Over the past 2 decades, general thoracic surgery has been revolutionized by rapid development and assimilation of minimally invasive techniques for lung cancer surgery. Whereas these gains have been impressive with great benefit to thousands of patients, focus upon mere minimization of number and size of incisions may distract surgeons from other vital considerations. In fact, surgical trauma includes not only incisional injury, but also functional loss due to organ removal, and also systemic and psychological trauma induced by surgical stress. Therefore, minimally invasive surgery (MIS) by its definition should be an idea to “minimize surgical trauma, but still achieve comparable or better therapeutic results.”1
In fact, the history of general thoracic surgery can be viewed as a gradual and inexorable development of MIS by the broad definition above. The first radical resection of lung cancer was completed via a left pneumonectomy by Dr Evarts Graham in 1933.2 Although lobectomy was described earlier and used for benign conditions, it was initially thought to be inadequate for patients with lung cancer. However, pneumonectomy was quickly replaced by lobectomy for patients with peripheral lung cancer in the next decade because the latter was shown to remarkably reduce operational mortality and morbidity without making impact on long-term survival. This landmark evolution directly led to the development of bronchoplasty and arterioplasty for the treatment of selected patients with central lung cancer, whose lung cancer and quality of life were greatly improved.3 Both examples highlight the importance of lung parenchyma preservation in reducing surgical trauma and thus should undoubtedly be considered MIS. However, the more modern concept of MIS was only realized and became popular in the early 1980s after the application of the “keyhole” video-assisted procedures which were quickly adopted by thoracic surgeons in the 1990s.4 Over the next years, advances in minimally invasive lung cancer surgery can be expected to occur in size/number of incisions, extent of resection, and systemic response to surgery.
MIS 1.0: IMPROVING SURGICAL OUTCOMES BY REDUCING INCISIONAL INJURY
The impact of video assisted thoracic surgery (VATS) on reducing incisional trauma is overt; both postoperative pain and recovery greatly improved as compared with conventional open surgery. Although randomized comparative evidence is still lacking, most retrospective studies demonstrate comparable oncological results of VATS to open surgery in selected patients with lung cancer (mainly clinical stage I).4 Many now promote VATS as the new standard of treatment for early-stage lung cancer. However, real challenges encountered by many VATS surgeons are efficacy of lymphadenectomy and use of endoscopic techniques in complicated cases. Fixed ports in VATS limit intrathoracic maneuverability of instrumentation, making complete lymph node dissection relatively difficult, especially to surgeons at the beginning phase of the learning curve. Meanwhile, for patients with difficult conditions such as a large nodule, central mass, or calcified lymph node, endoscopic operation is extremely difficult and VATS is often abandoned either preoperatively or intraoperatively. Each surgeon must continually evaluate his or her ability to perform an oncologically sound operation as incisional/technical changes are made.
Currently, there are 2 directions of development in thoracoscopic surgery. The first direction is to continuously reduce the size and number of incisions, or alter the location of the incision (subxiphoid or subcostal).5 The theoretical advantages of uniportal over multiportal approaches include improved postoperative pain control and shortened recovery time, but objective evidence is currently lacking. Before the advent of the uniportal approach, there was no consensus on the use of 2 ports, 3 ports, or 4 ports, suggesting that some surgeons believed that the use of more than 2 ports facilitated the completion of the procedures. Similarly, it is possible that the uniportal approach may further increase the difficulty of the procedure, if surgeons find it difficult to place all instruments and stapling devices in 1 incision. Also, it is possible that single-port access may cause more trauma to intercostal nerve, although this has not been studied. The other direction is the use of robot-assisted thoracoscopic surgery (RATS). Although the number of ports by RATS remains the same or greater than standard VATS, the 3-dimensional (3D) vision and wristed instruments provided by surgical robots may lower difficulty of the surgery and enable surgeons to operate on more complicated cases. So far, the limiting factors to more complete adoption of robotics include safety, access to training in residency programs, cost (especially in countries like China), and lack of evidence demonstrating superiority over other minimally invasive techniques.
MIS 2.0: IMPROVING MIS BY REDUCING EXTENT OF RESECTION
Intrathoracic injury in lung cancer surgery arises from lung resection and lymph node dissection. Lung parenchymal preservation is associated with reduced surgical trauma and improved postoperative lung function.3 However, the landmark Lung Cancer Study Group finding of a 3-fold increase in locoregional regional recurrence6 slowed momentum for sublobar resection for clinical stage I disease. Recently, with the spread of computed tomography (CT) screening programs and more lung cancer nodules detected at early stage,7 accumulating evidence is now showing comparative survival between lobectomy and sublobar resection in selected patients with early-stage lung cancer.8
As more lung cancers are sequenced and analyzed, we, as surgeons, should be involved in genetic risk assessment of tumors. There may come a time when extent of (or need for) surgical resection is dictated by which genes are driving tumor formation. However, as we await further advances, we need to refine criteria to select patients for sublobar resection. At present, evidence to support limited resection for tumor less than 2 cm is still controversial, and results from the Alliance randomized trial CALGB 140503 and the Japanese randomized trial JCOG0802/WJOG4607L are still pending. It has been suggested by the National Comprehensive Cancer Network (NCCN) guidelines in nonsmall cell lung cancer that the proportion of ground glass opacity (GGO) component more than 50% on CT may also be used as a selective indicator of limited resection, but methods to measure this are still variable. From our own experience, tumor histology determined by intraoperative frozen section may also be utilized for patient selection. It is safe to perform limited resection in patients with minimally invasive adenocarcinoma (MIA) and adenocarcinoma in situ (AIS) according to the frozen section, which is over 95% accurate as compared with the final paraffin pathology.9
Lymph node dissection is deemed essential in lung cancer surgery for the need of staging and the possibility of reducing locoregional recurrence rate. However, extensive lymph node dissection is also associated with increased operative time and damage to neurogenic, vascular, and lymphatic structures in the mediastinum. Several studies show in patients with subsolid nodules on CT, and also in patients with AIS and MIA nodules, the lymph node metastasis rate is close to 0,7,9 questioning the necessity of lymph node dissection in these groups of patients. However, the selection criteria for limited lymphadenectomy are not well-established.
MIS 3.0: IMPROVING MIS BY REDUCING SYSTEMIC DAMAGE
Another important aspect of MIS is to reduce systemic damage induced by surgical stress. This damage includes release of inflammatory factors during the operation and subsequently impaired immune function, which are not routinely evaluated by physicians, but are known to be associated with postoperative infection and recovery.10 In lung cancer surgery, increased pulmonary and systemic inflammation responses are associated with single lung ventilation and may correlate with numerous surgeon-related factors, including operative time.10 It is therefore important to also take operational time into account when evaluating the invasiveness of surgical procedures. The extent to which operative time alters recovery and the point at which a faster operation (with potentially more incisional trauma) should be considered are unknown.
As new techniques and instrumentation are emerging, the demand for MIS from patients has dramatically increased. Endoscopic procedures in the past greatly reduced surgical trauma and reshaped thoracic surgery. The transformation from open to thoracoscopic surgery, omitting rib retraction, resulted in improved quality of life, safety, and compliance with adjuvant therapy. However, the gain from continuously reducing incisional trauma is less likely to have an impact. Perhaps, a more meaningful direction is to develop selective strategies for determining the appropriate extent of resection for individual patient to reduce unnecessary organ loss in patients with early-stage cancers. It is of great importance we consider all elements of MIS and make attempts to further reduce surgical trauma to continue to improve provision of real benefit to our patients. Moreover, as surgical trauma encompasses not only incisional injury but also internal organ injury and systemic damage, validation of a new MIS should include assessment of all these aspects. The slope of the learning curve should also be considered. Lastly and most importantly, no MIS approach should be performed at the cost of compromised long-term survival for cancer patients.
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2. Graham EA, Singer JJ. Successful removal of an entire lung for carcinoma of the bronchus. By Evarts A. Graham and J. J. Singer. JAMA
3. Balduyck B, Hendriks J, Lauwers P, et al. Quality of life after lung cancer surgery: a prospective pilot study comparing bronchial sleeve lobectomy with pneumonectomy. J Thorac Oncol
4. Yan TD, Black D, Bannon PG, et al. Systematic review and meta-analysis of randomized and nonrandomized trials on safety and efficacy of video-assisted thoracic surgery lobectomy for early-stage non-small-cell lung cancer. J Clin Oncol
5. Gonzalez-Rivas D, Damico TA, Jiang G, et al. Uniportal video-assisted thoracic surgery: a call for better evidence, not just more evidence. Eur J Cardiothorac Surg
6. Ginsberg RJ, Rubinstein LV. Randomized trial of lobectomy versus limited resection for T1 N0 non-small cell lung cancer. Lung Cancer Study Group. Ann Thorac Surg
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7. Flores RM, Nicastri D, Bauer T, et al. Computed tomography screening for lung cancer: mediastinal lymph node resection in stage IA nonsmall cell lung cancer manifesting as subsolid and solid nodules. Ann Surg
8. Wisnivesky JP, Henschke CI, Swanson S, et al. Limited resection for the treatment of patients with stage IA lung cancer. Ann Surg
9. 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
10. Grichnik KP, D’Amico TA. Acute lung injury and acute respiratory distress syndrome after pulmonary resection. Semin Cardiothorac Vasc Anesth