Laparoscopic Hepatectomy for Liver Metastases from Colorectal Cancer: A Meta-analysis

Abstract

Background:

Liver resection can improve long-term survival for liver metastases from colorectal cancer. Laparoscopic hepatectomy is gaining increasing applications in colorectal liver metastases. We conducted a meta-analysis to investigate the safety, feasibility, and efficacy of laparoscopic liver resection compared with open hepatectomy for patients with colorectal liver metastases.

Materials and Methods:

We performed both database and manual searching for comparative studies published before June 2013 without language or region restriction. Outcomes of interest consisted of perioperative outcomes and oncologic outcomes.

Results:

Seven observational studies including 624 patients (241 in the laparoscopic group, 383 in the open group) were included. No randomized controlled trials were available. Pooled long-term oncologic outcomes of overall survival (hazard ratio=0.844; 95% confidence interval [CI] 0.412, 1.730; P=.644; I²=80.6%) and disease-free survival (hazard ratio=1.234; 95% CI 0.652, 2.333; P=.518; I²=79.6%) were similar in both groups. Subgroup analyses of studies with high quality and homogeneity confirmed the above outcomes. However, a lower incidence of R1 resection was observed in the laparoscopic group (relative risk [RR]=0.357; 95% CI 0.180, 0.708; P=.003; I²=0.0%) than in the open group. As for perioperative outcomes, laparoscopic hepatectomy presented a lower occurrence of postoperative complications (RR=0.647; 95% CI 0.477, 0.877; P=.005; I²=0.0%) and similar mortality (RR=0.625; 95% CI 0.12, 3.25; P=.576; I²=0.0%); less blood loss and less need for transfusion were also found in laparoscopic patients, whereas comparable operative time and length of hospital stay were required in the two groups.

Conclusions:

Laparoscopic hepatectomy is a safe procedure for colorectal liver metastases with long-term survival comparable to that of open hepatectomy. More prospective studies with adequate subgroup analyses are awaited to construct defined criteria for patient selection. Future randomized controlled trials are needed to eliminate potential selection bias and to confirm this conclusion.

Introduction

Since first reported by Gagner et al.¹ in 1992, laparoscopic hepatectomy (LH) has been accepted and applied in the fields of hepatic surgery. Although this minimally invasive approach, due to technical intricacy and oncologic concerns, has not gained routine and widespread applications like laparoscopic cholecystectomy or appendectomy, its feasibility, reproducibility, and efficacy are confirmed by an increasing number of hepatobiliary surgeons.^2–7 During the last two decades, LH has been used to handle both benign lesions and liver malignancies, showing benefits in comparison with open hepatectomy (OH).^8–12 The advance of LH also provides a new option for surgeons in the treatment of patients with colorectal cancer (CRC) liver metastases (CRCLM).

CRC remains the second of the most common causes of cancer-related death in Western Europe and America.^13,14 Approximately 50% of these patients have CRCLM during the natural course of disease, with 15%–25% having synchronous liver metastases detected at the initial diagnosis, with an additional 20%–30% developing metastases usually within 3 years.^15–17 Liver resection is recognized as the standard care for CRCLM and has been proved to improve long-term survival and provide potentially curative therapy.^18–20 With the gradually increasing use of laparoscopic technique in abdominal surgery, LH is now becoming a favorable alternative to OH for CRCLM patients. Studies comparing these two approaches are conducted by surgeons from specialized centers. However, no accordance on the exact benefits of either has been reached until today. Considerations and controversies lie in the selection of patients, resection types, and short-term and oncologic results.^21–30 Owing to the lack of a recognized view, options for a resectable CRCLM between LH and OH might mainly depend on the doctor's preference and discretion, rather than literature conclusions from any single study. An assessment of this issue may provide reliable public health and clinical implications. Thus we performed this meta-analysis, evaluating all published evidence including controlled trials and observational studies, in order to determine which of the two surgical approaches is preferable for CRCLM patients in both short-term and long-term results.

Materials and Methods

This meta-analysis report was conducted according to the Meta-analysis of Observational Studies in Epidemiology recommendations.³¹ Two reviewers (L.-X.L. and Z.-Y.Y.) independently accomplished the work of literature search, study selection, data extraction, and quality assessment. Disagreements were solved by rechecking and discussion.

Search strategy

Electronic databases including the Cochrane Central Register of Controlled Trials (CENTRAL), PubMed, and Embase were systemically searched for all related studies published before June 2013, without region or language restriction. The key words, in the form of both Medical Subject Headings terms and natural language terms, consisted of three subjects: “laparoscopic surgery,” “colorectal neoplasm,” and “liver metastasis.” Truncated terms with the wildcard “*” were used to make sure the search was comprehensive. The database searching was supplemented with manual searching for reference lists of obtained articles, unpublished studies, and conference abstracts. We also contacted the authors for full-text or original data of their investigations if possible.

Study selection

The eligible articles met the following criteria: (1) comparative study involving LH and OH groups for CRCLM; (2) hepatectomy without simultaneous resection of primary CRC; (3) with full-text available; (4) at least one of the perioperative or oncologic outcomes were described; and (5) if two or more reports shared the same or overlapping population and data, only the most recent, complete, or high-quality article was included. Review articles, nonhuman investigations, case reports, and letters were excluded.

Data extraction

Basic information extracted from each study included first author, country, year of publication, study duration, study type, sample size, patients age, sex ratio, and matching design of the two groups. Outcomes of interest were (1) perioperative results, including operative time, estimated blood loss, need for transfusion, length of hospital stay, postoperative complication, and mortality, and (2) oncologic results, including incidence of R1 resection and long-term outcomes of survival.

Quality assessment

Quality of all included observational studies was assessed by the Newcastle–Ottawa Scale (NOS), which was designed specially for observational studies.³² The scale focuses on three separate sections of a case control or cohort study, and the number of stars represents the assessment score. The maximal score of NOS is 9 stars: 4 stars for the selection process, 2 stars for comparability, and 3 stars for exposure/outcome. We additionally investigated the information of matching items between the two groups and details in the follow-up strategy.

Statistical analysis

We used the Stata version 12.0 software package (StataCorp, College Station, TX) to conduct this meta-analysis. Relative risk (RR) and weighted mean difference (WMD) with 95% confidence interval (CI) were used as the measurement of dichotomous and continuous variables, respectively. Medians with ranges or interquartile ranges were converted into means with standard deviations using the methods introduced by Hozo et al.³³ and the Cochrane Handbook for Systemic Review of Interventions.³⁴ Long-term outcomes were analyzed by hazard ratio (HR) extracted and incorporated from time-to-event data in each study according to the technique described by Tierney et al.³⁵ A value of RR or HR of less than 1 represented a beneficial outcome favoring the LH group. P values <.05 indicated statistical significance. Heterogeneity was quantified by the I² statistic. A study with an I² less than 40% was considered to have no evidence of heterogeneity, and then the fixed-effects model was applied to pool the results; otherwise, the random-effects model was used. Additionally, in the case of heterogeneity, we performed sensitivity analysis to investigate possible explanation and to test the robustness of pooled results as well. Subgroup analyses were also conducted when clinical or methodological heterogeneity might exist. Potential publication bias was screened by funnel plots and Begg rank correction.³⁶

Results

Characteristics of included studies

Figure 1 illustrates the process of study screening, through which, in total, 624 patients (241 in the LH group, 383 in the OH group) from seven comparative studies were finally enrolled. No randomized controlled trials but seven observational studies published from 2002 to 2013 were included after the literature search.^{21–23,25,27–29} In the investigation of Cannon et al.,²⁵ two propensity-matched groups were constructed, and we extracted the data of the “inclusive” cohort instead of the “restricted” cohort because the latter was subjected to greater selection bias as stated in the article. Table 1 lists the characteristics of each included study. Six of the seven studies were from European and American countries, and one was from Japan. There were three retrospective and four prospective studies, and three of the four prospective investigations were conducted with defined-group matching design (Table 2). Means of patients' age ranged from 54 to 68 years old.

FIG. 1.

Flowchart of study selection.

Table 1.

Description of the Characteristics of the Included Studies

				Patients		Gender (male/female)		Age (years) (mean/SD)
Reference (year)	Country	Study duration	Study type	LH	OH	LH	OH	LH	OH
Abu Hilal et al.²³ (2010)	United Kingdom	2004–2009	P	50	85	28/22	55/30	66/12.60	67/10.37
Cannon et al.²⁵ (2012)	United States	1995–2010	RM	35	140	—	—	62/10	62/11
Castaing et al.²² (2009)	France	1997–2007	PM	60	60	37/23	37/23	62/11	62/11
Guerron et al.²⁸ (2013)	United States	2006–2012	PM	40	40	21/19	15/25	66.2/12.02	62.2/11.38
Inoue et al.²⁹ (2013)	Japan	2008–2012	R	23	24	11/12	13/11	66.10/9.6	68/9.5
Mala et al.²¹ (2002)	Norway	1998–2001	R	13	14	9/4	10/4	66/5.32	54/14.72
Topal et al.²⁷ (2012)	Belgium	2002–2008	PM	20	20	10/10	8/12	57.6/—	66/—

A dash indicates no data are available.

P, prospective; PM, prospective, matched; R, retrospective; RM, retrospective, matched; SD, standard deviation.

Table 2.

Description of Quality Assessment

	NOS score
Reference (year)	Selection	Comparability	Outcome	Follow-up information	Matching ^a
Abu Hilal et al.²³ (2010)	^***	^*	^**	Details of follow-up strategy and missing data were not available.	9, 12
Cannon et al.²⁵ (2012)	^***	^**	^**	Details of follow-up strategy and missing data were not available.	1, 4–6, 12
Castaing et al.²² (2009)	^****	^**	^**	Follow-up consisted of clinical assessments, imaging (ultrasonography, CT, and/or PET), and monitoring of CEA. Patients were evaluated every 3–4 months for the first 3 postoperative years and every 6 months thereafter.	1, 2, 4–9, 12, 13
Guerron et al.²⁸ (2013)	^***	^*	^**	Follow-up consisted of CEA levels and CT scans of the chest, abdomen, and pelvis biannually after liver resection.	5, 12
Inoue et al.²⁹ (2013)	^**	^*	^***	Follow-up was based on regular outpatient clinic visits every 3 months and information obtained from medical records, correspondence, and telephone contact.	3, 5
Mala et al.²¹ (2002)	^***	^*	^**	Follow-up consisted of liver ultrasonography, CEA, and clinical examination.	12
Topal et al.²⁷ (2012)	^***	^**	^**	Follow-up consisted of CEA, contrast-enhanced CT and/or MRI of the abdomen and thorax, or PET/CT every 3–4 months.	1–4, 7, 10–13

Matching items: (1) age; (2) gender; (3) American Society of Anesthesiologists score; (4) Fong's Clinical Risk Score; (5) size of colorectal cancer liver metastases; (6) number of colorectal cancer liver metastases; (7) location of colorectal cancer liver metastases; (8) location of primary colorectal cancer; (9) presence of extrahepatic disease; (10) previous liver resection; (11) previous local ablative therapy; (12) period of surgery; and (13) pre- and postoperative chemotherapy.

CEA, carcinoembryonic antigen; CT, computed tomography; MRI, magnetic resonance imaging; NOS, Newcastle–Ottawa Scale; PET, positron emission tomography.

Quality assessment

Table 2 shows the detailed results of quality assessment. All of the seven articles in this meta-analysis were observational studies. No randomized controlled trial was available. NOS assessing resulted in similar quality among the seven studies, with the scores ranging from 6 stars to 8 stars. Details about follow-up strategy were described in five articles. However, the information of missing data was not mentioned in most included studies. Among all of the articles, six of the seven studies enrolled more than 20 patients in both the LH and OH groups. To detect any possible selection bias in patient allocation, we further evaluated the matching design of each study between the LH group and the OH group on 13 items. Three studies performed relatively rigorous matching, whereas the other four might have possible bias in allocation, including age, period of surgery, size, number, and location of CRCLM, previous liver resection, and others, which might have influences on the final research outcomes.

Perioperative outcomes

Characteristics and surgical procedures of the available patients were assessed as shown in Supplementary Table S1 (Supplementary Data are available online at www.liebertonline.com/lap). The maximal size of CRCLM in the LH group was nearly 0.5 cm smaller than those in the OH group (95% CI −0.846, −0.102; P=.012; I²=23.2%). No statistical difference was detected in number of CRCLM, presence of multiple CRCLM or bilobar CRCLM, serum carcinoembryonic antigen level, and rate of anatomic resection between the two groups.

LH was a relatively safe procedure for patients with CRCLM

Postoperative complication morbidity and mortality were the primary parameters for perioperative outcomes. Meta-analysis results illustrated in Figure 2A implied a lower incidence of postoperative complications in the LH group than in the OH group (pooled RR=0.647; 95% CI 0.477, 0.877; P=.005; I²=0.0%). As for postoperative mortality, data in Figure 2B showed no significant difference between the two groups (RR=0.625; 95% CI 0.12, 3.25; P=.576; I²=0.0%).

FIG. 2.

Forest plots for (A) postoperative complication morbidity and (B) mortality. CI, confidence interval; RR, relative risk.

Secondary outcomes

Table 3 lists the secondary outcomes of postoperative parameters. Pooled estimate of blood loss in the LH group was approximately 189 mL less than in the OH group (WMD=–188.858; 95% CI −294.033,−83.682; P<.001; I²=39.1%). Transfusion for the LH group was also needed less blood (RR=0.436; 95% CI 0.267, 0.711; P=.001; I²=0.0%). No statistical significance was observed in the difference of operative time (WMD=3.05; 95% CI −14.394, 20.494; P=.732; I²=2.4%) or length of hospital stay (WMD=–2.641; 95% CI −5.588, 0.306; P=.079; I²=86.9%) between the two groups.

Table 3.

Meta-analysis Results of Secondary Perioperative Outcomes

		Number of patients		Overall effect			Heterogeneity
Outcome of interests	Number of studies	LH	OH	WMD/RR	95% CI	P value	I²	P value
Blood loss	6	181	323	−188.858	−294.033, −83.682	<.001	39.1%	.145
Need for transfusion	4	158	264	0.44	0.267, 0.711	.001	0.0%	.635
Operative time	6	206	243	3.05	−14.394, 20.494	.732	2.4%	.401
Length of hospital stay	6	206	243	−2.641	−5.588, 0.306	.079	86.9%	<.001

CI, confidence interval; LH, laparoscopic hepatectomy; OH, open hepatectomy; RR, relative risk; WMD, weighted mean difference.

Oncologic outcomes

LH and OH shared similar long-term survival outcomes

In total, 550 patients from five included studies were enrolled. Both overall survival (OS) and disease-free survival (DFS) of these patients were analyzed (Fig. 3). The difference in OS between LH and OH patients was not statistically significant according to the pooled HR (HR=0.844; 95% CI 0.412, 1.730; P=.644; I²=80.6%). Meta-analysis for DFS also revealed a similar result between the LH and OH groups (HR=1.234; 95% CI 0.652, 2.333; P=.518; I²=79.6%). Owing to the relatively high heterogeneity of both OS and DFS outcomes, subgroup analyses were conducted as described in the following section. On the other hand, pooled RR showed a lower incidence of R1 resection in the LH group than in the OH group (RR=0.357; 95% CI 0.180, 0.708; P=.003; I²=0.0%) as shown in Figure 4.

FIG. 3.

Forest plots for (A) overall survival and (B) disease-free survival. CI, confidence interval; HR, hazard ratio.

FIG. 4.

Forest plots for meta-analysis of R1 resection. CI, confidence interval; RR, relative risk.

Subgroup, sensitivity analyses, and publication bias

To explore the potential source of heterogeneity revealed in pooled HRs for OS and DFS, we performed subgroup analyses based on the possible discrepancy caused by clinical or methodological factors. Studies included in long-term survival evaluation were divided into two subgroups on the basis of study type and quality. In other words, these studies with prospective type and well-matched design were picked to form a high-quality subgroup, whereas the left ones were assigned to a low-quality subgroup. As shown in Figure 5, the high-quality subgroup had prominent homogeneity in both OS and DFS outcomes (both I²=0.0%), and the pooled HRs also did not show a significant difference between the LH and OH groups in either OS (HR=0.851; 95% CI 0.568, 1.275; P=.434; I²=0.0%) or DFS (HR=0.913; 95% CI 0.627, 1.331; P=.637; I²=0.0%) patients, which were in accordance with the above analyses. Additionally, sensitivity analyses were consistent with the above results, indicating the robustness of this study. Begg's test and funnel plots proved no evidence of publication bias.

FIG. 5.

Subgroup analyses for (A) overall survival and (B) disease-free survival. CI, confidence interval; HR, hazard ratio.

Discussion

In this meta-analysis, we demonstrated that LH in CRCLM patients was associated with lower postoperative morbidity and similar mortality compared with OH. In the past two decades, staging laparoscopy and laparoscopic ultrasonography in preoperative assessment and patient selection for CRCLM have been reported in several studies, and their advantages have already been recognized.^37–39 Application of laparoscopic surgery for CRCLM is now gaining more attention. Because of its technical complexity and oncologic concerns, LH experienced a slower development in wide application than other abdominal surgeries. Although an increasing number of comparative investigations has emerged, confirming the feasibility and safety of LH,^8–12 the role of laparoscopic liver resection in CRCLM patients is still lacking common recognition.

In the first half of the last decade, literature reviews have pointed out that (1) laparoscopic liver surgery for CRCLM was an advanced procedure that should be performed by a surgeon with expertise, (2) the decision to conduct a major LH should be prudent, (3) control of bleeding is a great challenge, and (4) oncologic integrity remained unproven.⁴⁰ However, with more comparative investigations being conducted following the worldwide trend in laparoscopic operation, surgeons began to hold different views on LH for CRCLM patients. The feasibility of laparoscopic major hepatectomies for CRCLM has been proved in the reports of Topal et al.,²⁷ Koffron et al.,⁹ and Abu Hilal et al.²³ Comparable mortality of LH and OH was also demonstrated by previous studies. Postoperative complications were found with a lower incidence after LH in the investigation of Cannon et al.,²⁵ whereas other studies showed similar morbidity. According to the studies utilized in this meta-analysis, common complications after operation for CRCLM included bleeding, liver insufficiency, pulmonary infection, cardiac-related complication, urinary infection, and wound-related complication, some of which were not fatal—this might explain the difference between postoperative morbidity and mortality.

Concerning the indirect and complicated manipulation, LH for CRCLM was assumed to handle the difficulties in bleeding control and possibly longer operative duration. However, less blood loss during LH than during OH was reported by Guerron et al.,²⁸ Inoue et al.,²⁹ and Cannon et al.,²⁵ and barely any comparative studies have shown an opposite results. Operative time recorded in the existing investigation showed a similarity between the two procedures. As for hospital stay, opinions from current studies differed between a beneficial or comparable role of LH.^21,22,26,29 In the present meta-analysis, for LH patients, less operative bleeding was observed; less need for transfusion and similar length of hospital stay and operative time were required compared with OH patients. These analyses implied that laparoscopic liver resection was a safe and feasible alternative to open surgery.

Additionally, we conducted meta-analysis of patients' characteristics and surgical procedures, in order to assess the comparability of the included patients between the two groups (Supplementary Table S1). The number of CRCLM, the presence of multiple or bilobar CRCLM, the serum carcinoembryonic antigen level, and the rate of anatomic resection were found to be comparable. One exception was the 0.5 cm smaller size of maximal CRCLM in the LH group. Thus, it still should be mentioned that, owing to the source material of our analysis (with observational studies only), we could not exclude the bias that surgeons might tend to select patients with clear-cut resectable disease for LH.

In terms of oncologic outcomes, we did not detect significant difference regarding either OS and DFS. Subgroup analysis based on high-quality studies with a better-matched design validated our finding. Although the doctors of today have far more choices in handling CRCLM, such as ablative therapy, cryotherapy, perioperative chemotherapy, and hepatic artery infusion, liver resection remains the standard of care and potentially curative therapy, providing obvious improvement in long-term survival.^18–20 Previous studies on patient series undergoing LH for CRCLM have also shown favorable outcomes in long-term outcomes.^41,42 And, based on our analyses of existing comparative investigations, a conclusion could be draw that LH was as efficacious a procedure as OH for selected CRCLM patients.

Long-term survival of CRCLM patients after liver surgery was considered to be influenced by multiple factors. Pulitano et al.⁴³ declared there were four independent negative prognostic factors for survival: more than three metastases, a positive surgical margin, tumor size of >5 cm, and a clinical risk score of >2. A 10-year follow-up by Viganò et al.⁴⁴ also defined five independent negative prognostic factors: male sex, synchronous metastases, three metastases, metastatic infiltration of nearby structures, and postoperative morbidity. Other factors mentioned were lymph node metastases of primary tumor, the presence of an extrahepatic tumor, and neoadjuvant and adjuvant chemotherapy.⁴⁵

An R0 resection was thought to be less achievable in a laparoscopic approach because of the limitation in direct judgment of tumor margins during the operation. However, our pooled estimate revealed a higher incidence of R0 resection in LH. Surgeons might be more discreet and conservative when determining the resection margin, which could be a possible explanation. Nevertheless, another explanation might be the potential bias in patient allocation. Owing to the observational nature of existing studies, selection bias favoring the LH group could not be eliminated in this analysis.

It is noteworthy that, although the occurrence of R1 resection was found to be prominently lower in LH patients, the long-term survival was similar in both groups. This result opposes the finding of most existing literature that R1 resection was associated with increased risk of recurrence or poorer survival after liver resection for CRCLM.^43,45–52 On multivariate analyses, some of those studies confirmed R1 resection as an independent predictor of poorer survival,^43,49–51 whereas others did not.^45,48,52,53 Despite the surgical margin, predictors of increased long-term survival by multivariate analyses included (1) serum carcinoembryonic antigen level, (2) positive node of primary tumor, (3) number, size, or distribution of CRCLM, (4) disease-free interval from primary tumor, and (5) extrahepatic metastases, etc. There were also a few reports that presented a similar survival after R1 and R0 resection of CRCLM.^54–56

The correlation between oncologic outcome and surgical margin width also remains controversial, especially on the issue of the “1 cm rule.”^57,58 Are et al.⁵⁹ discovered that a margin width of >1 cm was an independent predictor of survival, and it is interesting that a margin width of <1 mm (which was defined as R1 resection or positive margin by most studies) had a similar effect compared with a margin width of 1–9 mm. The study of Inoue et al.⁵⁴ then presented that patients with a margin width of <1 mm (R1 resection), 1–9 mm, and >1 cm experienced comparable survival after hepatectomy for CRCLM.

In our meta-analysis, the discrepancy between R1 resection and long-term survival might in a way verify that multiple factors rather than the margin status only had effects on the long-term outcomes of CRCLM patients after liver resection. Potential indicators such as disease-free interval or extrahepatic metastases were not available from the included studies, which might also weaken the reliability of our results.

Now that LH could be considered safe and efficient, criteria for patient selection for the laparoscopic approach and choosing the surgical type are needed. According to the current reports of CRCLM, laparoscopic resection for all eight liver segments except segment I has been performed. Patients with small tumors located in the left lateral segments of the liver were considered most suitable for a laparoscopic approach.^60–62 The study of DeMatteo et al.⁶³ indicated that anatomic segmental resection was superior to wedge resection for CRCLM with improved tumor clearance and survival. However, in this report we failed to conduct a quantitative analysis on this issue because individual patient data or subgroup data of both LH and OH based on different perioperative parameters were not available.

The main limitation of this review lies in the lack of randomized controlled trials. Although some of the observational studies performed relatively rigorous matching, risk of selection bias still existed, for the allocation of patients to either LH or OH groups was mainly based on surgeons' preference and experiences. Within all the included observational studies, three of them were retrospective, which might raise difficulties in collecting complete data for outcomes of interest. The volume of included patients was relatively small. Handling of missing data during postoperative follow-up was not mentioned in most articles. Diverse data forms appeared in the included studies. Reliability of the conclusion could be reduced owing to these above points.

Conclusions

To sum up, according to this present meta-analysis, laparoscopic liver resection is a safe procedure for CRCLM patients and has outcomes of long-term survival comparable to those with OH. More well-matched prospective studies with adequate subgroup analyses are awaited to construct defined criteria for patient selection. Future randomized controlled trials are needed to confirm this conclusion.

Footnotes

Acknowledgments

The authors thank Yong Zeng, Hong Wu, and Ji-Wei Huang for scientific advice.

Disclosure Statement

No competing financial interests exist.

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