Surgical and Oncological Outcomes of Robotic Resection for Sigmoid and Rectal Cancer: Analysis of 109 Patients from A Single Center in China

Background: Robotic colorectal surgery has been increasingly performed in recent years. The safety and feasibility of its application has also been demonstrated worldwide. However, limited studies have presented clinical data for patients with colorectal cancer (CRC) receiving robotic surgery in China. The aim of this study is to present short-term clinical outcomes of robotic surgery and further conrm its safety and feasibility in Chinese CRC patients. Methods: The clinical data of 109 consecutive CRC patients whoreceived robotic surgery at Sun Yat-sen University Cancer Center between June 2016 and May 2019 were retrospectively reviewed. Patient characteristics,tumor traits, treatment details, complications, pathological details, and survival status were evaluated. Results: Among the 109 patients, 35 (32.1%) had sigmoid cancer, and 74 (67.9%) had rectal cancer. Thirty-seven (33.9%) patients underwent neoadjuvant chemoradiotherapy. Ten (9.2%) patients underwent sigmoidectomy, 38 (34.9%) underwent high anterior resection (HAR), 45 (41.3%) underwent low anterior resection (LAR), and 16 (14.7%) underwent abdominoperineal resection (APR). The median surgical procedure time was 270 min (range 120 - 465 min). Pathologically complete resection was achieved in all patients. There was no postoperative mortality. Complications occurred in 11 (10.1%) patients, including 3 (2.8%) anastomotic leakage, 1 (0.9%) anastomotic bleeding, 1 (0.9%) pelvic hemorrhage, 4 (3.7%) intestinal obstruction, 2 (1.8%) chylous leakage, and 1 (0.9%) delayed wound union. At a median follow-up of 17 months (range 1–37 months), 1 (0.9%) patient developed local recurrence and 5 (4.6%) developed distant metastasis, with one death due to disease progression. Conclusions: Our results suggest that robotic surgery is technically feasible and safe for Chinese CRC patients, especially for rectal cancer patients who received neoadjuvant treatment. A robotic laparoscope with large magnication showed a clear surgical space for pelvic autonomic nerve preservation in cases of mesorectal edema. especially for patients with locally advanced rectal cancer after treatment with preoperative chemoradiotherapy. In our study, 37.6% patients presented with a BMI ≥ 24 kg/m 2 , and 55.4% patients with rectal cancer received neoadjuvant treatment. No conversion occurred with a median procedure time of 270 min, a median estimated blood loss of 50 ml and a median length of stay of 7 days. Only 11 patients (10.1%) experienced postoperative complications, which shows the remarkable surgical advantages of robotic surgery in patients with rectal cancer who received neoadjuvant treatment.

from the umbilicus to the anterior superior iliac spine, one third of the way from the anterior superior iliac spine. Robotic arm 2 (8 mm) was placed 3-4 cm below the xiphoid process. An assistant port was placed (12 mm) at the intersection of the vertical line through McBurney's point and the horizontal line through the camera port.
Total mesorectal excision (TME) and tumor-speci c mesorectal excision (TSME) were performed as previously described (Xu and Qin, 2016). The procedure of pelvic autonomic nerves preservation (PANP) was performed at the same time. The sigmoid mesocolon was cut along the right pararectal sulcus using the middle approach, and the inferior mesenteric artery was fully exposed. The inferior mesenteric artery was clamped and cut off approximately 1 cm from the root of the blood vessel in order to protect the superior hypogastric plexus. The "cavity effect" of electric heating equipment was quickly exposed, and Toldt's plane was subsequently entered.The white lamentous connective tissue in Toldt's space was cut sharply using an electric knife and kept in the neurosurgical plane of the white lamentous connective tissue at all times. We separated the posterior wall of the rectum closely behind the fascia propria of the rectum under direct vision in order to protect the inferior hypogastric nerve and the anterior sacral vessel. Similarly, sharp separation of the rectal lateral walls was performed near the outer edge of the rectal ligament and the inside edge of the pelvic plexus to protect the pelvic plexus. The anterior rectal space between the anterior and posterior Denonvilliers' fascia was separated to protect the branches of the pelvic plexus.

Follow-up
Patients were scheduled for subsequent visits every 3 months for 2 years then semiannually until 3 years after surgery. Physical examination, blood tests for carcinoembryonic antigen (CEA) and carbohydrate antigen 19 − 9 (CA19-9) levels, abdominal ultrasonography, and chest X-rays were performed every

Intraoperative Outcomes
The intraoperative outcomes are presented in Table 2. The median operative time for robotic surgery was 270 min, with a range of 120 min to 465 min. Median intraoperative transfusion volume for the total cohort was 2000 ml (range 1000-4500 ml). Median intraoperative urine volume for the cohort was 400 ml (range 100-2100 ml). Median estimated blood loss for the cohort was 50 ml (range 20-400 ml). Three patients had blood transfusion, including 2 patients in the APR group (12.5%) and 1 patient in the sigmoidectomy and HAR group (2.1%). None of the cases was converted to an open or laparoscopic procedure, and no intraoperative ureteral injury occurred. Twenty-two patients underwent preventive ileostomy, including 4 patients in the sigmoidectomy and

Survival Analysis
The median follow-up period for all patients was 17 months (range 1-37 months). One hundred and two patients (93.6%) in our study cohort were alive with no evidence of disease. One (0.9%) patient developed local recurrence, and 5 (4.6) patients developed distant metastasis. One patient died due to disease progression. The 2-year OS rate of all patients (n = 109) was 97.2% (Fig. 3A), and the 2-year DFS rate of nonmetastatic patients (n = 104) was 92.9% ( Figure. 3B). The 2-year DFS rate of patients in stages 0, I, II, and III were 100%, 95.5%, 90.5%, and 88.8%, respectively ( Figure. 3C).

Discussion
In this retrospective study, we investigated the surgical and oncological outcomes of robotic resection for sigmoid and rectal cancer in Chinese patients. Our data found that robotic surgery had a low conversion rate, low morbidity rate, and remarkable oncological outcomes, which con rms its safety and feasibility in Chinese patients with sigmoid and rectal cancer.
Rectal cancer resection is very di cult to perform using traditional laparotomy, but laparoscopic surgery has an advantage for rectal surgery under a clearer view despite the narrow and deep pelvic space. Several studies (Pai et al., 2015;Gomez Ruiz et al., 2016;Shiomi et al., 2014;Tang et al., 2017;Park et al., 2011) con rmed that laparoscopic surgery presented better short-term outcomes and comparable long-term outcomes compared to traditional laparotomy. The surgical advantages and comparable oncological outcomes of laparoscopic surgery were clearly demonstrated in patients with locally advanced rectal cancer after preoperative chemoradiotherapy in the COREAN trial (Jeong et al., 2014). Because of the features of robotic technology, robotic surgery is much more advantageous, especially for patients with locally advanced rectal cancer after treatment with preoperative chemoradiotherapy. In our study, 37.6% patients presented with a BMI ≥ 24 kg/m 2 , and 55.4% patients with rectal cancer received neoadjuvant treatment. No conversion occurred with a median procedure time of 270 min, a median estimated blood loss of 50 ml and a median length of stay of 7 days. Only 11 patients (10.1%) experienced postoperative complications, which shows the remarkable surgical advantages of robotic surgery in patients with rectal cancer who received neoadjuvant treatment.
As previously reported, the most commonly encountered complication was anastomotic leakage, and its average occurrence rate was 8.6% (range from 1.2-20.5%) (Trastulli et al., 2012;Cong et al., 2013) and 1.8 to 13.6% in robotic surgery (Kwak et al., 2011;Baik et al., 2009). Its occurrence affects the patient's quality of life, increases hospitalization costs, delays the implementation of adjuvant chemotherapy, and shortens the overall survival (Baik et al., 2009;Kulu et al., 2015). Eleven patients (10.1%) had postoperative complications, which included 3 patients who suffered anastomotic leakage. Due to the advantages of robotic surgery, such as 3D magni ed view, wristed instruments and stable camera platform, surgeons are able to maintain the su cient surgical dissection plane down to the pelvic oor, which minimizes damage to marginal vessels and allows performance of the rectal division and reconstruction e ciently and safely to shorten the procedure time.
More precise surgery also helps protect the autonomic nerves and reduce the occurrence of long-term postoperative complications, including defecation, urinary and sexual dysfunction (Shiomi et al., 2014). Jiang and coworkers (Wang et al., 2017)

described a signi cant increase in International Prostate
Symptom Score (IPSS) after surgery in the laparoscopic group, and more patients in the laparoscopic group (34.8%) perceived a severe damage in their overall level of sexual function following surgery than the patients in the robotic group (18.3%). Several studies (Kim et al., 2012;Luca et al., 2013) also claimed that robotic TME improved the preservation of urinary and sexual functions because the arms of the robotic device are stable and highly exible in the separation and exposure of tissues. With the high-resolution lens of the da Vinci surgical system to effectively recognize the nerve, the application of the PANP technique resulted in a signi cant reduction in the incidence of urinary dysfunction (4.6%) and sexual dysfunction (7.3%) in our study.
A positive circumferential margin or insu cient harvested lymph nodes leads to local recurrence (Marinatou et al., 2014). Although the relationship between su ciently harvested lymph nodes and local recurrence rate is controversial, the guidelines list the harvesting of < 12 lymph nodes as risk factor and noted that the performance of TME with clear surgical margins and adequate lymph node dissection were related to lower recurrence rate (Benson et al., 2018a;Benson et al., 2018b). In our study, the median positive total harvested lymph nodes was 0 (range 0-22), and the total harvested lymph nodes was 12 (range 1-51).The 2-year DFS of patients in stages 0, I, II, and III were 100%, 95.5%, 90.5%, and 88.8%, respectively, and the 2-year DFS of patients in stage III was slightly better than previous studies (65.2% − 82.8%) (Pai et al., 2015;Gomez Ruiz et al., 2016;Park et al., 2011). The high quality of the procedure (no positive resection distal margin and su cient harvested lymph nodes) and neoadjuvant treatment contributed to the remarkable oncological outcomes.
Several limitations should be acknowledged in the present study. First, this retrospective descriptive study included an uncontrolled, single-arm methodology and a limited number of patients from a single cohort. Although our study con rms the safety and feasibility of robotic surgery in Chinese CRC patients, the ndings must be validated in a prospective, multicenter clinical trial with a large population in the future. Second, the short follow-up duration was insu cient to evaluate 5-year survival outcomes, which may have led to a misestimation of the effect of robotic surgery on OS and DFS. Additionally, selective bias undeniably exists in our cohort.

Conclusion
Robotic surgery is technically feasible and safe for Chinese CRC patients, especially for rectal cancer patients receiving neoadjuvant treatment because a robotic laparoscope with large magni cation shows a clear surgical space for tumor resection in cases of mesorectal edema. Due to the advantages of robotic surgery, surgeons are able to perform the procedure e ciently and safely and help protect marginal vessels and the autonomic nerves, which reduces the occurrence of short-term and long-term postoperative complications and ensures clear surgical margins and adequate lymph node dissection.

Declarations
Ethics approval and consent to participate The present study was performed according to the ethical standards of the World Medical Association Declaration of Helsinki and was approved by the Institutional Review Board and Independent Ethics Committees of Sun Yat-sen University Cancer Center. The informed consent requirement was waived by the ethics committees based on the nature of this retrospective study, in which patient data were kept con dential.

Availability of data and material
The datasets used and analyzed during the current study are available from the corresponding author on reasonable request. The authenticity of this article has been validated by uploading the key raw data onto the Research Data Deposit public platform (www. researchdata.org.cn).

Competing interests
The authors declare that they have no competing interests.