Systematic review and meta-analysis of robotic versus laparoscopic radical cholecystectomy for gallbladder cancer

Introduction

Gallbladder cancer (GBC) is a relatively rare but aggressive malignancy which arises from the mucosal lining of the gallbladder (1). GBC has an estimated incidence rate of 1.2% of all cancer diagnosis and 1.7% of all cancer deaths according to the International Agency for Research on Cancer’s GLOBOCAN 2024 estimate (2). GBC has a higher prevalence in regions such as South and Central America, South Asia and Eastern Europe (1). Risk factors for the development of GBC include age, gender, gallstones, chronic gallbladder inflammation, as well as genetic factors (1,3).

According to the National Comprehensive Cancer Network (NCCN) guidelines, curative treatment involves simple cholecystectomy for Tis and T1a disease (4,5). However, patients often present at a more advanced stage due to asymptomatic nature of the disease (1). For patients who are diagnosed with T1b and more advanced disease, radical cholecystectomy (RC) is recommended (4-6).

RC requires en-bloc resection of the gallbladder, along with resection of the liver, typically segment 4b/5 and regional lymphadenectomy (3,7). Due to the complexity of procedure as well as technical difficulties in achieving oncological resection, minimally invasive surgery has proven challenging (6,8,9). Lymph node dissection, particular near the hepatoduodenal ligament, is typically carried out in a confined space close to major vessels or bile ducts (6). The multiple variations in the vascular and biliary structures of the liver add further complexities to minimally invasive surgery (MIS) (6). Furthermore, due to the multidirectional resection axis, a straight laparoscopic instrument may not be adequate to visualise and carry out dissection (6). Due to the increased risk of gallbladder perforation with subsequent tumour exposure and implantation during minimally invasive surgery, laparoscopic cholecystectomy has been identified as a risk factor for port-site metastasis and peritoneal recurrence (10). Laparoscopic surgery is also thought to increase the risk of R1/2 resection due to positive surgical margins or cystic duct margins (11,12).

Robotic resection can overcome these difficulties due to its ability to achieve more precise movements, including suturing with its use of multi-jointed instruments and by providing a three-dimensional view (6,13,14). It is suggested that robotic surgery should have comparable or better surgical and oncological outcomes than laparoscopic surgery, including length of hospital stay, blood loss as well as have low rates of recurrence (15). However, robotic hepatobiliary resection has been a relative recent development and as such, there are relatively few papers on the oncological safety and surgical outcomes of RC (9,16). Furthermore, to the best of our knowledge, a systematic review comparing robotic radical cholecystectomy (RRC) with laparoscopic radical cholecystectomy (LRC) has not yet been conducted.

Hence, the aim of this systematic review and meta-analysis was to compare between surgical outcomes and long-term survival for robotic radical resection versus laparoscopic radical resection for GBC. We present this article in accordance with the PRISMA reporting checklist (available at https://hbsn.amegroups.com/article/view/10.21037/hbsn-24-457/rc) (17).

Methods

Search strategy

We searched human studies indexed in databases including Cochrane, PubMed, Embase and Ovid, focusing on the outcomes of robotic radical cholecystectomy (RRC) compared to LRC for GBC until November 2023. Various keywords including “gallbladder adenocarcinoma”, “gallbladder carcinoma”, “gallbladder cancer”, and “extended cholecystectomy” were employed. For RRC, the key terms were “robot*”, while the key terms for LRC was “minimally invasive” OR “laparoscopy*”.

Selection criteria

The search encompassed all types of articles from January 2000 to November 2023, with duplicates being removed. We included both elective RC, which was performed when GBC was suspected prior to cholecystectomy, as well as completion RC, which was carried out after an index cholecystectomy with a post-operative incidental diagnosis of GBC. Articles that covered resection of benign gallbladder diseases, gallbladder metastases, or cholangiocarcinoma were excluded. Additionally, studies covering liver resection, isolated lymphadenectomy, staging laparoscopy, case reports, or with case count <5, review articles, and guideline publications were excluded.

Screening

Laparoscopic

A total of 2,724 records on LRC were identified on the initial search, of which 126 records were marked as duplicate. A total of 2,598 records were screened through via their titles and abstracts, and a total of 156 articles were selected for full-text retrieval. Any incongruities on an article’s inclusion were deliberated on by the two authors before reaching consensus. A total of 8 studies on LRC and their outcomes were included for review (Figure 1).

Figure 1 PRISMA table on retrieval of articles on LRC. LRC, laparoscopic radical cholecystectomy.

Robotic

In similar fashion, 66 records were identified from PubMed, Embase, Ovid and Cochrane, and a total of 7 duplicate records were removed. Fifty-nine records underwent title and abstract screening, and a total of 18 full-text articles were retrieved. Consensus was obtained between the two authors in the event of disagreement on inclusion, and a total of 3 studies were included for analysis (Figure 2).

Figure 2 PRISMA table on retrieval of articles on RRC. RRC, robotic radical cholecystectomy.

Key outcomes were obtained on duration of surgery, blood loss, conversion rate, staging, lymph node yield, postop hospital stay and morbidity and mortality among patients undergoing laparoscopic as versus robotic surgery. Results were reported in the form of either mean or medial values.

Statistical analysis

For lymph node yield and postoperative hospital length of stay (LOS), some studies reported the median, minimum, and maximum, instead of the mean and standard deviation (SD). For these studies, we converted the reported values to mean and SD using the method described in Wan et al. (18). As most studies that were included had a small sample size and some outcomes had proportions that were near zero, we used the Freeman-Tukey double arcsine transformation to generate more reliable outcome proportion estimates.

Random effects meta-analyses were used to estimate the pooled mean (for numerical outcomes) or proportion (for binary outcomes), along with the corresponding 95% confidence intervals (CIs). The between-study variance (τ2) was estimated using the random effects maximum likelihood (REML) method. The I² statistic was used to indicate the proportion of total variation across studies that were due to heterogeneity rather than chance. Heterogeneity was also assessed via visual inspection of the forest plot. We performed subgroup analyses by surgery type (laparoscopic vs. robotic). Cochran’s Q test (via the Qb statistic) was used to determine if there were differences in the pooled estimates between subgroups. The possibility of publication bias was explored using funnel plots. Egger’s asymmetry test was not performed as none of the outcomes had at least ten studies for each surgery type.

Due to the small number of studies included, we did not perform a leave-one-out analysis to examine robustness of results to the exclusion of a specific study or perform meta-regression to identify the sources of heterogeneity. The risk of bias for each observational study was assessed using ROBINS-I (19). Although ROBINS-I is designed for non-randomized studies with comparator groups, we adapted its application to single-group studies by focusing on relevant domains. Statistical tests were two-sided with a 0.05 significance level. All analyses were conducted using the ‘meta’ package in Stata 18 (College Station, TX: StataCorp LLC) and the ‘robvis’ package in R version 4.4.2 (20).

Results

Table 1 summarizes the papers included in LRC (8 papers) and RRC (3 papers). A total of 11 (8 laparoscopic, 3 robotic) one-sample retrospective observational studies that fulfilled the inclusion and exclusion criteria were included in the analysis and subsequent meta-analysis. The total number of patients was 315 (263 laparoscopic, 52 robotic), ranging from years 2000 to 2020 (laparoscopic) and 2010 to 2019 (robotic). For LRC vs. RRC, there were no significant differences in patient characteristics, including age of patients as well as gender ratios.

Patients in the LRC had no difference in duration of surgery as well as blood loss when compared to RRC. Three out of 8 laparoscopic studies reported conversion rate. Vega et al. [2020] reported 19 patients underwent conversion out of 65 patients (21). Most patients in both LRC and RRC were diagnosed with stage I or stage II cancer. The summary of the surgical characteristics of patients including T status and American Joint Committee on Cancer (AJCC) staging included in LRC and RRC can be found in Table 2.

Table 3 summarises the post-operative outcomes of patients who underwent LRC and RRC, including lymph node yield, postoperative hospital stay, postoperative morbidity and 30-day mortality and recurrence rates.

Resection margins

Resection margins were reported in 6 laparoscopic papers and 1 robotic paper. Out of 189 patients in our pooled laparoscopic study, 171 patients achieved R0 resection (90%), while 18 patients had R1 or R2 resection. Tschuor et al. [2023] reported that in a study of 20 patients who under RRC, 16 (80%) achieved R0 resection (15).

Meta-analysis was not carried out as only 1 robotic paper reported on resection margins.

Recurrence rates and 5-year mortality

Out of 175 patients in our pooled LRC arm, there were a total of 16 recurrences. None of the papers reported port-site metastasis. In our RRC arm, 2 patients out of 32 patients presented with recurrence. Of these, 0 were port-site metastasis.

5-year mortality rates were not well reported among the papers. For the LRC arm, Castro et al. [2018] reported 5-year mortality rate of 19.3%, while Palanisamy et al. [2016] reported a 5-year mortality rate of 21.4% and Shirobe et al. [2015] reported a 5-year rate of 22% (22-24). For the RRC arm, no paper had a 5-year follow-up. Tschuor et al. [2023] reported 39.5% 5-year mortality (15).

Meta-analysis

Lymph node yield

All 11 studies reported summary data for lymph node yield. For the 8 studies on laparoscopic surgery, the random effects meta-analysis showed a pooled mean lymph node yield of 9.10 (95% CI: 7.45 to 10.75). There was high between-study heterogeneity (I²=99.1%). For the 3 studies on robotic surgery, the pooled mean lymph node yield was 8.62 (95% CI: 6.12 to 11.12), with high between-study heterogeneity (I²=78.4%). There was no evidence of a difference in pooled mean lymph node yield between the two surgery types (Cochran’s Q test of group differences P=0.75). Figure 3 demonstrates the summary of the mean lymph node yield by laparoscopic or robotic resection.

Figure 3 Summary mean lymph node yield, by LRC or RRC. CI, confidence interval; LNY, lymph node yield; LRC, laparoscopic radical cholecystectomy; REML, random effects maximum likelihood.

Postoperative LOS

Ten (7 laparoscopic, 3 robotic) studies reported summary data for postoperative LOS. For the 7 studies on laparoscopic surgery, the random effects meta-analysis showed a pooled mean postoperative hospital LOS of 7.90 days (95% CI: 6.20 to 9.61) (21-23,25-28). There was high between-study heterogeneity (I²=98.7%). For the 3 studies on robotic surgery, the pooled mean postoperative hospital LOS was 5.22 days (95% CI: 2.56 to 7.89), with high between-study heterogeneity (I²=97.8%) (15,29,30). There was no evidence of a difference in pooled mean postoperative hospital LOS between the two surgery types (P=0.10). Figure 4 shows the summary of the mean postoperative hospital LOS by LRC or RRC.

Figure 4 Summary mean postoperative hospital length of stay, by LRC or RRC. CI, confidence interval; LOS, length of stay; LRC, laparoscopic radical cholecystectomy; RRC, robotic radical cholecystectomy; REML, random effects maximum likelihood.

Postoperative adjuvant therapy

Six (5 laparoscopic, 1 robotic) studies reported summary data for postoperative adjuvant therapy. For the 5 studies on laparoscopic surgery, the random effects meta-analysis showed a pooled 42% (95% CI: 21% to 63%) of patients with postoperative adjuvant therapy (21-24,28). There was high between-study heterogeneity (I²=83.0%). One study on robotic surgery reported 81% (95% CI: 64% to 94%) of patients with postoperative adjuvant therapy (28). There may be a difference between surgery types (P<0.01). Figure 5 summarises the proportion with postoperative adjuvant therapy, by LRC or RRC.

Figure 5 Summary of the proportion with postoperative adjuvant therapy, by LRC or RRC. CI, confidence interval; FTT, Freeman-Tukey double arcsine transformed; LRC, laparoscopic radical cholecystectomy; RRC, robotic radical cholecystectomy; REML, Random effects maximum likelihood.

Postoperative morbidity

All 11 studies reported summary data for postoperative morbidity (Figure 6). For the 8 studies on laparoscopic surgery, the random effects meta-analysis showed a pooled 13% (95% CI: 7% to 20%) of patients with postoperative morbidity (21-28). There was moderate between-study heterogeneity (I²=49.1%). For the 3 studies on robotic surgery, there was a pooled 4% (95% CI: 0% to 13%) with postoperative morbidity (15,29,30). There was no evidence of a difference in pooled percentage with postoperative morbidity between the two surgery types (P=0.17).

Figure 6 Summary of the proportion with postoperative morbidity, by LRC or RRC. CI, confidence interval; FTT, Freeman-Tukey double arcsine transformed; LRC, laparoscopic radical cholecystectomy; RRC, robotic radical cholecystectomy; REML, Random effects maximum likelihood.

30-day mortality

Eleven (8 laparoscopic, 3 robotic) studies reported summary data for 30-day mortality. For the 8 studies on laparoscopic surgery, the random effects meta-analysis showed a pooled 0% (95% CI: 0% to 1%) of patients with 30-day mortality (20-27). There was little between-study heterogeneity above that expected by chance (I²=0%). For the 3 studies on robotic surgery, there was a pooled 0% (95% CI: 0% to 3%) with 30-day mortality, with little between-study heterogeneity (I²=0%) (15,29,30). There was no evidence of a difference in pooled percentage with 30-day mortality between the two surgery types (P=0.94). Figure 7 shows a summary of the proportion with 30-day mortality by LRC or RRC.

Figure 7 Summary of the proportion with 30-day mortality, by LRC or RRC. CI, confidence interval; FTT, Freeman-Tukey double arcsine transformed; LRC, laparoscopic radical cholecystectomy; RRC, robotic radical cholecystectomy; REML, Random effects maximum likelihood.

Risk of bias

Figure 8 shows the risk of bias across studies using ROBINS-I. Of the 11 studies, 6 (4 laparoscopic, 2 robotic) were at moderate overall risk of bias while 5 (4 laparoscopic, 1 robotic) were at serious overall risk of bias. As all 11 studies provided data on either robotic or laparoscopic surgery patients but did not directly compare between both groups, we could not assess the risk of bias due to confounding.

Figure 8 Risk of bias assessment using ROBINS-I.

Discussion

One of the critical endpoints in RC is the extent of lymph node dissection, which influences staging and prognosis. According to the AJCC guidelines, at least 6 lymph nodes are required for adequate lymph node yield for staging (31). Our analysis indicates that there is no significant difference in lymph node yield between robotic and laparoscopic approaches, and that both LRC and RRC can achieve adequate lymphadenectomy. All the papers included in this study reported adequate lymph node yield. Resection margins were all clear in the papers included. With further advancement in robotic techniques, robot-assisted techniques can also aid in improving dexterity and dissection of critical structures especially hilar structures in radical cholecystectomy (32). The three-dimensional vision also provides additional support and ergonomics (8).

While conversion rates were reported in all the robotic studies, conversion rates were only reported in three out of the eight laparoscopic studies included in our study, hence limiting our analysis. For RRC, two papers reported zero conversion rate (0 out of 25 patients), while Goel et al. reported a relatively high conversion rate of 14.8% (4 out of 27 patients) (29). This could possibly be attributed to the learning curve of surgeons when initially operating with robotic techniques, as the paper reported that two of the conversions were early in the series.

Another outcome that was reported in our study is the LOS. In current era of cost-effectiveness, increasing hospital cost has been a critical debate in robotic surgery. Additional day of hospitalization ought to add additional cost to hospitalisation. Our analysis suggests no significant disparity in mean hospital LOS between robotic and laparoscopic procedures for radical cholecystectomy. Both modalities appear to offer comparable postoperative recovery periods, indicating similar efficacy in minimizing hospitalization duration and facilitating early discharge. There was also no significant difference in postoperative morbidity and 30-day mortality between LRC and RRC, and the robotic arm reported no mortality within the 30-day period as well. As both LRC and RRC demonstrate comparable safety profiles, this paper would suggest that RRC is a feasible approach in managing GBC. This would also facilitate early initiation of adjuvant chemotherapy which is indicated in both locally advanced and nodal positive disease (33,34). The low rate of 30 days morbidity is imperative to facilitate this. One study on robotic surgery reported that 81% of patients eventually underwent adjuvant therapy, which could also have been related to lymph node yield and nodal positivity. As both LRC and RRC demonstrate comparable safety profiles, our paper would suggest that RRC is a feasible option in managing GBC.

In our RRC arm, most patients were diagnosed with AJCC stage 1 or 2 disease, while more patients in the LRC arm had more advanced disease. However, less than half of LRC patients eventually required adjuvant therapy, which could be due to differing guidelines between countries. One study on robotic surgery reported that 81% of patients eventually underwent adjuvant therapy, which could also have been related to lymph node yield and nodal positivity (29). Based on our paper, it can be postulated that there are advantages of lymphadenectomy in the robotic approach.

For Shirobe et al. in our LRC arm, none of the patients received chemotherapy, and two patients received post-operative radiation due to perineural invasion (22). Two patients in the study had R1 resection, which may have benefited from adjuvant chemotherapy (22,35). Although current evidence supports adjuvant chemotherapy in nodal disease or locally advanced disease, there is a lack of consensus on international guidelines for chemotherapy for GBC and hence this may account for relatively low adjuvant chemotherapy in our LRC arm (33,35).

Our paper also considered the rate of recurrences post-operatively, including port-site metastasis. Port-site metastasis has previously been reported as a concern in laparoscopic surgery due to the relatively high proportion of 10% of patients presenting with port-site metastasis in laparoscopic surgery (36). In our analysis, our robotic arm did not report any port-site metastasis as well as low recurrence rates. The only recurrence reported was Goel et al., which reported 2 liver recurrences out of 27 patients who underwent RRC (29). This would suggest that robotic surgery is safe, and techniques are adequate in mitigating the risk of recurrence. However, long-term data is lacking, especially for robotic surgery which is a relative nascent technique.

Our research is novel as, to the best of our understanding, there is no existing systematic review and meta-analysis directly comparing RRC with LRC in the current literature. While a recent systematic review has compared RRC and LRC, our meta-analysis component demonstrates the absence of significant differences in numerous surgical outcomes (37).

Limitations

While conversion rates were reported in all the robotic studies, rates were only reported in three out of the eight laparoscopic studies included in our study, hence limiting our analysis. For RRC, Goel et al. reported a relatively high conversion rate of 14.8% (total 4 out of 27 patients), while the other 2 studies report no conversion rates (total 25 patients) (15,29,30). This could possibly be attributed to the learning curve of surgeons when initially operating with robotic techniques, as the paper notes that two of the conversions were early in the series (29). There were also a higher proportion of T1 patients or early AJCC stage among the RRC arm, which may indicate a selection preference for patients with early-stage GBC, hence contributing to the comparable outcome.

Due to the small number of studies included, it was difficult to differentiate between true asymmetry and random variation in the funnel plots. We cannot exclude the possibility of publication bias towards more extreme outcome values, which can lead to an inaccurate representation of our data. Robotic surgery is a recent advance and with more papers published on RRC, we can expect more robust data to help support the findings of our paper.

As all the studies provided data on either robotic or laparoscopic surgery patients but did not directly compare between both groups, we could not assess the risk of bias due to confounding.

While the data demonstrates that the robotic approach is safe in terms of short-term perioperative outcomes, we currently have inadequate long-term outcomes such as overall survival and disease-free survival. It is also interesting to note that a significant proportion of patients who underwent robotic approach were early T stage and this may reflect a selection preference of patients which may have contributed to the comparable outcomes. None of the RRC papers were able to collect data on long term survival beyond 5 years, and data on recurrence was also collected over a relatively short period (15,29,30). As more papers are published on RRC, we hope to obtain more long-term data to support our findings.

Conclusions

In conclusion, our findings suggest that there is no significant difference in perioperative and oncological outcomes between radical cholecystectomy and laparoscopic cholecystectomy. However, there is still limited data on radical cholecystectomy owing to its recent advent and further research focused specifically on radical cholecystectomy is required to obtain more comprehensive and robust data, especially long-term and oncological data.

This paper highlights the promising potential of robotic cholecystectomy for GBC. More studies would be imperative to optimise outcomes and continued efforts in research and training of robotic techniques would assist to advance the management of GBC through innovative surgical approaches.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the PRISMA reporting checklist. Available at https://hbsn.amegroups.com/article/view/10.21037/hbsn-24-457/rc

Peer Review File: Available at https://hbsn.amegroups.com/article/view/10.21037/hbsn-24-457/prf

Funding: None.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://hbsn.amegroups.com/article/view/10.21037/hbsn-24-457/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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