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Ann Thorac Surg 2006;81:1013-1020
© 2006 The Society of Thoracic Surgeons
Accepted for publication June 24, 2005.
* Address correspondence to Dr Allen, Division of General Thoracic Surgery, Mayo Clinic, 200 First St SW, Rochester, MN 55905 (Email: allen.mark{at}mayo.edu).
Presented at the Forty-first Annual Meeting of The Society of Thoracic Surgeons, Tampa, FL, Jan 24–26, 2005. Winner of the J. Maxwell Chamberlain Memorial Award for General Thoracic Surgery.
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Abstract |
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METHODS: Prospectively collected 30-day postoperative data was analyzed from 1,111 patients undergoing pulmonary resection who were enrolled from July 1999 to February 2004 in a randomized trial comparing lymph node sampling versus mediastinal lymph node dissection for early stage lung cancer.
RESULTS: Of the 1,111 patients randomized, 1,023 were included in the analysis. Median age was 68 years (range, 23 to 89 years); 52% were men. Lobectomy was performed in 766 (75%) and pneumonectomy in 42 (4%). Pathologic stage was IA in 424 (42%), IB in 418 (41%), IIA in 37 (4%), IIB in 97 (9%), and III in 45 (5%). Lymph node sampling was performed in 498 patients and lymph node dissection in 525. Operative mortality was 2.0% (10 of 498) for lymph node sampling and 0.76% (4 of 525) for lymph node dissection. Complications occurred in 38% of patients in each group. Lymph node dissection had a longer median operative time and greater total chest tube drainage (15 minutes, 121 mL, respectively). There was no difference in the median hospitalization, which was 6 days in each group (p = 0.404).
CONCLUSIONS: Complete mediastinal lymphadenectomy adds little morbidity to a pulmonary resection for lung cancer. These data from a current, multiinstitutional cohort of patients who underwent a major pulmonary resection constitute a new baseline with which to compare results in the future.
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Introduction |
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Variability exits among surgeons' opinions as to whether to remove all, some, or none of the mediastinal lymph nodes at the time of pulmonary resection for lung cancer; therefore, practices vary widely throughout the world. Surgeons in some cancer centers perform a complete mediastinal lymphadenectomy, whereas others sample lymph nodes when a visual or palpable abnormality is found. Unfortunately, despite the fact that surgical staging of mediastinal lymph nodes is thought to be important, most surgeons do not perform a complete lymphadenectomy at the time of lung cancer resection. Reasons that a complete mediastinal lymphadenectomy is not performed include the perception that this may lead to more complications, prolonged hospitalization, or increased mortality, and may not affect long-term survival.
The American College of Surgery Oncology Group Z0030 study is a randomized, multiinstitutional, prospective trial designed to determine whether long-term survival is affected by mediastinal lymph node dissection (LND) versus lymph node sampling (LNS) at the time of pulmonary resection for lung cancer. A secondary objective is to compare morbidity and mortality between the two arms to determine whether mediastinal LND adversely affects the patient's outcome. This report presents the initial results from this randomized multiinstitutional trial and compares the short-term outcomes between patients who underwent LND and patients who underwent LNS only.
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Material and Methods |
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Exclusion criteria included patients who had T3 or T4 tumors, patients who were treated with pulmonary wedge excision, and patients who received prior chemotherapy or radiation therapy for their cancer. After randomization, retrospective review found 155 patients to be ineligible for participation. The reason for ineligibility was minor (eg, timing violation) in 67 of these patients, and they are therefore included in this analysis. The remaining 88 patients (56 in the LNS group and 33 in the LND group) were excluded. The reasons for exclusion were incorrect stage in 29 patients, inadequate LNS in 14, benign disease in 6, insufficient documentation in 5, and other reasons in 34 patients. The remaining 1,023 patients form the basis of this study.
All surgeons participating in the trial were general thoracic surgeons and diplomats of the American Board of Thoracic Surgery or the equivalent. There were 102 different surgeons from 63 institutions who enrolled patients into the trial. The enrolling surgeon was required to read a detailed description of the technique of mediastinal LND and watch a video that demonstrated the technique of a complete mediastinal LND. All operative notes were reviewed by the principal investigators (M.S.A. or G.E.D.) for completeness of the mediastinal dissection and adherence to the protocol. Lymph nodes were named according to The American Thoracic Society lymph node stations [2]. Lymph node stations sampled for tumors on the right were 2R, 4R, 7, and 10R. For tumors on the left, stations 5, 6, 7, and 10L were sampled. Any other lymph node that was thought to be suspicious for metastasis was also biopsied. If all required lymph nodes excised showed no evidence of cancer on frozen-section examination, patients were randomized to either LNS only with no further lymph node dissection or to complete mediastinal LND.
Complete mediastinal LND for tumors on the right involved removing all lymph tissue from an area bounded caudally by the takeoff of the right upper lobe, superiorly by the innominate artery, anteriorly by the superior vena cava, and posteriorly by the trachea. All tissue was removed from this area, and at the completion of the dissection the trachea, vagus nerve, and the superior vena cava were visible. Lymph nodes in the prevascular area, adjacent to the superior vena cava, were removed as were the lymph nodes in the retrotracheal area. Complete mediastinal LND for tumors on the left involved removing all lymph tissue from the area between the phrenic nerve anteriorly and the vagus nerve posteriorly. Superiorly, all lymph tissue was removed to the top of the aortic arch. The caudal boundary was the left mainstem bronchus. At the completion of the dissection the aortopulmonary window was free of lymph tissue and the recurrent nerve was preserved. Regardless of the side of the tumor, all subcarinal, inferior pulmonary ligament, periesophageal, lobar, and intralobar lymph nodes were resected. Complete subcarinal LND included removing all lymph tissue caudal to the carina and both left and right mainstem bronchi. All lymph nodes adjacent to the inferior pulmonary ligament and the caudal half of the esophagus were also removed. When the dissection was complete, both mainstem bronchi, the posterior pericardium, and the esophagus were free of all lymph tissue. During resection of the lung all lobar and interlobar lymph nodes were resected.
Fisher's exact test was used to compare treatment regimens relative to rates of operative mortality and morbidity [3]. Operative mortality included all patients who died within the first 30 days after surgery or during the same hospitalization. The Wilcoxon test was used to compare groups relative to ordinal variables such as chest tube drainage [4]. Logistic regression was used to assess the relationship between age and key measurements of morbidity. All statistical tests reported in the manuscript are two-sided. The threshold of significance was set at p less than 0.05.
The protocol was approved by the central Institutional Review Board, and the Institutional Review Board of each institution that enrolled patients. All patients signed informed consent.
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Results |
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One or more complications occurred in 38% of patients in each group. There was no difference in the rate of any specific complication between the two groups (Table 4). Specifically, there were no statistical differences in the frequency of chylothoraces, postoperative hemorrhage requiring reoperation, number of patients requiring a postoperative transfusion, recurrent nerve injuries, or bronchopleural fistulas.
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Operative mortality by the type of operation is shown in Table 5. There was no association between the type of resection and mortality. No patient died after a pneumonectomy. The operative mortality by age is shown in Table 6. Operative mortality was not associated with patient age. The cause of death was multisystem organ failure in 4, pneumonia in 3, cerebral vascular accident in 2, hepatic failure in 2, myocardial infarction in 1, and unknown in 2.
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Comment |
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Our findings are in general agreement with the study reported by Izbicki and associates [6], which described 201 randomized patients and demonstrated no increase in the rate of chylothorax, recurrent nerve injuries, or bronchopleural fistulas after mediastinal lymphadenectomy. In their trial, a more extensive LND was performed. They performed an extensive prevascular dissection for tumors located on the right side that also included a thymectomy and a phrenic nerve and brachiocephalic vein dissection. They also found an increase in operative time. Additionally, they had more prolonged air leaks and more hemorrhage in the LND group. The absence of additional complications associated with LND in our study may be explained by the decision not to include the more radical prevascular dissection as part of the LND protocol.
Because adjuvant chemotherapy is now the standard of care for patients with positive N2 lymph nodes, patients should be staged as accurately as possible. We found a small number of patients with positive N2 lymph nodes in the group that underwent LND. Presumably, these patients would have been understaged without the mediastinal dissection and not received appropriate postoperative therapy. Whether or not this stage migration will eventually be an important factor that affects overall long-term survival awaits further follow-up. However, given the absence of additional complications, complete mediastinal LND should be performed in all patients to accurately stage their disease.
The data from our current trial also sets a modern benchmark for operative mortality and morbidity for lung cancer patients after pulmonary resection. The design of our study is similar to that of the Lung Cancer Study Group, reported in the early 1980s [7]. Operative mortality in the 2,220 pulmonary resections reported by Ginsberg and colleagues [7] was 3.8%, compared with 1.4% in the current study. Operative mortality in the Lung Cancer Study Group for pneumonectomy and lobectomy was 6.2% and 2.9%, respectively, compared with 0% and 1.3%, respectively, in the current study. This improvement undoubtedly reflects the improvements that have occurred in preoperative selection, intraoperative techniques, and postoperative management that have occurred in the past 20 years. Another observed difference was the pneumonectomy rate in the two groups: 25.6% in the Lung Cancer Study Group and 4% in our group. This difference most likely reflects the fact that our series was limited to patients with early stage disease.
A smaller series, reported by Silvestri and coworkers [8], observed an operative mortality of 3% for lobectomy and 11.8% for pneumonectomy. These operations were also performed by board-certified thoracic surgeons; however, the results are quite different from ours. The apparent reduction in mortality in our series may reflect our different patient eligibility criteria.
A recent series of 2,044 patients from a single institution in Japan reported an overall 1.3% mortality and a 3.2% operative mortality for pneumonectomy [9]. Our multiinstitutional results compare favorably with this large, single-institution report, demonstrating that outstanding outcomes are also possible in a multiinstitutional trial. The result from these American College of Surgery Oncology Group data sets a modern standard for operative mortality for lung cancer patients undergoing pulmonary resection and should be used in the future when comparing nonoperative treatments to pulmonary resection for patients with early stage lung cancer.
We did not observe an association between age and mortality as others have reported [10, 11]. In the report by Wada and associates [9], operative mortality increased with advancing age. A similar finding was observed in the 1981 Lung Cancer Study Group report [7]. In these later two reports the most common cause of death was respiratory failure. In contrast, we did not identify a consistent cause of death. In our series the most common cause of death was multisystem organ failure, but this accounted for less than one third of our operative deaths. We were unable to identify any factors that consistently led to postoperative mortality.
Complications in our study, although not specific to mediastinal LND, were frequent (38%). The most common complications were atrial arrhythmias, prolonged air leaks, and excessive chest tube drainage. Although these are usually not life-threatening complications, they prolong hospitalization and reflect adverse patient experience. Unfortunately the frequency of these complications has not changed much in recent years, a fact which highlights the need for improvement. Reduction of the frequency of these problems will improve patient care, and their elimination should be an area of active research.
In summary we have demonstrated in a large, prospective, multiinstitutional randomized trial that mediastinal LND does not increase operative mortality or the number or type of complications when compared with LNS in patients undergoing pulmonary resection for early stage lung cancer. The 1.4% operative mortality should be the new standard of reference for surgical management of early stage lung cancer. This study demonstrated only a small effect of LND on the stage distribution of randomized patients. The impact of LND versus simple sampling on long-term cancer survival will require further follow-up and is reserved for future publications.
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Appendix |
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Abramson Cancer Center of the University of Pennsylvania: Joseph B. Shrager; Allegheny Cancer Center Network: Robert J. Keenan, Rodney J. Landreneau; Beth Israel Deaconess Medical Center, Boston, MA: Joseph LoCicero, Robert Lee Thurer; Beth Israel Medical Center, New York, NY: Steven M. Keller; Bethesda North Hospital: Donald C. Buckley; Cedars-Sinai Medical Center: Robert J. McKenna; Central Baptist Hospital; Creighton University Medical Center: Walter J. Scott; Veterans Affairs Medical Center: John D. Mitchell; Edward Hospital: Phyllis C. Bleck; Englewood Hospital and Medical Center; Fox Chase Cancer Center: Melvyn Goldberg, Walter J. Scott; Good Samaritan Hospital (Cincinnati): J. Michael Smith; Holmes Regional Medical Center: Michael A. Greene, Mark A. Malias; Huntington Memorial Hospital: Robbin G. Cohen; Jameson Hospital: Rodney J. Landreneau; Jewish Hospital: Roy G. Bowling; Lankenau Medical Research Center: Ned Z. Carp; Latter Day Saints Hospital: Michael P. Collins; Lenoir Memorial Hospital: Joseph D. Whitlark; London Health Sciences Centre (University of Western Ontario Medical Center): Richard I. Inculet, Richard A. Malthaner; Loyola University Medical Center: Wickii T. Vigneswaran; M.D. Anderson Cancer Center (University of Texas): Joe B. Putnam, David Christopher Rice, Jack A. Roth, Ara A. Vaporciyan; Mary Imogene Bassett Hospital: M. Bernadette Ryan; Massachusetts General Hospital: Henning A. Gaissert; Mayo Clinic (Rochester): Mark S. Allen, Claude Deschamps, Daniel L. Miller, Francis C. Nichols; Medical Center of Central Georgia; Medical Center of Southwest Louisiana: Mitchell D. Lirtzman; Medical College of Virginia Hospital (Virginia Commonwealth University): Neri M. Cohen; Memorial Medical Center (Southern Illinois University School of Medicine): Stephen R. Hazelrigg; Memorial Sloan-Kettering Cancer Center: Manjit S. Bains, Valerie W. Rusch, Robert J. Downey, Robert J. Ginsberg; Mobile Infirmary Medical Center: Scott Bradley, Gaylord T. Walker; New York Hospital—Cornell University Medical Center: Nasser K. Altorki, Jeffrey L. Port; Omaha Veterans Administration Medical Center: Walter J. Scott; Peter MacCallum Cancer Institute: Gavin M. Wright; Providence Portland Medical Center: Emery Charles Douville, John R. Handy, Gary Yee Ott, Andrew C. Tsen; Rhode Island Hospital: Henning A. Gaissert; Roswell Park Cancer Institute: Timothy M. Anderson, Todd L. Demmy, Chukwumere E. Nwogu; Saint Clair Hospital: Rodney J. Landreneau; Saint John's Hospital: Stephen R. Hazelrigg; Saint Luke's Hospital of Duluth: John M. Streitz; Saint Thomas Hospital (Nashville): Jonathan C. Nesbitt; Saint Vincent Hospital (Green Bay): Edward J. Coleman; Saint Vincent's Hospital, Melbourne: Gavin M Wright; Stanford University (Hospital): Richard I. Whyte; Stony Brook University Hospital; Thomas Jefferson University Hospital: Taine T. Pechet; Toronto General Hospital: Gail E. Darling, Michael R. Johnston, Shafique Keshavjee, Andrew F. Pierre, Thomas K. Waddell; Trinity Cancer Care Center (Minot): Martin L. Rothberg; University of California San Francisco Medical Center (Long-Moffitt): David M. Jablons; University of California, Irvine: Jeffrey C. Milliken; University of Chicago (Hospitals): Mark K. Ferguson; University of Cincinnati Medical Center: John A. Howington, Michael F. Reed; University of Miami: Kushagra Katariya, Richard J. Thurer; University of Missouri—Ellis Fischel: Todd L. Demmy; University of Pittsburgh—Presbyterian Hospital: Percival O. Buenaventura, Robert J. Keenan, Rodney J. Landreneau, James D. Luketich; University of Pittsburgh (Shadyside Hospital): Neil A. Christie, Rodney J. Landreneau, James D. Luketich; University of Pittsburgh Medical Center—St. Margaret Hospital: Rodney J. Landreneau; University of Rochester (Medical Center): Richard H. Feins, David W. Johnstone, Thomas J. Watson; University of South Alabama: Joseph LoCicero; University of Virginia (Medical Center): Thomas M. Daniel, David R. Jones; University of Washington Medical Center: Eric Vallieres, Douglas E. Wood; University of Wisconsin: Tracey L. Weigel; Upstate Medical University (SUNY-Upstate Syracuse): Elizabeth U. Dexter, Leslie J. Kohman; VA Medical Center—Cincinnati: John A. Howington, Michael F. Reed; Valley Hospital: Youngick Lee, Elias N. Tsoukas; Veterans Administration Center, Seattle (Puget Sound): Eric Vallieres; Veterans Administration Medical Center—Minneapolis: Rosemary F. Kelly; Washington University (Barnes Jewish Hospital): Richard J.Battafarano, Joel D. Cooper, Bryan F. Meyers, G. Alexander Patterson; West Virginia University (Mary Babb Randolph Cancer Center): Geoffrey M. Graeber; Western Pennsylvania Hospital: Robert J. Keenan, Rodney J. Landreneau; Westmoreland Hospital: Robert J. Keenan, Rodney J. Landreneau; William Beaumont Hospital (Royal Oak): Gary W. Chmielewski.
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Discussion |
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TopAbstractIntroductionMaterial and MethodsResultsCommentDiscussionFootnotesAcknowledgmentsReferences |
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In that series, 2,220 pulmonary resections done between 1979 and 1981 were analyzed, and the overall 30-day operative mortality was 3.7%; for lobectomy, the mortality rate was 2.89%; and for pneumonectomy, which included both simple and extended operations, it was 6.2%. Mortality rates increased according to the age of the patient; for example, patients in their seventh or eighth decade had mortality rates more than three times those of patients under the age of 60.
This morning, Dr Allen showed that with improved perioperative care, the mortality associated with surgery of lung cancer can be further lowered to 1.3%. Most importantly, he showed that there is no increase in operative mortality in older patients, as was the case in the Lung Cancer Study Group study.
What will be the impact of these important messages for the thoracic surgical community? First and foremost, new standards will be set, with the understanding that the cohort of patients presented today exclude individuals with higher stage tumors, which often require more extensive resections and are at higher risk of operative mortality. As a result of Dr Allen's paper, it is also likely that our medical colleagues will be expecting us to operate more liberally in elderly patients. I will venture to predict that the tradeoff will be a significant increase in both minor and major morbidities, especially in patients who are between 70 and 80 years of age.
The last message derived from this American College of Surgeons Oncology Group report is that complete mediastinal lymphadenectomy is safe. For those who believe that complete lymphadenectomy should be part of every lung cancer operation, this report has extra significance because it is the first one that shows through a randomized trial that mediastinal lymphadenectomy is not associated with increased morbidity.
In closing, I would like to congratulate the American College Study Oncology Group for their excellent clinical results and thank Dr Allen for sending me this manuscript way ahead of this meeting.
DR JOSEPH SHRAGER (Philadelphia, PA): Mark, correct me if I am wrong, but I think that the surgeons who participate in the ACOSOG thoracic studies are almost entirely thoracic surgeons—I may be wrong about that—and in fact, they're probably almost entirely highly specialized general thoracic surgeons. If you compare your results to a study that is going to be presented later today from the ACS (American Cancer Society) Commission on Cancer, with data that's from 729 hospitals that I think probably includes much more of a cross section of surgeons, including general surgeons, one sees that you report a mortality of 1.4% versus that study's 4.4%. I wonder if you could just comment on that, especially in light of other recent data that specialization, volume, et cetera, leads to improved outcome.
DR ALLEN: I would like to thank Dr Deslauriers for his kind comments. I think it is worth repeating, as Dr Deslauriers has just mentioned, that good results are possible in a clinical trial. This study highlights that fact and it should encourage us to tell our patients that clinical trials are good for them and we should try to enroll patients in clinical trials.
The fact that more older patients didn't die in our trial is probably a statistical anomaly. As you saw, there was a trend for more mortality or more complications as patients got older; however, it did not reach statistical significance.
Doctor Shrager, almost all of the surgeons participating in this trial were specialized in general thoracic surgery, they were all American board certified or the equivalent, so perhaps that made a difference. The other important point is that the group of patients that we operated on all had early stage lung cancer. Eligibility criteria excluded patients who had large complex cancers, or were given preoperative chemotherapy or radiation therapy.
In closing, I would like to express my appreciation to the late Dr Robert J. Ginsberg for his valuable leadership in designing and implementation of this clinical trial. This was really his vision, and it is unfortunate that he did not survive to see the results of his hard work and vision.
Thank you.
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Acknowledgments |
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 M. Lock and G. Rodrigues Computed tomographic screening for lung cancer Can Fam Physician, August 1, 2007; 53(8): 1334 - 1336. [Full Text] [PDF]
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M. Muraoka, S. Akamine, T. Oka, T. Tagawa, A. Nakamura, T. Tsuchiya, T. Hayashi, and T. Nagayasu Sentinel node sampling limits lymphadenectomy in stage I non-small cell lung cancer Eur. J. Cardiothorac. Surg., August 1, 2007; 32(2): 356 - 361. [Abstract] [Full Text] [PDF]
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C. A. Meyer "Transthoracic Needle Aspiration Biopsy of Benign and Malignant Lung Lesions"--A Commentary Am. J. Roentgenol., April 1, 2007; 188(4): 891 - 893. [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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 G. M Wright, J-E C Holty, and M K Gould When in doubt should we cut it out? The role of surgery in non-small-cell lung cancer Thorax, February 1, 2007; 62(2): 190 - 191. [Full Text] [PDF]
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A. Brunelli, N. J. Morgan-Hughes, M. Refai, M. Salati, A. Sabbatini, and G. Rocco Risk-adjusted morbidity and mortality models to compare the performance of two units after major lung resections J. Thorac. Cardiovasc. Surg., January 1, 2007; 133(1): 88 - 96. [Abstract] [Full Text] [PDF]
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E. Belcher and P. Goldstraw Is radical mediastinal dissection mandatory for curative resection of NSCLC? Eur. J. Cardiothorac. Surg., January 1, 2007; 31(1): 142 - 143. [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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S. Ganti, R. Milton, V. Anikin, and A. Thorpe Surgery for tumour recurrence in a pneumonectomy space. Eur. J. Cardiothorac. Surg., October 1, 2006; 30(4): 683 - 685. [Abstract] [Full Text] [PDF]
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F. Leo, P. Solli, G. Veronesi, D. Radice, A. Floridi, R. Gasparri, F. Petrella, A. Borri, D. Galetta, and L. Spaggiari Does chemotherapy increase the risk of respiratory complications after pneumonectomy? J. Thorac. Cardiovasc. Surg., September 1, 2006; 132(3): 519 - 523. [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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J-E C Holty and M K Gould When in doubt should we cut it out? The role of surgery in non-small cell lung cancer. Thorax, July 1, 2006; 61(7): 554 - 556. [Full Text] [PDF]
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