12 Laparoscopic Liver Resection for HCC 195 our series of 174 laparoscopic resections, mortality was nil and morbidity occurred in 14.4% of cases [25]. Considering the 69 patients affected by HCC morbidity rate was 21.7%, but it significantly decreased in the second half of our series (lower than 10%) [25]. Two complications are commonly feared in laparoscopic liver surgery: gas embolism and bleeding. As previously discussed, gas embolism is rarely reported and is usually without any clinical consequences, except for transient cardiovas- cular alterations. On the other side, hemorrhagic complications can occur during parenchymal transection and may lead to urgent conversion. In the literature some severe hemorrhagic complications have been reported, mainly related to hepatic veins injuries [11, 12, 22, 64]. These have been usually managed either laparoscopi- cally or by conversion to laparotomy without reported consequences except for two cases: one brain death [12] and one hypovolemic shock with postoperative renal failure requiring hemodialysis for 4 months [64]. No intraoperative death has been reported. In the published series, hemorrhagic risk was not increased in cirrhotic patients. In the literature, reported conversion rate is about 5–15% [11–13, 15, 22, 65]. Similar data have been reported in HCC cases [19, 21, 23, 25, 45, 57–61]. The rea- sons for conversion are essentially two. The first reason is, of course, bleeding. The second is a technical one, a composite association of difficult exposure, insufficient or poor quality view, fragile tumor with risk of rupture or uncertainty about the dis- tance between the tumor and the transection plane. In our series, the conversion rate was 9.8% in the whole series and 13% in HCC cases, with two-thirds for technical reasons and one-third for bleeding [25]. In our experience, massive bleeding requir- ing rapid conversion never occurred; they were rather situations that were difficult to control by laparoscopy and that, by their persistence, hampered the progress of the operation and were leading to a significant blood loss. Comparison with Open Liver Resections Three case–control studies (one from our group) [44, 60, 66] compared outcomes of laparoscopic and open liver resections in cirrhotic patients. Two comparative studies without any matching criteria compared laparoscopic and open resections for HCC [45, 57]. The outcomes of these studies are summarized in Table 12.3. Reduced morbidity, especially rare occurrences of postoperative ascites, was observed in patients operated through a laparoscopic approach [44, 66]. Operative time of laparoscopic resections was longer in two studies [45, 66],whileatrend toward reduced blood loss has been reported [44, 45, 66]. Hospital stay was shorter in laparoscopic group [40 , 45, 60]. Learning Curve In surgical procedures the so-called learning curve effect has been described, demonstrating improvement in results along with experience [67, 68]. In laparo- scopic liver surgery series, some authors reported reduced operative times, blood 196 L. Viganò and D. Cherqui Table 12.3 Studies comparing laparoscopic vs open liver resection for HCC # Operative time (min) Blood loss (mL) Blood tr. Morbidity Hospital stay (days) Author Year L O L O L O L O L O L O Case–control studies Laurent [66] 2003 13 14 267 ± 79 182 ± 57 620 ± 130 720 ± 240 8% 29% 36% 50% 15.3 ± 8.6 17.3 ± 18.9 Belli [44] 2007 23 23 148 ± 30 125 ± 17 260 ± 127 377 ± 114 0% 17% 13% 48% 8.2 ± 2.6 12.0 ± 4.0 Lai [60] 2009 25 33 150 (75–210) 135 (50–120) NR NR 16% 15% 7 (4–11) 9 (5–37) Comparative studies Shimada [45] 2001 17 38 325 280 400 800 6% 11% 6% 11% 12 ± 522± 8 Kaneko [57] 2005 30 28 182 ± 38 210 ± 40 350 ± 210 505 ± 185 NR 10% 18% 14.9 ± 7.1 21.6 ± 8.8 L: laparoscopic resections; O: open resections; Blood tr.: blood transfusion; Bold typed data p < 0.05; NR: data not reported 12 Laparoscopic Liver Resection for HCC 197 loss, and conversion rate when comparing early and late cases of their series [11, 16, 38, 69]. Our group recently studied the learning curve effect along our experi- ence of laparoscopic liver resections [ 25]. We split our series of 69 laparoscopic liver resections for HCC into three groups of 23 consecutive cases. Conversion rate progressively decreased (26.1, 8.7, and 4.3%). A significant decrease of pedicle clamping rate (from 100 to 17.4%), clamping duration when used (60 to 20 min), operative time (240 to 150 minutes), and blood loss (400 to 100 cc) was observed. Morbidity decreased from 43.5 to 13.0 and 8.7% and hospital stay passed from 9 to 7 and 6 days, respectively. Left Lateral Sectionectomy Left lateral sectionectomy has a privileged place in laparoscopic resections (Fig. 12.5). Our group demonstrated by a case–control study that, despite longer operative times, laparoscopy is associated with reduced blood loss and morbid- ity, especially in cirrhotic patients [70]. A further analysis on 36 laparoscopic left lateral sectionectomies reported no mortality and no liver-specific morbidity, low blood loss, and no transfusion [38]. Conversion occurred only in one patient during our experience. In addition a clear learning curve effect was demonstrated: opera- tive time, use of Pringle maneuver, and hospital stay were significantly reduced in the last 18 patients. All these data have been confirmed by further recent studies [71–73]. Laparoscopy can be recommended as the routine approach to left lateral sectionectomy. Fig. 12.5 Laparoscopic left lateral sectionectomy for HCC. (a) Preoperative CT scan. (b)The surgical field at the end of parenchymal transection. (c) The specimen 198 L. Viganò and D. Cherqui Other Minor Resections Antero-lateral liver segments (segments 2–6) are the so-called laparoscopic liver segments. Their non-anatomical resections are commonly reported in the literature and are associated with excellent outcomes [11–20, 22, 23] (Fig. 12.6). Even if no studies specifically compared their results with those of open counterparts, equiva- lence between the two procedures can be postulated and advantages of laparoscopic approach can be hypothesized. In fact, together with left lateral sectionectomies, they represent the majority of cases included in case–control studies comparing open and laparoscopic liver surgery. Fig. 12.6 Laparoscopic segmentectomy 4b for HCC. (a) Preoperative CT scan. (b) The surgical field at the end of parenchymal transection As mentioned above, non-anatomical resections of segments 7, 8, and 1 have been usually excluded from laparoscopic approach because of difficult visualiza- tion of surgical field. Similarly right liver segmental anatomic resections present many problems, mainly related to adequate exposure, the need for two transec- tion planes, and the difficulties to check margin adequacy [40]. Increased risk of intraoperative bleeding and positive surgical margin can be feared. Recently feasi- bility of these procedures has been reconsidered and successful laparoscopic cases have been reported, especially applying hand assistance [19, 21, 34, 74] (Fig. 12.7). Laparoscopic right posterior sectionectomies and caudate lobectomies have been performed with good outcomes [18, 20, 21, 43, 74]. Cho et al. compared outcomes of laparoscopic approach for lesion in antero-lateral segments vs. postero-superior ones and they did not report any differences, except for longer operative time and higher transfusion rate in the second group [21, 43]. Despite these positive results, little data are presently available and further studies are necessary to validate outcome of these procedures. Major Hepatectomy An increasing number of laparoscopic major hepatectomies have been reported in the literature [11–13, 18, 20–22, 56, 69, 75–77], including large series in the past 12 Laparoscopic Liver Resection for HCC 199 Fig. 12.7 Laparoscopic atypical resection of segment 8 for HCC. (a) Preoperative MRI. (b)Liver transection performed with harmonic scalpel. (c) Specimen is placed in a plastic bag. (d) Specimen extraction through a separate incision. (e) The surgical field at the end of parenchymal transection. (f) The specimen 2 years [11, 13, 18, 20–22, 75]. The majority of procedures were right or left hepate- ctomies. However, few specific data about these procedures are available and only a limited number of cases have been performed in patients with HCC [19–21, 25, 58, 60] (Table 12.2). Even if some authors suggest feasibility of right hepatectomy by 200 L. Viganò and D. Cherqui pure laparoscopic approach [75–77], the hand assistance can be useful in selected cases. It may help to mobilize the liver, to perform parenchymal transection and to control bleeding. At present, laparoscopic major hepatectomies are still limited to few expert centers and cannot be considered standard procedures. Further evaluation and tech- nical refinements are required before laparoscopic major liver resections can be recommended. Oncological Results Controversy about laparoscopy in cancer patients arose from unacceptable peri- toneal and port site seeding in early patients with incidental gallbladder cancer or with colon cancer [78, 79]. Proper use of oncological surgical principles has reduced this problem to the point that there are no more differences as compared to open surgery. It is highly important that oncological principles are strictly followed: “no touch”, no direct manipulation of the tumor, immediate conversion in case of locally advanced cancer, and protection for extraction. Up to December 2008, 12 papers (two from our group) specifically focused on laparoscopic resection of HCC [19, 42, 45, 57–61, 66, 80, 81]. Further data on HCC are included among other laparoscopic series [12, 20, 21, 23, 24, 30, 35, 62]. Published series including more than 10 patients are detailed in Table 12.4. Surgical margin width was adequate in the majority of cases: its median was over 1 cm in almost all series and few positive surgical margins have been reported [19–23, 30, 42, 45, 58, 59, 61]. Three-year overall and disease-free survival rates were about 65–75% and 50–70%, respectively [12, 19, 22, 23, 42, 57–59, 62]. In our series, 64 patients with HCC underwent laparoscopic liver resection: the mean surgical margin width was 13 mm and 5-year overall and disease-free survival rates were 65% and 34%, respectively [22]. These outcomes are similar or even better than those reported in open series, although high recurrence rates are observed at 5 years as expected with underlying chronic liver hepatitis or cirrhosis [23, 82–84]. No port site recurrences imputable to laparoscopy were noted. Direct comparison in case–control s tudies between laparoscopic and open resection for HCC reported no differences in terms of surgical margin width and midterm results [44, 60, 66]. Most recurrences observed in our experience occurred in a remote segment sug- gesting multicentric carcinogenesis due to underlying liver disease. Most were amenable to treatment including reresection, ablation, TACE, or transplantation. These results warrant close postoperative follow-up to allow early detection of recurrences. Indeed, 34% of patients with recurrences underwent salvage liver transplantation [22]. Laparoscopic approach may have a role even in recurrent HCC. A recent paper by Belli et al. demonstrated feasibility of redo laparoscopic treatment (12 resec- tions and 3 radiofrequency ablations), even in patients with previous open resection 12 Laparoscopic Liver Resection for HCC 201 Table 12.4 Laparoscopic liver resections for HCC (series including more than 10 patients). Overall a nd disease-free survival rates are reported only if detailed data were available in the paper (i.e., percentages or events with follow-up duration) Author Year # Diameter (cm) Surgical margin (mm) Overall survival Disease-free survival Shimada [45] 2001 17 2.6 ± 0.9 8 ± 7 NS vs open control group Teramoto [42] a 2003 11 NR 82% negative 5 yr 75% 5 yr 38.2% Kaneko [57] 2005 40 NR NR 5 yr 61% 5 yr 31% Tang [30] 2006 17 NR 70.6% > 10 mm 2 yr 59% NR Vibert [12] 2006 16 6.5 NR 3 yr 66% 3 yr 68% Belli [61] 2007 23 3.1 ± 0.7 91.4% > 10 mm NS vs open control group Cai [62] 2008 24 NR NR 5 y 56.2% NR Dagher [58] 2008 32 3.8 ± 2 10.4 ± 9 3 yr 72% 3 yr 55% Cho [21] 2008 57 3.5 ± 2.0 b 2.9 ± 1.3 c 16.4 ± 15.0 b 15.8 ± 18.8 c NR Chen [19] 2008 116 2.1 ± 0.8 d 3.2 ± 1.9 e 100% >10 mm 5 yr 59% d 5 yr 62% e NR Buell [20] 2008 36 4.6 7 mm (100% R0) NR g Sasaki [23] 2008 37 3.5 ± 3.7 8.7 ± 7.1 5 yr 52.7% NR Santambrogio [59] 2009 19 2.8 ± 1.0 100% > 5 mm 4 yr 50% 4 yr 24% Huang [35] 2009 27 2.5 (2–4) NR NR g NR g Lai [60] 2009 25 2.5 (1–7) 88% R0 3 yr 60% 3 yr 52% Inagaki [24] 2009 36 NR NR 5 yr 79.3% NR Bryant f [22] 2009 64 4.4 ± 2.6 13 ± 12 5 yr 65% 5 yr 34% a Laparoscopic and thoracoscopic resections b HCC in antero-lateral liver segments c HCC in postero-superior liver segments d patients with resection of ≤ 2 segments e patients with resection of > 2 segments f Author’s series g Insufficient follow-up data in the paper NR: data not reported; NS: not significant [81]. Previous laparoscopic resection enabled easier procedures thanks to fewer adhesions. Resection and Liver Transplantation: Does Laparoscopy Modify the Picture? The treatment of patients with HCC within Milan criteria is debated, because both liver transplantation and liver resection can be proposed. Liver transplantation is the ideal treatment by removing both the tumor and the underlying liver disease, but shortage of donors and its consequent dropout on the waiting list due to progression limit the number of patients who can receive it [3]. By contrast, liver resection is readily available, but is associated to high recurrence rates [8, 82–84]. In a modern 202 L. Viganò and D. Cherqui view, liver resection and transplantation should not be considered competitive but complementary and treatment should be tailored to each patient case. Resection can be used before liver transplantation in three different strategies: first, resection as primary therapy considering “salvage” liver transplantation in case of recurrence or liver failure [8]; second, resection as tool to select patients for the liver transplanta- tion on the basis of pathological data of the tumor and the surrounding parenchyma [85–87]; finally, “bridge” resection, i.e., resection as treatment on the waiting list. The advantages and the disadvantages of these options are not the topic of this chapter, but it should be emphasized that the laparoscopic approach could enhance the role of liver resection in case of peripheral nodules. It allows easy resections with early recovery and low morbidity. Oncological results are not infe- rior to open resections. Complete pathological data of both tumor and parenchyma can be safely obtained. Indications can be extended even to patients with mild compromised liver f unction (Child–Pugh B). Laparoscopic liver resection is also complementary to radiofrequency ablation which is associated with a higher risk of seeding in superficial lesions. Therefore, laparoscopic limited resection could be used in peripheral lesions and radiofrequency in deeply located nodules, which would otherwise require major liver resection. The main criticism to liver resection are the difficulties encountered at the sub- sequent liver transplantation if r equired. Adam et al. reported poor outcomes of salvage liver transplant after previous hepatectomy because of adhesions related to primary treatment and increased blood loss [88]. In our center, 12 patients under- went bridge or salvage transplantation after primary laparoscopic resection with no mortality. When transplantation was performed, they benefitted from the absence of adhesions and, in comparison with 12 transplantations after open hepatectomies, we observed lower operative time, blood loss, and transfusion rate [89]. Reduced adherences after laparoscopic liver surgery have been confirmed by Belli et al. in the analysis of the redo surgery [81]. Conclusions For laparoscopic liver resection to be effective, specific training and access to adequate technology are required. Patient selection must be accurate, and the avail- ability of laparoscopy should not change the indications for resection. The rules of oncological surgery must be followed for minimally invasive operations, just as in their open counterparts. At present, good candidates for laparoscopic liver resection are patients with peripheral HCC requiring limited hepatectomy or left lateral sec- tionectomy. In these cases surgery can be performed with early recovery and low morbidity. Oncological results appear to be similar to open surgery but further stud- ies are necessary. The laparoscopic approach strengthens the role of liver resection in the treatment strategy of peripheral HCC within Milan criteria. 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