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Is VATS Lobectomy Better: Perioperatively, Biologically and Oncologically?

Natasha M. Rueth, MD, and Rafael S. Andrade, MD Division of General Thoracic and Foregut Surgery, Department of Surgery, University of Minnesota, Minneapolis, Minnesota

The current review focuses on a clinical comparison of lobectomy by means of video-assisted thoracoscopic surgery (VATS) and open lobectomy. The best available evidence strongly suggests that VATS lobectomy is less morbid than open lobectomy, and that VATS lobectomy is less immunosuppressive and elicits a milder inflammatory response than open lobectomy. Midterm to longterm oncologic results of patients with early-stage non–

small cell lung cancer appear to be equivalent for VATS and open lobectomy. Because a large, prospective, randomized, multiinstitutional trial of open versus VATS lobectomy will likely never take place, we are dependent on the summarized information to draw practical conclusions.

(Ann Thorac Surg 2010;89:S2107–11) © 2010 by The Society of Thoracic Surgeons

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published from a national database, thus focusing on data that broadly reflect current national practices. We reviewed retrospective studies on VATS lobectomy that included 100 patients or more. Finally, we reviewed all available publications that directly compared VATS with open lobectomy.

Material and Methods We performed an extensive review of the currently available English-language literature from 1994 (the year of the first published report on VATS lobectomy) to present. For the purposes of this review, we included the most recently published multiinstitutional trial on open lobectomy for stage I NSCLC and the most recent report

Video-Assisted Thoracoscopic Surgery Versus Open Lobectomy: Perioperative Perspective A comparison of perioperative outcomes of VATS versus open lobectomy first requires an overview of the available data on each.

Open Lobectomy Two studies provide the most recent information on modern perioperative outcomes of open lobectomy for NSCLC: the first is the American College of Surgeons Oncology Group (ACOSOG) Z0030 trial [8]; the second is a report from the STS General Thoracic Surgery database [3].

Published in 2006, the ACOSOG Z0030 is a prospective, multiinstitutional trial of 766 patients who underwent open lobectomy for early-stage NSCLC (T1N0 through T2N1) [8]. In this study, Allen and colleagues reported a mortality rate of 1% and an overall complication rate of 37%. This study represents the results that can be obtained after open lobectomy under next-to-ideal clinical conditions: expert centers, carefully selected patients, and meticulous in-hospital follow-up.

Using the STS database from 1999 to 2006, Boffa and colleagues [3] provided a database analysis that included 6,042 patients undergoing lobectomy for NSCLC by board-certified thoracic surgeons. This study reported an

Presented at the 2nd International Bi-Annual Minimally Invasive Thoracic Surgery Summit, Boston, MA, October 9 –10, 2009.

Address correspondence to Dr Andrade, Division of Thoracic and Foregut Surgery, University of Minnesota Department of Surgery, MMC 207, 420 Delaware St. SE, Minneapolis, MN 55455; e-mail: andr0119@umn.edu.

© 2010 by The Society of Thoracic Surgeons Published by Elsevier Inc

Drs Rueth and Andrade have no conflicts of interest to disclose.

0003-4975/$36.00 doi:10.1016/j.athoracsur.2010.03.020

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ans Christian Jacobaeus (1879 –1937) provided the first description of a thoracoscopy in 1910 [1].

During the past two decades, thoracoscopic pulmonary procedures evolved dramatically, particularly after the initial 1994 report on video-assisted thoracoscopic (VATS) lobectomy by Robert McKenna [2]. Since then, VATS lobectomy has increasingly gained acceptance.

Data from The Society of Thoracic Surgeons (STS) General Thoracic Surgery database showed that by 2006, 32% of lobectomies for primary lung cancer were performed thoracoscopically [3]. Further experience has permitted more-complex procedures such as segmentectomy, pneumonectomy, lung resection after induction therapy, sleeve resections, and en-bloc chest wall resections to be performed with VATS [4 –7].

The vast majority of current reports on VATS lobectomy published in the English-language medical literature focus on patients with clinical stage I non–small cell lung cancer (NSCLC). In the current report, we review the most current available information comparing VATS lobectomy with open lobectomy for clinical stage I NSCLC from perioperative, biologic, and oncologic perspectives.

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Table 1. Perioperative Outcomes of Open Lobectomy Study, Year ACOSOG Z0030, 2006 [8] STS Database, 2008 [3] a

Air leak ⬎ 5 days.

b

n

Total Complication Rate (%)

Air Leak (%)

Arrhythmia (%)

Pneumonia (%)

LOS (days)

Mortality (%)

766 5,957c

37 32c

8b 8a,d

15 10.7d

6 3.9d

6 5d

1 2

Air leak ⬎ 7 days.

c

Open (80%), video-assisted thoracoscopic surgery (20%).

ACOSOG ⫽ American College of Surgeons Oncology Group;

LOS ⫽ length of stay (median or mean);

operative mortality rate of 2%; the overall morbidity of patients undergoing any lung resection for NSCLC in this report (n ⫽ 9,033) was 32%, but was not separately calculated for lobectomy alone. Limitations of this study include voluntary reporting, heterogeneous patient population (eg, 20% of lobectomies were by VATS, 19% of patients were greater than stage IIIA, 16% underwent neoadjuvant chemotherapy, and 11% had neoadjuvant radiation therapy), and an incomplete breakdown of data by type of lung resection. Nonetheless, the results of the STS database analysis are likely broadly reflective of current clinical care, and are strikingly similar to the results of the ACOSOG Z0030 trial.

Based on these reports, the current overall morbidity of open lobectomy ranges from 32% to 37%, with a perioperative mortality rate of 1% to 2%. The results from these studies are summarized in Table 1.

Video-Assisted Thoracoscopic Lobectomy One multiinstitutional, prospective study [9] and several single-institution retrospective case series of VATS lobectomy [6, 10 –18] describe perioperative outcomes in early-stage NSCLC patients.

In 2007, Swanson and colleagues [9] published the results from the Cancer and Leukemia Group B 39802 trial. This prospective, multiinstitutional study was designed to assess the perioperative outcomes of patients undergoing VATS lobectomy for early NSCLC between 1998 and 2001. In this series of 127 patients, the perioperative mortality rate was 2.7%. Patients in this series

d

All lung resections (66% were lobectomy).

STS ⫽ The Society of Thoracic Surgeons.

were generally healthy (performance status of 0 or 1) with small cancers (87% stage I). Importantly, the major perioperative morbidity rate (defined as complications grade 3 or greater) was only 7.4% for these ideal candidates.

Reviewing retrospective series with more than 100 patients, the reported incidence of overall complications (including minor, low-grade complications) is between 10% and 20%, whereas mortality rates range from 0% to 2%. On the basis of these individual retrospective series, outstanding results can be achieved at very experienced centers with appropriate patient selection. The results on operative morbidity and mortality from these reports are summarized in Table 2.

Comparison of Video-Assisted Thoracoscopic Lobectomy Versus Open Lobectomy Perioperative outcomes of VATS versus open lobectomy have been compared in one small prospective trial (55 patients), three retrospective case control series, and one large systematic review including more than 6,000 patients [19 –24]. All of these studies indicate less perioperative morbidity for VATS lobectomy (10% to 30%) than for open lobectomy (20% to 50%). The mortality rates are similar between the two procedures. Table 3 summarizes the published studies that directly compare VATS versus open lobectomy.

A prospective, randomized comparison of open versus VATS lobectomy will likely never occur, leaving us to rely on the best available current evidence to draw meaning-

Table 2. Perioperative Outcomes of Video-Assisted Thoracoscopic Lobectomy: Series With ⬎ 100 Patients Author, Year

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Yim, 1998 [18] Lewis, 1999 [11] Gharagozloo, 2003 [10] Walker, 2003 [17] Ohstuka, 2004 [13] Rovario, 2004 [15] McVay, 2005 [12] McKenna, 2006 [6] Onaitis, 2006 [14] Swanson, 2007 [9] Solaini, 2008 [16] a

Air leak ⬎ 5 days.

b

n

Conversion to Thoracotomy (%)

Total Complication Rate (%)

Air Leak (%)a

Arrhythmia (%)

Pneumonia (%)

LOS (days)

Mortality (%)

214 250 179 158 106 257 153 1,100 500 111 217

19.5 ...

0 11.2 10 22.5 1.3 2.5 1.6 13.5 12.6

22 11 20.6 36.6 9 ...

18 15.3 ...

9.5b 10.1

... ...

1.7 ... ... ...

4.4 0.5 4 1 ...

...

1 9.4 ...

2.1 ...

5 2.9 10 5.3 0.9

...

0.8 5.6 ...

2.1 ...

1.9 1.2 5 ...

1.4

...

2.8 4.1 6 7.6 5 4 4.8 3 ...

5.8

0.5 0 0.6 1.8 1.1 0.8 1.8 0.8 1.2 2.7 ...

Severe complication.

LOS ⫽ length of stay (median or mean).

Intention-to-treat analysis, conversions to open included in VATS group.

Video-Assisted Thoracoscopic Lobectomy Versus Open Lobectomy: Biologic Perspective The biologic advantages of VATS lobectomy compared with open lobectomy have been demonstrated in vitro in four studies on acute-phase reactants and cellular immune responses [25–28]. In summary, these studies show that VATS lobectomy leads to a reduced inflammatory response (lower interleukin and C-reactive protein levels), less postoperative reduction in CD4 and natural killer cells, and less impairment of cellular cytotoxicity than open lobectomy. These findings could partially explain why perioperative outcomes of VATS lobectomy are superior to the perioperative outcomes of open lobectomy. Whether these biologic differences translate into a long-term survival advantage is not known. Table 4 provides an overview of studies comparing the biologic impact of VATS versus open lobectomy.

Data represent results with propensity score-based matching.

Retrospective

Retrospective

Villamizar, 2009 [22]

Flores, 2009 [19]

VATS ⫽ video-assisted thoracoscopic surgery.

Patients with protensity score for VATS of 0.4 – 0.6.

Retrospective Handy, 2009 [20]

LOS ⫽ length of stay;

p ⬍ 0.05.

f

Systematic review Whitson, 2008 [24]

Air leak ⬎ 5 days.

Retrospective Whitson, 2007 [23]

b

Prospective Kirby, 1995 [21]

Author, Year

Study Type

c

Mean or median. a

VATS Open VATS Open VATS Open VATS Open VATS Open VATS Open

Procedure

d

Video-Assisted Thoracoscopic Lobectomy Versus Open Lobectomy: Oncologic Perspective To date, only one small prospective, randomized trial has compared oncologic results of VATS with open lobectomy [29]. In this study published in 2000, Sugi and colleagues reported that for 100 patients with stage IA NSCLC undergoing either open (n ⫽ 52) or VATS (n ⫽ 48) lobectomy, there was no difference in 3- and 5-year survival rates. Several additional retrospective reports support these findings [19, 30, 31]. In these separate reports, the 5-year survival for VATS lobectomy is near 80%, similar to that for open lobectomy (75% to 82%; Fig 1).

In a 2008 systematic review, Whitson and colleagues [24] provided an analysis of 39 studies comparing VATS with open lobectomy. In this study, patients with VATS lobectomy had similar survival at 1, 2, 3, and 5 years after resection when compared with those who underwent open resection; at 4 years, patients who underwent VATS lobectomy had improved survival versus patients with open lobectomy (88.4% vs 71%; p ⫽ 0.003); however, this particular finding is of questionable clinical relevance.

More recently, Yan and colleagues [32] performed a similar systematic review; the authors reported that 5-year survival was significantly improved for patients who undergo VATS lobectomy for early-stage NSCLC (VATS relative risk, 0.72; p ⫽ 0.04), further suggesting that VATS lobectomy is at least oncologically equivalent to open lobectomy. Whether VATS lobectomy has a long-term survival advantage over open lobectomy cannot be answered at this time.

Table 5 summarizes the most relevant recent information on oncologic outcomes of VATS versus open lobectomy for early-stage NSCLC.

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12 27 13.6 11.5 5 8.8 ... ...

12c 19 4.2 5.2 6.5 4.6 5 6.1 4.2c 5.7 ⬎5 (14%) ⬎5 (15%) 3c 4 ... ...

24c 53 ... ...

16.4c 31.2 10 22.5 31c 51 23c,f 33f ⬍250 (84%) ⬍250 (83%) 251 255 ... ...

204c 470 ... ... ... ...

25 30 59 88 3,114 3,256 49 192 284d 284d 398e 343

n

Total Complication Rate (%)

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ful clinical conclusions. Our review, despite limitations, suggests that VATS lobectomy is associated with less perioperative morbidity than open lobectomy.

e

Air Leak (%)b Chest Tube Duration (days)a

... ...

13.8 10.3 5.2 9 6.1c 17.3 13c 21 10.3 12.5

... ...

3.4c 19.3 2.7 6 4.1 7.1 5c 10 ... ...

7.1 8.3 6.4 7.7 8.3c 13.3 5.2c 6.6 4c 5 5c,f 7f

0 0 0 0 ... ...

4.1 2.6 3 5 0.3 0.3

MINIMALLY INVASIVE THORACIC SURGERY SUMMIT 2009 RUETH AND ANDRADE VATS LOBECTOMY REVIEW

Blood Loss (mL)

Table 3. Perioperative Outcomes of Lobectomy Comparing Video-Assisted Thoracoscopic Lobectomy With Open

Arrhythmia (%)

Pneumonia (%)

LOS (days)a

Mortality (%)

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Fig 1. Five-year survival of video-assisted thoracoscopic lobectomy (VATS; intent to treat) is compared with open lobectomy (thoracotomy). Shaded areas indicate 95% confidence intervals (CI). (Reprinted from J Thorac Cardiovasc Surg 2009;138:11– 8 [19] by permission of Elsevier.)

Table 4. Studies Comparing the Biologic Impact of Video-Assisted Thoracoscopic Lobectomy Versus Open Lobectomy Preoperative Clinical Stage

Author, Year

Study Type

Yim, 2000 [28]

Prospective nonrandomized

I

Craig, 2001 [26]

Prospective randomized

I

Leaver, 2000 [27]

Prospective randomized

I

Whitson, 2008 [25]

Prospective nonrandomized

I

CRP ⫽ C-reactive protein; IL ⫽ interleukin; cell reactive oxygen species production.

Procedure

n

VATS Open VATS Open VATS Open VATS Open

18 18 22 19 22 19 6 7

NK ⫽ natural killer;

Biologic Marker

Result

IL-6, IL-8, IL-10

VATS: fewer acute phase reactants

IL-6, CRP, WBC ROS

VATS: lower levels of IL-6, CRP, and WBC ROS

Lymphocytes (CD4), NK cells

VATS: less reduction in CD4 and NK cells

Cellular cytotoxicity

VATS: less impairment of cellular cytotoxicity

VATS ⫽ video-assisted thoracoscopic surgery;

WBC ROS ⫽ white blood

Table 5. Studies Comparing the Oncologic Outcomes of Video-Assisted Thoracoscopic Lobectomy Versus Open Lobectomy for Early-Stage Non–Small Cell Lung Cancer Author, Year

Preoperative Clinical Stage

Study Type

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Sugi, 2000 [29]

Prospective randomized

I

Yang, 2009 [31]

Retrospective

I

Flores, 2009 [19]

Retrospective

I

Farjah, 2009 [30]

Retrospectiveb

Whitson, 2008 [24]

Systematic review

VATS: 65% ⫽ I Open: 61% ⫽ I I

Yan, 2009 [32]

Systematic review

I

a

Not significant compared with open.

HR ⫽ hazard ratio;

b

Procedure

n

VATS Open VATS Open VATS Open VATS Open VATS Open VATS Open

48 52 43 98 398 343 721 12,237 3,114 3,256 1,391 1,250

Outcome Measured 3- and 5-year survival 5-year survival 5-year survival Overall survival (HR) 5-year survival 5-year survival

Data from the Surveillance Epidemiology and End Results (SEER) database.

CI ⫽ confidence interval;

RR ⫽ relative risk;

VATS ⫽ video-assisted thoracoscopic surgery.

Results 3y ⫽ 90%a; 5y ⫽ 90%a 3y ⫽ 93%; 5y ⫽ 85% 79%a 82% 79%a 75% HR ⫽ 0.97; (CI 0.88–1.07)a 80%a 65.6% RR ⫽ 0.72; (CI 0.45–0.97)

MINIMALLY INVASIVE THORACIC SURGERY SUMMIT 2009 RUETH AND ANDRADE VATS LOBECTOMY REVIEW

Conclusions Because a large, prospective, randomized, multiinstitutional trial of open versus VATS lobectomy will likely never take place, we are dependent on the herein summarized information to draw clinically applicable conclusions. The currently available clinical evidence indicates that VATS lobectomy for early-stage NSCLC is associated with fewer postoperative complications and less negative biologic impact on patients than open lobectomy. Furthermore, all data to date strongly suggest oncologic equivalence of VATS versus open lobectomy for patients with early-stage NSCLC.

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