Use of laparoscopic surgery for colorectal cancer (CRC) has been increasing rapidly1,2; its effectiveness has been established, and its surgical indication has been extended to advanced cases. Liver metastasis occurs in 23% to 29% of CRC patients.3,4 Thus, CRC with liver metastasis (CRCLM) has become the main condition to be treated laparoscopically.

Hepatectomy is recommended as the best effective therapy for CRCLM.5 For synchronous CRCLM, simultaneous resection has been controversial in terms of efficacy and safety because of its surgical invasiveness.6 However, recent reports suggest the effectiveness of simultaneous resection and establish the safety of hepatectomy.7–10 Its beneficial effect in shortening total hospital stay has also been reported.11

On the other hand, recently acquired surgical skills in laparoscopic hepatic resection have dramatically expanded the surgical criteria for this method of operation. Currently, the proportion of laparoscopic liver resections ranges from 20% to 80% of the total volume of liver surgery performed at a particular center.12

In this report, 7 patients with CRC and synchronous CRCLM treated by simultaneous laparoscopic resection and their surgical data were analyzed retrospectively to evaluate the feasibility, safety, and effectiveness of this procedure in terms of short- and long-term results. In addition, reported cases in the literature were reviewed.

Materials and Methods

Results

A total of 5 men and 2 women were treated. Average patient age at the time of operation was 58.6 years (range, 28–89 years; Table 1). The mean observation period was 18 months (range, 15–43 months). Perioperative mortality was not observed in patients in this study.

Table 1 Patient characteristics and perioperative data

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Primary CRC was found in the following locations: ascending colon (n  =  1), transverse colon (n  =  2), sigmoid colon (n  =  2), and rectum (n  =  3); 1 double cancer patient was identified (Case no.7). CRCLM was located in the following places: segment (S)2 (n  =  3), S3 (n  =  1), S5 (n  =  2), and S6 (n  =  1). Hepatectomy consisted of partial resection (n  =  5) and left lateral sectionectomy (n  =  2). Hepatectomy methods included laparoscopic-assisted open hepatic resection (hybrid) (n  =  3) using a small skin incision, HALS using a small incision produced for colonic anastomosis (n  =  2), and pure laparoscopic resection (n  =  2).

No case was converted to standard open surgery. Negative surgical margins at hepatectomy were achieved in all cases, with a mean surgical margin of 10.8 mm.

Mean total operative time was 407.1 minutes (range, 270–575 minutes), and intraoperative blood loss was 206.7 mL (range, 40–350 mL). Blood transfusion was not required in any case. Hepatic inflow occlusion by the Pringle maneuver was not applied during hepatectomy. Regarding the postoperative course, except in Case no. 1, in which percutaneous drainage for intra-abdominal abscess was required, all patients had no surgical complications. Anastomotic leakage was not observed. Postoperative hospital stay ranged from 7 to 38 days (longest in Case no.1), and average stay was 16.4 days (Table 1). Adjuvant chemotherapy was started at 45.7 days postoperatively on average, except for Case no. 5 because of advanced patient age.

Postoperative recurrence was observed in 3 cases (2 liver, 1 lung), but none of these was detected at the cut surface of the liver.

When results were compared with the historical control of patients (n  =  7) undergoing laparoscopic colorectal resection and simultaneous open minor hepatectomy for synchronous CRCLM at our institute, operative time (407.1 versus 360 minutes, lap-hepatectomy group versus open-hepatectomy group, respectively), intraoperative blood loss (206.7 versus 247.1 mL), postoperative hospital stay (16.4 versus 31.2 days), and surgical complication rates (14% versus 43%) were comparable. A tendency toward a shorter hospital stay was seen in the total laparoscopic group.

Discussion

Laparoscopic liver resection was first described in 1992, and its usefulness has been documented.15–23 Moreover, laparoscopic major hepatectomy has been reported since 2004.21,22,24,25 Compared with conventional liver resection, the skin incision is much smaller and the degree of body wall damage is obviously less. Simillis et al reported that intraoperative blood loss was decreased in laparoscopic surgery.26 In addition, Kaneko reported that postoperative recovery was accelerated in laparoscopic surgery.27 With respect to safety, according to the largest review series from Nguyen et al, overall mortality was 9 of 2804 patients (0.3%), morbidity was 10.5%, and no intraoperative deaths were reported.28 On the other hand, laparoscopic surgery for CRC has been established already and is widely accepted as effective therapy even in advanced cases, such as those with liver metastasis.

The recent advent of simultaneous laparoscopic resection of CRC and synchronous CRCLM is largely a result of the establishment of these 2 laparoscopic procedures. The feasibility and safety of this procedure have been reported since 2006, and it was introduced into clinical practice on the basis of a small case series. Leung et al reported a case of simultaneous laparoscopic resection of rectal cancer and liver metastasis with acceptable operative time and blood loss resulting in early postoperative recovery.29 Geiger et al presented a successful case of a 60-year-old male with sigmoid colon carcinoma and synchronous solitary CRCLM treated by simultaneous resection of the sigmoid colon and left lateral liver segment.30 Bretagnol et al reported their preliminary experience with 3 patients who underwent a 1-step totally laparoscopic resection of both colorectal and hepatic cancers, and stated that this procedure was feasible with low morbidity and a short hospital stay.31 Kim et al demonstrated the feasibility of this technique with considerable safety and effectiveness in what is so far the largest series of 10 cases.32 Patriti reported successful cases of 7 patients undergoing 1-stage laparoscopic or robot-assisted resection with no postoperative morbidity.33 Akiyoshi et al suggested the safety and feasibility of this procedure in selected patients, demonstrating no major morbidity in 3 laparoscopy-assisted liver resections concomitantly performed with laparoscopic colorectal resections.34 Huh et al reported 7 patients undergoing laparoscopic colorectal resection and simultaneous R0 resection for CRCLM with postoperative short-term advantages.35

Advantages of this approach include a shortened recovery period after radical resection, making it possible to induce adjuvant chemotherapy at an earlier stage. In cases of stage IV CRC with synchronous CRCLM, early induction of adjuvant chemotherapy would be mandatory36; in this regard, the current approach would have substantial advantages. Actually, in our series, postoperative hospital stay was less than 2 weeks in 5 of 7 cases, and we could start adjuvant chemotherapy on median postoperative day 46, which was a shorter wait than that reported for open hepatectomy simultaneously performed with laparoscopic colorectal resection at our institute (data not shown).

Other plausible advantages of this approach include savings in medical expenditures regarding laparoscopic devices, in that the same devices can be used for both colorectal and hepatic resection. Total cost reduction would not be ignorable because the second hospitalization for hepatectomy becomes unnecessary by virtue of this applied procedure. In addition, an earlier return to usual function as a result of more rapid recovery would benefit patients economically. One of the ancillary advantages is reduced adhesion associated with this approach, especially in cases in which subsequent re-hepatectomy is anticipated.37 Using the small wound created for colorectal anastomosis as the route for removal of a liver specimen would facilitate the procedure.

However, many obstacles still remain with respect to technical aspects. Although previous reports have suggested that laparoscopic hepatectomy offers the advantage of decreased intraoperative blood loss, adequate control of blood loss especially during hepatic parenchymal transection still represents the key point of this procedure. In our series, by using multidevices during the transection procedure, blood loss during the whole colorectal and hepatic resection could be decreased to less than 100 mL in 4 of 7 cases. In terms of secure hemostasis, the HALS technique would provide the advantage of facilitating this process more safely.38,39

In this series, the Pringle maneuver was not applied during hepatectomy. The potential risk of this maneuver is a topic of controversy,40 although enhancing the risk of anastomotic leakage caused by intestinal edema is theoretically plausible. Actually, in cases of low anterior rectal resection, the mortality rate has been high as the result of anastomotic leakage.41 In our series, because bleeding during hepatic transection was relatively well controlled, inflow occlusion was not required; thus median intraoperative blood loss was 206 mL and no anastomotic leakage occurred. In this context, more complicated cases, such as larger tumors, multiple tumors, or deeply located tumors—which we did not include as indications in this series—would be forthcoming challenges.

Lack of bimanual palpation examination to exclude occult hepatic metastatic lesions is one of the unavoidable issues associated with this procedure. HALS may resolve this problem in part, but its usefulness is limited in most cases. Practically, thorough and vigorous examination using intraoperative laparoscopic US would be the only way to address the apparent disadvantage of this procedure so far.42 Moreover, US observation prior to hepatectomy would avoid unnecessary operation thereafter, because a 10% to 25% detective rate has been reported with the use of intraoperative US in cases in which preoperative CT failed to detect the presence of occult CRCLM.43–47

The other notable disadvantage of this procedure compared with open surgery is the theoretical difficulty of obtaining a negative hepatic margin, although the problem is not unique to this simultaneous procedure. In particular, with the use of pure laparoscopic technique, deliberate confirmation of surgical margins of the liver would be required with vigorous use of intraoperative US.

Although satisfying short-term results have been reported, information regarding long-term outcomes is scarce to date. In our study, although the observation period was limited, the recurrence rate was comparable with those in cases of open hepatectomy (data not shown). In addition, local recurrence at the cut surface of the liver was not observed. Because randomized study on open versus laparoscopic surgery was not performed, and because the sample size in this study was small, statistical analysis was not available; however, when an appropriate indication is held, this approach would not present substantial risk of enhancing the recurrence rate. Further study, including a randomized controlled study, will be needed to clarify this matter.

The optimal indication for this procedure needs to be established. In the current study, we limited the indication for simultaneous hepatectomy to those patients with CRCLM of a solitary tumor, smaller than 5 cm, and relatively peripheral and superficial in location (i.e., segments 2–6), because these are considered universally acceptable criteria for safe laparoscopic hepatectomy to date.12 Further expansion of these criteria to more challenging CRCLM cases is anticipated in accordance with accumulation of experience with laparoscopic hepatectomy; nonetheless, care should be taken to avoid compromising the simultaneously resected and anastomosed colon or rectum, as well as the patient per se. In this context, laparoscopic major hepatectomy, defined as resection of 3 or more Couinaud segments (which would often necessitate the Pringle maneuver), and hepatectomy for liver in the parenchyma (which is occasionally compromised because of the effects of neoadjuvant chemotherapy)48 need to be adequately and deliberately addressed as indications for this procedure.

Although simultaneous resection of CRC and initially resectable CRCLM has been advocated because of the benefits of avoiding a second operation and reducing morbidity, whether simultaneous resection for synchronous metastasis is superior to a staged operation after a certain interval as a “waiting time” remains a topic of controversy.7,49–53 Given that liver metastatic lesion(s) would occasionally emerge or would be detected on follow-up despite their not appearing at the first presentation of metastasis, a laparoscopic approach would offer advantages to some extent by reducing operative stress and postoperative adhesion, should re-hepatectomy become necessary. With regard to multiple metastases, which were excluded from the indication in our current protocol, further study is necessary to determine the appropriateness of including this status as an indication for the procedure, taking into consideration that both recurrence rate and technical difficulty would be aggravated by these conditions.8,54

In conclusion, for selected patients with CRC and synchronous CRCLM, simultaneous laparoscopic resection would provide good outcomes in terms of early postoperative recovery without enhancing surgical risk, as well as acceptable long-term outcomes, including reducing recurrent disease.