JOURNAL OF LAPAROENDOSCOPIC & ADVANCED SURGICAL TECHNIQUES Volume 24, Number 4, 2014 ª Mary Ann Liebert, Inc. DOI: 10.1089/lap.2013.0502 Laparoscopic Resection of Hepatocellular Carcinoma: When, Why, and How? A Single-Center Experience Paulo Herman, MD, Marcos Vinicius Perini, MD, Fabricio Ferreira Coelho, MD, Jaime Arthur Pirolla Kruger, MD, Renato Micelli Lupinacci, MD, Gilton Marques Fonseca, MD, Felipe de Lucena Moreira Lopes, MD, and Ivan Cecconello, MD Abstract Purpose: The aim of this study was to evaluate short- and intermediate-term results of laparoscopic liver resection in selected patients with hepatocellular carcinoma (HCC). Patients and Methods: Eighty-five patients with HCC were subjected to liver resection between February 2007 and January 2013. From these, 30 (35.2%) were subjected to laparoscopic liver resection and were retro- spectively analyzed. Special emphasis was given to the indication criteria and to surgical results. Results: There were 21 males and 9 females with a mean age of 57.4 years. Patients were subjected to 10 nonanatomic and 20 anatomic resections. Two patients were subjected to hand-assisted procedures (right posterior sectionectomies); all other patients were subjected to totally laparoscopic procedures. Conversion to open surgery was necessary in 4 patients (13.3%). Postoperative complications were observed in 12 patients (40%), and the mortality rate was 3.3%. Mean overall survival was 29.8 months, with 3-year overall and disease-free survival rates of 76% and 58%, respectively. Conclusions: Laparoscopic treatment of selected patients with HCC is safe and feasible and can lead to good short- and intermediate-term results. Introduction organ needs. The disproportion between the growing number of transplant candidates on the waiting list and the epatocellular carcinoma (HCC) is the most com- shortage of donors leads to a long waiting list time, raising Hmon primary liver cancer and the fifth most common the risk of tumor progression and causing a significant malignancy worldwide.1–3 In about 90% of the cases, it oc- number of dropouts.7 curs in patients with chronic liver disease,2,4 and, in the last Resection, a therapeutic alternative that can be performed few years, there has been a clear increase in prevalence, es- readily and with lower costs compared with liver transplan- pecially in Western countries, that is directly related to tation, has become a safe procedure in the last years with hepatitis C virus infection.4,5 Curative therapeutic options mortality rates in specialized centers lower than 5%.8,9 In available are surgical resection and liver transplantation. The selected cases, good long-term results can be achieved (50%– choice between transplantation and resection is controversial, 70% 5-year overall survival). However, resection is followed and there are no controlled trials comparing these modalities. by high rates of morbidity and mortality in patients with The best potential curative procedure seems to be liver chronic liver disease, being possible only in patients with transplantation because it can treat simultaneously the tu- preserved liver function.10 mor and the underlying liver disease.6 On the other hand, Despite the controversy between resection and transplan- the best results are achieved in patients within a strict se- tation, groups specializing in both liver surgery and liver lection criterion set known as the Milan criteria.6 More- transplantation, in the context of a long waiting list for over, in a context of a lack in liver grafts availability seen transplant (more than 6–9 months), have advocated resection worldwide and the increasing prevalence of HCC, the for the treatment of solitary HCC in patients with preserved number of donors is much lower than necessary to meet the liver function. It has also been shown that in patients within Liver Surgery Unit, Department of Gastroenterology, University of Sa˜o Paulo Medical School, Sa˜o Paulo, Brazil. 223 224 HERMAN ET AL. the Milan criteria, the long-term outcome of those listed for liver transplantation (intention-to-treat analysis) was similar HCC < 5cm when compared with patients who underwent resection.11 There are many other arguments other than the avoidance of a long waiting list favoring liver resection for HCC: im- mediately applicability, lower mortality rate, the availability CHILD A CHILD B/C of a surgical specimen for histological and molecular eval- uation, and good long-term results.12 Most of the groups that deal with patients with liver diseases Peripheral Central OLT use a screening program to detect early HCC, thereby in- creasing the number of patients diagnosed with small HCC nodules in the last few years.13,14 It has already been shown that laparoscopic liver resection (LLR) for HCC, especially when LLR >3cm <3cm indicated for solitary, small, and peripheral tumors in patients with preserved liver function, is safe and can lead to good short- 15 Open and long-term results. The enthusiasm for minimally invasive Recurrence resection/ +– RFA treatment of HCC led to the publication of many case series within Milan showing very good results.16–19 Recent meta-analyses showed PVE that laparoscopic resection led to shorter hospital stay, de- creased blood loss, and lower rates of postoperative morbidity Recurrence OLT OLT (less ascites) compared with open liver resection.8,20,21 within Milan The aim of this study was to evaluate short- and interme- diate-term results of LLR for selected patients with HCC. The authors also present their guidelines for the treatment of HCC. OLT Patients and Methods From a prospective hepatobiliary surgical database, 85 pa- LLR tients with HCC were subjected to liver resection in our unit between February 2007 and January 2013. From these patients, FIG. 1. Guidelines for the treatment of single hepatocel- 30 (35.2%) were subjected to LLR and were retrospectively analyzed. All patients were subjected to clinical evaluation and lular carcinoma (HCC) within the Milan criteria. LLR, laparoscopic liver resection; OLT, orthotopic liver trans- liver function laboratory tests. Preoperative workup included plant; RFA, radiofrequency ablation; PVE, portal vein em- helicoidal computed tomography (CT) scan or magnetic reso- bolization. nance, thoracic CT, and bone scintigraphy. Diagnosis was based on image characteristics; none of the patients was sub- jected to liver biopsy. In patients in whom CT or magnetic section, the transection of the portal pedicle and hepatic veins resonance imaging depicted signs of portal hypertension, upper was done with the use of vascular staplers. Specimen removal digestive endoscopy was performed. Radiological studies were was done inside a plastic bag through the umbilical or a su- reviewed in a multidisciplinary meeting held weekly. prapubic incision. During parenchyma transection all patients Treatment guidelines for HCC in our unit are shown in were maintained with low central venous pressure levels (be- Figure 1. tween 3 and 5 cm H2O). No routine drainage was used. The selection criteria for the laparoscopic approach were In the last 2 patients with tumors located in the right pos- as follows: terior section, a hand-assisted procedure was performed through a small upper midline incision.22 Solitary nodule, smaller than 5 cm in diameter Liver resections were defined according to the Brisbane Preserved liver function (Child–Pugh Class A) 2000 classification.23 Intraoperative and immediate postop- Peripheral location on the liver erative data collected included perioperative transfusions, Resection of up to two segments of the liver conversions to open procedure (hybrid procedure), surgical Platelet count of >100,000/mL margins, postoperative complications, length of hospital stay, American Society of Anesthesiologists score lower than 3 and mortality. Postoperative complications were classified ac- Patients with portal hypertension and esophageal varices cording to the Clavien–Dindo classification.24 Postoperative Grade 1 or 2 (with platelet count of >100,000/mL) in follow-up was performed every 4 months, including clinical, Child Class A patients were not excluded. laboratory, and radiological evaluation. Data collected included In brief, all patients were positioned in a supine French disease recurrence and mortality. position with the surgeon positioned between the legs. For Continuous variables were expressed as median (range) right lateral resections, the patient was placed in a left lateral and were compared by means of the Mann–Whitney test. (45°) position. Pneumoperitoneum was set at 12 mm Hg, and Categorical variables were compared by the chi-squared test intraoperative staging was performed. Parenchyma transection or Fisher’s exact test. Survival and recurrence-free survival was performed with the use of a HarmonicÒ scalpel (Ultraci- were measured from the date of operation to the time of death sionÒ; Ethicon Endosurgery, Cincinnati, OH) or LigaSureÔ or at the time when a recurrent tumor was first diagnosed, (Valleylab, Boulder, CO). For the resection of a segment or respectively. Survival analysis was estimated by the Kaplan– RESECTION OF HEPATOCELLULAR CARCINOMA 225 Meier survival method, and the differences in survival in 1, and sepsis due to pneumonia in 1 (right hepatectomy). An between the groups were compared by the log-rank test. unidentified colonic perforation was diagnosed after 7 days, Differences were considered as statistically significant when leading to re-operation, multi-organ dysfunction, and death the P value was <.05. after 24 days, leading to a mortality rate of 3.3%. During long-term follow-up 1 patient developed an umbili- Results cal hernia that was surgically treated with good outcome. Ten of 29 patients (34.4%) had recurrent disease as follows: liver- There were 21 males and 9 females with a mean age of 57.4 only in 6, lung in 2, adrenal gland in 2, and epigastric port site in years (ranging from 28 to 77 years). The etiology of liver 1. Of the 6 patients with liver-only recurrence, 4 were subjected cirrhosis is depicted in Table 1. All patients presented a to intra-arterial embolization or radiofrequency ablation as a solitary nodule with a mean size of 3.7 cm (range, 2–5 cm).