Current literature reports significant efficacy of repeat hepatectomies in the treatment of recurrent malignant diseases (both primary and secondary) of the liver.[
We previously published data on laparoscopic re-interventions for hepatocellular carcinoma (HCC) in cirrhotic liver that described peri-operative outcomes, safety, and feasibility of this procedure.[
From January 2004 to December 2013, 24 patients underwent a laparoscopic re-intervention (hepatic resection and radiofrequency ablation [RFA]) for recurrent HCC in cirrhosis (
The inclusion criteria for the laparoscopic re-intervention were: A well-compensated chronic liver disease (Child-Pugh Class A) without signs of severe portal hypertension in cirrhotic patients, a performance status of Karnosky ≥ 70, an American Society of Anesthesiology status ≤ 3, either a single HCC (≤ 5 cm) or 1 or more metastases when located in the anterior hepatic segments (segments II, III, IVb, V and VI), or a small (3 cm) deep HCC for laparoscopic RFA in which major hepatectomy is not recommended. No tumor was biopsied pre-operatively.
The patients were divided into two groups according to the first surgical approach
Features of hepatic procedures
Patients | First approach | First procedure | Recurrence site | Second approach | Redo procedure for recurrence | Operative time for second procedure (min) | Type of lesion (number) | Size (mm) |
---|---|---|---|---|---|---|---|---|
1 | OR | Subsegmentectomy | II | LR | Left lateral sectionectomy | 115 | HCC (1) | 40 |
2 | OR | Segmentectomy | III | LR | Left lateral sectionectomy | 100 | HCC (1) | 38 |
3 | OR | Segmentectomy | IV | LR | Subsegmentectomy (converted to laparotomy) | 120 | HCC (1) | 38 |
4 | OR | Segmentectomy | IV | LR | Subsegmentectomy | 130 | HCC (1) | 40 |
5 | OR | Subsegmentectomy | VIII | L-RFA | L-RFA | 120 | HCC (1) | 28 |
6 | LR | Left lateral sectionectomy | VII-VIII | L-RFA | L-RFA | 100 | HCC (1) | 33 |
7 | LR | Subsegmentectomy | II | LR | Left lateral sectionectomy | 60 | HCC (1) | 48 |
8 | LR | Segmentectomy | IV | LR | Subsegmentectomy | 80 | HCC (1) | 30 exophityc |
9 | LR | Subsegmentectomy | IV | LR | Subsegmentectomy | 60 | HCC (1) | 48 exophityc |
10 | LR | Subsegmentectomy | V | LR | Segmentectomy | 50 | HCC (1) | 40 |
11 | LR | Subsegmentectomy | VIII | L-RFA | L-RFA | 80 | HCC (1) | 35 |
12 | LR | Segmentectomy | VI | LR | Segmentectomy | 40 | HCC (1) | 38 |
13 | LR | Segmentectomy | II | LR | Left lateral sectionectomy | 80 | HCC (1) | 45 |
14 | LR | Subsegmentectomy | II-III | LR | Left lateral sectionectomy | 65 | HCC (1) | 38 |
15 | LR | Subsegmentectomy | V | LR | Segmentectomy | 60 | HCC (1) | 45 |
16 | LR | Segmentectomy + L-RFA | VII | L-RFA | L-RFA | 50 | HCC (1) | 28 |
17 | LR | Left lateral sectionectomy | II | LR | Segmentectomy | 50 | HCC (1) | 35 |
18 | LR | WR | IV | LR | WR | 60 | MTX (1) | 28 |
19 | LR | WR | III, VI | LR | WR | 100 | MTX (3) | 10, 23, 25 |
20 | LR | WR | VI, V | LR | WR | 80 | MTX (3) | 17, 20, 27 |
21 | OR | WR | II, V, VI | LR | WR | 120 | MTX (3) | 10, 28, 25 |
22 | OR | Left hemicolectomy + cholecystectomy + left lateral sectionectomy | IV-V | LR | BisegmentectomyThird procedure: WR | 220 | MTX (1) | 76 |
23 | LR | Left hemicolectomy + WR | II, III, IV | LR | Left lateral sectionectomy + WR Third procedure: WR | 240 | MTX (4) | 28, 35, 30, 38 |
24 | LR | WR | VI | LR | WR | 120 | MTX (1) | 22 |
OR: open resection; LR: laparoscopic resection; WR: wedge resection; MIX: metastases; HCC: hepatocellular carcinoma; L-RFA: laparoscopic radiofrequency ablation
Perioperative results
Group 1 (%) | Group 2 (%) |
|
S/NS | |
---|---|---|---|---|
Extensive adhesions (grade 3-4) | 5 (71.4) | 2 (11.7) | 0.01 | S |
Operative time, min (mean ± SD) | 220.14 ± 80.06 | 150 ± 56.18 | 0.03 | S |
Blood loss, mL (mean ± SD) | 297 ± 134 | 272.2 ± 120 | 1.0 | NS |
Morbidity | 5 (29.4) | 2 (28.5) | 1.0 | NS |
Grade I atelectasis | 1 | 1 | - | - |
Grade I ascites | 1 | 0 | - | - |
Grade II pneumonia | 2 | 0 | - | - |
Grade II bleeding | 1 | 0 | - | - |
Grade IIIa perforation | 0 | 1 | - | - |
Mortality | Nil | Nil | - | - |
Conversion | 1 | 0 | - | - |
S/NS: significant/nonsignificant; SD: standard deviation
Classification of adhesions
Grade | Description of adhesions |
---|---|
0 | None |
1 | Thin film, divided by blunt dissection |
2 | Thin vascular, easily divided by sharp dissection |
3 | Extensive thick vascular, requires division by sharp dissection |
4 | Dense, bowel at risk of injury with division |
The surgical technique for the repeat laparoscopic hepatic resection was described elsewhere.[
During the exploratory laparoscopy, parietal and visceral adhesions were dissected. Such adhesions had to be dissected carefully with the use of specific surgical devices without causing any damage to the gastrointestinal tract before obtaining surgical access to the liver. In this phase, the pneumoperitoneum allowed adhesions to become strained to allow more meticulous assessment and lysis of adherences. The Pringle maneuver was prepared for all patients but was performed only in selected cases (8/24).
Anatomical resections (segmentectomy, subsegmentctomy of IVb, bisegmentectomy, and left lateral sectionectomy) were performed for treatment of HCC, and WR was performed for liver metastases.
After an extensive adhesiolysis has been performed, staging abdominal laparoscopy and laparoscopic ultrasonography were carried out to confirm the extension of the lesions and their relationships to the vasculature, to visualize their margins inside the parenchyma, and to exclude a widespread peritoneal carcinosis that might hinder the procedure. Laparoscopic transections were performed with a harmonic scalpel (Harmonic Ace Shears®; Ethicon, Endo-Surgery, Cincinnati, OH, USA) or with a vessel sealer (Enseal Tissue Sealer®; Ethicon, Endo-Surgery, Cincinnati, OH, USA) or (Ligasure™; Covidien, Mansfield, MA, USA), and was performed with reduced bleeding, due to a reduction of portal inflow of up to 30% because of the pneumoperitoneum. The resection bed surfaces were treated with a biologic fibrin glue (Tissucol; Baxter, Wien, Österreich), or a hemostatic gel (Floseal; Baxter, Wien, Österreich), or a sealant patch (TachoSil®; Takeda, Linz, Österreich) to minimize risk of biliary leak and to ensure hemostasis.
Bipolar electrocoagulation was used for minor bleeding, and larger structures were secured with ties or either multiple absorbable or nonabsorbable clips.
In order to facilitate the maneuver of left lateral sectionectomy, the left hepatic vein was stapled, and the device was introduced through the trocar located on the right of the patient, and then angled toward the left.
A three-trocar configuration was routinely used. A 12-mm port at the umbilicus housed the 30° laparoscope. After an extensive adhesiolysis has been performed, staging abdominal laparoscopy and laparoscopic ultrasonography were carried out to identify the positions of the lesions.
As previously described,[
After track ablation, hemostasis of the liver surface was ensured by bipolar electrocoagulation.
Repeat laparoscopic hepatic procedures were performed in 24 patients: 6 were treated by left lateral sectionectomy (1 associated with a WR), 4 by segmentectomy, 4 by subsegmentectomy (1 had conversion to laparotomy), 1 by bysegmentectomy associated with a WR, 4 by laparoscopic RFA of HCC, and 5 by WR. Two patients were subjected to a third repeat procedure consisting of laparoscopic WR of segment II and VI, respectively, for a second recurrence of liver metastases.
The laparoscopic procedure was successfully completed in 23 cases (95.9%). Adhesions were graded by the staff surgeons using the scale presented in Table 3, similar to that used in a multi-center study on adhesion prevention.[
Of the 24 patients, one underwent conversion to laparotomy in Group 1, not because of adhesions but due to inadequate control of the resection margin for a HCC located in segment IV. One patient, receiving a laparoscopic RFA of a HCC of 28 mm in VII segment after primary intervention of segmentectomy associated with laparoscopic RFA, was subjected to intestinal resection associated with ileostomy to treat peritonitis from intestinal perforation that occurred during laparoscopic RFA.
The mean operative time for re-intervention was significantly longer for Group 1 (220.14 ± 80.06 min) than for Group 2 (150 ± 56.18 min;
The overall post-operative morbidity and mortality rates were 29.1% (7/24) and 0%, respectively. According to Dindo-Clavien classification,[
Long-term outcomes in terms of hepatic recurrence have not yet been evaluated.
Recurrence rate for liver malignancy is estimated at 77-100% for HCC[
Retrospective studies about laparoscopic repeat surgery of the liver
Year | Author | Number | Tumor |
---|---|---|---|
2009 | Belli |
12 cases | HCC |
2009 | Liang |
1 case | HCC |
2010 | Cheung |
1 case | HCC |
2011 | Hu |
6 cases | HCC |
2011 | Shafaee |
76 cases | HCC + metastasis |
2011 | Nakahira |
15 cases | HCC + metastasis |
2012 | Tsuchiya |
16 cases | HCC |
2013 | Kanazawa |
40 cases | HCC |
2014 | Shelat |
19 cases | HCC + metastasis |
2015 | Cioffi |
24 cases | HCC + metastasis |
HCC: hepatocellular carcinoma
Tsuchiya
Indeed, the surgical strategy can be changed, and survival can be impaired because of the presence of concomitant peritoneal recurrence or because of extensive peritoneal adhesiolysis. Biopsies of suspicious lesions are mandatory to identify carcinomatous foci in dense adhesions to treat the extrahepatic recurrence if possible, or to abstain from a surgical procedure.
Shafaee
Kanazawa
Shelat
In previous papers that reported our experience in repeat surgery for HCC in cirrhotic liver, we highlighted that a minimally invasive approach applied during the first hepatectomy determines minimal post-operative adhesions and faster and safer adhesiolysis in terms of blood loss and risk of visceral injuries.[
In our study, patients with HCC on cirrhosis represent the most part of the cases. This is because patients with multiple lesions in recurrent liver metastases are less often selected for a multiple laparoscopic WR. The mean operative time for re-intervention was significantly longer for the group with previous OR, whereas the mean blood loss and the hospital stay were comparable in both groups. The resection margins were disease-free in all the patients.
A good training in laparoscopic adhesiolysis during minimally invasive incisional hernia repair even in cirrhotic patients can accelerate the learning curve in the lysis of hypervascularized adhesions, facilitated by laparoscopic pneumoperitoneum and optical magnification.[
The only case of severe complication in our study was in a patient previously treated with a LR followed by a laparoscopic RFA for a recurrent HCC. At the time of re-operation, he was affected by severe thrombocytopenia. The need to perform a safe hemostasis by electrocoagulation on the liver surface after extraction of the RFA probe from the hepatic parenchyma induced us to perform a RFA with the laparoscopic approach. During laparoscopy, the presence of a few thin adhesions (grade evaluated: 0-1) induced us to consider the visceral damage not as a specific complication of adhesiolysis
In conclusion, this study suggests that repeat laparoscopic surgery for recurrent hepatic malignant diseases in selected patients is a feasible and safe procedure with good short-term outcomes, but further prospective studies are needed to support these results.
Nil.
There are no conflicts of interest.