Semin Respir Crit Care Med 2016; 37(05): 708-715
DOI: 10.1055/s-0036-1592173
Review Article
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Surgical Treatment of Early l Stage Lung Cancer: What has Changed and What will Change in the Future

Huan H. Sun
1   Department of Cardiothoracic Surgery, NYU School of Medicine, New York, New York
,
Joanna Sesti
2   Department of Cardiothoracic Surgery, University of Pittsburgh, Pittsburgh, Pennsylvania
,
Jessica S. Donington
1   Department of Cardiothoracic Surgery, NYU School of Medicine, New York, New York
› Author Affiliations
Further Information

Publication History

Publication Date:
12 October 2016 (online)

Abstract

Recent advances in the surgical treatment of early stage non-small cell lung cancer (NSCLC) have focused heavily on making procedures less invasive, less radical, and better tolerated. Advances in accuracy and increased utilization of cross-sectional imaging allows for diagnosis of smaller and more indolent tumors and preinvasive lesions. Similar to advanced disease, early-stage treatment is now being tailored to individual patients and their tumors. Sublobar resections are gaining acceptance as an oncologically equivalent approach to lobectomy in well-selected stage I patients. Minimally invasive approaches either by video-assisted thoracoscopic surgery (VATS) or robotic-assisted thoracic surgery are becoming the procedures of choice for anatomic NSCLC resections and provide decreased perioperative complications and increased tolerability, especially in the elderly and medically high-risk patients. Reports of even less invasive techniques including uniportal VATS and nonintubated lobar resections are now appearing in the literature.

 
  • References

  • 1 Rami-Porta R, Ball D, Crowley J , et al; International Staging Committee; Cancer Research and Biostatistics; Observers to the Committee; Participating Institutions. The IASLC Lung Cancer Staging Project: proposals for the revision of the T descriptors in the forthcoming (seventh) edition of the TNM classification for lung cancer. J Thorac Oncol 2007; 2 (7) 593-602
  • 2 Goldstraw P, Crowley J, Chansky K , et al; International Association for the Study of Lung Cancer International Staging Committee; Participating Institutions. The IASLC Lung Cancer Staging Project: proposals for the revision of the TNM stage groupings in the forthcoming (seventh) edition of the TNM Classification of malignant tumours. J Thorac Oncol 2007; 2 (8) 706-714
  • 3 Swanson SJ, Herndon II JE, D'Amico TA , et al. Video-assisted thoracic surgery lobectomy: report of CALGB 39802—a prospective, multi-institution feasibility study. J Clin Oncol 2007; 25 (31) 4993-4997
  • 4 Sugiura H, Morikawa T, Kaji M, Sasamura Y, Kondo S, Katoh H. Long-term benefits for the quality of life after video-assisted thoracoscopic lobectomy in patients with lung cancer. Surg Laparosc Endosc Percutan Tech 1999; 9 (6) 403-408
  • 5 Flores RM, Park BJ, Dycoco J , et al. Lobectomy by video-assisted thoracic surgery (VATS) versus thoracotomy for lung cancer. J Thorac Cardiovasc Surg 2009; 138 (1) 11-18
  • 6 Scott WJ, Allen MS, Darling G , et al. Video-assisted thoracic surgery versus open lobectomy for lung cancer: a secondary analysis of data from the American College of Surgeons Oncology Group Z0030 randomized clinical trial. J Thorac Cardiovasc Surg 2010; 139 (4) 976-981 , discussion 981–983
  • 7 Ilonen IK, Räsänen JV, Knuuttila A, Salo JA, Sihvo EI. Anatomic thoracoscopic lung resection for non-small cell lung cancer in stage I is associated with less morbidity and shorter hospitalization than thoracotomy. Acta Oncol 2011; 50 (7) 1126-1132
  • 8 Lee PC, Nasar A, Port JL , et al. Long-term survival after lobectomy for non-small cell lung cancer by video-assisted thoracic surgery versus thoracotomy. Ann Thorac Surg 2013; 96 (3) 951-960 , discussion 960–961
  • 9 Higuchi M, Yaginuma H, Yonechi A , et al. Long-term outcomes after video-assisted thoracic surgery (VATS) lobectomy versus lobectomy via open thoracotomy for clinical stage IA non-small cell lung cancer. J Cardiothorac Surg 2014; 9: 88
  • 10 Sugi K, Kaneda Y, Esato K. Video-assisted thoracoscopic lobectomy achieves a satisfactory long-term prognosis in patients with clinical stage IA lung cancer. World J Surg 2000; 24 (1) 27-30 , discussion 30–31
  • 11 Li Z, Liu H, Li L. Video-assisted thoracoscopic surgery versus open lobectomy for stage I lung cancer: A meta-analysis of long-term outcomes. Exp Ther Med 2012; 3 (5) 886-892
  • 12 Sugi K, Kaneda Y, Esato K. Video-assisted thoracoscopic lobectomy reduces cytokine production more than conventional open lobectomy. Jpn J Thorac Cardiovasc Surg 2000; 48 (3) 161-165
  • 13 Scott WJ, Allen MS, Darling G , et al. Video-assisted thoracic surgery versus open lobectomy for lung cancer: a secondary analysis of data from the American College of Surgeons Oncology Group Z0030 randomized clinical trial. J Thorac Cardiovasc Surg 2010; 139 (4) 976-981 , discussion 981–983
  • 14 Whitson BA, Andrade RS, Boettcher A , et al. Video-assisted thoracoscopic surgery is more favorable than thoracotomy for resection of clinical stage I non-small cell lung cancer. Ann Thorac Surg 2007; 83 (6) 1965-1970
  • 15 Cattaneo SM, Park BJ, Wilton AS , et al. Use of video-assisted thoracic surgery for lobectomy in the elderly results in fewer complications. Ann Thorac Surg 2008; 85 (1) 231-235 , discussion 235–236
  • 16 Handy Jr JR, Asaph JW, Douville EC, Ott GY, Grunkemeier GL, Wu Y. Does video-assisted thoracoscopic lobectomy for lung cancer provide improved functional outcomes compared with open lobectomy?. Eur J Cardiothorac Surg 2010; 37 (2) 451-455
  • 17 Port JL, Mirza FM, Lee PC, Paul S, Stiles BM, Altorki NK. Lobectomy in octogenarians with non-small cell lung cancer: ramifications of increasing life expectancy and the benefits of minimally invasive surgery. Ann Thorac Surg 2011; 92 (6) 1951-1957
  • 18 Scott WJ, Matteotti RS, Egleston BL, Oseni S, Flaherty JF. A comparison of perioperative outcomes of video-assisted thoracic surgical (VATS) lobectomy with open thoracotomy and lobectomy: results of an analysis using propensity score based weighting. Ann Surg Innov Res 2010; 4 (1) 1
  • 19 Chen FF, Zhang D, Wang YL, Xiong B. Video-assisted thoracoscopic surgery lobectomy versus open lobectomy in patients with clinical stage I non-small cell lung cancer: a meta-analysis. Eur J Surg Oncol 2013; 39 (9) 957-963
  • 20 Lau KK, Martin-Ucar AE, Nakas A, Waller DA. Lung cancer surgery in the breathless patient—the benefits of avoiding the gold standard. Eur J Cardiothorac Surg 2010; 38 (1) 6-13
  • 21 Berry MF, Villamizar-Ortiz NR, Tong BC , et al. Pulmonary function tests do not predict pulmonary complications after thoracoscopic lobectomy. Ann Thorac Surg 2010; 89 (4) 1044-1051 , discussion 1051–1052
  • 22 Kachare S, Dexter EU, Nwogu C, Demmy TL, Yendamuri S. Perioperative outcomes of thoracoscopic anatomic resections in patients with limited pulmonary reserve. J Thorac Cardiovasc Surg 2011; 141 (2) 459-462
  • 23 Ceppa DP, Kosinski AS, Berry MF , et al. Thoracoscopic lobectomy has increasing benefit in patients with poor pulmonary function: a Society of Thoracic Surgeons Database analysis. Ann Surg 2012; 256 (3) 487-493
  • 24 Cerfolio RJ, Bryant AS, Skylizard L, Minnich DJ. Initial consecutive experience of completely portal robotic pulmonary resection with 4 arms. J Thorac Cardiovasc Surg 2011; 142 (4) 740-746
  • 25 Kent M, Wang T, Whyte R, Curran T, Flores R, Gangadharan S. Open, video-assisted thoracic surgery, and robotic lobectomy: review of a national database. Ann Thorac Surg 2014; 97 (1) 236-242 , discussion 242–244
  • 26 Lee BE, Shapiro M, Rutledge JR, Korst RJ. Nodal upstaging in robotic and video assisted thoracic surgery lobectomy for clinical N0 lung cancer. Ann Thorac Surg 2015; 100 (1) 229-233 , discussion 233–234
  • 27 Park BJ, Melfi F, Mussi A , et al. Robotic lobectomy for non-small cell lung cancer (NSCLC): long-term oncologic results. J Thorac Cardiovasc Surg 2012; 143 (2) 383-389
  • 28 Veronesi G, Agoglia BG, Melfi F , et al. Experience with robotic lobectomy for lung cancer. Innovations (Phila) 2011; 6 (6) 355-360
  • 29 Wilson JL, Louie BE, Cerfolio RJ , et al. The prevalence of nodal upstaging during robotic lung resection in early stage non-small cell lung cancer. Ann Thorac Surg 2014; 97 (6) 1901-1906 , discussion 1906–1907
  • 30 Dylewski MR, Ohaeto AC, Pereira JF. Pulmonary resection using a total endoscopic robotic video-assisted approach. Semin Thorac Cardiovasc Surg 2011; 23 (1) 36-42
  • 31 Giulianotti PC, Buchs NC, Caravaglios G, Bianco FM. Robot-assisted lung resection: outcomes and technical details. Interact Cardiovasc Thorac Surg 2010; 11 (4) 388-392
  • 32 Deen SA, Wilson JL, Wilshire CL , et al. Defining the cost of care for lobectomy and segmentectomy: a comparison of open, video-assisted thoracoscopic, and robotic approaches. Ann Thorac Surg 2014; 97 (3) 1000-1007
  • 33 Yang CF, Sun Z, Speicher PJ , et al. Use and outcomes of minimally invasive lobectomy for stage I non-small cell lung cancer in the National Cancer Data Base. Ann Thorac Surg 2016; 101 (3) 1037-1042
  • 34 Burt BM, Kosinski AS, Shrager JB, Onaitis MW, Weigel T. Thoracoscopic lobectomy is associated with acceptable morbidity and mortality in patients with predicted postoperative forced expiratory volume in 1 second or diffusing capacity for carbon monoxide less than 40% of normal. J Thorac Cardiovasc Surg 2014; 148 (1) 19-28 , 28–29.e1
  • 35 Gonzalez D, Paradela M, Garcia J, Dela Torre M. Single-port video-assisted thoracoscopic lobectomy. Interact Cardiovasc Thorac Surg 2011; 12 (3) 514-515
  • 36 Akter F, Routledge T, Toufektzian L, Attia R. In minor and major thoracic procedures is uniport superior to multiport video-assisted thoracoscopic surgery?. Interact Cardiovasc Thorac Surg 2015; 20 (4) 550-555
  • 37 Nezu K, Kushibe K, Tojo T, Takahama M, Kitamura S. Thoracoscopic wedge resection of blebs under local anesthesia with sedation for treatment of a spontaneous pneumothorax. Chest 1997; 111 (1) 230-235
  • 38 Pompeo E, Mineo D, Rogliani P, Sabato AF, Mineo TC. Feasibility and results of awake thoracoscopic resection of solitary pulmonary nodules. Ann Thorac Surg 2004; 78 (5) 1761-1768
  • 39 Rocco G, Martucci N, La Manna C , et al. Ten-year experience on 644 patients undergoing single-port (uniportal) video-assisted thoracoscopic surgery. Ann Thorac Surg 2013; 96 (2) 434-438
  • 40 Gonzalez-Rivas D, Bonome C, Fieira E , et al. Non-intubated video-assisted thoracoscopic lung resections: the future of thoracic surgery?. Eur J Cardiothorac Surg 2016; 49 (3) 721-731
  • 41 Liu J, Cui F, Li S , et al. Nonintubated video-assisted thoracoscopic surgery under epidural anesthesia compared with conventional anesthetic option: a randomized control study. Surg Innov 2015; 22 (2) 123-130
  • 42 Ginsberg RJ, Rubinstein LV ; Lung Cancer Study Group. Randomized trial of lobectomy versus limited resection for T1 N0 non-small cell lung cancer. Ann Thorac Surg 1995; 60 (3) 615-622 , discussion 622–623
  • 43 Lederle FA. Lobectomy versus limited resection in T1 N0 lung cancer. Ann Thorac Surg 1996; 62 (4) 1249-1250
  • 44 Koike T, Yamato Y, Yoshiya K, Shimoyama T, Suzuki R. Intentional limited pulmonary resection for peripheral T1 N0 M0 small-sized lung cancer. J Thorac Cardiovasc Surg 2003; 125 (4) 924-928
  • 45 Okada M, Koike T, Higashiyama M, Yamato Y, Kodama K, Tsubota N. Radical sublobar resection for small-sized non-small cell lung cancer: a multicenter study. J Thorac Cardiovasc Surg 2006; 132 (4) 769-775
  • 46 Kodama K, Doi O, Higashiyama M, Yokouchi H. Intentional limited resection for selected patients with T1 N0 M0 non-small-cell lung cancer: a single-institution study. J Thorac Cardiovasc Surg 1997; 114 (3) 347-353
  • 47 Bando T, Yamagihara K, Ohtake Y , et al. A new method of segmental resection for primary lung cancer: intermediate results. Eur J Cardiothorac Surg 2002; 21 (5) 894-899 , discussion 900
  • 48 El-Sherif A, Gooding WE, Santos R , et al. Outcomes of sublobar resection versus lobectomy for stage I non-small cell lung cancer: a 13-year analysis. Ann Thorac Surg 2006; 82 (2) 408-415 , discussion 415–416
  • 49 Martin-Ucar AE, Nakas A, Pilling JE, West KJ, Waller DA. A case-matched study of anatomical segmentectomy versus lobectomy for stage I lung cancer in high-risk patients. Eur J Cardiothorac Surg 2005; 27 (4) 675-679
  • 50 Kilic A, Schuchert MJ, Pettiford BL , et al. Anatomic segmentectomy for stage I non-small cell lung cancer in the elderly. Ann Thorac Surg 2009; 87 (6) 1662-1666 , discussion 1667–1668
  • 51 Altorki NK, Yip R, Hanaoka T , et al; I-ELCAP Investigators. Sublobar resection is equivalent to lobectomy for clinical stage 1A lung cancer in solid nodules. J Thorac Cardiovasc Surg 2014; 147 (2) 754-762 , Discussion 762–764
  • 52 Clinical Trials.gov. Cancer and Leukemia Group B. Comparison of different types of surgery in treating patients with stage IA non-small cell lung cancer. NCT00499330. National Institutes of Health. Available online at https://clinicaltrials.gov/ct2/show/NCT00499330?term=stage+ia+non-small+cell&rank=1 . Accessed on August 29, 2016
  • 53 Nakamura K, Saji H, Nakajima R , et al. A phase III randomized trial of lobectomy versus limited resection for small-sized peripheral non-small cell lung cancer (JCOG0802/WJOG4607L). Jpn J Clin Oncol 2010; 40 (3) 271-274
  • 54 Kent M, Landreneau R, Mandrekar S , et al. Segmentectomy versus wedge resection for non-small cell lung cancer in high-risk operable patients. Ann Thorac Surg 2013; 96 (5) 1747-1754 , discussion 1754–1755
  • 55 Miller DL, Rowland CM, Deschamps C, Allen MS, Trastek VF, Pairolero PC. Surgical treatment of non-small cell lung cancer 1 cm or less in diameter. Ann Thorac Surg 2002; 73 (5) 1545-1550 , discussion 1550–1551
  • 56 Okada M, Nishio W, Sakamoto T , et al. Effect of tumor size on prognosis in patients with non-small cell lung cancer: the role of segmentectomy as a type of lesser resection. J Thorac Cardiovasc Surg 2005; 129 (1) 87-93
  • 57 Watanabe A, Koyanagi T, Obama T , et al. Assessment of node dissection for clinical stage I primary lung cancer by VATS. Eur J Cardiothorac Surg 2005; 27 (5) 745-752
  • 58 El-Sherif A, Fernando HC, Santos R , et al. Margin and local recurrence after sublobar resection of non-small cell lung cancer. Ann Surg Oncol 2007; 14 (8) 2400-2405
  • 59 Sienel W, Dango S, Kirschbaum A , et al. Sublobar resections in stage IA non-small cell lung cancer: segmentectomies result in significantly better cancer-related survival than wedge resections. Eur J Cardiothorac Surg 2008; 33 (4) 728-734
  • 60 Nakamura H, Taniguchi Y, Miwa K , et al. Comparison of the surgical outcomes of thoracoscopic lobectomy, segmentectomy, and wedge resection for clinical stage I non-small cell lung cancer. Thorac Cardiovasc Surg 2011; 59 (3) 137-141
  • 61 Smith CB, Swanson SJ, Mhango G, Wisnivesky JP. Survival after segmentectomy and wedge resection in stage I non-small-cell lung cancer. J Thorac Oncol 2013; 8 (1) 73-78
  • 62 Warren WH, Faber LP. Segmentectomy versus lobectomy in patients with stage I pulmonary carcinoma. Five-year survival and patterns of intrathoracic recurrence. J Thorac Cardiovasc Surg 1994; 107 (4) 1087-1093 , discussion 1093–1094
  • 63 Rami-Porta R, Ball D, Crowley J , et al; International Staging Committee; Cancer Research and Biostatistics; Observers to the Committee; Participating Institutions. The IASLC Lung Cancer Staging Project: proposals for the revision of the T descriptors in the forthcoming (seventh) edition of the TNM classification for lung cancer. J Thorac Oncol 2007; 2 (7) 593-602
  • 64 Bando T, Miyahara R, Sakai H , et al. A follow-up report on a new method of segmental resection for small-sized early lung cancer. Lung Cancer 2009; 63 (1) 58-62
  • 65 Fernando HC, Santos RS, Benfield JR , et al. Lobar and sublobar resection with and without brachytherapy for small stage IA non-small cell lung cancer. J Thorac Cardiovasc Surg 2005; 129 (2) 261-267
  • 66 Sawabata N, Ohta M, Matsumura A , et al; Thoracic Surgery Study Group of Osaka University. Optimal distance of malignant negative margin in excision of nonsmall cell lung cancer: a multicenter prospective study. Ann Thorac Surg 2004; 77 (2) 415-420
  • 67 Schuchert MJ, Pettiford BL, Keeley S , et al. Anatomic segmentectomy in the treatment of stage I non-small cell lung cancer. Ann Thorac Surg 2007; 84 (3) 926-932 , discussion 932–933
  • 68 Ettinger DS, Akerley W, Borghaei H , et al; National comprehensive cancer network. Non-small cell lung cancer, version 2.2013. J Natl Compr Canc Netw 2013; 11 (6) 645-653 , quiz 653
  • 69 Travis WD, Brambilla E, Noguchi M , et al; American Thoracic Society. International Association for the Study of Lung Cancer/American Thoracic Society/European Respiratory Society: international multidisciplinary classification of lung adenocarcinoma: executive summary. Proc Am Thorac Soc 2011; 8 (5) 381-385
  • 70 Yoshizawa A, Motoi N, Riely GJ , et al. Impact of proposed IASLC/ATS/ERS classification of lung adenocarcinoma: prognostic subgroups and implications for further revision of staging based on analysis of 514 stage I cases. Mod Pathol 2011; 24 (5) 653-664
  • 71 Nakayama H, Yamada K, Saito H , et al. Sublobar resection for patients with peripheral small adenocarcinomas of the lung: surgical outcome is associated with features on computed tomographic imaging. Ann Thorac Surg 2007; 84 (5) 1675-1679
  • 72 Shimada Y, Yoshida J, Hishida T, Nishimura M, Ishii G, Nagai K. Predictive factors of pathologically proven noninvasive tumor characteristics in T1aN0M0 peripheral non-small cell lung cancer. Chest 2012; 141 (4) 1003-1009
  • 73 Takahashi M, Shigematsu Y, Ohta M, Tokumasu H, Matsukura T, Hirai T. Tumor invasiveness as defined by the newly proposed IASLC/ATS/ERS classification has prognostic significance for pathologic stage IA lung adenocarcinoma and can be predicted by radiologic parameters. J Thorac Cardiovasc Surg 2014; 147 (1) 54-59
  • 74 Nitadori J, Bograd AJ, Morales EA , et al. Preoperative consolidation-to-tumor ratio and SUVmax stratify the risk of recurrence in patients undergoing limited resection for lung adenocarcinoma ≤2 cm. Ann Surg Oncol 2013; 20 (13) 4282-4288
  • 75 Suzuki K, Koike T, Asakawa T , et al; Japan Lung Cancer Surgical Study Group (JCOG LCSSG). A prospective radiological study of thin-section computed tomography to predict pathological noninvasiveness in peripheral clinical IA lung cancer (Japan Clinical Oncology Group 0201). J Thorac Oncol 2011; 6 (4) 751-756
  • 76 Liu S, Wang R, Zhang Y , et al. Precise diagnosis of intraoperative frozen section is an effective method to guide resection strategy for peripheral small-sized lung adenocarcinoma. J Clin Oncol 2016; 34 (4) 307-313
  • 77 Pignon JP, Tribodet H, Scagliotti GV , et al; LACE Collaborative Group. Lung adjuvant cisplatin evaluation: a pooled analysis by the LACE Collaborative Group. J Clin Oncol 2008; 26 (21) 3552-3559
  • 78 Wakelee HA, Dahlberg SE, Brahmer JR , et al; Eastern Cooperative Oncology Group. Differential effect of age on survival in advanced NSCLC in women versus men: analysis of recent Eastern Cooperative Oncology Group (ECOG) studies, with and without bevacizumab. Lung Cancer 2012; 76 (3) 410-415
  • 79 PORT Meta-analysis Trialists Group. Postoperative radiotherapy in non-small-cell lung cancer: systematic review and meta-analysis of individual patient data from nine randomised controlled trials. Lancet 1998; 352 (9124) 257-263
  • 80 Burdett S, Stewart LA, Rydzewska L. A systematic review and meta-analysis of the literature: chemotherapy and surgery versus surgery alone in non-small cell lung cancer. J Thorac Oncol 2006; 1 (7) 611-621
  • 81 Lally BE, Zelterman D, Colasanto JM, Haffty BG, Detterbeck FC, Wilson LD. Postoperative radiotherapy for stage II or III non-small-cell lung cancer using the surveillance, epidemiology, and end results database. J Clin Oncol 2006; 24 (19) 2998-3006