The lobar vs. sublobar “limited” resection respiratory function preservation debate: learning to speak the same language

“Do we speak the same language?”

It is in the nature of surgeons to evolve towards performing smaller incisions and less invasive techniques for the benefit of their patients. From an open pneumonectomy we have moved on to lobectomies and then sublobar resections; from an open thoracotomy we have evolved to a smaller “mini” thoracotomy, multiport and uniportal video assistant thoracic surgery (VATS) incisions and now robotic surgery (1-5). The quest to support the implementation of the limited resection into the cancer surgery armamentarium started many years ago. However, the concern with lung-sparing and minimal access techniques is that the oncological outcome may be compromised (6,7).

In an effort to address this concern, a randomized trial was conducted, which was not in support of the superiority of the “limited” resections over the traditional lobectomies in terms of oncological result and postoperative outcome (8). That study was, however, criticized due to inconsistencies regarding the collection of data; several non-anatomical resections (wedges) were included in the “limited” resection group, which may have altered the overall outcome of the study. More importantly, the aforementioned study unfortunately shed light on the discrepancies and the multitude of variables among data investigated and reported in different studies (7,9-12).

Therefore, before reaching a conclusion, it is of the utmost importance that studies incorporate all the possible confounding variables that could potentially influence the outcome and perform relevant analysis based on a “commonly agreed vocabulary”, allowing the rest of the thoracic surgical community to understand the “common language”.

“The respiratory benefit of segmental resections: a factitious observation or a fictional understanding of a different language?”

Why offer a less extended operation to patients, if there is nothing to earn in return? Therefore, the first and logical step in answering this query is to prove that a “limited” resection provides exactly what it implies: the advantage of limited reduction of pulmonary function. In the effort to investigate the former, pulmonary function tests (PFTs) measuring forced expiratory volume in the 1^st second (FEV1), ± forced vital capacity (FVC), ± diffusional lung capacity for carbon dioxide (DLCO) have been investigated over the years. Moreover, several retrospective studies, lately with propensity scoring, have seen publicity in an effort to clarify if “limited” resections preserve respiratory function; results did not favor either way, with many studies showing preserved PFTs after segmentectomy when compared to lobectomy (13-16) and others unable to support this finding, with segmentectomies showing similar pulmonary function reduction with lobectomies (8,17,18). Unfortunately, again a lot of confusion has arisen, because once more we are not “speaking the same language”.

Firstly, the timing of the PFTs performed after surgery is crucial because the amount of pain is different in the early postoperative period compared to, for instance, after 6 months, when the patient is resuming normality (8,19,20). Most studies do not provide a uniform timing of measurements and most importantly provide no information regarding the pain status of patients at the time of the measurements (19,20). Additionally, no other post-operative recovery data have been recorded/reported at the time of the performed measurements; reduced mobility or the development of postoperative complications along with their overall WHO performance score may impact on their ability to “blow” during the early postoperative spirometry.

Secondly, most studies do not discriminate between thoracotomies and VATS procedures, an omission extremely crucial for understanding the postoperative recovery of patients. It has been well established that VATS is associated with less early postoperative pain and greater discharge independence, among other benefits (11). In regards to PFTs, VATS procedures outperform open procedures (21).

Furthermore, anatomic segmentectomies are mingled in with wedge resections and all are regarded as “sublobar” or “limited” resections in many publications. These two types of resections are distinctly different, both in technical and oncological features (7,10). Additionally, the amount of parenchyma removed per case may vary. For example, the amount of lung removed during a small wedge resection is obviously of significant difference when compared to a left apical trisegmentectomy. However, a “generous” wedge could be similar to a superior segmentectomy or even similar to a middle lobectomy in terms of lung parenchyma removed! When studies report wedge resections, further details as to the extent of the actual parenchyma removed are usually not provided.

The site of the part of lung removal is another important factor, in our opinion, affecting the postoperative pulmonary function. This is supported with the fact that lung volume loss has been shown to be different between the various sites of lobectomies; for example upper right lobectomies lead to more volume loss than the lower ones, despite the fact that the upper right lobe is smaller than the ipsilateral lower one (22). Only recently has this factor started to undergo investigation, showing conflicting results regarding the preservation of FEV1 and DLCO after upper right or middle lobectomy in VATS procedures when considering the expected volume loss (16,23,24). This discrepancy has brought about the conception of post-removal compensatory hyperinflation of the remaining lung parenchyma (16,23), which, however, proves difficult to be quantified.

Furthermore, most of the patients suffer from different grades of chronic obstructive pulmonary disease (COPD), are active or ex-smokers and therefore an element of emphysema always exists; however, the total lung capacity (TLC) or residual volume (RV) is not reported. It is different when dealing with patients with low FEV1 and FVC, due to COPD compared to dealing with patients presenting with apical predominant emphysema with a high TLC and RV, who would benefit from a larger parenchymal resection (lobectomy) mimicking a LVRS (7,25,26).

Most importantly, the criteria by which a segmentectomy or wedge resection is offered instead of a lobectomy are varied with several studies not even reporting a reason (9). A “limited” resection has traditionally been offered to poor cardiorespiratory candidates who it is felt would not withstand a lobectomy. But it is often not clear “who” has been deemed a poor candidate for a lobectomy and on what grounds. Different co-morbidities may characterize a patient as “high risk” for morbidity. Additionally, cardiopulmonary limits and “cut-off points” are being challenged as VATS techniques are constituting the majority of our practice and as our experience in performing complicated procedures through VATS approaches is solidifying and increasing (27,28). On the other hand, “high-risk” patients are logically accompanied with a higher probability for morbidity and therefore the postoperative respiratory recovery will be different in these patients. It is evident that who is suffering from what and to what extend does play a key role in identifying the “limited” resection offering criteria and consequently the postoperative respiratory behaviour.

Finally, how efficient are the calculated preoperative predicted FEV1 or DLCO (ppoFEV1, ppoDLCO) in providing an estimate of respiratory morbidity and long-term respiratory benefit? The answer to the first part of the question is depicted in the information that “the actual FEV1 measured immediately postoperatively” is possibly more accurate than ppoFEV1 (29) and “unknown” is the answer to the second part of the question, since no definite studies regarding the quality of life after segmentectomy versus lobectomy have been published.

Can we “speak the same language”?

In order to obtain a more accurate pulmonary function measurement, perfusion (Q) imaging, dynamic perfusion magnetic resonance imaging (MRI) and quantitative CT scans have previously been used in order to stratify patients, in terms of operability, in an effort not to exclude patients from the best treatment available because of an exaggerated low pulmonary function calculated with the traditional ppo FEV1 and/or ppoDLCO (30,31). An effort to bring this technology to the debate of lobar versus “limited” resection was made by Nomori and associates, who used lung perfusion single-photon emission computed tomography (SPECT) to prove the parenchymal preservation benefit with less parenchyma removed (32). In this study, the smaller the number of segments resected, the better preserved the lung parenchyma, with the exception of an upper left division segmentectomy, which was found to have the same postoperative lung function with an upper left lobectomy. This article might just represent the first objective attempt in depicting the lung parenchymal differences according to number of segments resected apart from PFTs. However, a few drawbacks that could potentially diminish the end-result characterize this article: (I) no VATS cases were included and only lateral thoracotomy incisions were taken into account; (II) no data regarding the emphysematous status of the preoperative lungs was provided; (III) the follow up PFTs were performed variably before 6 months and within a range of 6–13 months after the first measurement; (IV) no specific data on how much parenchyma is preserved after other specific types of resections i.e., basal segmentectomies, right middle lobectomies etc. were provided and (V) bigger tumours were resected in the upper left division and upper left lobectomy cases, which means that more parenchyma was involved by the tumor preoperatively.

Based on this study however, it becomes apparent that we can apply technology to lift the bias of the variation of data resulting from simple spirometric measurements.

After all: do we really need to “speak the same language”?

All the above suggest that most probably there may be a respiratory benefit of some of the “limited” resections over the traditional lobectomies. However, we need to somehow coordinate and objectively measure that benefit, in order to prove that it constitutes a fact and not a random statistical finding! The aforementioned is of utmost significance, especially for the respiratory compromised “high-risk” patients who would otherwise be deemed inoperable.

Nevertheless, the fact that we “can do it” or that we are “skillful” enough as surgeons to do a very limited and complicated key hole operation, even if it is oncologically similar to the old fashioned lobectomy, does not mean that we will do so, unless the benefit from such an operation will be passed onto the patients’ recovery! How much deterioration in FEV1/DLCO corresponds to clinical deterioration and impact? Did the operated patients stop smoking? Did they complete a rehabilitation program? What was their postoperative quality of life even after a “limited” resection? Achieving to avoid a pulmonary function deterioration of i.e., 20%, by performing a “limited” resection, does not contribute to a better quality of life for a patient who smokes and presents with respiratory infections every 2 months or whose exercise tolerance is limited by peripheral vascular disease or rheumatoid arthritis, for instance. On the contrary, in some cases it would be preferable to proceed with an open, “quicker” lobectomy than persevering with a VATS lengthy segmentectomy, of course depending on the surgeon’s experience.

Therefore, all the above confusing and conflicting terms and conditions in thoracic surgery ought to be addressed, resolved and clarified, in order to allow us to compare apples with apples and oranges with oranges, and ultimately to support recommendations to patients and the evolution of surgeons based on best evidence practice.

Acknowledgments

None.

Footnote

Conflicts of Interest: The authors have no conflicts of interest to declare.

References

1. Graham EA, Singer JJ. Successful removal of an entire lung for carcinoma of the bronchus. JAMA 1933;101:1371-4. [Crossref] [PubMed]
2. Cahan WG. Radical lobectomy. J Thorac Cardiovasc Surg 1960;39:555-72. [PubMed]
3. Jensik RJ, Faber LP, Milloy FJ, et al. Segmental resection for lung cancer. A fifteen-year experience. J Thorac Cardiovasc Surg 1973;66:563-72. [PubMed]
4. Shen Y, Wang H, Feng M, et al. Single- versus multiple-port thoracoscopic lobectomy for lung cancer: a propensity-matched study†. Eur J Cardiothorac Surg 2016;49 Suppl 1:i48-53. [PubMed]
5. Veronesi G, Novellis P, Voulaz E, et al. Robot-assisted surgery for lung cancer: State of the art and perspectives. Lung Cancer 2016;101:28-34. [Crossref] [PubMed]
6. Weissberg D, Straehley CJ, Scully NM, et al. Less than lobar resections for bronchogenic carcinoma. Scand J Thorac Cardiovasc Surg 1993;27:121-6. [Crossref] [PubMed]
7. Rami-Porta R, Tsuboi M. Sublobar resection for lung cancer. Eur Respir J 2009;33:426-35. [Crossref] [PubMed]
8. 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 1995;60:615-22; discussion 622-3. [Crossref] [PubMed]
9. Nakamura H, Kawasaki N, Taguchi M, et al. Survival following lobectomy vs limited resection for stage I lung cancer: a meta-analysis. Br J Cancer 2005;92:1033-7. [Crossref] [PubMed]
10. De Zoysa MK, Hamed D, Routledge T, et al. Is limited pulmonary resection equivalent to lobectomy for surgical management of stage I non-small-cell lung cancer? Interact Cardiovasc Thorac Surg 2012;14:816-20. [Crossref] [PubMed]
11. Schuchert MJ, Abbas G, Pennathur A, et al. Sublobar resection for early-stage lung cancer. Semin Thorac Cardiovasc Surg 2010;22:22-31. [Crossref] [PubMed]
12. Sakurai H, Asamura H. Sublobar resection for early-stage lung cancer. Transl Lung Cancer Res 2014;3:164-72. [PubMed]
13. Takizawa T, Haga M, Yagi N, et al. Pulmonary function after segmentectomy for small peripheral carcinoma of the lung. J Thorac Cardiovasc Surg 1999;118:536-41. [Crossref] [PubMed]
14. Keenan RJ, Landreneau RJ, Maley RH Jr, et al. Segmental resection spares pulmonary function in patients with stage I lung cancer. Ann Thorac Surg 2004;78:228-33; discussion 228-33. [Crossref] [PubMed]
15. Harada H, Okada M, Sakamoto T, et al. Functional advantage after radical segmentectomy versus lobectomy for lung cancer. Ann Thorac Surg 2005;80:2041-5. [Crossref] [PubMed]
16. Kim SJ, Ahn S, Lee YJ, et al. Factors associated with preserved pulmonary function in non-small-cell lung cancer patients after video-assisted thoracic surgery. Eur J Cardiothorac Surg 2016;49:1084-90. [Crossref] [PubMed]
17. Deng B, Cassivi SD, de Andrade M, et al. Clinical outcomes and changes in lung function after segmentectomy versus lobectomy for lung cancer cases. J Thorac Cardiovasc Surg 2014;148:1186-92.e3. [Crossref] [PubMed]
18. Suzuki H, Morimoto J, Mizobuchi T, et al. Does segmentectomy really preserve the pulmonary function better than lobectomy for patients with early-stage lung cancer? Surg Today 2017;47:463-9. [PubMed]
19. Macke RA, Schuchert MJ, Odell DD, et al. Parenchymal preserving anatomic resections result in less pulmonary function loss in patients with Stage I non-small cell lung cancer. J Cardiothorac Surg 2015;10:49. [Crossref] [PubMed]
20. Park TY, Park YS. Long-term respiratory function recovery in patients with stage I lung cancer receiving video-assisted thoracic surgery versus thoracotomy. J Thorac Dis 2016;8:161-8. [PubMed]
21. Nakata M, Saeki H, Yokoyama N, et al. Pulmonary function after lobectomy: video-assisted thoracic surgery versus thoracotomy. Ann Thorac Surg 2000;70:938-41. [Crossref] [PubMed]
22. Sengul AT, Sahin B, Celenk C, et al. Postoperative lung volume change depending on the resected lobe. Thorac Cardiovasc Surg 2013;61:131-7. [Crossref] [PubMed]
23. Kim SJ, Lee YJ, Park JS, et al. Changes in pulmonary function in lung cancer patients after video-assisted thoracic surgery. Ann Thorac Surg 2015;99:210-7. [Crossref] [PubMed]
24. Kent MS, Mandrekar SJ, Landreneau R, et al. Impact of Sublobar Resection on Pulmonary Function: Long-Term Results from American College of Surgeons Oncology Group Z4032 (Alliance). Ann Thorac Surg 2016;102:230-8. [Crossref] [PubMed]
25. Santambrogio L, Nosotti M, Baisi A, et al. Pulmonary lobectomy for lung cancer: a prospective study to compare patients with forced expiratory volume in 1 s more or less than 80% of predicted. Eur J Cardiothorac Surg 2001;20:684-7. [Crossref] [PubMed]
26. Ueda K, Murakami J, Sano F, et al. Assessment of volume reduction effect after lung lobectomy for cancer. J Surg Res 2015;197:176-82. [Crossref] [PubMed]
27. Kouritas VK, Kefaloyannis E, Milton R, et al. Performance of wider parenchymal lung resection than preoperatively planned in patients with low preoperative lung function performance undergoing video-assisted thoracic surgery major lung resection. Interact Cardiovasc Thorac Surg 2016;23:889-94. [Crossref] [PubMed]
28. Burt BM, Kosinski AS, Shrager JB, et al. 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;148:19-28, dicussion 28-29.e1.
29. Varela G, Brunelli A, Rocco G, et al. Measured FEV1 in the first postoperative day, and not ppoFEV1, is the best predictor of cardio-respiratory morbidity after lung resection. Eur J Cardiothorac Surg 2007;31:518-21. [Crossref] [PubMed]
30. Bolliger CT, Gückel C, Engel H, et al. Prediction of functional reserves after lung resection: comparison between quantitative computed tomography, scintigraphy, and anatomy. Respiration 2002;69:482-9. [Crossref] [PubMed]
31. Eslick EM, Bailey DL, Harris B, et al. Measurement of preoperative lobar lung function with computed tomography ventilation imaging: progress towards rapid stratification of lung cancer lobectomy patients with abnormal lung function. Eur J Cardiothorac Surg 2016;49:1075-82.32.
32. Nomori H, Cong Y, Sugimura H. Systemic and regional pulmonary function after segmentectomy. J Thorac Cardiovasc Surg 2016;152:747-53. [Crossref] [PubMed]