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Original Research: Cardiothoracic Surgery |

Thoracoscopic PneumonectomyThoracoscopic Pneumonectomy: An 11-Year Experience FREE TO VIEW

Athar Battoo, MD; Ariba Jahan; Zhengyu Yang, MS; Chukwumere E. Nwogu, MD; Sai S. Yendamuri, MD, FCCP; Elisabeth U. Dexter, MD; Mark W. Hennon, MD; Anthony L. Picone, MD, FCCP; Todd L. Demmy, MD, FCCP
Author and Funding Information

From the Roswell Park Cancer Institute, Buffalo, NY.

CORRESPONDENCE TO: Todd L. Demmy, MD, FCCP, Thoracic Surgery, Roswell Park Cancer Institute, Buffalo, NY 14263; e-mail: Todd.Demmy@roswellpark.org


This was a poster presentation at the International Association for the Study of Lung Cancer 15th World Conference on Lung Cancer, October 30, 2013, Sydney, NSW, Australia.

FUNDING/SUPPORT: The authors have reported to CHEST that no funding was received for this study.

Reproduction of this article is prohibited without written permission from the American College of Chest Physicians. See online for more details.


Chest. 2014;146(5):1300-1309. doi:10.1378/chest.14-0058
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BACKGROUND:  It is unclear whether thoracoscopic (video-assisted thoracoscopic surgery [VATS]) pneumonectomy improves outcomes compared with open approaches.

METHODS:  One hundred seven consecutive pneumonectomies performed at an experienced center from January 2002 to December 2012 were studied retrospectively. Forty cases were open, and 50 successful VATS and 17 conversions were combined (intent-to-treat [ITT] analysis).

RESULTS:  The VATS cohort had more preoperative comorbidities (three vs two, P = .003), women (57% vs 30%, P = .009), and older ages (65 years vs 63 years, P = .07). Although advanced clinical stage was less for VATS (26% vs 50% stage III, P = .035), final pathologic staging was similar (25% vs 38%, P = .77). Pursuing a VATS approach yielded similar complications (two vs two, median, P = .73) with no catastrophic intraoperative events like bleeding. Successful VATS pneumonectomy rates rose from 50%-82% by the second half of the series (P < .001). Completion pneumonectomy cases (13.4% VATS, 7.5% open) had similar outcomes. Having similar initial discomforts as patients undergoing open surgery, more patients undergoing VATS were pain-free at 1 year (53% vs 19%, P = .03). Conversions resulted in longer ICU stays (4 days vs 2 days, P = .01). Advanced clinical stage (III-IV) ITT VATS had longer median overall survival (OS) (42 months vs 13 months, log-rank P = .042). Successful VATS cases with early pathologic stage (0-II) had a median OS of 80 vs 16 months for converted and 28 months for open (log rank = 0.083).

CONCLUSIONS:  Attempting thoracoscopic pneumonectomy at an experienced center appears safe but does not yield the early pain/complication reductions observed for VATS lobectomy. There may be long-term pain/survival advantages for certain stages that warrant further study and refinement of this approach.

Figures in this Article

Worldwide, video-assisted thoracoscopic surgery (VATS) approaches for pulmonary lobectomies remain in the minority (approximately 20%), despite their salutary effects.14 Thoracoscopic lung resection results in less postoperative pain, decreased atrial fibrillation, better lung function preservation, shorter convalescence, and earlier return to normal activities.59 If needed, adjuvant therapy can be started sooner with fewer dose reductions.10 A minimally invasive approach is associated with less postoperative immunosuppression, which in turn can be beneficial against any residual tumor.1114 Oncologic validity and survival rates for VATS are at least equivalent when compared with open resections for lung cancer.1519

As we reached high reliability and safety for VATS lobectomy, it was a natural extension for us and others to attempt more complex resections, such as pneumonectomy, with acceptable short-term results.2027 In this report, we study longer-term results with pneumonectomy.

The Roswell Park Cancer Institute Institutional Review Board approved a retrospective chart and cancer registry review of all consecutive patients who underwent open or VATS pneumonectomy from January 2002 to December 2012 (#EDR 201211). Statistical analyses compared demographics, perioperative outcomes, pathologies, and survival rates between VATS and open cases with and without the matching of different preoperative variables. Conversions to open surgery were assigned to the VATS group (intent-to-treat [ITT]). First and second 5.5-year cases were compared with study experience effects. Converted and completion pneumonectomy (previous ipsilateral lung resection) cases were also analyzed separately. Fisher exact tests were applied for categorical data, and Wilcoxon rank sum tests were performed on median comparisons for continuous data. Kaplan-Meier curves were plotted and compared using log-rank tests for both overall survival (OS) and disease-free survival measures. The Cox proportional hazard model was used for univariate and multivariate analysis to detect risk factors. Statistical significance in this study was set at α level 0.05, and all reported P values were two-sided. All analyses were performed in SAS 9.3 (SAS Institute Inc).

Technique and Criteria

Patients underwent surgical staging or restaging using mediastinoscopy or transcervical extended mediastinal lymphadenectomy. VATS excluded unresectable disease and enhanced lighting and exposure even in open cases. Imaging-based concerns were generally confirmed or down-graded by VATS inspection. If VATS inspection prompted immediate thoracotomy (generally same reasons as conversion, see later), the procedure was classified as open. With selective ventilation, incision sites were placed and VATS pneumonectomy was performed as described previously following the same exposure guidelines as lobectomy (Table 1).3,2830 Any dissection carried with the intent of VATS pneumonectomy classified the patient as VATS even if conversion was required. Endoscopic 30-mm linear cutting staplers (Covidien) with vascular (white/tan) curved-tip cartridges were used to divide vessels. Avoiding pneumonectomy by sleeve resection (preferably VATS) was always attempted if technically feasible and valid oncologically.

Table Graphic Jump Location
TABLE 1 ]  Salient Points of VATS Pneumonectomy

VATS = video-assisted thoracoscopic surgery.

Pneumonectomies were performed on 107 patients using VATS in 67 (62.6%) and open technique in 40 (37.4%). Seventeen patients (15.9%) were converted from VATS to open (thoracotomy) pneumonectomy. Nine patients undergoing VATS (all successful) and three patients undergoing open surgery underwent completion pneumonectomy. During the initial 5.5 years (n = 43), the ratio of VATS to open was 0.6 as compared with 3.9 in the later 5.5 years (P < .001) (Fig 1).

Figure Jump LinkFigure 1 –  Number of VATS and open pneumonectomies over 11 y. VATS = video-assisted thoracoscopic surgery.Grahic Jump Location

Preoperative characteristics are summarized in Table 2. The VATS group trended toward older age and had significantly more women and preoperative comorbidities. The groups were well matched with respect to smoking history, weight loss, performance status, lung function, and neoadjuvant treatment, including the time interval between the induction treatment and surgery. More than one-half of the patients undergoing open pneumonectomy had clinically staged III/IV disease compared with only 27% of patients undergoing VATS. A subanalysis comparing the men undergoing open pneumonectomy and women undergoing VATS showed a significant difference in their clinical staging (patients with stage III/IV disease, 51.8% vs 10.8%; P < .001).The ratio of left- to right-sided resections was similar in both groups (VATS 1.16 vs open 1.2; P = 1.000). The operating time for VATS was significantly longer (median, 289 min vs 225 min open; P < .001; ranges, 165-615 min vs 120-834 min). The median estimated blood loss (EBL) during surgery was more for VATS (400 mL vs 225 mL open; P = .844), and 36% (n = 24) of patients undergoing VATS received intraoperative blood transfusion compared with 30% (n = 12) in the open group (P = .452). The trend in operating room time and EBL over time is shown in Figure 2.

Table Graphic Jump Location
TABLE 2 ]  Demographics and Preoperative Characteristics

Data presented as % or median (minimum-maximum). The preoperative comorbidities include those listed for Society of Thoracic Surgeons database plus any previous malignancies. Dlco = diffusing capacity of the lung for carbon monoxide; ECOG = Eastern Cooperative Oncology Group. See Table 1 legend for expansion of other abbreviation.

Figure Jump LinkFigure 2 –  A, The changes in median operating room time (min) of VATS and open pneumonectomies over 11 y. B, The changes in median estimated blood loss (mL) of VATS and open pneumonectomies over 11 y. See Figure 1 legend for expansion of abbreviation.Grahic Jump Location

Eight patients (12%) undergoing VATS and eight patients (20%) undergoing open surgery were down-staged from clinical stage (c-stage) III/IV to pathologic stage (p-stage) 0/I/II, whereas seven patients (10%) undergoing VATS and two patients (5%) undergoing open surgery increased from c-stage I/II to p-stage III/IV (P = .22). The distribution of different pathologic characteristics is summarized in Table 3. There was no significant difference between the VATS and open group in p-stage distribution, but an open approach tended to be used for bulkier tumors. VATS was as effective as open surgery for lymphadenectomy and had a nonsignificant lower rate of resection with positive microscopic margins (R1 resection). On matched univariate analysis, none of the pathologic characteristics showed any significant deviation from the previous results when adjusted for different preoperative variables.

Table Graphic Jump Location
TABLE 3 ]  Pathologic Characteristics

Data presented as % or median (minimum-maximum). Pathologic stage 0 is a complete response to neoadjuvant treatment. R1 resection = resection with positive microscopic margins. See Table 1 legend for expansion of other abbreviation.

a 

An open pneumonectomy was performed for an extremely large right lung adenocarcinoma involving > 90% of both upper and lower lobes and measuring (38 × 32 × 17.5 cm).

The postoperative outcome results are summarized in Table 4. Both groups had a similar number and type of postoperative complications. Hospital stay, ICU stay, mortality, and tolerance of adjuvant therapy were similar. The 30-day mortality for nonemergent cases was also similar (VATS, 7.5% vs open, 5%; P = .709). At the end of the first year, of the 30 surviving patients who underwent VATS, 16 (53.3%) were not taking any pain medication compared with only three out of 13 patients who underwent open surgery (18.8%) (P = .031). Figure 3 depicts the comparison of patients who underwent VATS and patients who underwent open surgery who were not on any analgesics at different time intervals after surgery.

Table Graphic Jump Location
TABLE 4 ]  Comparison of Postoperative Outcomes

Data presented as % or median (minimum-maximum). See Table 1 legend for expansion of abbreviation.

a 

Excludes emergent case deaths (one VATS and one open).

Figure Jump LinkFigure 3 –  Pain resolution in patients undergoing VATS and open procedure over 12 mo. See Figure 1 legend for expansion of abbreviation.Grahic Jump Location

Twenty patients (29.8%) who underwent VATS had disease recurrences (any site) compared with 15 patients (37.5%) who underwent open surgery (P = .52). Locoregional recurrence was also similar (10.4% vs 10%, P = 1.000). On follow-up, 36 patients (53.7%) who underwent VATS and 27 patients (67.5%) who underwent open surgery died. Of these, 19.4% of VATS and 32.5% of open deaths were lung cancer or pneumonectomy related (P = .16). Stage-adjusted OS for ITT VATS and open procedures is shown in Figure 4. Hazard ratio multivariate analysis showed age and mediastinal lymph node positivity (not approach) as the only independent factors affecting the survival.

Figure Jump LinkFigure 4 –  Stage-adjusted OS (in mo) shown by Kaplan-Meier curves for intent-to-treat VATS and open cases. A, Clinical stage 1 and 2. B, Clinical stage 3 and 4. C, Pathologic stage 0, 1, and 2. D, Pathologic stage 3 and 4. Clin = clinical; OS = overall survival; Path = pathologic. See Figure 1 legend for expansion of other abbreviation.Grahic Jump Location
Outcomes of Converted Cases

To evaluate for potential harm, converted pneumonectomies were analyzed separately. In the first 5.5 years, 18% of all pneumonectomies (50% of ITT VATS) and in the second 5.5 years 14% of all pneumonectomies (18% of ITT VATS) were converted from VATS to open pneumonectomy (P < .001). The various reasons for conversion were tumor size/extension causing limited exposure (n = 8), dense adhesions or scarring (n = 5), bleeding (n = 1), positive margins (n = 1), difficulty in lesion identification (n = 1), and diffuse disease (n = 1). There were no cases of catastrophic bleeding, such as a main pulmonary artery injury, in the VATS pneumonectomy group. Table 5 shows the pertinent results of the three-way comparison between successful VATS, conversions, and open cases. The other perioperative characteristics were similar. The effect of conversion on OS is shown in Figure 5.

Table Graphic Jump Location
TABLE 5 ]  Comparison of Pertinent Perioperative Characteristics and Outcomes for Converted Cases

Data presented as % or median (minimum-maximum). The postoperative complications are same as in Table 3. EBL = estimated blood loss (during surgery). See Table 1 legend for expansion of other abbreviation.

Figure Jump LinkFigure 5 –  Stage-adjusted OS (in mo) shown by Kaplan-Meier curves for successful VATS, conversions, and open cases. A, Clinical stage 1 and 2. B, Clinical stage 3 and 4. C, Pathologic stage 0, 1, and 2. D, Pathologic stage 3 and 4. See Figure 1 and 4 legends for expansion of abbreviations.Grahic Jump Location
Outcomes of Completion Cases

Nine VATS and three open cases were completion pneumonectomies (13.4% vs 7.5%, P = .528). All VATS and two of the open completion cases occurred in the second 5.5-year period. Comparing perioperative outcomes of VATS and open completion pneumonectomies, the only significant difference was EBL (357 mL vs 190 mL open, P = .020). In comparing VATS completion cases with VATS total pneumonectomies, there were similar median ICU days (two vs two, P = .513), hospital days (7 vs 6 days, P = .200), and postoperative complications (three vs two, P = .802). Fifty-six percent of VATS completion cases had clinical and p-stage I disease. All other outcomes were similar to VATS total pneumonectomies.

This study demonstrates that thoracoscopic pneumonectomy can be attempted safely at an experienced VATS center with oncologic validity and reasonable midterm results. This is despite the VATS group having somewhat greater age and more preoperative comorbidities. The higher rate of female sex in the VATS group (a better outcome characteristic for lung resections, in general) has not been commonly reported to favor survival in pure pneumonectomy series.31 The cause of this sex difference is unclear but may reflect a patient self-selection or referral bias.

Compared with VATS, operating room time and EBL in open surgery increased significantly during the second time-half. This suggests an experience bias with progressively more difficult cases chosen for VATS but leaving relatively few, especially challenging cases in the open group. Large central tumors with invasive features, increased adhesions, and tedious hilar dissections were frequently operated by open approach or had a higher conversion rate (also supported by the somewhat higher R1 resection rate). Over the course of the series, adhesions became less of an obstacle to attempting VATS; currently, most open cases have excessive tumor size or inability to achieve negative margins after attempted open vascular or bronchial sleeve lobectomy. VATS was comparable regarding the adequacy of mediastinal lymph node dissection, possibly because of the excellent view after complete lung resection for both approaches. The higher EBL in VATS completion pneumonectomies, typically, was from adhesions. Diffuse oozing from chest wall adhesions slows VATS technical progress relatively more than open cases because of its tendency to increase telescope cleaning and dissection time, thus, allowing more blood to accumulate. Newer hemostatic technologies, particularly laparoscopic cold cautery (Aquamantys; Medtronic, Inc), have reduced this problem.

Thoracoscopic approaches rose from 0% of all lobectomies at the beginning of the first interval to 80% by its end and remained that high after. Our thoracoscopic lobectomy conversion rate (7%) is relatively low, considering a VATS approach was attempted in all but two of 171 cases in 2013. Similarly for thoracoscopic pneumonectomies, our learning curve is evident, with significantly fewer conversions and establishment of VATS completion pneumonectomies in the second half. Many of the patients (76%) undergoing converted pneumonectomy were undergoing right-sided resection; whether this effect was related to a side-specific difference in hilar anatomy or tumor relation to mediastinal structures is not certain. The most frequent cause of conversion was a safety concern due either to tumor characteristics or surrounding adhesions.

The percent share of each procedure type across a given range of a tumor volume or diameter was calculated from Table 5. With tumor volume between 50 and 75 cm3, the conversion rate was 25%, whereas for > 75 cm3, high conversion rate was probably avoided by prudent selection of one-half of the patients for open procedure. Similarly for maximum tumor diameter > 7 cm (T3 size), there was again a higher conversion rate of 25% despite more than one-half of pneumonectomies selected for the open procedure. The number of patients, however, in these high ranges of tumor volume and diameter was small, and, therefore, statistical significance was not reached. Therefore, at present, we are not able to provide any cutoff value for these tumor parameters that might serve as guideline for patient selection when extrapolated to tumor measurements on preoperative imaging. VATS pneumonectomy conversion rates should approach that of thoracoscopic lobectomy as enabling technologies improve exposure and induction chemotherapy shrinks large tumors more reliably. Unfortunately, the required surgeon experience is limited by the need to avoid pneumonectomy because of its high mortality/morbidity rate. Technical advice to aid others in this endeavor is supplied in Table 1.

Acute postthoracotomy pain syndrome is related to factors like rib spreading and intrapleural inflammation, whereas chronic postthoracotomy pain (lasting for > 2 months) results from neuropathy and CNS nociceptive sensitization. A significant benefit was seen in patients who underwent VATS with respect to chronic postthoracotomy pain at 1-year follow-up. The pain benefits in VATS pneumonectomy are, however, not as profound or as immediate as VATS lobectomy. The reasons for this are unclear but may relate to the documented association of low residual pulmonary function to chronic pain, generalized deconditioning, and increased hemithoracic remodeling that occurs following pneumonectomy.8,3235

There are studies that have shown comparable survival figures for VATS and open lobectomies.15,36 Careful patient selection for the procedure type is reflected in an improved median OS for all c- and p-stages in the ITT VATS group; however, statistical significance was reached only for c-stage III/IV. When the conversions were considered separately, the successful VATS group showed a trend toward improved median OS compared with open procedure for p-stages 0/I/II, possibly reflecting less postoperative decompensation (log rank = 0.083, statistical significance not reached). This might emulate a similar protective effect that has been observed for VATS lobectomy in low pulmonary reserve patients.37

In the aggregate of ITT VATS patients, conversions did not harm the patient outcome in comparison with the open cohort. However, as a separate group, converted patients probably suffered deconditioning, transfusion consequences, and so forth, that increased ICU and in-hospital stays and may also have been the reason for lower median OS in c- and p-stage ≤ II. At the same time, the postoperative complications did not increase significantly.

Currently, every pneumonectomy (total or completion) begins with videothoracoscopic exploration to exclude pleural or T4 disease. Tumors that leave no scope space contraindicate VATS. Dense adhesions were a barrier before modern energy devices. Cases are performed or converted to open to divide vascular structures safely or spare lung parenchyma by “sleeve” techniques; however, we attempt these by VATS currently, if appropriate. Improving conversion rates comes from an analysis and problem-solving of previous failures and investing time during difficult cases to try new tools and exposure methods to overcome these challenges. Some aspects can be learned from others, and the authors frequently assist one another to transfer technical points learned from other patients. Other aspects have to be learned individually to adapt to the surgeon’s environment, tools, and port placement that may be idiosyncratic. Within reason, the extra time to do this generally is well tolerated by the patient because the surgical stress is proportionally less. However, one needs to be concerned about very prolonged operations in that the chance of wound complications, pressure sores, and organ malperfusion increases because of volume restriction.

Our retrospective study of a modest experience is limited by selection bias. With differing levels of surgeon experience, alternate case selection criteria and disparate conversion thresholds might have occurred. This possibly resulted in relatively higher number of intended open cases in the first and VATS in the second time-half, although this is partially controlled by the censoring methodologies in the Kaplan-Meier analyses. Some preoperative imaging records, especially those from outside facilities, were inconsistent in tumor parameter description (information bias). The operative notes might not have accurately documented the surgeon’s intent in the initial phase of the procedure (information bias). Also, certain patient-specific personal, social, and other qualitative factors could have influenced the decision-making that might not have been evident from the patient records (recall bias).

Attempting thoracoscopic pneumonectomy at an experienced center appears safe but does not yield the early pain/complication reductions observed for VATS lobectomy. It seems reasonable for comparable centers to continue such investigations for advanced tumors. This is because controlled conversions performed prudently appear tolerable, minimally invasive technology continues to improve, and some of the long-term benefits suggested by this limited retrospective study may be emerging as conversion rates fall.

Author contributions: A. B., A. J., Z. Y., and T. L. D. had full access to all the data and take responsibility for its integrity and accuracy, including the analysis. T. L. D. contributed as principal investigator and manuscript editor, supervised the study, and had major contribution in study concept and design; A. B. and A. J. contributed to data collection and analysis; Z. Y. contributed as the primary statistician; C. E. N. contributed significantly to earlier reports of this research; A. B. contributed to manuscript writing; A. J. and Z. Y. contributed to manuscript preparation and approved the final version; and C. E. N., S. S. Y., E. U. D., M. W. H., and A. L. P. contributed to technique refinement, assisted in manuscript preparation, and approved the final version.

Financial/nonfinancial disclosures: The authors have reported to CHEST that no potential conflicts of interest exist with any companies/organizations whose products or services may be discussed in this article.

Other contributions: We thank William Brady, PhD, senior statistician, who extended resources to this effort.

c-stage

clinical stage

EBL

estimated blood loss (during surgery)

ITT

intent-to-treat

OS

overall survival

p-stage

pathologic stage

R1 resection

resection with positive microscopic margins

VATS

video-assisted thoracoscopic surgery

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Figures

Figure Jump LinkFigure 1 –  Number of VATS and open pneumonectomies over 11 y. VATS = video-assisted thoracoscopic surgery.Grahic Jump Location
Figure Jump LinkFigure 2 –  A, The changes in median operating room time (min) of VATS and open pneumonectomies over 11 y. B, The changes in median estimated blood loss (mL) of VATS and open pneumonectomies over 11 y. See Figure 1 legend for expansion of abbreviation.Grahic Jump Location
Figure Jump LinkFigure 3 –  Pain resolution in patients undergoing VATS and open procedure over 12 mo. See Figure 1 legend for expansion of abbreviation.Grahic Jump Location
Figure Jump LinkFigure 4 –  Stage-adjusted OS (in mo) shown by Kaplan-Meier curves for intent-to-treat VATS and open cases. A, Clinical stage 1 and 2. B, Clinical stage 3 and 4. C, Pathologic stage 0, 1, and 2. D, Pathologic stage 3 and 4. Clin = clinical; OS = overall survival; Path = pathologic. See Figure 1 legend for expansion of other abbreviation.Grahic Jump Location
Figure Jump LinkFigure 5 –  Stage-adjusted OS (in mo) shown by Kaplan-Meier curves for successful VATS, conversions, and open cases. A, Clinical stage 1 and 2. B, Clinical stage 3 and 4. C, Pathologic stage 0, 1, and 2. D, Pathologic stage 3 and 4. See Figure 1 and 4 legends for expansion of abbreviations.Grahic Jump Location

Tables

Table Graphic Jump Location
TABLE 1 ]  Salient Points of VATS Pneumonectomy

VATS = video-assisted thoracoscopic surgery.

Table Graphic Jump Location
TABLE 2 ]  Demographics and Preoperative Characteristics

Data presented as % or median (minimum-maximum). The preoperative comorbidities include those listed for Society of Thoracic Surgeons database plus any previous malignancies. Dlco = diffusing capacity of the lung for carbon monoxide; ECOG = Eastern Cooperative Oncology Group. See Table 1 legend for expansion of other abbreviation.

Table Graphic Jump Location
TABLE 3 ]  Pathologic Characteristics

Data presented as % or median (minimum-maximum). Pathologic stage 0 is a complete response to neoadjuvant treatment. R1 resection = resection with positive microscopic margins. See Table 1 legend for expansion of other abbreviation.

a 

An open pneumonectomy was performed for an extremely large right lung adenocarcinoma involving > 90% of both upper and lower lobes and measuring (38 × 32 × 17.5 cm).

Table Graphic Jump Location
TABLE 4 ]  Comparison of Postoperative Outcomes

Data presented as % or median (minimum-maximum). See Table 1 legend for expansion of abbreviation.

a 

Excludes emergent case deaths (one VATS and one open).

Table Graphic Jump Location
TABLE 5 ]  Comparison of Pertinent Perioperative Characteristics and Outcomes for Converted Cases

Data presented as % or median (minimum-maximum). The postoperative complications are same as in Table 3. EBL = estimated blood loss (during surgery). See Table 1 legend for expansion of other abbreviation.

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