Laparoscopic Colectomy Versus Open Colectomy for Treatment of Transverse Colon Cancer: A Systematic Review and Meta-Analysis

Abstract

Background:

The surgical management of transverse colon cancer (TCC) is still not standardized. The aim of this meta-analysis was to evaluate the effect of laparoscopic colectomy (LC) for treatment of TCC in terms of short-term and long-term outcomes compared with open colectomy.

Method:

A systematic literature search with no limits was performed in PubMed and Embase. The last search was performed on September 15, 2016. The short-term outcomes included intraoperative outcomes, postoperative outcomes, and oncological surgical quality. The long-term outcomes included overall survival (OS) and disease-free survival (DFS).

Results:

Thirteen articles and one conference abstract published between 2010 and 2016 with a total of 1728 patients were enrolled in this meta-analysis. LC was associated with significant less estimated blood loss, fewer total postoperative complications, and shorter time to first flatus, time to liquid diet, length of hospital stay, and length of postoperative hospital stay. However, longer operative time was needed in LC. There was no statistically significant difference between the groups concerning the intraoperative complications, mortality, ileus, anastomotic leakage, bleeding, wound infection, abdominal infection, lymph nodes harvested, proximal resection margin, distal resection margin, OS, or DFS.

Conclusion:

Our meta-analysis suggests that LC is a safe and feasible technique for TCC associated with less estimated blood loss, fewer total postoperative complications, quicker recovery of intestinal function, shorter length of hospital stay, and equivalent long-term outcomes. Furthermore, a large-scaled, prospective randomized controlled study is warranted to verify those results.

Introduction

Laparoscopic colectomy (LC) was first described in 1991.¹ Since then, LC has been widely accepted for treatment of colorectal disease, and a trend of increasing usage of LC for colon cancer has been witnessed in the past 10 years.² Several large, multicenter, prospective randomized controlled trials (RCTs) have demonstrated that LC for colon cancer has excellent short-term outcomes such as less blood loss, quicker recovery of bowel function, shorter hospital stay, reduced postoperative pain and better cosmesis, and equivalent long-term oncologic outcomes compared to open colectomy (OC).^3–7 In addition, those results have been also verified by Cochrane database reviews.^8,9 However, the role of LC in the treatment of transverse colon cancer (TCC) is still controversial because TCC was excluded from those RCTs, presumably due to the following reasons.

First, TCC has a relatively low incidence, accounting 10% of all colon cancers, which makes surgeons have limited experience to do LC for TCC.^10,11 Second, the type of surgical procedure and the extent of lymph node dissection vary according to the cancer's location. Third, it is difficult to perform lymphadenectomy around the middle colic artery by LC.^12,13 Fourth, the mobilization of the transverse colon, which is always needed to perform anastomosis without tension, is usually technically difficult due to its flaccidity and mobility. Fifth, many important structures are around transverse colon, such as pancreas, duodenum, spleen, and superior mesenteric vein.¹⁴

In recent years, with accumulating experience of performing LC and continued developments in laparoscopic instruments, some experienced surgeons attempt to perform LC for TCC. Several studies have compared LC and OC for treatment of TCC and concluded that LC is a safe and feasible procedure for treatment of TCC.^15–19 But the results of these studies should be interpreted carefully because none of them was RCT, and the sample size of these studies was small. Although there is a meta-analysis comparing LC and OC for TCC, it only included six studies (245 by LC and 199 by OC), and it did not analyze the survival outcomes.²⁰ Herein, we conducted this meta-analysis to evaluate the effect of LC for treatment of TCC in terms of short-term and long-term outcomes compared with OC.

Materials and Methods

This meta-analysis was performed according to the recommendations of the preferred items for systematic reviews and meta-analyses (PRISMA) statement.²¹ In this study, TCC was defined as tumor located between the hepatic and splenic flexures.

Study selection

A systematic literature search with no limits was performed in PubMed and Embase. The search terms were “laparoscopies, laparoscopic, laparoscopy, or laparoscopic-assisted” and “transverse colon cancers, transverse colon cancer, transverse colon carcinomas, or transverse colon carcinoma.” The last search was performed on September 15, 2016. Besides, to include additional potentially eligible studies, a manual search of references of articles and reviews was also performed.

Inclusion and exclusion criteria

The inclusion criteria of this meta-analysis were as follows: (1) comparative studies (LC versus OC), (2) studies with each group sample size more than 10, and (3) short-term or long-term outcomes were reported. The exclusion criteria were as follows: (1) noncomparative studies, (2) mixed series colectomy, TCC data not extractable, (3) study with sample size of LC or OC less than 10, and (4) studies without short-term or long-term outcomes. If studies included overlap patients of same center, study with larger sample size was enrolled.

Data extraction

Two authors (Q.B.W. and M.T.W.) reviewed all identified studies independently. A third reviewer (Z.Q.W.) was needed to resolve disagreements, which existed between those two authors. The following items were extracted from each study: first author's name, year of publication, country, sample size of each arm, gender (male), age, body mass index (BMI), previous abdominal surgery, surgical procedures, stage, and short-term and long-term outcomes.

Short-term and long-term outcomes

Intraoperative outcomes: operative time, estimated blood loss, intraoperative complications, and conversion to laparotomy.

Postoperative outcomes: total postoperative complications, mortality, time to first flatus, time to liquid diet, length of hospital stay, length of postoperative hospital stay, ileus, anastomotic leakage, bleeding, wound infection, and abdominal infection.

Oncological surgical quality and long-term outcomes: tumor size, lymph nodes harvested, proximal resection margin, distal resection margin, and the hazard ratio (HR) with 95% confidence intervals (CI) of overall survival (OS) and disease-free survival (DFS).

Quality assessment

The revised and modified grading system of the Scottish Intercollegiate Guidelines Network was used to assess the methodological quality of the enrolled retrospective studies: total score 20, poor quality < 8 scores, fair quality 8–14 scores, and good quality >14 scores.²²

Statistical analysis

Review Manager version 5.3 (The Cochrane Collaboration, Software Update, Oxford) was used for data analyses. P value < .05 was considered statistically significant. Weighted mean difference (WMD) was calculated for the continuous outcomes, while pooled odds ratios (OR) or risk ratios (RR) were calculated for the dichotomous outcomes. For continuous outcomes, if the study did not provide means and standard deviations (SDs), the means and SDs were calculated from means and range values or medians and range values using methods described by Hozo et al.²³ Benefit in OS and DFS from LC to OC was assessed using HR and its 95% CI. HRs with 95% CIs were directly extracted from studies. If the studies did not report HRs or 95% CI, we used software DigitizeIt to obtain the needed data from published Kaplan–Meier curves according to the method described by Parmar et al.²⁴ Then, we used those obtained data to calculate HRs and its 95% CIs using the spreadsheet developed by Tierney.²⁵ Heterogeneity was calculated by Chi-squared test and Higgins I-squared test. We considered that high heterogeneity existed if the value of P < .05 and I² > 50%. If there existed high heterogeneity, a random-effects model was applied. Otherwise, a fixed-effects model was applied. If high heterogeneity existed, the sensitivity analysis was conducted by removing one study each time to decrease heterogeneity. Begg's funnel plot was used to evaluate publication bias.

Results

A PRISMA flowchart of the literature search is shown in Figure 1. After duplication, a total of 266 studies existed. After the initial review, 66 relevant studies were further evaluated. Of these studies, 52 reports were excluded due to following reasons: 23 studies were conference abstract without sufficient data; 1 study included mixed series colectomy, TCC data cannot be extracted; 3 studies were review or meta-analysis; 16 studies were not case–control study; 2 studies were case report; and 7 studies were duplicate study from same center which had overlap data. Thus, 13 articles^{15–19,26–33} and 1 conference abstract³⁴ published between 2010 and 2016 were included in this meta-analysis. All of them were retrospective studies. The characteristics of the included studies are summarized in Table 1. A total of 1728 patients (894 by LC and 834 by OC) were enrolled.

FIG. 1.

PRISMA diagram. PRISMA, preferred items for systematic reviews and meta-analyses.

Table 1.

Characteristics of the Included Studies

			No. of patients		Gender (male)		Age		BMI		PAS
First author	Year	Country	Lap	Open	Lap	Open	Lap	Open	Lap	Open	Lap	Open
Agarwal³³	2015	United States	41	123	25	60	67.0 ± 13.7	68.6 ± 12.7	—	—	—	—
Akiyoshi¹⁹	2010	Japan	53	39	32	21	66.0 ± 13.0	62.0 ± 15.5	22.7 ± 2.8	21.7 ± 3.5	18	13
Fernandez-Cebrian¹⁷	2012	Spain	34	52	21	25	60.3 ± 8.1	62.4 ± 6.8	24.2 ± 6.1	24.1 ± 8.3	—	—
Kim²⁸	2016	Korea	103	123	68	66	65.6 ± 12.1	62.8 ± 14.0	23.5 ± 4.0	23.1 ± 3.1	23	21
Kim³²	2015	Korea	79	23	45	16	65.7 ± 10.0	56.0 ± 15.9	24.0 ± 3.2	22.6 ± 3.1	15	8
Kim¹⁶	2014	Korea	84	47	45	27	62.3 ± 11.6	59.7 ± 13.2	23.6 ± 3.7	22.5 ± 3.3	—	—
Mistrangelo³¹	2015	Italy	66	57	32	33	65.8 ± 13.3	69.8 ± 10.3	24.8 ± 2.3	25.0 ± 2.8	—	—
Naito³⁴	2013	Japan	29	25	—	—	—	—	—	—	—	—
Okuda (1)²⁷	2016	Japan	28	15	14	9	67.0 ± 15.8	67.0 ± 8.3	—	—	—	—
Okuda (2)²⁷	2016	Japan	33	19	15	9	64.0 ± 9.5	63.0 ± 13.0	—	—	—	—
Sheng³⁰	2015	China	59	59	34	32	59.0 ± 8.5	59.25 ± 7.25	—	—	—	—
Storli²⁶	2016	Norway	33	23	11	10	73.0 ± 11.4	68.0 ± 13.3	—	—	—	—
Zeng²⁹	2015	China	156	122	85	67	56.5 ± 14.5	56.8 ± 14.8	24.0 ± 3.5	24.8 ± 4.0	23	20
Zhao¹⁵	2014	China	74	83	43	48	54.0 ± 14.8	55.7 ± 14.8	22.6 ± 2.6	23.3 ± 3.0	11	14
Zmora¹⁸	2010	Israel	22	24	14	12	—	—	—	—	8	5

	Surgical procedures
First author	Lap	Open	Lap	Open
Agarwal³³	—	—	I 16, II 14, III 11	I 47, II 43, III 33
Akiyoshi¹⁹	RH 29, TC 12, LH 12	RH 27, TC 5, LH 7	—	—
Fernandez-Cebrian¹⁷	ERC 15, TC 3, ELC 12, STC 4	ERC 26, TC 6, ELC 8, STC 12	I 5, II 13, III 16	I 7, II 24, III 21
Kim²⁸	RH 72, TC 3, LH 29	RH 85, TC 16, LH 21	I 26, II 45, III 32	I 18, II 58, III 47
Kim³²	RH or ERC 55, TC 3, LH or ELC 20, STC 1	RH or ERC 19, TC 2, LH or ELC 2	II 48, III 31	II 15, III 8
Kim¹⁶	ERC 57, TC 11, ELC 16	ERC 24, TC 10, ELC 11, STC 2	Tis/I 28, II 37, III 19	Tis/I 6, II 21, III 20
Mistrangelo³¹	RH 12, TC 39, LH 15	RH 14, TC 27, LH 16	I 15, II 25, III 18, IV 8	I 9, II 26, III 13, IV 9
Naito³⁴	RH or ERC 8, TC 16, LH 5	RH or ERC 12, TC 9, LH 4	—	—
Okuda (1)²⁷	—	—	II 28	II 15
Okuda (2)²⁷	—	—	III 33	III 19
Sheng³⁰	ERC 26, TC 17, ELC 16	ERC 23, TC 18, ELC 18	I 6, II 26, III 27	I 7, II 28, III 24
Storli²⁶	ERC 20, TC 1, ELC 9, STC 3	ERC 12, TC 7, ELC 4	I 4, II 16, III 13	I 4, II 11, III 8
Zeng²⁹	ERC 88, TC 39, ELC 29	ERC 70, TC 28, ELC 24	I 19, II 77, III 60	I 12, II 58, III 52
Zhao¹⁵	ERC 53, TC 11, ELC 10	ERC 55, TC 12, ELC 16	II 36, III 38	II 45, III 38
Zmora¹⁸	ERC or STC 12, TC 3, LH 7	ERC 20, LH 4	—	—

BMI, body mass index; ERC, extended right colectomy; Lap, laparoscopic colectomy; LH, left hemicolectomy; Open, open colectomy; PAS, previous abdominal surgery; RH, right hemicolectomy; STC, subtotal colectomy; TC, transverse colectomy; —, not reported.

Patient demographics

There was no significant difference between two groups in age (P = .66, WMD = 0.27, 95% CI −0.93 to 1.47, I² = 44%), male gender (P = .39, WMD = 1.09, 95% CI 0.89–1.33, I² = 0%), BMI (P = .58, WMD = 0.18, 95% CI −0.42 to 0.78, I² = 54%), or previous abdominal surgery (P = .98, WMD = 1.00, 95% CI 0.72–1.40, I² = 1%). What's more, surgical procedures and tumor stage were similar in both groups.

Quality of included studies

The scores of methodological quality assessment of the enrolled 13 retrospective articles are shown in Table 2. Of those 13 studies, 11 studies had fair quality (9–13 scores),^{15–17,19,26,28–33} and 2 studies had poor quality (6–7 scores).^18,27

Table 2.

Evaluation of Methodological Qualities of Included Retrospective Studies

Items/first authors	Agarwal ³³	Akiyoshi ¹⁹	Fernandez-Cebrian ¹⁷	Kim ²⁸	Kim ³²	Kim ¹⁶	Mistrangelo ³¹	Okuda ²⁷	Sheng ³⁰	Storli ²⁶	Zeng ²⁹	Zhao ¹⁵	Zmora ¹⁸
Inclusion criteria	1	1	1	1	1	1	1	0	1	1	1	1	1
Exclusion criteria	1	0	1	1	1	1	1	0	1	1	1	1	0
Demographics comparable?	1	1	1	1	0	1	1	1	1	1	1	1	1
Can the number of participating centers be determined?	1	1	1	1	1	1	1	1	1	1	1	1	1
Can the number of surgeons who participated be determined?	0	0	0	0	0	0	1	0	0	0	0	0	0
Can the reader determine where the authors are on the learning curve for the reported procedure?	0	0	0	0	0	0	0	0	0	0	0	0	0
Are diagnostic criteria clearly stated for clinical outcomes if required?	1	1	1	1	1	1	1	0	1	1	1	1	1
Is the surgical technique adequately described?	0	1	0	1	1	0	0	0	0	1	1	0	1
Is there any way that they have tried to standardize the surgical technique?	1	1	1	1	1	1	1	1	1	1	1	1	1
Is there any way that they have tried to standardize perioperative care?	0	0	0	0	0	0	1	0	0	0	0	1	0
Is the age and range given for patients in the laparoscopic colectomy group?	0	1	1	0	0	0	1	1	1	0	1	0	0
Do authors address whether there are any missing data?	0	0	0	0	0	0	0	0	0	0	0	0	0
Is the age and range given for patients in the open colectomy group?	0	1	1	0	0	0	1	1	1	0	1	0	0
Did all the patients asked to enter the study take part?	0	0	0	0	0	0	0	0	0	0	0	0	0
Dropout rates stated?	0	0	0	0	0	0	0	0	0	0	0	0	0
Were patients in each group treated along similar timelines?	1	1	1	1	1	1	1	1	1	0	1	1	0
Outcomes clearly defined?	1	0	1	1	1	1	1	0	1	1	1	1	0
Blind assessors?	0	0	0	0	0	0	0	0	0	0	0	0	0
Standardized assessment tools?	1	1	1	1	1	1	1	0	1	1	1	1	1
Analysis by intention to treat?	0	0	0	0	0	0	0	0	0	0	0	0	0
Score	9	10	11	10	9	9	13	6	11	9	12	10	7

Methodological qualities of included retrospective studies were assessed using the revised and modified grading system of the Scottish Intercollegiate Guidelines Network. Total score, 20; < 8, poor quality; 8–14, fair quality; >14, good quality.

Meta-analysis of intraoperative outcomes

Compared with OC, LC had a longer operative time (P < .001, WMD = 43.60, 95% CI 29.12–58.08, I² = 89%), but less estimated blood loss (P < .001, WMD = −97.45, 95% CI −126.54 to 68.36, I² = 73%). There was no statistically significant difference between the groups concerning the intraoperative complications (P = .39, OR = 2.63, 95% CI 0.28–24.35, I² = 0%) (Fig. 2). The conversion rate of LC was 10.5%.

FIG. 2.

Meta-analysis of intraoperative outcomes. Lap, laparoscopic colectomy; Open, open colectomy.

Meta-analysis of postoperative outcomes

Total postoperative complications were fewer in LC group (P = .001, OR = 0.66, 95% CI 0.51–0.85, I² = 0%). Besides, we observed a shorter time to first flatus (P < .001, WMD = −0.98, 95% CI −1.50 to −0.46, I² = 92%), time to liquid diet (P < .001, WMD = −1.31, 95% CI −1.74 to −0.89, I² = 72%), length of hospital stay (P < .001, WMD = −5.53, 95% CI −7.98 to −3.08, I² = 90%), and length of postoperative hospital stay (P < .001, WMD = −1.93, 95% CI −2.79 to −1.07, I² = 0%) in LC group. No significant differences were observed between two groups in terms of mortality (P = .87, RR = 0.89, 95% CI 0.22–3.53, I² = 0%) (Fig. 3).

FIG. 3.

Meta-analysis of postoperative outcomes. Lap, laparoscopic colectomy; Open, open colectomy.

There was no statistical significance between the two groups in terms of ileus (P = .53, OR = 0.84, 95% CI 0.48–1.46, I² = 0%), anastomotic leakage (P = .20, OR = 0.66, 95% CI 0.35–1.25, I² = 0%), bleeding (P = .70, OR = 0.87, 95% CI 0.44–1.74, I² = 0%), wound infection (P = .30, OR = 0.74, 95% CI 0.42–1.31, I² = 0%), or abdominal infection (P = .75, OR = 0.87, 95% CI 0.37–2.05, I² = 0%) (Fig. 4).

FIG. 4.

Meta-analysis of postoperative complications particularly associated with surgery. Lap, laparoscopic colectomy; Open, open colectomy.

Oncological surgical quality and long-term outcomes

Tumor size was smaller in LC group (P < .001, WMD = −0.55, 95% CI −0.83 to −0.27, I² = 15%). Nevertheless, lymph nodes harvested (P = .07, WMD = −1.71, 95% CI −3.58 to 0.15, I² = 77%), proximal resection margin (P = .85, WMD = −0.09, 95% CI −0.98 to 0.81, I² = 0%), and distal resection margin (P = .43, WMD = 0.28, 95% CI −0.41 to 0.96, I² = 0%) were comparable between two groups (Fig. 5). Table 3 shows the comparability of long-term outcomes. A pool HR of 1.072 (95% CI 0.608–1.890) showed that OS was similar in two groups, as well as DFS (HR 1.072, 95% CI 0.713–1.611).

FIG. 5.

Meta-analysis of oncological surgical quality. Lap, laparoscopic colectomy; Open, open colectomy.

Table 3.

Meta-Analysis of Survival Data

						5-Year survival rate
	Model	No. of studies	HR	95% CI	P	Lap (%)	Open (%)
OS	Fixed	7	1.072	0.608–1.890	.811	61.0–90.4	59.0–90.5
DFS	Fixed	7	1.072	0.713–1.611	.738	60.3–86.1	56.7–78.9

CI, confidence interval; DFS, disease-free survival; HR, hazard ratio; Lap, laparoscopic colectomy; Open, open colectomy; OS, overall survival.

Publication bias

A funnel plot of the studies reporting on total postoperative complications shows that there was no publication bias among the studies. None of studies lay outside the limits of the 95% CI (Fig. 6).

FIG. 6.

Funnel plots of the studies reporting on postoperative complications.

Discussion

Several large RCTs and Cochrane database reviews have revealed that LC for colon cancer has excellent short-term outcomes and equivalent long-term oncologic outcomes compared to OC.^3–9 However, the safety and feasibility of LC for TCC are unclear because those RCTs excluded patients with TCC. The main reasons are that TCC has a relatively low incidence, and LC for TCC is more difficult than that for other site colon cancers.^10–13 Recently, with accumulating experience of performing LC and continued developments in laparoscopic instruments, LC for TCC has increasingly drawn surgeons' attention. Several retrospective studies have compared LC and OC for TCC patients. However, the sample sizes are small, and none of them is RCT. The surgical management of TCC is still not standardized. So, we performed this meta-analysis to compare LC with OC for TCC.

In the present meta-analysis, we included 14 studies with 1728 TCC patients. The results showed that although longer operative time was needed in LC group, LC group had a significantly less estimated blood loss, fewer total postoperative complications, shorter time to first flatus, shorter time to liquid diet, shorter length of hospital stay, shorter length of postoperative hospital stay, and equivalent oncological surgical quality and long-term outcomes compared to OC.

Regarding the intraoperative outcomes, the pooled data showed that operative time was significantly longer in LC group, which is in keeping with the literature.²⁰ The reason might be that the vascular ligation, lymphadenectomy, and mobilization of the transverse colon in LC are more difficult than those in OC. Mean operative times for TCC varied between 135 and 332 minutes in LC and between 136 and 241 minutes in OC. This might be because the experience of surgery for TCC is different among surgeons. However, LC group had less estimated blood loss, where the difference was 97.45 mL. It is consistent with literatures, which reflect the more precise nature of dissection in laparoscopy.^35,36 Although only three studies reported intraoperative complications, it was similar in both groups. LC group had a very low rate of intraoperative complications (2.4%), while no intraoperative complication occurred in OC group. In LC group, the conversion rate was 10.5%, which is in line with the rate of LC for other site colon cancers (3%–25%).³⁷ The main reasons for conversion were similar with previous study, including advanced disease, large tumor size, extensive adhesions, and intraoperative complications.³⁷

In terms of postoperative outcomes in our study, LC had fewer total postoperative complications (15.1% in LC and 21.9% in OC), but complications particularly associated with surgery (ileus, anastomotic leakage, bleeding, wound infection, and abdominal infection) were comparable in two groups. The possible explanation was that other postoperative complications, such as cardiopulmonary complications, occurred easily in OC group.³⁸ Both groups had a very low mortality rate (0.49% in LC and 0.51% in OC). LC group needed shorter time to first flatus and liquid diet, which was contributed to that LC allowed for less handling of the bowel.³⁹ The consequence of faster recovery of the bowel function helps in shortening hospital stay. From above, it can be concluded that LC is a safe and feasible procedure for TCC with advantages of less estimated blood loss, fewer total postoperative complications, quicker recovery of intestinal function, and shorter length of hospital stay compared to OC.

For oncological surgical quality, the tumor size in LC group was slightly smaller than that in OC group. The difference was only 0.55 cm. We think that differences have little influence on survival. Both groups had comparable lymph nodes harvested, proximal resection margin, and distal resection margin. Enough lymph node dissection is associated with better survival.^40,41 It has been suggested by National Comprehensive Cancer Network guideline that a minimum of 12 lymph nodes should be retrieved for colorectal cancer resection. In the present meta-analysis, the mean lymph nodes in LC and OC were both nearly above 12 (11.8–27.4 in LC and 14.2–28 in OC). Thus, we considered that this requirement was met. Long-term effectiveness is one of the most important and basic criteria to evaluate the tumor radical operation. In this study, although the 5-year survival rate of OS and DFS ranged widely (OS: 61.0%–90.4% in LC and 59.0%–90.5% in OC; DFS: 60.3%–86.1% in LC and 56.7%–78.9% in OC), the OS and DFS were comparable in two groups. Thus, we consider that there is similar long-term effectiveness between LC and OC.

The strength of our meta-analysis comes as that: (1) this meta-analysis included more articles and more patients than that previous study; (2) to the best of our knowledge, this study is the first meta-analysis comparing long-term survival outcomes of LC and OC; and (3) the results showed that compared to OC, LC could provide a quicker postoperative recovery, lesser total postoperative complications, and equivalent long-term survival outcomes for TCC patients. However, some limitations of this study must be acknowledged. First, there existed high heterogeneity in some analyses. Although we conducted sensitivity analysis by removing one study each time, the outcomes remained unchanged. We thought some factors might influence it, such as the experience of surgeon, port sites of LC, and perioperative care. Second, all of the enrolled articles were retrospective studies, which might induce patient selection bias. Third, chemotherapy after colon cancer surgery is a quite important prognostic factor. However, those enrolled studies did not report chemotherapy data. We could not analyze the influence of chemotherapy on the long-term survival. Despite these limitations, we believe that our results provide valuable support for LC of TCC.

In conclusion, our meta-analysis suggests that LC is a safe and feasible technique for TCC patients associated with less estimated blood loss, fewer total postoperative complications, quicker recovery of intestinal function, shorter length of hospital stay, and equivalent long-term survival outcomes. Furthermore, a large-scaled, prospective randomized controlled study is warranted to verify the safety and efficacy of LC for TCC.

Footnotes

Acknowledgments

This work was supported by the Science and Technology Support Program of the Science & Technology Department of Sichuan Province (Grant no. 2016SZ0043) and the National Natural Science Foundation of China (Grant no. 81172373).

Disclosure Statement

No competing financial interests exist.

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