World J Surg DOI 10.1007/s00268-015-3034-4
ORIGINAL SCIENTIFIC REPORT
Laparoscopic Simultaneous Resection of Colorectal Primary Tumor and Liver Metastases: Results of a Multicenter International Study Stefano Ferretti1 • Hadrien Tranchart1 • Joseph F. Buell2 • Constantino Eretta3 Alberto Patriti4 • Marcello Giuseppe Spampinato5 • Jung Wook Huh6 • Luca Vigano7 • Ho Seong Han8 • Giuseppe Maria Ettorre9 • Elio Jovine10 • Thomas Clark Gamblin11 • Giulio Belli12 • Go Wakabayashi13 • Brice Gayet14 • Ibrahim Dagher1
•
Ó Socie´te´ Internationale de Chirurgie 2015
Abstract Background With the advance of modern laparoscopic technology, laparoscopic colorectal surgery and laparoscopic liver surgery are both worldwide accepted. Preliminary brief series have shown the feasibility of combined laparoscopic resection of colorectal cancer (CRC) and synchronous colorectal liver metastases (SCRLM). We aim to report a large International multicenter series of laparoscopic simultaneous resection of CRC and SCRLM. Methods Between 1997 and 2013, 142 laparoscopic liver resections were performed with simultaneous colorectal surgery for SCRLM. The surgical and postoperative variables evaluated were the duration of the intervention, blood loss, transfusion rate, conversion rate, resection margin, specific and overall morbidity, perioperative mortality, length of hospital stay, and survival. Univariate and multivariate analyses were performed examining postoperative morbidity in the all cohort of patients. Results The median number of liver lesions was 1 (1–9) and the median larger diameter at diagnosis was 28 (2–100) mm. The median operative time was 360 (120–690) min. Seven patients (4.9 %) required conversion. The global morbidity was 31.0 % and the mortality was 2.1 %. After a median follow-up of 29 (1–108) months, 40 patients (28.2 %) developed tumor recurrence. Curative treatment of recurrence was possible in 17 patients (12.0 %), including a second liver resection in 13 patients (9.1 %), which was performed by laparoscopy in 7 patients (4.9 %). Overall 1-, 3-, and 5-year survivals were 98.8, 82.1, and 71.9 %, respectively. By multivariate analysis, ASA score C3 [OR 13.6 (1.8–99.6); P = 0.01] and operative time [OR 1.008 (1.001–1.016); P = 0.03] were independent predictors of postoperative morbidity. Conclusions Our combined data show that in experienced centers, simultaneous laparoscopic approach is technically feasible, safe, and associated with good oncological outcomes.
Stefano Ferretti and Hadrien Tranchart have contributed equally to this work. & Hadrien Tranchart [email protected] 1
Department of Minimally Invasive Digestive Surgery, Antoine Be´cle`re Hospital, AP-HP, Paris-Sud University, 157 rue de la Porte de Trivaux, 92141 Clamart, France
2
Department of Surgery, Tulane Abdominal Transplant Institute, New Orleans 70112, USA
3
Division of General Surgery, Sant’Andrea Hospital, 19100 La Spezia, Italy
4
Division of General Minimally Invasive and Robotic Surgery, San Matteo degli Infermi Hospital, 06049 Perugia, Italy
5
HPB and Advanced Laparoscopic Surgical Unit, Policlinico of Abano Terme, 35031 Abano Terme, Italy
6
Department of Surgery, Chonnam National University Hwasun Hospital and Medical School, Seoul 135-710, South Korea
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Introduction Colorectal cancer (CRC) is one of the most common causes of cancer death in the Western world with more than 940,000 new cases annually and nearly 500,000 deaths each year worldwide [1]. Up to 50 % of patients with CRC might have liver metastases during the course of the disease, and 15–20 % have synchronous colorectal liver metastases (SCRLM) at the time of diagnosis, whereas an additional 20–25 % develop metachronous hepatic tumors [2, 3]. The presence of liver metastases has an important influence on patient prognosis, and the median survival is 2–21 months for patients in whom the cancer is non-resected [4–6]. Furthermore, liver resection has been accepted as the only treatment offering the chance for cure and long-term survival, with 5-year survival rates of 25–60 % and 10-year survival rates of 22–26 %, respectively reported in the literature [7–15]. During the past decade, most studies have recommended a staged operation with initial resection of the colorectal primary cancer followed by hepatic resection of the SCRLM 2–6 months later [16, 17]. However, the optimal strategy for the management of SCRLM remains controversial including primary resection first followed by liver [18], liver resection first followed by primary resection [19], or simultaneous resection. Several reports, including a recent meta-analysis, have shown the benefit of a simultaneous open resection of primary tumor and SCRLM compared with a staged approach [20–23]. Simultaneous resection did not increase mortality or morbidity rates compared with delayed resection. Moreover, the combination of major hepatectomy and colorectal tumor resection was not associated with increased morbidity [23, 24]. With the advance of modern laparoscopic technology, laparoscopic colorectal surgery and laparoscopic liver surgery are both accepted worldwide. Laparoscopic colorectal resection for cancer has been shown to be safe and oncologically equivalent to conventional surgery [25–28]. Moreover, it reduces hospital stay, shortens recovery times and reduces postoperative complications [29–32]. On the other hand, laparoscopic liver surgery is now recognized as
7
8
9
safe, and showed some improvement in postoperative outcomes compared with open resection [33, 34]. Furthermore, several series have shown that the margin after LLR of colorectal liver metastases as well as oncological outcomes were equivalent compared with open resection [35–38]. Preliminary brief series have shown the feasibility of combined laparoscopic resection of both CRC and SCRLM [37, 39–41]. We report a large International multicenter retrospective series of laparoscopic simultaneous resection of colorectal primary tumor and liver metastases. Univarite and multivariate analyses were performed examining postoperative morbidity in all cohort of patients.
Methods Patient demographics Between 1997 and 2013, 142 LLR were performed with simultaneous colorectal surgery for SCRLM. All centers involved in this study have more than 4 years of experience in the laparoscopic liver surgery field: seven from Italy, two from France, two from USA, two from Korea, and one from Japan. There were 66 male (46.5 %) and 76 women (53.5) with a median age of 66 (32–85) years. Characteristics of patients are summarized in Table 1. In the 14 centers, patients with solitary lesions of 5 cm or less, located in liver segments II to VI were considered as more suitable to laparoscopic liver resection (LLR) [33]. Exclusion criteria were tumors close to the portal pedicle or hepatic veins, an American Society of Anesthesiologists score (ASA) exceeding III, a decompensated cirrhosis, esophageal varices grade [1, and a platelet count \80 9 109/L. However, those criteria were not exclusive in all centers and evolved with time and experience. Operative and perioperative management Twenty-five patients (17.6 %) had neoadjuvant chemotherapy including 5 patients (3.5 %) that had radiotherapy for a
Department of HPB and Digestive Surgery, Ospedale Mauriziano Umberto I, 10100 Turin, Italy
12
Division of General Surgery, S. Maria di Loreto Nuevo Hospital, 80142 Naples, Italy
Department of Surgery, Seoul National University Bundang Hospital, Seoul, 135-710, South Korea
13
Department of Surgery, Iwate Medical University School of Medicine, Morioka 020-8505, Japan
General Surgery and Liver Transplantation Unit, San Camillo Forlanini Hospital, 00152 Rome, Italy
14
Department of Digestive Diseases, Institut Mutualiste Montsouris, 75014 Paris, France
10
Department of Surgery, Maggiore Hospital, 40133 Bologna, Italy
11
Division of Surgical Oncology, Medical College of Wisconsin, Milwaukee 53226, USA
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World J Surg Table 1 Demographics and liver and colorectal characteristics of patients undergoing laparoscopic liver resection with simultaneous colorectal surgery for synchronous colorectal liver metastases
Table 2 Types of resection for patients undergoing laparoscopic liver resection with simultaneous colorectal surgery for synchronous colorectal liver metastases
Variable
Variable
Data
Totally laparoscopic, n (%)
127 (89.4)
Data
Patients Gender (female/male)
76/66
Hand-assisted, n (%)
15 (10.6)
Age (years), median (range) BMI (kg/m2), median (range)
66 (32–85) 24.3 (18.3–38)
Colorectal resection Rectal resection, n (%)
58 (40.8)
ASA I, n (%)
37 (26.0)
Stoma covering low anastomosis, n (%)
ASA II, n (%)
57 (40.1)
Abdominoperineal resection, n (%)
ASA III, n (%)
45 (31.7)
ASA IV, n (%)
3 (2.1)
Colorectal tumor
10 (7.0) 3 (2.1)
Liver resection A typical resection, n (%)
103 (72.5)
Left lateral sectionectomy, n (%)
22 (15.5) 13 (9.2)
Rectal tumor
58 (40.8)
Right hepatectomy, n (%)
Right colon
38 (26.8)
Left hepatectomy, n (%)
Left colon
46 (32.4)
Pringle’s maneuver, n (%)
4 (2.8) 17 (12.0)
Liver metastases Number of lesions, median (range)
1 (1–9)
Number of lesions [2/[3, n (%)
35 (24.6)/22 (15.5)
Bilobar, n (%)
28 (19.7)
Larger diameter at diagnosis (mm), median (range)
28 (2–100)
CEA at diagnosis (ng/mL), median (range)
36 (0.8–315)
BMI body mass index, ASA American society of anesthesiologists physical status score, CEA carcinoembryonic antigen
were specific and overall morbidity, perioperative mortality, length of hospital stay, and survival. Mortality and morbidity were defined as death or complications occurring within 30 days after surgery. Complication severity was stratified according to the modified Clavien classification [42]. Statistical analysis
rectal cancer. The first operating procedures was the LLR in 33 patients (23.2 %) and the colorectal resection in 109 patients (76.8 %). Both colorectal and liver resections were performed by the same team in 87 patients (61.3 %). Four centers systematically used two different surgical teams. Six patients (4.2 %) underwent a rectal resection combined with a major liver resection. Eleven centers performed only pure laparoscopic liver and colonic resection and the other three centers performed 15 (10.6 %) hand-assisted LLR procedures. Pringle’s maneuver was never used systematically in any center but in case of bleeding. Liver transection was performed with thermofusion in four centers, with ultrasound section in six centers, and with an ultrasonic surgical aspirator in four centers. Hepatic veins were divided using a linear stapler. The resected liver specimen was extracted in a plastic bag, without fragmentation, along a suprapubic or a right transverse incision that was used to extract the colorectal specimen. The types of resection performed are detailed in Table 2. Study criteria The surgical variables evaluated were the duration of the intervention, blood loss, transfusion rate, conversion rate, and resection margin. The postoperative variables assessed
Statistical analyses were carried out with SPSS software (IBM Company, Los Angeles, CA). Continuous variables were expressed as median (range) and were compared using the student t test or the Mann–Whitney U tests, as appropriate. v2 test or Fisher’s exact test were used for comparisons of categorical variables, as appropriate. Values of P \ 0.05 were considered statistically significant. To test the independence of the risks factors, the significant pre- and intraoperative variables in the univariate analyses were entered into a multivariate logistic regression model with likelihood ratio forward selection. Disease-free and overall survival rates were calculated using the Kaplan–Meier method.
Results Intraoperative results The median operative time was 360 (120–690) min and the LLR was significantly shorter than the colorectal resection (P = 0.04). Seven patients (4.9 %) required conversion due to: an uncertain liver margin (n = 2), a right ureteral injury (n = 1), an hemorrhage during LLR (n = 1),
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adhesions (n = 1), difficult progression (n = 1), or an intraoperative discovery of carcinomatosis (n = 1). The procedure was successfully completed by open approach in those seven cases of conversion. Surgical and histological results are detailed in Table 3.
Table 4 Postoperative results for patients undergoing laparoscopic liver resection with simultaneous colorectal surgery for synchronous colorectal liver metastases Variable
Data
Mortality, n (%)
3 (2.1)
Specific morbidity, n (%)
Postoperative results The global morbidity rate was 31.0 % and the specific liver and colorectal morbidities did not differ significantly (P = 1.00). Eight patients (5.6 %) presented an anastomotic leakage. Seven of those patients required reoperation for creation of a covering ostomy and/or drainage. One patient was treated by prolonged drainage without reoperation. Six patients (4.2 %) presented a biliary collection and were treated by percutaneous drainage. Three patients (2.1 %) presented an hemorrhage after LLR and required reoperation. Three patients died: one patient after a postoperative hemorrhage which required reoperation, one patient presented multiple organ failure and one patient died of acute coronary syndrome. Postoperative results are detailed in Table 4. Oncological results After a median follow-up of 29 (1–108) months, 40 patients (28.2 %) developed tumor recurrence; 16 patients (11.3 %) had exclusive liver recurrence and two patients Table 3 Surgical and histological results for patients undergoing laparoscopic liver resection with simultaneous colorectal surgery for synchronous colorectal liver metastases
Colorectal morbidity, n (%) Leakage, n Abdominal abscess, n
1
Segmental ischemic colitis, n
1
Prolonged ileus, n
1
Liver morbidity, n (%) Ascites, n
Data
Colorectal operative time (min), median (range)
156 (80–405)
Liver operative time (min), median (range)
120 (15–600)
Blood loss (mL), median (range)
200 (0–1800)
Transfusion, n (%)
12 (8.5)
Packed red blood cell units, median (range) Conversion to laparotomy, n (%)
3 (1–6) 7 (4.9)
Colorectal tumor characteristics T1, n (%)
8 (5.6)
T2, n (%)
22 (15.5)
T3, n (%) T4, n (%)
87 (61.3) 25 (17.6)
Tumor well/moderately/poorly/un/ differentiated, n (%) N?, n (%) Positive liver metastasis surgical margin (%)
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24 (16.9)/84 (59.1)/22 (15.5)/12 (8.5) 88 (62.0) 10 (7.0)
11 (7.7) 1
Liver failure, n
1
Biliary collection, n
6
Hemorrhage, n General morbidity, n (%)
3 22 (15.5)
Heart failure, n
1
Pulmonary, n
7
Incisional abscess, n
3
Acute renal failure, n
1
Distal deep vein thrombosis, n Urinary tract infection, n
1 2
Pancreatitis, n
1
Cholangitis due to bile duct stone, n
1
Multi organ failure, n
1
Acute coronary syndrome, n
2
Central venous catheter infection, n
1
Unexplained fever, n
1
Clavien classification Grades I, II, IIIa, IIIb, IVa, IVb, V
Variable
22 (15.5) 11 (7.7) 8
Reoperation, n (%)
2/14/9/11/5/0/3 11 (7.7)
First oral intake of solid food (d), median (range)
3 (1–20)
Intensive care unit stay (d), median (range)
1 (1–16)
Hospital stay (d), median (range)
8 (3–84)
(1.4 %) had anastomotic recurrence. The median delay between surgery and recurrence was 12 (1–78) months. Curative treatment of recurrence was possible in 17 patients (12.0 %), including a second liver resection in 13 patients (9.1 %) which was performed by laparoscopy in 7 patients (4.9 %). During the study period, six patients (4.2 %) displayed peritoneal carcinomatosis and none had port-site recurrence. Twenty-seven patients (19.0 %) died during the study period, including three patients who died during the postoperative period. Overall 1-, 3-, and 5-year survivals were 98.8, 82.1, and 71.9 %, respectively. Disease-free 1-, 3-, and 5-year survivals were 85.6, 65.9, and 63.0 %, respectively (Fig. 1).
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Fig. 1 Overall (continuous line) and disease-free (dotted line) survival curves
Uni- and multi-variate analyses of postoperative complications No factors were found to be predictors of postoperative specific colorectal or liver postoperative morbidity in univariate analysis. Seven factors were found to be risk factors for postoperative complications: ASA score CIII (P = 0.007), BMI (P = 0.04), global operative time (P = 0.01), blood loss (P = 0.01), transfusion (P \ 0.0001), Pringle’s maneuver (P = 0.04), and length of stay (P \ 0.0001). By multivariate analysis, ASA score CIII [OR 13.6 (1.8–99.6); P = 0.01] and global operative time [OR 1.008 (1.001–1.016); P = 0.03] were independent predictors of postoperative morbidity (Table 5).
Discussion Technical refinements and anesthesia progress have enabled surgical groups to perform laparoscopic synchronous colorectal and liver resection. However, concerns persist regarding the safety and the oncological equivalence of minimally invasive approach for one-stage resection compared to open surgery. We report in this series a multicenter study concerning laparoscopic approach for the synchronous management of liver metastases and CRC in selected patients.
Simultaneous resection of liver and colon or rectum for patients with SCRLM was initially associated with a perceived increased risk of complications and mortality [16, 17, 43]. Authors reluctant to the combined approach argue that the association of a clean surgical procedure with one likely to cause contamination may result in higher morbidity rates [44]. Furthermore, the risk of intestinal edema after pedicle clamping [44, 45] and vulnerability to infection due to postoperative impaired liver function could be associated with an increased risk of anastomotic leakage [44]. However, in high-volume centers with appropriate experience in both liver and colorectal resection, simultaneous surgery has been shown to be safe and efficient [46]. Repeated surgery is often required for patients with colorectal liver metastases, making the laparoscopic approach particularly beneficial for those patients. Some teams initially have performed the colorectal resection by laparoscopy with a concomitant open liver resection [47]. Most experienced centers in LLR have initiated laparoscopic combined resection for minor [14] and major liver resection [48]. However, only few limited single center series are available in the literature, which led us to conduct this multicenter study associating 14 experienced centers in both liver and colorectal laparoscopic surgery. The main finding of this series was that global morbidity (31 %) and mortality (2 %) were comparable to rates reported by experienced teams performing open synchronous resection [23] or colorectal laparoscopic resection followed
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World J Surg Table 5 Uni- and multi-variate analyses of postoperative complications for patients undergoing laparoscopic liver resection with simultaneous colorectal surgery for synchronous colorectal liver metastases Variable
Postoperative complication, n (%)
UV P
MV P
Table 5 continued Variable
0.20
Male
24 (16.9)
Female
20 (14.1)
Agea a
BMI ASA score
–
0.48
–
–
–
0.04 0.007
NS 0.01
– 13.6 (1.8–99.6)
18 (12.6)
III–IV
26 (18.3)
11 (7.8)
No
33 (23.2)
Radiotherapy
0.30
Yes
1 (0.7)
No
43 (30.2)
Colorectal tumor 26 (18.3)
Rectum
18 (12.7)
Yes
9 (6.4)
No
35 (24.7)
Blood lossa
–
–
–
–
–
Yes
10 (7.0)
No
34 (23.9)
Conversion to laparotomy
–
MV P
OR (95 % CI)
0.04
NS
–
0.01
0.03
1.008 (1.001–1.016)
0.01
NS
–
\0.0001
NS
–
–
NS
–
–
0.49
Yes
3 (2.1)
No
41 (28.9)
Hospital staya 0.92
Colon
39 (27.5)
Transfusion
0.29
Yes
5 (3.5)
No
Global operative timea
Preoperative management Chemotherapy
Yes Pringle’s maneuver
–
–
I–II
UV P
OR (95 % CI)
Patients Gender
Postoperative complication, n (%)
–
\0.0001
UV univariate analysis, MV multivariate analysis, OR odd ratio, CI confidence interval, NS not significant, BMI body mass index, ASA American society of anesthesiologists physical status score a
Continuous variable
Liver metastases Number of lesionsa
–
Bilobar Yes
9 (6.3)
No
35 (24.7)
Larger diameter at diagnosisa
–
0.11
–
–
0.74
–
–
0.95
–
–
0.56
–
–
0.31
–
–
0.92
–
–
0.88
–
–
Surgery Colorectal and liver procedures performed by different teams Yes
14 (9.8)
No
30 (21.1)
Hand-assisted Yes
3 (2.1)
No
41 (28.9)
Rectal resection Yes
26 (18.3)
No
18 (12.7)
Major liver resection
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by open hepatectomy [47] (Table 6). Furthermore, the anastomotic leakage rate (5.6 %) was not increased by the association of LLR in comparison to the rates reported by experienced teams performing isolated laparoscopic colorectal resection [31, 49] and despite an important rate of rectal procedures (40.8 %). Indeed, the Pringle’s maneuver was described as a risk factor for postoperative anastomotic leakage [44, 45]. In our series, clamping was never used in any center on purpose but just in the cases of uncontrolled bleeding (12 %).This may have contributed to this rate of postoperative fistula. However, the majority of patients in this study underwent the colorectal resection as the first operating procedure and an intention-to-treat analysis was not possible with our data. Data concerning patients in whom the preoperative synchronous strategy was not finally performed due to a difficult first-step procedure were not available. In combined resections, the liver-specific morbidity was 7.7 %. Indeed, the association of laparoscopic colorectal resection did not seem to increase the liver-specific morbidity in comparison to the rates reported by expert teams performing isolated LLR [14]. In the 12 % of patients who underwent left or right hepatectomy there was no association between major resection and adverse postoperative course as observed in our multivariate analysis. However,
World J Surg Table 6 Recent (last 10 years) series of laparoscopic primary colorectal tumor resection with simultaneous open liver resection and large (n [ 100) series of open liver resection with simultaneous colorectal surgery for synchronous colorectal liver metastases Surgical procedure
Authors
Laparoscopic primary colorectal tumor resection with simultaneous open liver resection
Hatwell[47]
44
55
Akiyoshi[58]
10
10
Bretagnol[59] Lin[60]
10 154
Open liver resection with simultaneous colorectal surgery
n
Morbidity (%)
40 29.9
5-year overall survival (%) – – 46
Yoshioka[61]
127
61.5
64
Mayo[62]
329
19
42
Luo[63]
129
47.3
–
de Santiban˜es[64]
185
20.5
36.1
Reddy[65]
135
36.3
–
Capussoti[66]
172
35.7
Minagawa[67]
187
–
blood loss and transfusion rates were found to be risk factors for postoperative complications as previously reported [24]. Multivariate analysis showed that ASA score CIII and global operative time were the two independent factors of adverse postoperative outcomes. Thus, laparoscopic synchronous procedures that are expected to take a long time should be considered for primary open resection or early conversion. Indeed, expected operative time should be assessed before and during surgery, especially when dealing with patients presenting significant preoperative disease state. Starting with the theoretically more difficult part of the procedure might also be an option in order to potentially switch from a synchronous strategy to a two-step procedure. In this series, most surgical teams started with the colorectal procedure since liver resections were mostly performed for single unilobar lesion, with a size inferior to 5 cm, requiring a typical or left lateral sectionectomy. Furthermore, 60 % of patients who underwent major hepatectomy combined with colorectal resection had liver surgery first. Perioperative complications influence recurrence and survival after resection of CRC [50] and colorectal liver metastases [51]. Indeed, enhanced recovery and reduced postoperative complications after laparoscopic surgery may facilitate the early use of adjuvant therapy, which may also improve outcomes for cancer patients [52]. In our series, overall and disease-free survival were similar to survivals reported in large series of patients that underwent open synchronous resections [53]. The 5-year overall survival (72 %) was even particularly good compared to previous large series of open simultaneous resections (Table 6). This result is probably related to the important selection of those patients for the laparoscopic approach and to the fact that the majority of them had a solitary liver metastasis.
30.8 35
However, it shows that in selected patients, survival is not impaired by the laparoscopic approach. Besides, the liver resection margin was positive in 7 % of our patients which is similar to positive margin rates that were previously reported in the literature during LLR [14] or open resections [54]. Schiffman et al. [55] recently demonstrated in a large meta-analysis that in carefully selected patients with limited liver metastases (1 or 2 lesions), LLR provides perioperative benefits without compromising oncologic outcomes. One-third of patients with SCRLM at the time of diagnosis will develop metachronous liver metastases after liver resection and may be candidates to second liver resection [53]. Since the minimally invasive surgery is associated with decreased adhesions [56] this may facilitate a second laparoscopic procedure. Indeed, as previously reported [57], intra-abdominal adhesions after primary laparoscopic surgery are minor and located at wounds used for port sites and for specimen removal, and at liver resection surface. In our multicenter study, in the 13 patients (9.1 %) which required second liver resection due to tumor recurrence, seven of them underwent LLR re-resection. Our study has several limitations. First of all, this is a non-comparative study. Indeed, no sufficient data concerning open synchronous resections were available in those centers to perform this analysis. Furthermore, percentages of synchronous resections performed by laparoscopy varied widely, depending mostly upon the different types of surgical activity and recruitment of each centers. Two types of activities were recognized: hepatic surgery centers performing laparoscopic synchronous resections selectively (1–5 %) and centers known for miniinvasive surgery performing most synchronous resections by laparoscopy (20–60 %). Thus, a variable but generally strict selection of patients is required to perform
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laparoscopic synchronous resections, which explains the necessity to combine several institutions’ data to obtain this series. Indeed, the contribution of each institution to this series reaches an average of approximately one patient per year and per institution. One could argue that our data are rather a combination of multiple limited experiences rather than a real series. Finally, the majority of liver resections were minor procedures and only 12 % of the patients had hemihepatectomies. Therefore, our conclusions are essentially available is the setting of minor LLR and more important data are necessary to validate the safety of a combined laparoscopic strategy for major liver resections. To the best of our knowledge, this study is the largest report concerning laparoscopic synchronous resection of CRC and liver metastases. Our combined data show that in experienced centers, simultaneous laparoscopic approach is technically feasible, safe, and associated with good oncological outcomes. Acknowledgment The authors want to thank Dr Satoshi Ogiso, Dr Marco Colasanti, Dr Stefano Berti, and Dr Martin Gaillard for their assistance in the acquisition of data. All the authors agree with the submission. Conflicts of interest All authors have no conflicts of interest or financial ties to disclose. Disclosure
Nothing to disclose.
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49. van der Pas MH, Haglind E, Cuesta MA et al (2013) Laparoscopic versus open surgery for rectal cancer (COLOR II): shortterm outcomes of a randomised, phase 3 trial. Lancet Oncol 14:210–218 50. Kang SB, Park JS, Kim DW et al (2010) Intraoperative technical difficulty during laparoscopy-assisted surgery as a prognostic factor for colorectal cancer. Dis Colon Rectum 53:1400–1408 51. Correa-Gallego C, Gonen M, Fischer M et al (2013) Perioperative complications influence recurrence and survival after resection of hepatic colorectal metastases. Ann Surg Oncol 20:2477–2484 52. Krarup PM, Nordholm-Carstensen A, Jorgensen LN et al (2014) Anastomotic leak increases distant recurrence and long-term mortality after curative resection for colonic cancer: a nationwide cohort study. Ann Surg 259:930–938 53. Vigano L, Ferrero A, Amisano M et al (2013) Comparison of laparoscopic and open intraoperative ultrasonography for staging liver tumours. Br J Surg 100:535–542 54. Soubrane O, Goumard C, Laurent A et al (2013) Laparoscopic resection of hepatocellular carcinoma: a French survey in 351 patients. HPB (Oxford) 16:357–365 55. Schiffman SC, Kim KH, Tsung A et al (2014) Laparoscopic versus open liver resection for metastatic colorectal cancer: a metaanalysis of 610 patients. Surgery 157:211–222 56. Gutt CN, Oniu T, Schemmer P et al (2004) Fewer adhesions induced by laparoscopic surgery? Surg Endosc 18:898–906 57. Hu M, Zhao G, Xu D et al (2011) Laparoscopic repeat resection of recurrent hepatocellular carcinoma. World J Surg 35:648–655. doi:10.1007/s00268-010-0919-0 58. Akiyoshi T, Kuroyanagi H, Saiura A et al (2009) Simultaneous resection of colorectal cancer and synchronous liver metastases: initial experience of laparoscopy for colorectal cancer resection. Dig Surg 26:471–475 59. Bretagnol F, Hatwell C, Farges O et al (2008) Benefit of laparoscopy for rectal resection in patients operated simultaneously for synchronous liver metastases: preliminary experience. Surgery 144:436–441 60. Lin Q, Ye Q, Zhu D et al (2014) Determinants of long-term outcome in patients undergoing simultaneous resection of synchronous colorectal liver metastases. PloS One 9:e105747 61. Yoshioka R, Hasegawa K, Mise Y et al (2014) Evaluation of the safety and efficacy of simultaneous resection of primary colorectal cancer and synchronous colorectal liver metastases. Surgery 155:478–485 62. Mayo SC, Pulitano C, Marques H et al (2013) Surgical management of patients with synchronous colorectal liver metastasis: a multicenter international analysis. J Am Coll Surg 216:707–716 63. Luo Y, Wang L, Chen C et al (2010) Simultaneous liver and colorectal resections are safe for synchronous colorectal liver metastases. J Gastrointest Surg 14:1974–1980 64. de Santibanes E, Fernandez D, Vaccaro C et al (2010) Short-term and long-term outcomes after simultaneous resection of colorectal malignancies and synchronous liver metastases. World J Surg 34:2133–2140. doi:10.1007/s00268-010-0654-6 65. Reddy SK, Pawlik TM, Zorzi D et al (2007) Simultaneous resections of colorectal cancer and synchronous liver metastases: a multi-institutional analysis. Ann Surg Oncol 14:3481–3491 66. Capussotti L, Vigano L, Ferrero A et al (2007) Timing of resection of liver metastases synchronous to colorectal tumor: proposal of prognosis-based decisional model. Ann Surg Oncol 14:1143–1150 67. Minagawa M, Yamamoto J, Miwa S et al (2006) Selection criteria for simultaneous resection in patients with synchronous liver metastasis. Arch Surg 141:1006–1012
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ORIGINAL SCIENTIFIC REPORT
Laparoscopic Simultaneous Resection of Colorectal Primary Tumor and Liver Metastases: Results of a Multicenter International Study Stefano Ferretti1 • Hadrien Tranchart1 • Joseph F. Buell2 • Constantino Eretta3 Alberto Patriti4 • Marcello Giuseppe Spampinato5 • Jung Wook Huh6 • Luca Vigano7 • Ho Seong Han8 • Giuseppe Maria Ettorre9 • Elio Jovine10 • Thomas Clark Gamblin11 • Giulio Belli12 • Go Wakabayashi13 • Brice Gayet14 • Ibrahim Dagher1
•
Ó Socie´te´ Internationale de Chirurgie 2015
Abstract Background With the advance of modern laparoscopic technology, laparoscopic colorectal surgery and laparoscopic liver surgery are both worldwide accepted. Preliminary brief series have shown the feasibility of combined laparoscopic resection of colorectal cancer (CRC) and synchronous colorectal liver metastases (SCRLM). We aim to report a large International multicenter series of laparoscopic simultaneous resection of CRC and SCRLM. Methods Between 1997 and 2013, 142 laparoscopic liver resections were performed with simultaneous colorectal surgery for SCRLM. The surgical and postoperative variables evaluated were the duration of the intervention, blood loss, transfusion rate, conversion rate, resection margin, specific and overall morbidity, perioperative mortality, length of hospital stay, and survival. Univariate and multivariate analyses were performed examining postoperative morbidity in the all cohort of patients. Results The median number of liver lesions was 1 (1–9) and the median larger diameter at diagnosis was 28 (2–100) mm. The median operative time was 360 (120–690) min. Seven patients (4.9 %) required conversion. The global morbidity was 31.0 % and the mortality was 2.1 %. After a median follow-up of 29 (1–108) months, 40 patients (28.2 %) developed tumor recurrence. Curative treatment of recurrence was possible in 17 patients (12.0 %), including a second liver resection in 13 patients (9.1 %), which was performed by laparoscopy in 7 patients (4.9 %). Overall 1-, 3-, and 5-year survivals were 98.8, 82.1, and 71.9 %, respectively. By multivariate analysis, ASA score C3 [OR 13.6 (1.8–99.6); P = 0.01] and operative time [OR 1.008 (1.001–1.016); P = 0.03] were independent predictors of postoperative morbidity. Conclusions Our combined data show that in experienced centers, simultaneous laparoscopic approach is technically feasible, safe, and associated with good oncological outcomes.
Stefano Ferretti and Hadrien Tranchart have contributed equally to this work. & Hadrien Tranchart [email protected] 1
Department of Minimally Invasive Digestive Surgery, Antoine Be´cle`re Hospital, AP-HP, Paris-Sud University, 157 rue de la Porte de Trivaux, 92141 Clamart, France
2
Department of Surgery, Tulane Abdominal Transplant Institute, New Orleans 70112, USA
3
Division of General Surgery, Sant’Andrea Hospital, 19100 La Spezia, Italy
4
Division of General Minimally Invasive and Robotic Surgery, San Matteo degli Infermi Hospital, 06049 Perugia, Italy
5
HPB and Advanced Laparoscopic Surgical Unit, Policlinico of Abano Terme, 35031 Abano Terme, Italy
6
Department of Surgery, Chonnam National University Hwasun Hospital and Medical School, Seoul 135-710, South Korea
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World J Surg
Introduction Colorectal cancer (CRC) is one of the most common causes of cancer death in the Western world with more than 940,000 new cases annually and nearly 500,000 deaths each year worldwide [1]. Up to 50 % of patients with CRC might have liver metastases during the course of the disease, and 15–20 % have synchronous colorectal liver metastases (SCRLM) at the time of diagnosis, whereas an additional 20–25 % develop metachronous hepatic tumors [2, 3]. The presence of liver metastases has an important influence on patient prognosis, and the median survival is 2–21 months for patients in whom the cancer is non-resected [4–6]. Furthermore, liver resection has been accepted as the only treatment offering the chance for cure and long-term survival, with 5-year survival rates of 25–60 % and 10-year survival rates of 22–26 %, respectively reported in the literature [7–15]. During the past decade, most studies have recommended a staged operation with initial resection of the colorectal primary cancer followed by hepatic resection of the SCRLM 2–6 months later [16, 17]. However, the optimal strategy for the management of SCRLM remains controversial including primary resection first followed by liver [18], liver resection first followed by primary resection [19], or simultaneous resection. Several reports, including a recent meta-analysis, have shown the benefit of a simultaneous open resection of primary tumor and SCRLM compared with a staged approach [20–23]. Simultaneous resection did not increase mortality or morbidity rates compared with delayed resection. Moreover, the combination of major hepatectomy and colorectal tumor resection was not associated with increased morbidity [23, 24]. With the advance of modern laparoscopic technology, laparoscopic colorectal surgery and laparoscopic liver surgery are both accepted worldwide. Laparoscopic colorectal resection for cancer has been shown to be safe and oncologically equivalent to conventional surgery [25–28]. Moreover, it reduces hospital stay, shortens recovery times and reduces postoperative complications [29–32]. On the other hand, laparoscopic liver surgery is now recognized as
7
8
9
safe, and showed some improvement in postoperative outcomes compared with open resection [33, 34]. Furthermore, several series have shown that the margin after LLR of colorectal liver metastases as well as oncological outcomes were equivalent compared with open resection [35–38]. Preliminary brief series have shown the feasibility of combined laparoscopic resection of both CRC and SCRLM [37, 39–41]. We report a large International multicenter retrospective series of laparoscopic simultaneous resection of colorectal primary tumor and liver metastases. Univarite and multivariate analyses were performed examining postoperative morbidity in all cohort of patients.
Methods Patient demographics Between 1997 and 2013, 142 LLR were performed with simultaneous colorectal surgery for SCRLM. All centers involved in this study have more than 4 years of experience in the laparoscopic liver surgery field: seven from Italy, two from France, two from USA, two from Korea, and one from Japan. There were 66 male (46.5 %) and 76 women (53.5) with a median age of 66 (32–85) years. Characteristics of patients are summarized in Table 1. In the 14 centers, patients with solitary lesions of 5 cm or less, located in liver segments II to VI were considered as more suitable to laparoscopic liver resection (LLR) [33]. Exclusion criteria were tumors close to the portal pedicle or hepatic veins, an American Society of Anesthesiologists score (ASA) exceeding III, a decompensated cirrhosis, esophageal varices grade [1, and a platelet count \80 9 109/L. However, those criteria were not exclusive in all centers and evolved with time and experience. Operative and perioperative management Twenty-five patients (17.6 %) had neoadjuvant chemotherapy including 5 patients (3.5 %) that had radiotherapy for a
Department of HPB and Digestive Surgery, Ospedale Mauriziano Umberto I, 10100 Turin, Italy
12
Division of General Surgery, S. Maria di Loreto Nuevo Hospital, 80142 Naples, Italy
Department of Surgery, Seoul National University Bundang Hospital, Seoul, 135-710, South Korea
13
Department of Surgery, Iwate Medical University School of Medicine, Morioka 020-8505, Japan
General Surgery and Liver Transplantation Unit, San Camillo Forlanini Hospital, 00152 Rome, Italy
14
Department of Digestive Diseases, Institut Mutualiste Montsouris, 75014 Paris, France
10
Department of Surgery, Maggiore Hospital, 40133 Bologna, Italy
11
Division of Surgical Oncology, Medical College of Wisconsin, Milwaukee 53226, USA
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World J Surg Table 1 Demographics and liver and colorectal characteristics of patients undergoing laparoscopic liver resection with simultaneous colorectal surgery for synchronous colorectal liver metastases
Table 2 Types of resection for patients undergoing laparoscopic liver resection with simultaneous colorectal surgery for synchronous colorectal liver metastases
Variable
Variable
Data
Totally laparoscopic, n (%)
127 (89.4)
Data
Patients Gender (female/male)
76/66
Hand-assisted, n (%)
15 (10.6)
Age (years), median (range) BMI (kg/m2), median (range)
66 (32–85) 24.3 (18.3–38)
Colorectal resection Rectal resection, n (%)
58 (40.8)
ASA I, n (%)
37 (26.0)
Stoma covering low anastomosis, n (%)
ASA II, n (%)
57 (40.1)
Abdominoperineal resection, n (%)
ASA III, n (%)
45 (31.7)
ASA IV, n (%)
3 (2.1)
Colorectal tumor
10 (7.0) 3 (2.1)
Liver resection A typical resection, n (%)
103 (72.5)
Left lateral sectionectomy, n (%)
22 (15.5) 13 (9.2)
Rectal tumor
58 (40.8)
Right hepatectomy, n (%)
Right colon
38 (26.8)
Left hepatectomy, n (%)
Left colon
46 (32.4)
Pringle’s maneuver, n (%)
4 (2.8) 17 (12.0)
Liver metastases Number of lesions, median (range)
1 (1–9)
Number of lesions [2/[3, n (%)
35 (24.6)/22 (15.5)
Bilobar, n (%)
28 (19.7)
Larger diameter at diagnosis (mm), median (range)
28 (2–100)
CEA at diagnosis (ng/mL), median (range)
36 (0.8–315)
BMI body mass index, ASA American society of anesthesiologists physical status score, CEA carcinoembryonic antigen
were specific and overall morbidity, perioperative mortality, length of hospital stay, and survival. Mortality and morbidity were defined as death or complications occurring within 30 days after surgery. Complication severity was stratified according to the modified Clavien classification [42]. Statistical analysis
rectal cancer. The first operating procedures was the LLR in 33 patients (23.2 %) and the colorectal resection in 109 patients (76.8 %). Both colorectal and liver resections were performed by the same team in 87 patients (61.3 %). Four centers systematically used two different surgical teams. Six patients (4.2 %) underwent a rectal resection combined with a major liver resection. Eleven centers performed only pure laparoscopic liver and colonic resection and the other three centers performed 15 (10.6 %) hand-assisted LLR procedures. Pringle’s maneuver was never used systematically in any center but in case of bleeding. Liver transection was performed with thermofusion in four centers, with ultrasound section in six centers, and with an ultrasonic surgical aspirator in four centers. Hepatic veins were divided using a linear stapler. The resected liver specimen was extracted in a plastic bag, without fragmentation, along a suprapubic or a right transverse incision that was used to extract the colorectal specimen. The types of resection performed are detailed in Table 2. Study criteria The surgical variables evaluated were the duration of the intervention, blood loss, transfusion rate, conversion rate, and resection margin. The postoperative variables assessed
Statistical analyses were carried out with SPSS software (IBM Company, Los Angeles, CA). Continuous variables were expressed as median (range) and were compared using the student t test or the Mann–Whitney U tests, as appropriate. v2 test or Fisher’s exact test were used for comparisons of categorical variables, as appropriate. Values of P \ 0.05 were considered statistically significant. To test the independence of the risks factors, the significant pre- and intraoperative variables in the univariate analyses were entered into a multivariate logistic regression model with likelihood ratio forward selection. Disease-free and overall survival rates were calculated using the Kaplan–Meier method.
Results Intraoperative results The median operative time was 360 (120–690) min and the LLR was significantly shorter than the colorectal resection (P = 0.04). Seven patients (4.9 %) required conversion due to: an uncertain liver margin (n = 2), a right ureteral injury (n = 1), an hemorrhage during LLR (n = 1),
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adhesions (n = 1), difficult progression (n = 1), or an intraoperative discovery of carcinomatosis (n = 1). The procedure was successfully completed by open approach in those seven cases of conversion. Surgical and histological results are detailed in Table 3.
Table 4 Postoperative results for patients undergoing laparoscopic liver resection with simultaneous colorectal surgery for synchronous colorectal liver metastases Variable
Data
Mortality, n (%)
3 (2.1)
Specific morbidity, n (%)
Postoperative results The global morbidity rate was 31.0 % and the specific liver and colorectal morbidities did not differ significantly (P = 1.00). Eight patients (5.6 %) presented an anastomotic leakage. Seven of those patients required reoperation for creation of a covering ostomy and/or drainage. One patient was treated by prolonged drainage without reoperation. Six patients (4.2 %) presented a biliary collection and were treated by percutaneous drainage. Three patients (2.1 %) presented an hemorrhage after LLR and required reoperation. Three patients died: one patient after a postoperative hemorrhage which required reoperation, one patient presented multiple organ failure and one patient died of acute coronary syndrome. Postoperative results are detailed in Table 4. Oncological results After a median follow-up of 29 (1–108) months, 40 patients (28.2 %) developed tumor recurrence; 16 patients (11.3 %) had exclusive liver recurrence and two patients Table 3 Surgical and histological results for patients undergoing laparoscopic liver resection with simultaneous colorectal surgery for synchronous colorectal liver metastases
Colorectal morbidity, n (%) Leakage, n Abdominal abscess, n
1
Segmental ischemic colitis, n
1
Prolonged ileus, n
1
Liver morbidity, n (%) Ascites, n
Data
Colorectal operative time (min), median (range)
156 (80–405)
Liver operative time (min), median (range)
120 (15–600)
Blood loss (mL), median (range)
200 (0–1800)
Transfusion, n (%)
12 (8.5)
Packed red blood cell units, median (range) Conversion to laparotomy, n (%)
3 (1–6) 7 (4.9)
Colorectal tumor characteristics T1, n (%)
8 (5.6)
T2, n (%)
22 (15.5)
T3, n (%) T4, n (%)
87 (61.3) 25 (17.6)
Tumor well/moderately/poorly/un/ differentiated, n (%) N?, n (%) Positive liver metastasis surgical margin (%)
123
24 (16.9)/84 (59.1)/22 (15.5)/12 (8.5) 88 (62.0) 10 (7.0)
11 (7.7) 1
Liver failure, n
1
Biliary collection, n
6
Hemorrhage, n General morbidity, n (%)
3 22 (15.5)
Heart failure, n
1
Pulmonary, n
7
Incisional abscess, n
3
Acute renal failure, n
1
Distal deep vein thrombosis, n Urinary tract infection, n
1 2
Pancreatitis, n
1
Cholangitis due to bile duct stone, n
1
Multi organ failure, n
1
Acute coronary syndrome, n
2
Central venous catheter infection, n
1
Unexplained fever, n
1
Clavien classification Grades I, II, IIIa, IIIb, IVa, IVb, V
Variable
22 (15.5) 11 (7.7) 8
Reoperation, n (%)
2/14/9/11/5/0/3 11 (7.7)
First oral intake of solid food (d), median (range)
3 (1–20)
Intensive care unit stay (d), median (range)
1 (1–16)
Hospital stay (d), median (range)
8 (3–84)
(1.4 %) had anastomotic recurrence. The median delay between surgery and recurrence was 12 (1–78) months. Curative treatment of recurrence was possible in 17 patients (12.0 %), including a second liver resection in 13 patients (9.1 %) which was performed by laparoscopy in 7 patients (4.9 %). During the study period, six patients (4.2 %) displayed peritoneal carcinomatosis and none had port-site recurrence. Twenty-seven patients (19.0 %) died during the study period, including three patients who died during the postoperative period. Overall 1-, 3-, and 5-year survivals were 98.8, 82.1, and 71.9 %, respectively. Disease-free 1-, 3-, and 5-year survivals were 85.6, 65.9, and 63.0 %, respectively (Fig. 1).
World J Surg
Fig. 1 Overall (continuous line) and disease-free (dotted line) survival curves
Uni- and multi-variate analyses of postoperative complications No factors were found to be predictors of postoperative specific colorectal or liver postoperative morbidity in univariate analysis. Seven factors were found to be risk factors for postoperative complications: ASA score CIII (P = 0.007), BMI (P = 0.04), global operative time (P = 0.01), blood loss (P = 0.01), transfusion (P \ 0.0001), Pringle’s maneuver (P = 0.04), and length of stay (P \ 0.0001). By multivariate analysis, ASA score CIII [OR 13.6 (1.8–99.6); P = 0.01] and global operative time [OR 1.008 (1.001–1.016); P = 0.03] were independent predictors of postoperative morbidity (Table 5).
Discussion Technical refinements and anesthesia progress have enabled surgical groups to perform laparoscopic synchronous colorectal and liver resection. However, concerns persist regarding the safety and the oncological equivalence of minimally invasive approach for one-stage resection compared to open surgery. We report in this series a multicenter study concerning laparoscopic approach for the synchronous management of liver metastases and CRC in selected patients.
Simultaneous resection of liver and colon or rectum for patients with SCRLM was initially associated with a perceived increased risk of complications and mortality [16, 17, 43]. Authors reluctant to the combined approach argue that the association of a clean surgical procedure with one likely to cause contamination may result in higher morbidity rates [44]. Furthermore, the risk of intestinal edema after pedicle clamping [44, 45] and vulnerability to infection due to postoperative impaired liver function could be associated with an increased risk of anastomotic leakage [44]. However, in high-volume centers with appropriate experience in both liver and colorectal resection, simultaneous surgery has been shown to be safe and efficient [46]. Repeated surgery is often required for patients with colorectal liver metastases, making the laparoscopic approach particularly beneficial for those patients. Some teams initially have performed the colorectal resection by laparoscopy with a concomitant open liver resection [47]. Most experienced centers in LLR have initiated laparoscopic combined resection for minor [14] and major liver resection [48]. However, only few limited single center series are available in the literature, which led us to conduct this multicenter study associating 14 experienced centers in both liver and colorectal laparoscopic surgery. The main finding of this series was that global morbidity (31 %) and mortality (2 %) were comparable to rates reported by experienced teams performing open synchronous resection [23] or colorectal laparoscopic resection followed
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World J Surg Table 5 Uni- and multi-variate analyses of postoperative complications for patients undergoing laparoscopic liver resection with simultaneous colorectal surgery for synchronous colorectal liver metastases Variable
Postoperative complication, n (%)
UV P
MV P
Table 5 continued Variable
0.20
Male
24 (16.9)
Female
20 (14.1)
Agea a
BMI ASA score
–
0.48
–
–
–
0.04 0.007
NS 0.01
– 13.6 (1.8–99.6)
18 (12.6)
III–IV
26 (18.3)
11 (7.8)
No
33 (23.2)
Radiotherapy
0.30
Yes
1 (0.7)
No
43 (30.2)
Colorectal tumor 26 (18.3)
Rectum
18 (12.7)
Yes
9 (6.4)
No
35 (24.7)
Blood lossa
–
–
–
–
–
Yes
10 (7.0)
No
34 (23.9)
Conversion to laparotomy
–
MV P
OR (95 % CI)
0.04
NS
–
0.01
0.03
1.008 (1.001–1.016)
0.01
NS
–
\0.0001
NS
–
–
NS
–
–
0.49
Yes
3 (2.1)
No
41 (28.9)
Hospital staya 0.92
Colon
39 (27.5)
Transfusion
0.29
Yes
5 (3.5)
No
Global operative timea
Preoperative management Chemotherapy
Yes Pringle’s maneuver
–
–
I–II
UV P
OR (95 % CI)
Patients Gender
Postoperative complication, n (%)
–
\0.0001
UV univariate analysis, MV multivariate analysis, OR odd ratio, CI confidence interval, NS not significant, BMI body mass index, ASA American society of anesthesiologists physical status score a
Continuous variable
Liver metastases Number of lesionsa
–
Bilobar Yes
9 (6.3)
No
35 (24.7)
Larger diameter at diagnosisa
–
0.11
–
–
0.74
–
–
0.95
–
–
0.56
–
–
0.31
–
–
0.92
–
–
0.88
–
–
Surgery Colorectal and liver procedures performed by different teams Yes
14 (9.8)
No
30 (21.1)
Hand-assisted Yes
3 (2.1)
No
41 (28.9)
Rectal resection Yes
26 (18.3)
No
18 (12.7)
Major liver resection
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by open hepatectomy [47] (Table 6). Furthermore, the anastomotic leakage rate (5.6 %) was not increased by the association of LLR in comparison to the rates reported by experienced teams performing isolated laparoscopic colorectal resection [31, 49] and despite an important rate of rectal procedures (40.8 %). Indeed, the Pringle’s maneuver was described as a risk factor for postoperative anastomotic leakage [44, 45]. In our series, clamping was never used in any center on purpose but just in the cases of uncontrolled bleeding (12 %).This may have contributed to this rate of postoperative fistula. However, the majority of patients in this study underwent the colorectal resection as the first operating procedure and an intention-to-treat analysis was not possible with our data. Data concerning patients in whom the preoperative synchronous strategy was not finally performed due to a difficult first-step procedure were not available. In combined resections, the liver-specific morbidity was 7.7 %. Indeed, the association of laparoscopic colorectal resection did not seem to increase the liver-specific morbidity in comparison to the rates reported by expert teams performing isolated LLR [14]. In the 12 % of patients who underwent left or right hepatectomy there was no association between major resection and adverse postoperative course as observed in our multivariate analysis. However,
World J Surg Table 6 Recent (last 10 years) series of laparoscopic primary colorectal tumor resection with simultaneous open liver resection and large (n [ 100) series of open liver resection with simultaneous colorectal surgery for synchronous colorectal liver metastases Surgical procedure
Authors
Laparoscopic primary colorectal tumor resection with simultaneous open liver resection
Hatwell[47]
44
55
Akiyoshi[58]
10
10
Bretagnol[59] Lin[60]
10 154
Open liver resection with simultaneous colorectal surgery
n
Morbidity (%)
40 29.9
5-year overall survival (%) – – 46
Yoshioka[61]
127
61.5
64
Mayo[62]
329
19
42
Luo[63]
129
47.3
–
de Santiban˜es[64]
185
20.5
36.1
Reddy[65]
135
36.3
–
Capussoti[66]
172
35.7
Minagawa[67]
187
–
blood loss and transfusion rates were found to be risk factors for postoperative complications as previously reported [24]. Multivariate analysis showed that ASA score CIII and global operative time were the two independent factors of adverse postoperative outcomes. Thus, laparoscopic synchronous procedures that are expected to take a long time should be considered for primary open resection or early conversion. Indeed, expected operative time should be assessed before and during surgery, especially when dealing with patients presenting significant preoperative disease state. Starting with the theoretically more difficult part of the procedure might also be an option in order to potentially switch from a synchronous strategy to a two-step procedure. In this series, most surgical teams started with the colorectal procedure since liver resections were mostly performed for single unilobar lesion, with a size inferior to 5 cm, requiring a typical or left lateral sectionectomy. Furthermore, 60 % of patients who underwent major hepatectomy combined with colorectal resection had liver surgery first. Perioperative complications influence recurrence and survival after resection of CRC [50] and colorectal liver metastases [51]. Indeed, enhanced recovery and reduced postoperative complications after laparoscopic surgery may facilitate the early use of adjuvant therapy, which may also improve outcomes for cancer patients [52]. In our series, overall and disease-free survival were similar to survivals reported in large series of patients that underwent open synchronous resections [53]. The 5-year overall survival (72 %) was even particularly good compared to previous large series of open simultaneous resections (Table 6). This result is probably related to the important selection of those patients for the laparoscopic approach and to the fact that the majority of them had a solitary liver metastasis.
30.8 35
However, it shows that in selected patients, survival is not impaired by the laparoscopic approach. Besides, the liver resection margin was positive in 7 % of our patients which is similar to positive margin rates that were previously reported in the literature during LLR [14] or open resections [54]. Schiffman et al. [55] recently demonstrated in a large meta-analysis that in carefully selected patients with limited liver metastases (1 or 2 lesions), LLR provides perioperative benefits without compromising oncologic outcomes. One-third of patients with SCRLM at the time of diagnosis will develop metachronous liver metastases after liver resection and may be candidates to second liver resection [53]. Since the minimally invasive surgery is associated with decreased adhesions [56] this may facilitate a second laparoscopic procedure. Indeed, as previously reported [57], intra-abdominal adhesions after primary laparoscopic surgery are minor and located at wounds used for port sites and for specimen removal, and at liver resection surface. In our multicenter study, in the 13 patients (9.1 %) which required second liver resection due to tumor recurrence, seven of them underwent LLR re-resection. Our study has several limitations. First of all, this is a non-comparative study. Indeed, no sufficient data concerning open synchronous resections were available in those centers to perform this analysis. Furthermore, percentages of synchronous resections performed by laparoscopy varied widely, depending mostly upon the different types of surgical activity and recruitment of each centers. Two types of activities were recognized: hepatic surgery centers performing laparoscopic synchronous resections selectively (1–5 %) and centers known for miniinvasive surgery performing most synchronous resections by laparoscopy (20–60 %). Thus, a variable but generally strict selection of patients is required to perform
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laparoscopic synchronous resections, which explains the necessity to combine several institutions’ data to obtain this series. Indeed, the contribution of each institution to this series reaches an average of approximately one patient per year and per institution. One could argue that our data are rather a combination of multiple limited experiences rather than a real series. Finally, the majority of liver resections were minor procedures and only 12 % of the patients had hemihepatectomies. Therefore, our conclusions are essentially available is the setting of minor LLR and more important data are necessary to validate the safety of a combined laparoscopic strategy for major liver resections. To the best of our knowledge, this study is the largest report concerning laparoscopic synchronous resection of CRC and liver metastases. Our combined data show that in experienced centers, simultaneous laparoscopic approach is technically feasible, safe, and associated with good oncological outcomes. Acknowledgment The authors want to thank Dr Satoshi Ogiso, Dr Marco Colasanti, Dr Stefano Berti, and Dr Martin Gaillard for their assistance in the acquisition of data. All the authors agree with the submission. Conflicts of interest All authors have no conflicts of interest or financial ties to disclose. Disclosure
Nothing to disclose.
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