Robotic versus laparoscopic right hemicolectomy with complete mesocolic excision using a cranial approach: A propensity score-matched retrospective cohort study

doi:10.21203/rs.3.rs-4619616/v1

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Robotic versus laparoscopic right hemicolectomy with complete mesocolic excision using a cranial approach: A propensity score-matched retrospective cohort study

https://doi.org/10.21203/rs.3.rs-4619616/v1

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Background

This retrospective study compared the surgical outcomes of robotic and laparoscopic right hemicolectomies using the cranial approach for complete mesocolic excision (CME) and central vascular ligation (CVL).

Methods

Patients who underwent right hemicolectomy with either robotic CME (R-CME, 48 patients) or laparoscopic CME (L-CME, 123 patients) between April 2016 and December 2023 were retrospectively analyzed using propensity score matching (PSM).

Results

After matching, the R-CME and L-CME groups each included 40 patients. The R-CME group had less intraoperative blood loss (P = 0.007), a shorter median time to first flatus (P < 0.001), and a shorter median postoperative hospital stay (P = 0.012) than the L-CME group. The other surgical outcomes were not significantly different between the two groups.

Conclusions

R-CME using a cranial approach demonstrated the advantages of reduced intraoperative blood loss without prolonging the operative time and improved surgical outcomes, including quicker recovery of bowel function and earlier postoperative discharge, compared to L-CME.

Robotic surgery

laparoscopic surgery

right colectomy

complete mesocolic excision

central vascular ligation

cranial approach

propensity score matching

Complete mesocolic excision (CME) with central vascular ligation (CVL) for right-sided colon cancer has demonstrated better oncological results and survival benefits than the conventional lymphadenectomy approach [1]. Hohenberger et al. applied the basic principles of total mesorectal excision (TME) to right colectomy, which consisted of preserving the embryological mesocolic plane, dissecting the vessels centrally at the superior mesenteric artery (SMA) and vein, and extending the lymphadenectomy along the superior mesenteric vessels (SMV), including the infrapancreatic and gastroepiploic arcade nodes[1]. Although laparoscopy offers better short-term postoperative recovery for patients with colon cancer, performing laparoscopic CME (L-CME) presents challenges owing to the complex and variable vascular anatomy of the right colon [2, 3]. In addition, the Hohenberger procedure involves kocherization of the pancreatic head and lymphadenectomy around the central vessels, which significantly increases the complexity. Although initially described as an open surgery, modifications have facilitated a laparoscopic approach, resulting in reduced morbidity [4, 5]

In recent years, the implementation of robotic systems, with their technical benefits, such as enhanced vision, superior ergonomics, and precise dissection capabilities, has advanced the minimally invasive approach to colorectal surgery [6, 7]. In Japan, health insurance began covering rectal cancer in 2018 and colon cancer in 2022. Consequently, many institutions now perform robotic colorectal surgeries. Several studies have demonstrated the usefulness of robotic surgery over laparoscopic surgery for rectal cancer [8]. However, using robotic instruments for colon cancer surgery is still controversial, and the benefits of robotic colectomy compared to laparoscopic colectomy are unclear [9]. One reason is that robotic surgery for colon cancer requires a wider surgical field and working space than those for rectal cancer, and taking advantage of the features of robotic surgery is difficult. Utilizing robotic surgery for colon cancer may be most beneficial in complex and difficult surgeries such as CME, and an appropriate approach, including port placement, is important. The medial-to-lateral, retroperitoneal, and cranial approaches are used for laparoscopic surgery for right-sided colon cancer. The medial approach was recommended by the Consensus of the European Association of Endoscopic Surgery (EAES) in 2004 [10] and is the most selected approach worldwide. However, the concept of using CME for right-sided colon cancer has emerged, and the retroperitoneal approach is useful due to the easy dissection along the embryological plane. The cranial approach was first reported in 2012 [11] and has the potential to reduce the risk of intraoperative organ damage. A network meta-analysis comparing these three approaches concluded that each approach has advantages and disadvantages but failed to demonstrate the definitive superiority of any approach [12]

Some reports have described the usefulness of the medial-to-lateral and retroperitoneal approaches for right-sided colectomy using robotic surgery [13–17]; however, few reports have demonstrated the usefulness of robotic CME (R-CME) with the cranial approach [18, 19].

This study aimed to compare the perioperative outcomes of R-CME with a cranial approach with those of L-CME for right-sided colon cancer using propensity score matching (PSM) analysis.

Patients

This case series included consecutive patients who underwent robotic or extended right hemicolectomy with CME/CVL for pStage Ⅰ-Ⅲ colon cancer. Data were sourced from the Nagasaki Colorectal Oncology Group (NCOG) database, which was prospectively collected and approved by the Ethics Committee. This retrospective analysis was conducted to evaluate the feasibility and safety of robotic right colectomy for right-sided colon tumors. Patients were eligible if they presented with tumors located at the hepatic flexure, ascending colon, or transverse colon, where lymphatic drainage followed the right or middle colic vessels. Demographic information, intraoperative parameters, and postoperative outcomes were examined. In a subset analysis, the initial R-CME group was compared with the L-CME group in a 1:1 propensity-matched analysis. For propensity score matching, all patients who underwent L-CME for right-sided colon cancer at our hospital between 2016 and 2023 were included. R-CME procedures were conducted between 2022 and 2023. All cancer patients underwent discussions at a colorectal multidisciplinary meeting (MDT) before surgical intervention, and ethical approval was obtained from the hospital research ethics committee.

R-CME surgical technique

In the R-CME group, all surgeries were performed using the da Vinci Surgical Xi System (Intuitive Surgical, Sunnyvale, CA, USA). Intraoperatively, the patient was placed in the lithotomy position, with the head elevated at 10˚ and tilted 5˚ to the right, under general anesthesia. A 5 cm Pfannenstiel incision was made in the lower left abdomen, and a LAP PROTECTOR (Hakko Co. Ltd., Nagano, Japan) was inserted. The EZ access (Hakko) was adjusted, and a da Vinci 12 mm assistant port was placed on it (Fig. 1). Pneumoperitoneum was established at a pressure of 10 mmHg.

Four 8-mm trocars were strategically placed in an arc towards the target area in the upper right abdomen, ranging from 2 cm medial to the anterior superior iliac spine to 2 cm medial to the left costal arch. The greater omentum was dissected, and the transverse mesocolon was separated from the stomach and duodenum using a vessel sealer (SynchroSeal®) in the left hand and bipolar forceps in the right hand. The trunk of Henle, situated on the anterior surface of the pancreas, and the accessory right colic vein (ARCV) branching from it were identified. After dividing the ARCV, the SMV was exposed at the lower edge of the pancreas. Dissection was performed caudally along the surface of the SMV to confirm the root of the middle colic vein (MCV), which was clipped and divided. Subsequently, the patient's position was adjusted with the head down at 5˚ and tilted 5˚ to the right. Dissection was initiated around the caudal dissected margin of the SMV. After confirming the root of the ileocolic vessels, the iliocolic artery (ICA) and vein (ICV) were clipped and divided, respectively, as part of CVL. Dissection continued cranially along the surface of the SMV and SMA, opening the cranial dissection space.

After identifying the root of the middle colic artery (MCA) from the caudal side, the D3 dissection was completed using CVL, by dividing the MCA root. Following full mobilization of the right side of the colon via medial-to-lateral dissection, the distal mesocolon and mesoileum were divided to extract the specimen. After dividing the distal colon and proximal ileum, specimens were extracted through the Pfannenstiel incision. The choice between extracorporeal and intracorporeal reconstruction procedures was at the surgeon's discretion. (https://figshare.com/s/55cf3a43fa64c14b2b64)

L-CME surgical technique

Intraoperatively, the patient was placed in the reverse Trendelenburg position under general anesthesia. The surgeon was positioned on the patient's left side, and pneumoperitoneum was established via a 12 mm umbilicus port placed using the Hasson technique. The four ports were placed in a square. Three 5 mm trocars and one 12 mm trocar were placed under laparoscopic guidance (Fig. 1). The omental bursa was opened widely, and the transverse mesocolon was mobilized from the greater omentum using ultrasonic coagulating shears (UCS; Harmonic HD1100, Ethicon Endo-Surgery Inc. or the Sonicision device, Medtronic). The pedicle of the right gastroepiploic vessels was lifted anteriorly, revealing the gastrocolic trunk of Henle. After releasing the transverse mesocolon, the ARCV and MCV were identified and separated at their origins. Consequently, hepatic flexure mobilization was performed, and the transverse mesocolon was mobilized cranially from the pancreatic head and duodenum, as much as possible. Subsequently, the patient was adjusted to the Trendelenburg position. Dissection was performed along the left side of the SMV. The ICA and ICV roots were clipped and divided, respectively. Finally, the MCA was divided at its origin, and lymph node dissection was performed. After achieving full mobilization of the right colon, the distal colon and proximal ileum were divided.

The choice between extracorporeal and intracorporeal reconstruction procedures was at the surgeon's discretion.

Statistical analysis

Statistical analyses were performed using the JMP Pro 17 software (SAS Institute, Cary, NC, USA). Continuous variables are summarized as means and standard deviations or medians and ranges, and categorical variables are summarized as numbers and frequencies. Median and mean values were compared between groups using the Mann–Whitney U or chi-squared test. Statistical significance was set at P-values < 0.05.

Propensity score matching (PSM)

PSM was conducted to minimize the effects of intergroup differences. Propensity scores were calculated for each patient using bivariate logistic regression based on the following covariates: age, sex, body mass index (BMI), American Society of Anesthesiologists (ASA) score, and the T, N, and clinical stage. These propensity scores were used for 1:1 matching of patients in the L-CME and R-CME groups. We used the nearest-available Mahalanobis distance matching, with calipers defined by the propensity score (caliper = 0.02).

Patient Adjustment with PSM

The study population consisted of 48 and 123 patients without remote metastasis who underwent robotic and laparoscopic right colectomy, respectively. Following PSM, the R-CME and L-CME groups each included 40 patients (Fig. 2).

Characteristics before and after PSM

Before PSM, the age (P = 0.097), cT (P = 0.16), cN (P = 0.084), cM (P = 0.065), and cStage (P = 0.021) were significantly different between the two groups (Table 1). After PSM, each group of 40 patients did not differ significantly in age (P = 0.78), sex (P = 0.82), BMI (P = 0.23), ASA (P = 0.97), cT (P = 0.55), cN (P = 0.84), cM (N/A), or cStage (P = 0.9) (Table 2).

Postoperative outcomes after PSM

The perioperative outcomes after PSM are summarized in Table 3. The incidence of adjacent organ resection (2.5 vs. 0%; P = 1.0), median operative time (193.5 vs. 184ml; P = 0.29), postoperative complications (22.5 vs. 27.5%; P = 0.79), postoperative nausea and vomiting (7.5 vs. 15.0%; P = 0.48), and time to the first solid diet (3.0 vs. 3.0 days; P = 0.15) were not significantly different between the two groups. However, the incidence of intracorporeal anastomosis (95 vs. 20%; P < 0.001), intraoperative blood loss (10.0 vs. 28.5 mL; P = 0.007), time to first flatus (1 vs. 2 days; P < 0.001), and length of postoperative stay (9 vs. 11 days; P = 0.012) were significantly different. Neither group had any conversions to laparotomy or mortalities.

Pathological findings after PSM

The pathological and oncological outcomes after PSM are summarized in Table 4. The median number of harvested lymph nodes (23 vs. 24; P = 0.9), tumor size (34.5 vs. 36 mm; P = 0.9), degree of differentiation, pT (P = 0.06), pN (P = 0.25), pStage (P = 0.41), proximal resection margin (N/A), distal resection margin (N/A), resection margin (N/A), and residual tumor (N/A) were not significantly different between the groups.

In recent decades, the survival rates of patients with rectal cancer have notably improved following the adoption of TME [20]. In 2009, Hohenberger et al. introduced a similar concept, CME, for individuals with colon cancer [1]. CME uses the TME principles that prioritize CVL and meticulous dissection along embryological planes to enable en bloc removal of the affected colon and its mesentery, thereby reducing the risk of microscopic tumor cell dissemination. However, this concept is controversial because of concerns regarding the increased risk of intraoperative complications [21, 22].

Laparoscopic surgery presents several inherent technical challenges in patients requiring right hemicolectomy with CME. Furthermore, achieving central lymphadenectomy at the level of the MCA, as per the CVL concept, using laparoscopic instruments, is technically demanding.

Robotic surgery has potential advantages over conventional laparoscopic surgery for performing complex procedures. These advantages are derived from features such as a stable 3-D surgeon-controlled camera and wrist-mounted instruments, which allow precise dissections around the pancreas and along the SMA and SMV, which are difficult to perform laparoscopically [19].

Only one randomized controlled trial (RCT) compared robotic and laparoscopic right colectomies; the main findings were that robotic right colectomy increases costs and prolongs operative times compared to laparoscopic right colectomy [9]. However, recent meta-analyses have indicated that robotic right colectomy results in a reduced length of hospital stay, quicker time to flatus, increased lymph node harvest, decreased estimated blood loss, reduced conversion rates, and fewer overall complications than laparoscopic right colectomy. In contrast, robotic right colectomy is associated with longer operative durations and higher expenses [23, 24].

In CME for right-sided colon cancer, dissection of the pancreatic head is critical. Uyama et al. suggested that robotic surgery, compared to laparoscopy, decreases the incidence of pancreatic leakage in gastric cancer surgeries that require pancreatic head dissection [25]. Therefore, we believe that robotic operations with joint functions can be utilized for dissection around the head of the pancreas.

Additionally, to ensure safe execution of CME/CVL, we employed a cranial approach. This method offers the following advantages: 1) early transection of the base of the transverse mesocolon, which is central to the lymphatic flow; 2) safe management of the venous system around the pancreatic head; and 3) elimination of the need to remove the small intestine from the surgical field. By initiating the dissection cranially, we can prepare these critical areas for optimal visualization, thereby enhancing the safety and precision of CME.

To date, only a few studies [18, 26]have reported on robotic surgery using a cranial approach, and few have verified its usefulness. In this study, robotic CME was comparable to laparoscopic CME in terms of the operative time and showed good results in terms of intraoperative blood loss. Several studies comparing robotic and laparoscopic colectomy have reported that robotic surgery takes longer than laparoscopic surgery [27, 28]. However, the results of this study indicated that the cranial approach has the potential to shorten the surgical time compared with other approaches. One reason is that manipulation of the small intestine is avoided, which is the most difficult aspect of robotic surgery. In robotic surgery, where the gripping force of the forceps is strong, there is a high possibility of damage to the small intestine due to compression; therefore, the cranial approach, which involves minimal removal of the small intestine in the surgical field, is particularly useful in robotic surgery compared to other approaches.

Additionally, surgical procedures involving bipolar dissection with joint function enable safe CME. For example, using an energy device in the left hand reduces the number of forceps exchanges and is also useful in shortening the operative time [29].

In this study, the time to first flatus was significantly earlier and the length of hospital stay was shorter in the R-CME group than in the L-CME group. This occurred due to the reduced need to grasp the small intestine to create a surgical field and the high rate of intracorporeal anastomosis.

Regarding intracorporeal anastomosis, the quick recovery of digestive tract peristalsis leads to a shorter hospital stay [30, 31]. Owing to the multi-joint function and good operability of robotic surgery, intracorporeal anastomosis is easier to perform than laparoscopic surgery; as a result, intracorporeal anastomosis can be promoted. In contrast, some reports have shown that intracorporeal anastomosis by robotic surgery results in longer operative times than extracorporeal anastomosis [32, 33]. However, if the surgical strategy takes advantage of the characteristics of robotic surgery, even intracorporeal anastomosis can have shorter operative times and ultimately improved perioperative outcomes.

A Pfannenstiel incision was made in the lower abdomen before the procedure to enable specimen extraction without undocking the robot. A Pfannenstiel incision reduces postoperative incisional hernias and the incidence of surgical site infections (SSI) [34]. To maximize the benefits of robotic right-sided colectomy, the combination of intracorporeal anastomosis and a Pfannenstiel incision is very promising.

To the best of our knowledge, this is the first study to compare R-CME with L-CME using a cranial approach. Nevertheless, this study had several limitations, primarily owing to its small sample size and retrospective design. Additionally, the lack of mesocolic plane grading, which is a key component of CME and CVL, is noteworthy. As previously mentioned, most R-CME procedures use intracorporeal anastomosis, whereas many L-CME procedures use extracorporeal anastomosis. This distinction may affect short-term outcomes. Furthermore, not all team members performed R-CME, and we lacked the long-term data needed to determine whether the short-term advantages of R-CME would lead to oncological benefits over L-CME. These factors may have introduced bias into our conclusions. To overcome the limitations of this retrospective analysis, a multicenter randomized controlled trial involving this procedure will be conducted.

In our study, R-CME was associated with less blood loss, quicker bowel function recovery, and a shorter postoperative hospital stay than L-CME. Further studies are needed to validate these results and provide long-term oncological outcomes.

Funding: Not applicable

Conflict of interest: The authors declare that they have no conflict of interest.

Ethics approval: All procedures involving human participants in this study were in accordance with the ethical standards of the Trust and the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

Consent to participate: Not applicable

Consent for publication: Written informed consent was obtained from all patients for the publication of the accompanying images.

Availability of data and material: Data sharing not applicable to this article as no datasets were generated or analyzed during the current study.

Code availability: Not applicable

Author Contribution

Takashi Nonaka wrote the main manuscript text and Tetsuro Tominaga, Yuma Takamura,Oishi Kaido and Keisuke Noda prepared each datas. Terumitsu Sawai and Keitaro Matsumoto reviced this manuscript. All authors reviewed the manuscript.

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No competing interests reported.

RoboticCME.mp4
Table1.png
Table 1. Patient and tumor characteristics before PSM *Data are presented as median (range). *P< 0.05 was considered statistically significant. BMI, body mass index; ASA, American Society of Anesthesiologists; R-CME, robotic complete mesocolic excision; L-CME, laparoscopic complete mesocolic excision.
Table2.png
Table 2. Patient and tumor characteristics after PSM *Data are presented as median (range). *P< 0.05 was considered statistically significant. BMI, body mass index; ASA, American Society of Anesthesiologists; R-CME, robotic complete mesocolic excision; L-CME, laparoscopic complete mesocolic excision.
Table3.png
Table 3. Comparison of intraoperative and postoperative outcomes *Data are presented as median (range). *P< 0.05 was considered statistically significant. Postoperative complications were graded using the Clavien–Dindo classiﬁcation system. R-CME, robotic complete mesocolic excision; L-CME, laparoscopic complete mesocolic excision.
Table4.png
Table 4. Comparison of pathologic outcomes *Data are presented as median (range). *P< 0.05 was considered statistically significant. R-CME, robotic complete mesocolic excision; L-CME, laparoscopic complete mesocolic excision.

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Robotic versus laparoscopic right hemicolectomy with complete mesocolic excision using a cranial approach: A propensity score-matched retrospective cohort study

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Abstract

Background

Methods

Results

Conclusions

Figures

Introduction

Patients and Methods

Patients

R-CME surgical technique

L-CME surgical technique

Statistical analysis

Propensity score matching (PSM)

Results

Patient Adjustment with PSM

Characteristics before and after PSM

Postoperative outcomes after PSM

Pathological findings after PSM

Discussion

Conclusion

Declarations

References

Additional Declarations

Supplementary Files

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Version 1