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Page 2 of 7 Hokuto et al. Hepatoma Res 2020;6:81 I http://dx.doi.org/10.20517/2394-5079.2020.78

a difficult procedure due to adhesions associated with previous liver resection and changes in anatomical
[4-6]
recognition. In fact, several studies have reported high morbidity rates after RLR . With advances in
[7]
laparoscopic liver resection (LLR), RLR has been increasingly performed laparoscopically . LLR is a less
invasive procedure that is associated with better short-term outcomes compared with open liver resection
[8,9]
(OLR) . Similarly, the superiority of laparoscopic RLR over open RLR in short-term outcomes has been
reported [10-12] . However, none of the studies were randomized controlled trials and laparoscopic RLR
might be performed in select patients. Laparoscopic RLR was discussed at the first European Guidelines
[13]
Meeting on Laparoscopic Liver Surgery (Southampton 2017) and considered an appropriate option .
However, most laparoscopic liver surgeons suggest that repeat liver resection significantly increases the
[14]
difficulty of LLR . Currently, the indications for laparoscopic RLR vary between centers. Considered a
difficult procedure, RLR poses a range of challenges depending on the location of recurrent tumor and
[15]
previous liver resections. A recent report has introduced a difficulty classification for laparoscopic RLR .
Specifically, the level of difficulty was determined on the basis of the type of previous liver resection (open
or laparoscopic), number of previous liver resections, surgical procedure and tumor location in previous
[16]
liver resections, and difficulty score of LLR for recurrent HCC . RLR after LLR has been increasing in
parallel with the increasing number of LLR for HCC. In colorectal surgery, the laparoscopic approach has
[17]
been reported to reduce adhesion formation . Similarly, RLR after LLR is associated with less adhesion
formation compared with RLR performed after OLR. Therefore, RLR in the era of LLR has distanced
characteristics. Conversely, percutaneous radiofrequency ablation (RFA), a technique developed in the
[20]
last two decades [18,19] , has been demonstrated to be useful in small HCCs . In general, patients who
previously undergo hepatectomy for HCC are examined regularly by imaging studies, which facilitate the
frequent detection of small-diameter recurrent HCCs. Within this framework, the role of liver resection for
recurrent HCC might be changing. In this review, we describe the current status of laparoscopic RLR for
HCC in the era of LLR and RFA.

SIGNIFICANCE OF REPEAT LIVER RESECTION FOR RECURRENT HEPATOCELLULAR
CARCINOMA
Relatively good survival outcomes of RLR for HCC have been reported since the 1990s [21-24] . These earlier
studies reported that 5-year survival rate after RLR was around 50%, which was comparable to the prognosis
of primary liver resection and was better than the prognosis of transarterial chemoembolization [25,26] .
However, RLR was performed in select patients with relatively better liver function and tumor factors
compared to those undergoing transarterial chemoembolization. Moreover, disease-free survival rates were
[2,3]
significantly lower with RLR compared to initial liver resection . Studies investigating prognostic factors
after RLR for HCC reported that portal vein invasion at the time of first liver resection, portal vein invasion
in RLR, multiple HCCs at the time of first liver resection, and disease-free interval of less than one year
were independent prognostic factors after RLR [1,3,27] . The 5-year survival rate was 86.0% in patients without
[1]
prognostic factors . These results provide clear evidence that RLR for recurrent HCC is a useful treatment
option for select patients.

In the last decade, several studies investigating long-term outcomes in patients undergoing three or more
RLRs reported that the 5-year survival and disease-free survival rates after the third RLR were 40.0%-68.2%
and 12.8%-33.8%, respectively [6,28,29] . These results were comparable to those observed after the second RLR.
[6]
Regarding short-term outcomes, Mise et al. reported significantly longer surgical duration and higher
postoperative morbidity with three or more RLRs, whereas Yamashita et al. reported no significant
[28]
differences. These results indicated that three or more RLRs might be considered an acceptable treatment
approach in patients whose liver function and tumor factors were within surgical indications.