, CA); Clifton F. Mountain, Kay Hermes, John M. Lukeman, Anne Murphy (University of Texas Reference Center for Anatomic and Pathologic Classification, Houston, TX); Steven Piantadosi, Steve Goodman (The Johns Hopkins Oncology Center, Baltimore, MD); Lawrence V. Rubinstein, Mitchell H. Gail, Jr (National Cancer Institute, Rockville, MD); Marilyn Bossenga, William H. Lake, Jr, Sherrill Long (Information Management Services, Inc, Rockville, MD).
Footnotes
Address reprint reuests to Dr Ginsberg, Thoracic Service, Department of Surgery, Memorial Sloan-Kettering Cancer Center, 1275 York Ave, New York, NY 10021.
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M. J. Schuchert, B. L. Pettiford, S. Keeley, T. A. D'Amato, A. Kilic, J. Close, A. Pennathur, R. Santos, H. C. Fernando, J. R. Landreneau, et al. Anatomic Segmentectomy in the Treatment of Stage I Non-Small Cell Lung Cancer Ann. Thorac. Surg., September 1, 2007; 84(3): 926 - 933. [Abstract] [Full Text] [PDF]
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W. J. Scott, J. Howington, S. Feigenberg, B. Movsas, and K. Pisters Treatment of Non-small Cell Lung Cancer Stage I and Stage II: ACCP Evidence-Based Clinical Practice Guidelines (2nd Edition) Chest, September 1, 2007; 132(3_suppl): 234S - 242S. [Abstract] [Full Text] [PDF]
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A. El-Sherif, H. C. Fernando, R. Santos, B. Pettiford, J. D. Luketich, J. M. Close, and R. J. Landreneau Margin and Local Recurrence After Sublobar Resection of Non-Small Cell Lung Cancer Ann. Surg. Oncol., August 1, 2007; 14(8): 2400 - 2405. [Abstract] [Full Text] [PDF]
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T. Tsuchiya, S. Hashizume, S. Akamine, M. Muraoka, S. Honda, K. Tsuji, S. Urabe, T. Hayashi, N. Yamasaki, and T. Nagayasu Upstaging by Vessel Invasion Improves the Pathology Staging System of Non-Small Cell Lung Cancer Chest, July 1, 2007; 132(1): 170 - 177. [Abstract] [Full Text] [PDF]
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B. A. Whitson, R. S. Andrade, A. Boettcher, R. Bardales, R. A. Kratzke, P. S. Dahlberg, and M. A. Maddaus Video-Assisted Thoracoscopic Surgery is More Favorable Than Thoracotomy for Resection of Clinical Stage I Non-Small Cell Lung Cancer Ann. Thorac. Surg., June 1, 2007; 83(6): 1965 - 1970. [Abstract] [Full Text] [PDF]
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M. Okada, S. Tauchi, K. Iwanaga, T. Mimura, Y. Kitamura, H. Watanabe, S. Adachi, T. Sakuma, and C. Ohbayashi Associations among bronchioloalveolar carcinoma components, positron emission tomographic and computed tomographic findings, and malignant behavior in small lung adenocarcinomas J. Thorac. Cardiovasc. Surg., June 1, 2007; 133(6): 1448 - 1454. [Abstract] [Full Text] [PDF]
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P. Vaughan, I. Oey, A. Nakas, A. Martin-Ucar, J. Edwards, and D. Waller Is there a role for therapeutic lobectomy for emphysema? Eur. J. Cardiothorac. Surg., March 1, 2007; 31(3): 486 - 490. [Abstract] [Full Text] [PDF]
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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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M. Okada, T. Mimura, J. Ikegaki, H. Katoh, H. Itoh, and N. Tsubota A novel video-assisted anatomic segmentectomy technique: Selective segmental inflation via bronchofiberoptic jet followed by cautery cutting J. Thorac. Cardiovasc. Surg., March 1, 2007; 133(3): 753 - 758. [Abstract] [Full Text] [PDF]
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