Journal of Minimal Access Surgery

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Year : 2011  |  Volume : 7  |  Issue : 4  |  Page : 222--226

Laparoscopic liver resection for hepatocellular carcinoma in cirrhotic patients. Feasibility of nonanatomic resection in difficult tumor locations

Marco Casaccia, Enzo Andorno, Stefano Di Domenico, Ilaria Nardi, Giuliano Bottino, Maximiliano Gelli, Umberto Valente 
 Department of General and Transplant Surgery, Advanced Laparoscopy Unit, St. Martino Hospital, University of Genoa, Italy

Correspondence Address:
Marco Casaccia
Department of General and Transplant Surgery, St. Martino Hospital, University of Genoa, Italy; Largo Rosanna Benzi n 10, 16132 - Genova, Italia


Background: Surgical resection for hepatocellular carcinoma (HCC) in cirrhotic patients remains controversial because of high morbidity and recurrence rates. Laparoscopic resection of liver tumors has recently been developed and could reduce morbidity. The aim of this study was to evaluate retrospectively our results for laparoscopic liver resection (LLR) for HCC including lesions in the posterosuperior segments of the liver in terms of feasibility, outcome, recurrence and survival. Materials and Methods: Between June 2005 and February 2009, we performed 20 LLR for HCC. Median age of the patients was 66 years. The underlying cirrhosis was staged as Child A in 17 cases and Child B in 3. Results: LLR included anatomic resection in six cases and nonanatomic resection in 14. Eleven procedures were associated in nine (45%) patients. Median tumor size and surgical margins were 3.1 cm and 15 mm, respectively. A conversion to laparotomy occurred in one (5%) patient for hemorrhage. Mortality and morbidity rates were 0% and 15% (3/20). Median hospital stay was 8 days (range: 5-16 days). Over a mean follow-up period of 26 months (range: 19-62 months), 10 (50%) patients presented recurrence, mainly at distance from the surgical site. Treatment of recurrence was possible in all the patients, including orthotopic liver transplantation in three cases. Conclusions: LLR for HCC in selected patients is a safe procedure with good short-term results. It can also be proposed in tumor locations with a difficult surgical access maintaining a low morbidity rate and good oncological adequacy. This approach could have an impact on the therapeutic strategy of HCC complicating cirrhosis as a treatment with curative intent or as a bridge to liver transplantation.

How to cite this article:
Casaccia M, Andorno E, Di Domenico S, Nardi I, Bottino G, Gelli M, Valente U. Laparoscopic liver resection for hepatocellular carcinoma in cirrhotic patients. Feasibility of nonanatomic resection in difficult tumor locations.J Min Access Surg 2011;7:222-226

How to cite this URL:
Casaccia M, Andorno E, Di Domenico S, Nardi I, Bottino G, Gelli M, Valente U. Laparoscopic liver resection for hepatocellular carcinoma in cirrhotic patients. Feasibility of nonanatomic resection in difficult tumor locations. J Min Access Surg [serial online] 2011 [cited 2021 Dec 3 ];7:222-226
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In recent years the progress of laparoscopic procedures and the development of new and dedicated technologies have made endoscopic hepatic surgery feasible and safe. [1],[2],[3] Almost all types of liver resection have already been performed by laparoscopy. [4],[5] However, few major laparoscopic hepatectomies have been reported to date. [6],[7] In fact, the use of this technique has been limited to easily accessible lesions, namely, tumors in the peripheral portion of the liver's anterolateral segments (segments 2, 3, 5 and 6, and the inferior part of 4) according to the classification of Couinaud. Accordingly, most surgeons consider that lesions located in the posterior or superior part of the liver (segments 1, 7, and 8, and the superior part of 4) are not appropriate because of the limited visualization and the difficulty of controlling bleeding. [8],[9]

Because of concerns about using laparoscopy to treat malignant tumors and the fear of compromising the oncological resection, most surgeons have concentrated on laparoscopic liver operations for benign conditions. [10] Advances in laparoscopic cancer care and increasing experience of liver surgeons with laparoscopy have carved out a new role for laparoscopic surgery in the management of hepatic tumors. It is now widely accepted that laparoscopy will be increasingly used in liver surgery and the indications extended to patients with hepatocellular carcinoma (HCC) and cirrhosis. [7],[11],[12]

The aim of this study was to evaluate retrospectively our results for laparoscopic liver resection (LLR) for HCC including lesions in the posterosuperior segments of the liver in terms of feasibility, safety, outcome, recurrence and survival.

 Materials and Methods


Twenty LLR for HCC performed between June 2005 and February 2009 were retrospectively reviewed. In the same period, 51 patients underwent liver transplantation without prior resective surgery and 32 patients underwent open liver resection.

Selection criteria for laparoscopic approach in HCC patients included the following: well compensated Child's class A/B cirrhosis, esophageal varices ≤ grade 2, platelet count ≥ 40 × 10 9 /L, and solitary lesion of ≤ 5 cm in diameter accessible to the laparoscopic approach (i.e., located in the peripheral segments of the liver) and treatable by limited resection (<3 segments). Only one patient was operated on in emergency situation for a hemoperitoneum from a ruptured HCC located in segment III.

If severe impairment of the coagulation tests was assessed preoperatively (platelets <40,000 and/or international normalized ratio >1.6), patients were excluded from the procedure.

Imaging assessment of the liver included CT, MRI or both and Doppler ultrasonography. Portal vein invasion and evidence of extrahepatic disease were considered exclusion criteria.

Most resections were intended to be anatomic (i.e., resection of 1 or more anatomic segments) in order to resect the portal territory of the tumor. Segmentectomies were defined by their numbers and performed according to external segmental borders and use of intraoperative ultrasound. However, in small lesions developed in patients with portal hypertension and hepatic dysmorphy, nonanatomic resections were performed. These consisted of resection of less than one segment including the tumor and an intended 1-cm tumor-free margin.

Survival and tumor recurrence rates were studied at follow-up through liver function tests, α-fetoprotein, and computed tomographic or magnetic resonance scan at 1 month and then every 6 months.

Parameters assessed were duration of surgery, blood loss, perioperative transfusions, pathological margins, postoperative variations of liver tests, mortality, morbidity, hospital stay, recurrence rate and survival. The results were expressed as medians (range). All comparisons between groups were performed using the Student t-test. P< 0.05 was considered statistically significant.

Surgical Technique

The patients were placed in the supine position with lower limbs apart, except for isolated resections of segment 6-7 where the left lateral decubitus position was used. The procedures were performed with CO 2 pneumoperitoneum, and abdominal pressure was electronically maintained below 11 mmHg. In general, four trocars and a 30° optic were necessary.

The liver was examined by vision and intraoperative ultrasonography to confirm the number and size of the lesions and define their relationship with the intrahepatic vascular structures. A tourniquet for portal triad clamping was passed in few cases and the Pringle maneuver was used in one.

Hepatic transection was performed using an ultrasonic dissector (Ultracision, Ethicon, USA) in the first four patients and a thermofusion device [Ligasure; Covidien Italia, Segrate (Mi), Italy] in the last 16 patients.

Bipolar electrocoagulation was used for minor bleeding, and larger structures were secured with clips. Portal pedicles and major hepatic veins were divided by application of a linear stapler (Endo GIA roticulator; Covidien Italia). The resected specimen was placed in a plastic bag and externalized, without fragmentation, through the enlarged umbilical port incision or through a suprapubic incision. This incision was immediately closed and the abdomen reinflated. The surgical field was irrigated and checked for bleeding or bile leak, and residual fluid was removed by suction. A drain was left in situ in all patients.


Between June 2005 and February 2009, 20 liver resections for HCC were performed by laparoscopy. These 20 resections were carried out on 12 men and 8 women with a median age of 66 years (range: 47-76 years). The characteristics of the patients are summarized in [Table 1]. Tumor location according to Couinaud hepatic segmentation is presented in [Figure 1]. {Table 1}{Figure 1}

The median size of the resected tumor was 3.1 cm (range: 0.9-5.0 cm). The median surgical margin was 15 mm (range: 0-40 mm) and exceeded 5 mm in 18 patients (90%). At hystological examination, the severity of cirrhosis was established, showing moderate activity in 11 patients and mild activity in 9. Twenty-three HCC nodules were resected. There were 14 (70%) atypical and 6 (30%) anatomic resections. The types of liver resection and the results are detailed in [Table 2].{Table 2}

The median duration of the operation was 300 min (range: 120-560 min). The median operative blood loss was 55 ml (20-1400 ml). Bleeding resulted from parenchymal transection in all cases. Ten patients (50%) required blood transfusion (median 1 packed red cell unit, range: 1-4 units). Conversion to laparotomy was required in one patient (5%), due to important continuous bleeding during parenchymal transection (segmentectomy V). The decision to convert to laparotomy was not once taken in emergency conditions or due to life-threatening bleeding or major vessel injury. One patient was operated on in emergency situation for hemoperitoneum (2500 ml) from a ruptured HCC located in segment III. An atypical resection of a 4-cm lesion was performed in this case.

Eleven procedures were associated in nine (45%) patients. A cholecystectomy was necessary in five cases to maintain a clear resection margin in HCC nodules located in segment IV or V. Radiofrequency ablation was used to treat a second tumor located away from the resected tumor and undetected at preoperative imaging in three cases. Adhesiolysis was realized for previous upper quadrant surgery in two cases and lymphnode sampling of the hepatic pedicle was made in one case.

Specific postoperative complications occurred in three (15%) patients. These complications included ascites well controlled by diuretics, mild transient jaundice and biliary collection drained percutaneously in one case each. Median hospital stay was eight days (range: 5-16 days). Over a mean follow-up period of 26 months (range: 19-62 months), ten (50%) patients presented recurrence. With respect to surgery performed, all recurrences were located in another liver segment; an associated local recurrence adjacent to the stump was present in three patients.

No statistical differences were noted between recurrent and non recurrent patients in terms of tumor pathologic grading, presence of a capsule, presence of satellite nodules and surgical margins (18 ± 10 vs. 15.2 ± 9, respectively; P = 0.52). A statistical significance was found in tumor diameter, being larger in recurrent than in nonrecurrent patients (37.1 ± 11 vs. 26.7 ± 10, respectively; P = 0.048).

Treatment of recurrence was possible in all patients, including chemoembolization in seven cases, orthotopic liver transplantation in three cases (two patients receiving both treatments), and percutaneous radiofrequency ablation in two.

Three (15%) patients died after 19, 25 and 33 months of follow-up, respectively, of severe liver function impairment and multifocal hepatic recurrence with extrahepatic metastases in one.


LLR for HCC is limited to centers with experience in both laparoscopic surgery and the management of cirrhotic patients. Considering LLR requires an accurate assessment of the indications in terms of tumor location and underlying liver function and specific expertise and training in both hepatic and laparoscopic surgery, as well as access to adequate technology.

The most frequently required type of liver resection for small single HCC is limited anatomic resection. Such resections are particularly suitable for laparoscopy. However, liver resections in cirrhotic patients are technically more difficult than in patients with a normal liver, presenting added complications, such as profuse bleeding during liver mobilization and parenchymal transection. A few reports have already suggested that laparoscopic resections may be successfully performed in patients with HCC and cirrhosis. [13],[14]

In this study, an LLR was successfully performed in 95% of the patients. Only one patient required conversion to open surgery, due to important continuous bleeding during parenchymal transection (segmentectomy V). In our experience, as in other laparoscopic studies, [9],[14] blood loss was acceptable. This was probably due to the use of new coagulation and transection devices.

Operative durations of LLRs are significantly longer than those of matched open counterparts. [9],[15] This was confirmed in the present study with a 5-hour mean operative time which, however, improved with the learning curve. It is worth saying that 11 procedures were associated in nine (45%) patients, further increasing the operative time. The safety of the procedure is attested by the absence of mortality and the low specific morbidity (15%). There were only two cases of transient postoperative liver failure. These findings are important since ascites and jaundice are the main complications of liver resection, even minor ones, in cirrhotic patients.

The recurrence rate was similar to those reported for other laparoscopic studies [2],[13] and for open resection of HCC. [16],[17] As often observed following HCC resections, most recurrences occurred away from the hepatic stump. The only local recurrences occurred in three (30%) patients after a segmentectomy V, a segmentectomy VI and an atypical resection of segment VII, respectively. The parenchymal margin in our study was free of tumor cells in all patients, with a margin of less than 5 mm in only one case. However, the free parenchymal margin in the patients with recurrence near the stump was 10 mm in two patients and 40 mm in one. Among tumor characteristics (tumor diameter, pathologic grading, presence of a capsule, presence of satellite nodules and surgical margins), only the tumor diameter differed significantly between recurrent and nonrecurrent patients. A correlation between recurrence and tumor diameter has already been postulated. A retrospective study by Yeh et al., [18] analyzed the surgical outcomes of HCC concomitant with liver cirrhosis in 218 patients who underwent hepatic resection. Tumor size >2 cm was found to be a significant adverse prognostic parameter affecting recurrence and survival rates.

When considering the type of liver resection to be performed, some considerations need to be made. Segmental and nonanatomic resections are more suitable for a laparoscopic approach when in the peripheral "laparoscopic" segments 2 to 6. Segments 7 and 8 are more difficult to access as the approach angle of the instruments is limited by the costal margin. The major problems then become ensuring an adequate oncological margin and difficult-to-control bleeding from venous tributaries in the depth of the tumorectomy. In our series, six (33%) resected nodules were located in segments 7 and 8. Despite difficult location of the lesions, a non-anatomic resection was completed laparoscopically in all cases. The procedures were long and technically demanding, but the use of a 30° optic joined to an extended right triangular ligament division and to a consequent lowering of the hepatic dome by use of a palpator has made it possible with respect to the surgical margins.

Although parenchymal-sparing resection is required by the presence of underlying liver disease and impaired liver regeneration, anatomical resection has always to be considered and pursued. In fact, it has been shown to reduce local recurrence and improve survival in HCC patients when compared with nonanatomic wedge resections. [19],[20]

This is attributed to the mode of dissemination of HCC through microvascular portal invasion, which justifies anatomical resection of a portal territory around the tumor.

According to previous studies, [10],[21] we can state that a laparoscopic approach to a limited resection for a single lesion in segment 7 or 8 would only be suitable where the lesion is particularly small and superficial. A single larger lesion must, therefore, be considered for either an open limited resection or a laparoscopic right hemihepatectomy. Besides the advantages of minimally invasive surgery, another important issue includes preservation of abdominal collateral venous circulation, which may contribute to the absence of postoperative ascites, and avoidance of peritoneal adhesions, valuable in these patients who may require repeat operations for tumor recurrence.

This advantage is particularly appreciated in patients undergoing liver transplantation, as it occurred in 3 patients of our series. Absent or limited postoperative adhesions were noted at this time.

In conclusion, our study shows that LLR for small peripheral HCC in patients with chronic liver disease and preserved liver function is a safe procedure with good short-term results. It also can be proposed in tumor locations with a difficult surgical access maintaining a low morbidity rate and good oncologic adequacy. It suggests that LLR represents an acceptable alternative to open resection in this setting and could have an impact on the therapeutic strategy of HCC complicating cirrhosis, as a treatment with curative intent or as a bridge to liver transplantation.


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