Laparoscopic versus open liver resection for metastatic colorectal cancer

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Laparoscopic versus open liver resection for metastatic colorectal cancer I. Nachmany*,a, N. Pencovich a, N. Zohar, A. Ben-Yehuda, C. Binyamin, Y. Goykhman, N. Lubezky, R. Nakache, J.M. Klausner Department of General Surgery B, Division of General Surgery, Tel-Aviv Sourasky Medical Center, The Nikolas & Elizabeth Shlezak Fund for Experimental Surgery, Sackler Faculty of Medicine, Tel-Aviv University, Tel-Aviv, Israel Accepted 7 September 2015 Available online - - -

Background: Application of minimally invasive surgery for oncologic liver resection is still limited to expert centers. We describe our experience in laparoscopic liver resection (LLR) for colorectal liver metastases (CLM). Patients and methods: Between February 2010 and February 2015, 174 patients underwent resection of CLM. LLR was chosen according to surgeon’s preferences. Data was retrieved from the institutes’ electronic charts and retrospectively analyzed. Results: LLR was performed in 42 patients (24.5%) and OLR in 132. Increased number of metastases were found in OLR (2.82
2.81 versus 1.78
1.16, P ¼ 0.02), with no difference in maximal lesion size (33.1
22 versus 34.9
27.5 cm, P ¼ 0.7). Altogether 55 patients underwent major hepatectomy, and 50 of the OLR group (37.8%, 37 right hepatectomy and 7 left hepatectomy) (P ¼ 0.02). In 5 patients (11.6%) a conversion to open surgery was indicated. Operative time was longer in LLR. Estimated blood loss was decreased in laparoscopic minor resections. One OLR patient died during the postoperative period (0.7%). Eight patients in the OLR group had major complications, versus 1 in the LLR group (P ¼ 0.0016). Reoperation within 30 days was performed in 4 OLR patients and none in the LLR group. Patients in the LLR group had shorter length of stay (LOS) (6.78
2.75 versus 8.39
5.64 days, P ¼ 0.038). R0 resection was 88% in both groups. Conclusions: In selected patients with CLM, LLR is feasible, safe and may achieve shorter LOS without inferior oncologic outcome. Ó 2015 Published by Elsevier Ltd.

Keywords: Liver resection; Laparoscopy; Hepatectomy; Metastasis; Surgery

Introduction Colorectal cancer (CRC) remains a leading cause of cancer death globally. In spite of major advances in surveillance and treatment, a large proportion of CRC patients develop liver metastases during the course of their disease. Approximately 15%e25% of CRC patients present with synchronous liver metastases detected during initial workup, with additional 20%e30% developing metastases within few years following diagnosis.1,2 When applicable, surgical resection of colorectal cancer liver metastases (CRLM) prolongs survival and may achieve cure.3e5 * Corresponding author. Tel-Aviv Sourasky Medical Center, 6 Weizmann St., Tel-Aviv 64239, Israel. Tel.: þ972 3 6973554; fax: þ972 3 6972419. E-mail address: [email protected] (I. Nachmany). a Equal contributors.

As the benefits of minimally invasive surgery are increasingly recognized, the rate of laparoscopic liver resections (LLR) for CRLM is rapidly increasing.6 While initially applied for limited resections, mainly in the anterior segments, LLR is more commonly utilized for major hepatectomies, and resection of lesions in the posterior and superior segments.7,8 Previous studies comparing laparoscopic to open resections of CRLM suggested that LLR is associated with reduced intraoperative blood loss, fewer postoperative complications, shorter length of hospital stay, and decreased health care costs. These benefits are achieved with equivalent overall survival (OS) and disease free survival (DFS).9,10 Moreover, it was suggested that due to reduced adhesions, LLR may allow for higher reoperability, when new lesions appear during followup.11e15

http://dx.doi.org/10.1016/j.ejso.2015.09.014 0748-7983/Ó 2015 Published by Elsevier Ltd. Please cite this article in press as: Nachmany I, et al., Laparoscopic versus open liver resection for metastatic colorectal cancer, Eur J Surg Oncol (2015), http://dx.doi.org/10.1016/j.ejso.2015.09.014

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I. Nachmany et al. / EJSO xx (2015) 1e6

Not all lesions can routinely be approached by LLR, and although there are reports of LLR in all liver territories, minimally invasive techniques are far from being widely utilized for CRLM. Another limitation on the universal acceptance of LLR is the fact that data regarding the above mentioned benefits, is coming from retrospective studies, many with methodological limitations. Currently, the laparoscopic approach for resection of CRLM is mainly used in experienced centers, while many still offer only the open approach. In this study we evaluated the safety and efficacy of LLR compared to the open approach for CRLM in a recently established minimally invasive, hepatobiliary surgery service. The perioperative course as well as the long term outcomes are presented.

cases an inflow control was achieved prior to parenchymal separation and a Pringle maneuver was used selectively for intervals of 15 min with a rest periods of 5 min between intervals. Central venous pressure was kept below 5 mmHg. The low CVP in LLR cases was assessed by the surgeon, according to retro-hepatic IVC filling and fluctuation. Parenchymal separation was done using a combination of cavitron ultrasound surgical aspirator (CUSAÒ by Olympus) and an energy device (LigaSureÔ by Covidien or HARMONIC ACEÒ by Ethicone, Johnson & Johnson). Major vessels were transected with a vascular stapler. Specimen was wrapped in an endo-bag and extracted intact. Statistical analysis

Patients and methods Patients Retrospective analysis of patients that underwent LLR or open liver resection (OLR) for CRLM between February 2010 and February 2015. Patients were excluded if the hepatic lesion was of non-colorectal origin. Patients were designated for LLR or OLR according to surgeon’s preference. All LLR cases were done by a single surgeon. With time and experience, more complex cases were chosen for LLR. All operations were performed with curative intent. Patients’ demographics, comorbidities, tumor characteristics, and pre-operative treatments were evaluated. Additionally, perioperative course, length of stay, pathology reports, and long term outcome including overall survival (OS), and recurrence-free survival (RFS) were analyzed and compared between LLR and OLR patients. Major hepatectomy was defined as the resection of 3 or more contiguous segments. Postoperative mortality was defined as any death within 60 days after the liver resection. Postoperative morbidity was graded according to the ClavieneDindo classification,16 and a major complication was defined as one of grade  III severity. This study was approved by the Tel-Aviv Sourasky Medical Center institutional review board (IRB). Surgical technique Open resection was done through a subcostal incision with upper-midline extension or a midline incision only, according to surgeon’s preference and lesion location. LLR was done by pure laparoscopic technique, using 4e6 ports, with an extraction incision of 4e6 cm, in the midline or suprapubic area. All cases included an exploration of the abdominal cavity and intraoperative ultrasound of the liver. Whenever possible, a non-anatomic, parenchymal-sparing resection was preferred over an anatomic one, for both LLR and OLR. This was true also for laparoscopic cases in segments 4a, 8 and 7, and even when a laparoscopic trans-thoracic approach was needed. In most

Statistical analysis was performed using the IBM SPSS statistics data editor. Continuous data is expressed as median values with the corresponding standard deviation. Student’s T-test was used for continues data, and Chi-square test was used for categorical data. Cumulative survival curves were plotted using the KaplaneMeier method and statistically compared using the log-rank test. Results Patient characteristics Between February 2010 and February 2015, 174 patients underwent liver resection for CLM. Of those, 42 patients underwent LLR and 132 underwent OLR. The median follow-up period for LLR patients was 21 months (range, 1e50), and that of OLR was 41.8 months (range, 1e57) (P < 0.001). Patient characteristics are summarized in Table 1. No difference in gender distribution or age was demonstrated between the groups. Apart from higher rate of DM within the LLR group, no difference in other comorbidities was noticed. The location of the primary tumor, rate of patients with synchronous disease, rate of patients with primary lymph nodes (LN) metastasis, rate of patients who received pre-hepatic chemotherapy, as well as timing of liver metastasis were similar between groups (Table 1). Patients of the OLR groups had higher number of liver metastases compared to the LLR group, with comparable maximal lesion size. No difference in lobar distribution was noticed (Table 1). Operative data The extent, location and procedure performed are summarized in Table 2. Most major hepatectomies were performed by an open approach, especially the right hemihepatectomy (Table 2). The majority of LLR consisted of minor resections. Nevertheless, 6 patients underwent laparoscopic right posterior sectionectomy (14.2%) compared to 7 by the open approach (5.3%). Involvement

Please cite this article in press as: Nachmany I, et al., Laparoscopic versus open liver resection for metastatic colorectal cancer, Eur J Surg Oncol (2015), http://dx.doi.org/10.1016/j.ejso.2015.09.014

I. Nachmany et al. / EJSO xx (2015) 1e6 Table 1 Patient characteristics.

Gender e m/f (ratio) Age (average) Comorbidities: HTN e n (%) IHD e n (%) DM e n (%) COPD e n (%) Rectum primary e n (%) Synchronous CLM e n (%) Positive LN e n (%) Pre-hepatic chemotherapy Mean time from bowel resection, months (mean, range) Number of metastases Maximal lesion size (mm) Lobar involvement: Right lobe Left lobe Bi-lobar

Table 3 Operative results e all cases. OLR n ¼ 132

LLR n ¼ 42

P

70/62 (1.13) 62
11.9

22/20 (1.1) 64.5
12

0.92 0.35

49 (37.1%) 12 (9%) 20 (15.1%) 8 (6%) 30 (22.7%) 53 (40.1%) 58 (43.9%) 96 (72.7%) 25.7
35

21 (50%) 5 (11.9%) 13 (30.9%) 2 (4.7%) 8 (25%) 18 (42.8%) 21 (50%) 28 (66.6%) 27.7
38

0.69 0.26 0.039 0.36 0.29 0.85 0.72 0.57 0.91

2.82
2.81 34.9
27.5

1.75
1.16 32.5
21.9

0.01 0.6

76 (57%) 18 (13.6%) 38 (28.8%)

25 (59%) 9 (21.4%) 8 (19%)

0.91 0.11 0.32

HTN e hypertension, IHD e ischemic heart disease, DM e diabetes mellitus, COPD e chronic obstructive pulmonary disease, LN e lymph node.

of the caudate lobe usually dictated open resection (Table 2). The overall perioperative results are summarized in Table 3. Conversion from laparoscopy to open resection was indicated in 5 patients (11.9%); in 4 due to bleeding and in 1 due to insufficient progression during surgery (Table 3). The mean LLR operative time was longer then OLR (282
120 min vs. 241
107 min, P ¼ 0.02). No statistically significant difference was demonstrated in mean operative blood loss between the groups (Table 3). The rate of minor postoperative complications (ClavieneDindo < 3) was comparable between groups. However, major complications (ClavieneDindo  3) occurred significantly more often following an OLR (6%

Table 2 Operative method.

Major hepatectomy n (%) Right hemihepatectomy Left hemihepatectomy Right trisegmentectomy Central bisectionectomy Minor hepatectomy n (%) Right anterior sectionectomy Right posterior sectionectomy Left lateral sectionectomy Left medial sectionectomy Segmentectomy Non-anatomic resection Caudate lobe involvement

3

OLR n ¼ 132

LLR n ¼ 42

P

50 34 11 4 1 82 1 7 13 3 13 36 9

5 2 3 1 e 37 e 6 7 2 1 21 1

0.028 <0.005 0.06 0.42 e 0.028 e <0.005 0.017 0.002 <0.005 0.29 <0.005

(37.8%) (25.7%) (8.3%) (3%) (0.7%) (62.2%) (0.7%) (5.3%) (9.8%) (2.2%) (9.8%) (27.2%) (6.8%)

(11.9%) (4.7%) (7.1%) (2.35%) (85.8%) (14.2%) (16.6%) (4.7%) (2.35%) (50%) (2.35%)

Conversion to open approach Mean estimated blood loss (ml) Mean operation time (minutes) Postoperative complications: ClavieneDindo < 3 ClavieneDindo  3 Bile leak Reoperation within 30 days Death within 60 days Length of stay (days) R0 resection

OLR n ¼ 132

LLR n ¼ 42

P

e 422.7
410 241
107

5 (11.9%) 251
305 282
120

e 0.13 0.02

46 (34.8%) 8 (6%) 8 (6%) 4 (3%) 1 (0.7%) 8.4
5.6 117 (88.6%)

10 (23.8%) 1 (2.3%) e e e 6.7
2.7 38 (90.4%)

0.44 0.0016 e e e 0.03 0.82

vs. 2.3%, P ¼ 0.0016). Of note, Bile leak occurred in 8 (6%) patients who underwent OLR and in none of those who underwent LLR (Table 3). Reoperation within 30 days was performed in 4 patients (3%) overall, all following an OLR. One patient (0.7%) that underwent OLR died within 60 days following surgery (Table 3). Length of hospital stay was shorter in LLR patients compared to those following OLR (6.7
2.7 days vs. 8.4
5.6 days respectively, P ¼ 0.03). The rate of pathologically negative surgical margins was comparable between the groups (90.4% vs. 88.6% in the LLR and OLR groups respectively, P ¼ 0.82). Operative results e subgroup analysis Major liver resection Major hepatectomy was performed in 5 patients laparoscopically, and in 50 patients by an open approach (Table 4). No conversions were indicated during laparoscopic major hepatectomy. Mean estimated blood loss was comparable between groups. Overall, operative time was longer in the LLR (413
56 min versus 290
60, P ¼ 0.004, Table 4). No major postoperative complications or reoperation within 30 days occurred in patients that underwent laparoscopic major hepatectomy (Table 4). One patient in this group had minor postoperative complication consisting of persisting pulmonary atelectasis with decreased blood oxygen saturation and fever eventually resolving without pharmacologic intervention (Table 4). Mean length of stay (LOS) was shorter in the LLR group (7.6
1 days versus 9.15
6.5 but this did not reach statistical significance) (Table 4). Non-major liver resections Minor hepatectomy was performed laparoscopically in 37 patients, and by an open approach in 82 patients (Table 4). As in major hepatectomy, operative time for LLR was longer than OLR in non-major resections (274
73 vs. 211
71. P ¼ 0.03). Intraoperative blood lose was lower in LLR non-major hepatectomy

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I. Nachmany et al. / EJSO xx (2015) 1e6

Table 4 Operative results by resection type. Major hepatectomy

Conversion to open approach Mean estimated blood loss (ml) Mean operation time (minutes) Postoperative complications: ClavieneDindo < 3 ClavieneDindo  3 Bile leak Reoperation within 30 days Death within 30 days Length of stay (days) a

Non-anatomical, LLSa

Non-major hepatectomy

OLR n ¼ 50

LLR n¼5

P

OLR n ¼ 82

LLR n ¼ 37

P

OLR n ¼ 52

LLR n ¼ 25

P

e 410
270 290
60

e 400
260 413
56

e 0.89 0.004

e 431
356 211
71

5 (13.5%) 235
170 274
73

e 0.002 0.03

e 391
220 183
83

2 (8%) 213
120 254
107

e 0.001 0.003

20 (40%) 4 (8%) 5 (10%) 3 (6%) 1 (2%) 9.15
6.5

1 (20%) e e e e 7.6
1

0.45 e e e e 0.3

26 (32%) 4 (4.8%) 3 (3.6%) 1 (1.2%) e 7.98
5.1

9 (24%) 1 (2.7%) e e e 6.6
2.9

0.65 0.07 e e e 0.075

15 (29%) 2 (3.8%) 2 (3.8%) 1 (1.9%) e 7.4
5.2

2 (8%) 1 (4%) e e e 5.5
2.1

0.009 0.83 e e e 0.04

Non-anatomical resections in anterior sections and left lateral sectionectomies.

(235
170 ml vs. 451
356 ml, P ¼ 0.002; Table 4). The rates of minor and major postoperative complications were comparable between groups (Table 4). Mean LOS was 6.6
2.9 days and 7.98
5.1 days in the laparoscopic and open minor resection groups, respectively (P ¼ 0.075) (Table 4). Out of the non-major hepatectomy groups, a proportion of patients underwent either non-anatomical resection of lesions that were located in anterior segments, or left lateral sectionectomies. In this subgroup, 25 and 52 patients underwent LLR and OLR respectively (Table 4). Patients who had laparoscopic non-anatomical resections or left lateral sectionectomy had decreased intraoperative blood loss (213
120 ml vs. 391
220 ml, P ¼ 0.001), less minor postoperative complications (8% vs. 29%, ClavieneDindo < 3, P ¼ 0.009) and shorter LOS (5.5
2.1 days vs. 7.4
5.2 day, P ¼ 0.04) (Table 4). Mean RFS was 848
32 days and 765
63 days in OLR and LLR groups respectively (Figure 1). The 3-year overall survival rate was comparable between groups with 72.5% and 64.3% of patients surviving over 3 years following OLR and LLR respectively (Figure 1). Ninety and 92%, and 81% and 76% of patients survived 1 and 2 years following surgery in the OLR and LLR groups, respectively. Discussion Minimally invasive surgery has made a significant change in the surgical landscape. In some cases, such as cholecystectomy, the laparoscopic technique had replaced the open procedure altogether, bringing with it new challenges, potential complications, like major bile duct injury, but at the same time significant benefits as reduced pain, faster recuperation and better cosmetic outcome. Some subspecialties, like bariatric surgery, had practically become a pure MIS field. In the era of data availability and patient’s involvement, MIS is also a strong recruiting force for patients, whether benefits are evidence-based or not.

The case of minimally invasive hepatectomy is more complex. Laparoscopy was slow to develop as a significant tool in liver surgery, mainly due to technical challenges such as manipulating the heavy organ, the location behind the rib cage, as well as fear of significant bleeding, loss of dissection plane, and uncertain long term oncologic outcome. Although multiple groups had shown good outcome, these usually represent the activity in highly experienced referral centers, many with special interest in MIS. Indeed, Farges et al. recently showed the low adoption rate of laparoscopic liver surgery in France.17 This low acceptance rate may be influenced by the complexity of LLR, the above mentioned challenges and to some degree, lack of double training e in hepatic surgery as well as MIS. Another issue may be the concern of overcoming the learning curve, which is expected to be relatively long and may be associated with higher rate of complications. Nonetheless, LLR is expected to be rewarding e the work is located in a single territory of the abdomen, the procedures rarely ever have reconstructive component, and the open incision spared, is usually large. Therefore there are many potential benefits to LLR, mainly easier and faster recuperation and shorter length of hospital stay. Although never demonstrated, this may also translate into faster return of cancer patients to systemic chemotherapy, when indicated. A number of studies compared LLR to OLR for CLM and showed improved results in terms of intraoperative blood loss, postoperative complications, narcotic consumption, length of hospital stay, health care costs, and at the same time comparable long term oncological outcome.10,18e24 This study represents our early experience in establishing an MIS-liver service within a busy general surgery department. The results presented in this study stand in good agreement with previously published data, in terms of surgical and oncologic outcome. Moreover, we show that the benefits of LLR are largely related to the extents

Please cite this article in press as: Nachmany I, et al., Laparoscopic versus open liver resection for metastatic colorectal cancer, Eur J Surg Oncol (2015), http://dx.doi.org/10.1016/j.ejso.2015.09.014

I. Nachmany et al. / EJSO xx (2015) 1e6

A

Cumulative Recurrence free survival

1 OLR

0.8 0.6 0.4

LLR

0.2

Log Rank = 0.32

0 0

200 400 600 800 1000 1200 Days from surgery

B

1 OLR

Cumulative overall survival

0.8 0.6 LLR 0.4 0.2

Log Rank = 0.7

5

were achieved with no oncologic compromise and comparable long term survival rates. Major LLR and laparoscopic resections in “difficult” territories, including posterior segments, caudate lobe, and adjacent to major vasculature, is continually reported.24e28 However, most reports fail to show a substantial advantage for laparoscopy in these cases.15,24 Additionally, LLR in “difficult” areas demand outstanding surgical skills and experience found in highly specialized centers, and therefore hard to reproduce. Our data demonstrate that the main benefits of laparoscopy are achieved in minor hepatectomies and in relatively “easy” territories of the liver. These procedures are usually less time consuming, are associated with decreased bleeding and achieve the benefits expected from minimally invasive procedures. Additionally, they can be executed safely by most hepatobiliary surgeons trained in MIS. Other, more challenging cases are doable, but demand much higher technical ability, and the benefits expected should be lower. The study has the limitations of its retrospective nature, the relatively small cohort, and the natural selection bias of more “simple” cases to LLR (mainly in the earlier part of the study). The shorter follow-up for the LLR group is mainly due to the fact that most cases were operated on in the later part of the study. Nonetheless, we believe that programs planning to develop LLR as part of their treatment options may benefit from this experience. To conclude, in selected patients with CLM, LLR is feasible, safe and may achieve shorter LOS without inferior oncologic outcome. The benefits of LLR are achieved mostly in minor liver resections. Conflict of interest statement The authors have no conflict of interest to disclose.

0 0

200 400 600 800 1000 1200 Days from surgery

Figure 1. RFS and OS in CLM patients following OLR and LLR. Recurrence-free survival curve (A) and overall survival curve (B) for patients with CRLM that underwent LLR (green) and OLR (blue). No significant difference in DFS or OS rates was demonstrated (Log-rank 0.32 and 0.7 respectively).

of the procedure and the accessibility of the lesion. Overall, LLR was associated with decreased major postoperative complications and shorter length of stay. Patients that underwent a non-major hepatectomy had significant decrease in intraoperative blood lose. Patients that underwent laparoscopic non-anatomical resections or left lateral sectionectomies, benefited the most, with significantly decreased blood lose, decreased major and minor postoperative complications, and a significant, 2-day shorter LOS. These results

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Please cite this article in press as: Nachmany I, et al., Laparoscopic versus open liver resection for metastatic colorectal cancer, Eur J Surg Oncol (2015), http://dx.doi.org/10.1016/j.ejso.2015.09.014