Comparing short-term outcomes of robot-assisted and conventional laparoscopic total mesorectal excision surgery for rectal cancer in elderly patients

Abstract

BACKGROUND

Da Vinci Robotics-assisted total mesorectal excision (TME) surgery for rectal cancer is becoming more widely used. There is no strong evidence that robotic-assisted surgery and laparoscopic surgery have similar outcomes in elderly patients with TME for rectal cancer.

AIM

To determine the improved oncological outcomes and short-term efficacy of robot-assisted surgery in elderly patients undergoing TME surgery.

METHODS

A retrospective study of the clinical pathology and follow-up of elderly patients who underwent TME surgery at the Department of Gastrointestinal Oncology at the Affiliated Hospital of Nanjing University of Chinese Medicine was conducted from March 2020 through September 2023. The patients were divided into a robot-assisted group (the R-TME group) and a laparoscopic group (the L-TME group), and the short-term efficacy of the two groups was compared.

RESULTS

There were 45 elderly patients (≥ 60 years) in the R-TME group and 50 elderly patients (≥ 60 years) in the L-TME group. There were no differences in demographics, conversion rates, or postoperative complication rates. The L-TME group had a longer surgical time than the R-TME group [145 (125, 187.5) vs 180 (148.75, 206.25) min, P = 0.005), and the first postoperative meal time in the L-TME group was longer than that in the R-TME (4 vs 3 d, P = 0.048). Among the sex and body mass index (BMI) subgroups, the R-TME group had better outcomes than did the L-TME group in terms of operation time (P = 0.042) and intraoperative assessment of bleeding (P = 0.042). In the high BMI group, catheter removal occurred earlier in the R-TME group than in the L-TME group (3 vs 4 d, P = 0.001), and autonomous voiding function was restored.

CONCLUSION

The curative effect and short-term efficacy of robot-assisted TME surgery for elderly patients with rectal cancer are similar to those of laparoscopic TME surgery; however, robotic-assisted surgery has better short-term outcomes for individuals with risk factors such as obesity and pelvic stenosis. Optimizing the learning curve can shorten the operation time, reduce the recovery time of gastrointestinal function, and improve the prognosis.

Key Words: Robotic surgery, Laparoscopy, Rectal cancer, Total mesorectal excision, Elderly

Core Tip: Previous studies have shown that laparoscopic total mesorectal excision (TME) surgery for rectal cancer has been widely used worldwide. Robotic-assisted systems are capable of achieving finer anatomical manipulation and better surgical outcomes with high-definition cameras, but TME surgery has not been widely promoted in elderly rectal cancer patients. In this retrospective study, we enrich the evidence that robotic-assisted systems deserve to be widely used over laparoscopy.

INTRODUCTION

Colorectal cancer has the third highest incidence and second highest mortality rate in the world[1]. The incidence rate in elderly patients is also gradually increasing. The treatment of choice for rectal cancer is surgical resection. Total mesorectal excision (TME), defined by sharp dissection and complete removal of the rectal mesentery envelope in the rectum, is the gold standard surgical treatment for rectal cancer, and it provides excellent control of local recurrence and overall survival[2,3]. To date, TME surgery has been frequently performed with the aid of laparoscopic techniques[4]. However, the evaluation of laparoscopic rectal cancer resection is not comprehensive and remains controversial. The main concerns are damage to adjacent tissues and the fact that tumor clearance and the number of dissected lymph nodes, which are markers of surgical success, may not be comparable to those of open surgery[5]. With robot-assisted surgery, the patient’s vision becomes increasingly wider, which may effectively remedy the limitations of laparoscopy. Pigazzi et al[6] first described robot-assisted laparoscopic TME surgery for rectal cancer in 2006, and since then, robot-assisted laparoscopic surgery for rectal cancer has been widely used. However, there is still a lack of large, multicenter, randomized, controlled clinical trials demonstrating the clear superiority of robotic assistance over laparoscopic techniques in TME surgery. Moreover, due to the unique physical characteristics of elderly patients, they may have poor cardiopulmonary function, and there is still a lack of evidence demonstrating the advantages of these two surgical methods for resection of elderly rectal cancer patients. Therefore, we enrolled elderly rectal cancer patients from the Department of Gastrointestinal Oncology at the Affiliated Hospital of Nanjing University of Chinese Medicine from March 2020 to April 2023 and observed and compared the short-term outcomes of robotic-assisted and conventional laparoscopy in geriatric TME surgery.

MATERIALS AND METHODS

This retrospective cohort study was approved by the Institutional Review Board of Nanjing University of Chinese Medicine Hospital. Due to the retrospective nature of the study, the requirement for informed consent was waived.

Patients

The study reviewed the data of elderly patients who underwent rectal TME between March 2020 and September 2023 using laparoscopic or robotic approaches. The inclusion criteria for patients were as follows: (1) Rectal adenocarcinoma confirmed by preoperative or postoperative pathology; (2) aged ≥ 60 years; and (3) had a preoperative examination excluding distant metastasis. Exclusion criteria: (1) emergency surgical treatment due to acute intestinal obstruction; (2) multiple primary colorectal malignancies; (3) local resection; (4) history of other malignant tumors; (5) the American society of anesthesiologists [American Society of Anesthesiologists (ASA)] score > Ⅲ; (6) preoperative treatment other than neoadjuvant therapy; (7) palliative resection; and (8) transvaginal surgery. Patients were divided into robot and laparoscopic groups according to the surgical treatment equipment.

The patient data used in this study came from the medical records of our hospital. These data were retrospectively analyzed and included information on patient characteristics, perioperative data, severity of complications according to the Clavien–Dindo classification, and pathology. Finally, 95 elderly patients with rectal cancer were enrolled in this study. Forty-five patients were assigned to the R-TME group, and another 50 were assigned to the L-TME group.

Surgical methods

This study was performed at a single center, and both the conventional laparoscopic and robotic approaches were managed by the same surgical team, who performed more than 2000 Laparoscopic-assisted surgeries. All patients voluntarily chose the surgical approach to which they wanted to be subjected. All patients included in the study underwent TME, abdominal lymph node dissection, and pelvic autonomic nerve preservation. The scope of surgery was the same for robot-assisted and laparoscopic procedures, and all procedures were performed in the colonic and pelvic stages. The colon phase includes submesenteric artery and vein ligation and left mesenteric mobilization; the pelvic phase includes pelvic dissection using TME or tumor-specific mesenterectomy principles and enterostomy with double anastomosis or hand-stitched coloanal suture; and when incisions are made for any reason other than specimen extraction, open surgery may be considered instead. Preventive ostomy was performed at the discretion of the surgeon.

Outcome measures

In this study, the outcome parameters were: operation time, conversion to laparotomy, transfusion, intraoperative bleeding, stoma condition, number of lymph node dissection, nature of pathological circumferential margin, time to recovery of intestinal function was assessed by first eating a liquid diet, postoperative hospital stay, drainage tube removal time, Foley catheter removal time, postoperative complications. Postoperative complications, reoperations, and mortality were defined as events that occurred during postoperative hospitalization or within 30 days after surgery. Postoperative complications were classified by the Clavien-Dindo (CD) classification. All of these events were assessed by clinicians and recorded in a database.

Statistical analyses

All statistical analyses were performed using SPSS (statistical Product and Service Solutions version 25.0; IBM Corporation, Armonk, NY, United States). Quantitative data that conformed to normal distribution were expressed as mean ± SD, and quantitative data that did not conform to normal distribution were expressed as Md (Q1, Q3) (Md stands for the median, Q1 for the 25^th percentile of all values in the sample ranked in descending order, and Q3 for the 75^th percentile of all values in the sample ranked in descending order), and the hypotheses of the above data were tested using the t-test and rank-sum test, respectively. Categorical data are presented as the number of cases and percentages, and chi-square (χ²) or Fisher’s exact tests were used to test the hypothesis. Univariate and multifactorial logistic analyses were used to correct for confounders and to predict factors influencing complications. Statistical significance was considered to exist when P < 0.05.

RESULTS

Comparison of baseline data between two groups of patients

There were 95 patients who met the criteria, 45 in the R-TME group and 50 in the L-TME group. Table 1 The baseline characteristics of the overall cohort are shown. There were no significant differences (P > 0.05) between the two groups in terms of age, sex, BMI, hemoglobin (HGB), albumin (ALB), tumor level from the anal verge, history of cardiopulmonary disease, history of neoadjuvant therapy or ASA level. With regard to baseline characteristics, the R-TME and L-TME groups were comparable.

Table 1 Baseline data between the two groups of patients.

	R-TME (n = 45)	L-TME (n = 50)	t/Z/χ2 value	P value
Age [yr, Md (IQR)]	68 (64, 71)	69 (65, 75)	-1.7631	0.078
Gender, n (%)			0.682	0.409
Male	26 (57.7)	33 (66.0)
Female	19 (42.3)	17 (34.0)
BMI (kg/m2, mean ± SD)	23.43 ± 2.52	23.85 ± 3.02	-0.733	0.467
Tumor level from anal verge (cm), n (%)			0.8182	0.664
5-10	25 (55.6)	24 (48.0)
11-15	14 (31.1)	20 (40.0)
> 15	6 (13.3)	6 (12.0)
History of cardiopulmonary disease, n (%)			0.0682	0.794
Yes	21 (46.7)	22 (44.0)
No	24 (53.3)	28 (56.0)
HGB (g/L, mean ± SD)	125.22 ± 12.31	127.22 ± 17.86	-0.6283	0.532
ALB (g/L, mean ± SD)	39.82 ± 2.77	39.19 ± 3.18	1.023	0.31
History of abdominal surgery, n (%)			3.2142	0.073
Yes	9 (20.0)	17 (34.0)
No	36 (80.0)	33 (66.0)
History of neoadjuvant therapy, n (%)			0.2532	0.615
Yes	7 (15.6)	6 (12.0)
No	38 (84.4)	44 (88.0)
ASA level, n (%)			1.1332	0.287
II	30 (66.7)	28 (56.0)
III	15 (33.3)	22 (44.0)

¹Z value.

²χ² value.

³t value.

R-TME: Robot-assisted total mesorectal excision; L-TME: Laparoscopic-assisted total mesorectal excision; BMI: Body mass index; HGB: Hemoglobin; ALB: Albumin; ASA: American Society of Anesthesiologists.

Perioperative and pathological data between the two groups of patients

Table 2 shows that neither group of patients underwent a switch to laparotomy during surgery, and there was no positive surgical margin according to postoperative pathology. Moreover, there were no significant differences between the two groups in terms of intraoperative bleeding, transfusion volume, stoma rate, lymph node clearance, postoperative hospital stay, drainage tube removal time, or Foley catheter removal time (P > 0.05). The operation time in the R-TME group was significantly shorter than that in the L-TME group (P < 0.05). In terms of the time to first meal, the R-TME group was significantly better than the L-TME group (P = 0.005). However, the cost of R-TME was significantly greater than that of L-TME (P < 0.005).

Table 2 Perioperative and pathological data between the two groups of patients.

	R-TME (n = 45)	L-TME (n = 50)	t/Z/χ2 value	P value
Operation time [min, Md (IQR)]	145 (125, 187.5)	180 (148.75, 206.25)	-2.8051	0.005
Intraoperative bleeding [mL, Md (IQR)]	80 (40, 100)	100 (30, 162.5)	-0.981	0.327
Conversion to laparotomy, n (%)	0	0	-	-
Transfusion, n (%)	0 (0)	1 (2)	-	1.0
Ostomy, n (%)	16 (35.56)	26 (52.0)	2.8062	0.246
No	29	24
Ileostomy	12	21
Colostomy	4	5
Positive rate of cutting edge, n (%)	0	0	-	-
Number of lymph node dissection [n, Md (IQR)]	16 (12, 20)	15 (12, 17)	1.0931	0.278
Postoperative hospitalization days [d, Md (IQR)]	8 (7, 9)	7 (7, 10)	-0.5661	0.571
Time of first liquid feeding [d, Md (IQR)]	3 (3, 4)	4 (3, 5)	-1.9771	0.048
Drainage tube removal time [d, Md (IQR)]	6 (6, 7)	6 (5, 7)	-0.171	0.865
Foley catheter removal time [d, Md (IQR)]	3 (3, 4.5)	4 (3, 5)	-1.6671	0.096
Expenditure [RMB, Md (IQR)]	77528.84 (67871.24, 92400.57)	61756.95 (54587.1, 71251.51)	-5.2311	< 0.005

¹Z value.

²χ² value.

R-TME: Robot-assisted total mesorectal excision; L-TME: Laparoscopic-assisted total mesorectal excision.

Postoperative complications

Table 3 shows a comparison of postoperative complications between the two groups. The incidence of postoperative complications was 8.89% in the R-TME group compared with that in the L-TME group. Among them, L-TME had 1 patient with intestinal obstruction combined with abdominal infection and 1 patient with intestinal obstruction combined with pulmonary infection, and there was no significant difference in the incidence of various complications or CD grade between the two groups.

Table 3 Postoperative complications, n (%).

Intraoperative complication	R-TME (n = 45)	L-TME (n = 50)	P value
Ureteral injury	0	0	-
Acute cardiovascular disease	0	0	-
Postoperative complication	4 (8.89)	6 (12.0)	0.874
Postoperative complication	0	0	-
Significant blood loss	0	0	-
Ileus	2 (4.44)	4 (8.0)	0.773
Abdominal infection	1 (2.22)	2 (4.0)	1
Pneumonia	0	1 (2.0)	1
Acute cerebral infarction	0	0	-
Urinary retention	1 (2.22)	1 (2.0)	1
Acute cardiovascular disease	0	0	-
Acute respiratory failure	0	0	-
Ureteral fistula	0	0	-
Chylous fistula	0	0	-
Complication Clavien-Dindo			0.644
II	4 (4.44)	5 (10.0)	0.854
III	0	1 (2.0)	0.343
IV	0	0	-
V	0	0	-

R-TME: Robot-assisted total mesorectal excision; L-TME: Laparoscopic-assisted total mesorectal excision.

Univariate and multifactorial analysis of complications

Table 4 shows the analysis of factors related to postoperative complications, including age; sex; distance of the tumor from the anal margin; history of cardiopulmonary disease; history of abdominal surgery; BMI; HGB; ALB; history of neoadjuvant chemotherapy; surgical path; intraoperative blood loss; operation time; and whether or not to have a stoma. The results suggested that the operative time and degree of intraoperative bleeding were related to the occurrence of complications. On this basis, the results of multifactor analysis showed that there was no significant relationship between operation time and the occurrence of intraoperative bleeding or complications.

Table 4 Univariate and multifactorial analysis of postoperative complications.

Factors	Single factor analysis			Multiple factor analysis
	OR	95%CI	P Value	OR	95%CI	P Value
Age	1.054	0.961-1.157	0.263
Gender	0.375	0.075-1.874	0.232
Tumor level from anal verge	0.26	0.06-1.121	0.071
History of cardiopulmonary disease	2.074	0.502-8.563	0.313
BMI	1.123	0.893-1.413	0.321
History of abdominal surgery	0.674	0.133-3.411	0.633
HGB	1.028	0.985-1.074	0.2
ALB	0.974	0.78-1.217	0.818
History of neoadjuvant therapy	0	0	0.999
Operation time	1.016	1.004-1.028	0.009	1.007	0.989-1.025	0.461
Surgical path	0.715	0.188-2.718	0.623
Intraoperative bleeding	1.009	1.002-1.015	0.006	1.008	0.999-1.018	0.075
Ostomy	2.279	0.915-5.68	0.077

BMI: Body mass index; HGB: Hemoglobin; ALB: Albumin.

DISCUSSION

Compared with open surgery, laparoscopy has the advantages of being minimally invasive and allowing rapid recovery in the treatment of colorectal cancer[7], and laparoscopic surgery has been widely used to treat rectal cancer surgery. However, laparoscopic surgery also has limitations. Laparoscopic surgery is limited by the pelvis and operation angle, and surgical instruments can easily interfere with each other, which affects the separation of the local tissue in the surgical area. It is easy to injure the ureter and pelvic nerve to maintain urinary and sexual function, and suturing, knotting, and other surgeries are difficult, thus affecting the short-term efficacy of surgery[8]. In terms of the selection of surgical procedures, TME is currently the main surgical treatment for rectal cancer, and some studies have noted that TME has a high long-term survival rate after surgery and can also reduce damage to pelvic nerves and blood vessels and destruction of anal function; however, TME also has disadvantages, such as increased intraoperative bleeding, high need for surgical techniques, a long postoperative hospital stay, and a high incidence of complications. Moreover, the risk of anesthesia, cardiovascular accidents, obesity, and other factors affecting the treatment of elderly patients with rectal cancer increase the uncertainty of the curative effect of laparoscopic TME surgery. With the development of minimally invasive surgery, Da Vinci robots have been used in TME surgery; however, evidence of their clinical superiority in terms of short-term outcomes over conventional rectal surgery conducted by expert surgeons is still lacking[9].

In this study, we compared the short-term efficacy of robot-assisted and laparoscopic TME surgery for elderly patients to determine the advantages of robot-assisted TME surgery for elderly patients. After a comprehensive evaluation of intraoperative and postoperative rehabilitation and pathological radical treatment, it was found that robot-assisted TME surgery had a similar or better short-term prognosis than laparoscopic surgery.

The completeness of TME specimen data reflects the quality of the tumor anatomy during rectal cancer surgery. Neither the robot-assisted surgery group nor the laparoscopic surgery group reported incomplete TME specimens (the results were not shown), which is similar to the conclusion of the prospective study conducted by Kim et al[10]. Therefore, it is not difficult to see that the robot can better complete the tumor results required by TME surgery and has sufficient tumor safety. Because patients who are transferred from minimally invasive surgery to open surgery are more prone to postoperative complications and local recurrence, the conversion rate of surgery is one of the key indicators for demonstrating the progress of surgical technology[11]. In this study, there was no conversion to open surgery in either group, which is similar to the findings of Yamanashi et al[12]. This benefits from the rich expertise of the surgical team in treating rectal cancer, which also proves the surgical safety of robot-assisted surgery.

The number of lymph node dissections and the positive margin of tumor specimens are the main indicators used to evaluate whether rectal cancer surgery is radical[13]. The results of this study showed that there was no significant difference in the number of lymph node dissections or positive margins of tumor specimens between the R-TME group and L-TME group (P > 0.05), which is consistent with the results of Grosek et al[14], Feroci et al[15] and other studies. In terms of operation time, in contrast to the findings of previous studies, the operation time of the robotic group was significantly shorter than that of the laparoscopic group (P < 0.05), which was attributed to the following reasons: (1) The scrub nurses in the robot group needed extensive experience in Da Vinci robot installation and working with the surgeon, had a higher degree of cooperation with the surgeon, and completed more quickly. Studies have shown[16,17] that skilled Da Vinci robotic surgery experience can significantly shorten operation time; and (2) The ostomy rate in the laparoscopic group (51.06%) was greater than that in the robotic group (41.03%), which affected the operation time.

In terms of treatment expenditure, we compared the cost of treatment between the two groups, mainly by calculating the cost before the use of health insurance. The cost of R-TME was significantly greater than that of L-TME (P < 0.005), which may be due to the maintenance of the machine and the failure of widespread popularity of the machine. Additionally, the price will be correspondingly greater, but we can observe that after the use of health insurance, the cost will be greatly reduced, which reduces the burden of the treatment to a certain extent.

Several studies have reported that the pelvis is an associated factor affecting TME operation[18]. The male pelvis is significantly different from the female pelvis. We believe that due to the special physiological structure of male and female patients, surgical data may be different; therefore, we used sex as a variable to investigate the intraoperative and postoperative conditions of male and female patients in the two groups. There were 26 males (57.8%) and 19 females (42.2%) in the R-TME group and 33 males (66%) and 17 females (34%) in the L-TME group, with no significant difference in demographic characteristics at baseline. We also conducted multivariate ANOVA for intraoperative conditions and postoperative recovery. Moreover, there were no significant differences in operation time, intraoperative bleeding, or hospitalization days. However, in terms of the individual statistics for males, the R-TME group had significant differences in operation time (P = 0.042) and intraoperative bleeding evaluation (P = 0.042) compared with the L-TME group, and the robot-assisted effect was significantly better than that of laparoscopy. Although the number of people is small, this may also indicate that robot-assisted surgery does not cause a difference in the outcome of surgery according to sex and may even be more advantageous.

A meta-analysis revealed that a considerable number of elderly patients are at risk for obesity, which significantly affects the quality of surgery and increases the risk of postoperative complications[19]. Therefore, we defined obese patients with a BMI ≥ 25 kg/m² as obese and subdivided them into 13 (28.9%) patients in the R-TME group and 15 (30%) patients in the L-TME group. In this subgroup, there were no significant differences between the two groups in terms of baseline characteristics, operation time or intraoperative bleeding. In terms of postoperative rehabilitation, there were no significant differences in length of stay, intestinal recovery time or postoperative complications. However, in terms of catheter removal time, catheter removal occurred significantly earlier in the R-TME group than in the L-TME (3 vs 4 d, P = 0.001), which was also reflected in Fleming et al’s[19] meta-analysis. This is because the Da Vinci robotic system has a better field of view, can eliminate tremors and movements caused by internal wrist instruments, and allows for more precise anatomical tissue, even in the case of individuals with a high BMI, rich visceral fat and a small operating space; moreover, this system effectively avoids damage to the genitourinary system.

In terms of postoperative recovery, the time of the first postoperative liquid food intake reflects the recovery of intestinal function to a certain extent. This study showed that the time to first postoperative fluid intake in the robotic group was significantly earlier than that in the laparoscopic group (P < 0.05), which was similar to the results obtained by Feng et al[20]. This was mainly because, relative to laparoscopic surgery, robotic surgery was performed through a smaller incision, which reduced the stimulation of abdominal organ tissues and the degree of body damage, and the patients recovered their gastrointestinal function faster after surgery. In contrast, there was no significant difference between the two groups in terms of observational indicators, such as postoperative hospitalization time, drain removal, or catheter removal time (P > 0.05). In terms of complications, there were no serious complications or anastomotic fistulas in either group. The complication rate in the robotic group (8.9%) was lower than that in the laparoscopic group (12.0%). These findings are similar to the results of the retrospective analysis by Xu et al[21], which may be a consequence of the precision of the technique through improved vision and tremorless motion[22].

CONCLUSION

The overall radical outcome and short-term efficacy of robot-assisted TME in the treatment of elderly rectal cancer are similar to those of laparoscopic TME in the treatment of elderly rectal cancer, but robot-assisted TME is better than laparoscopic TME to a certain extent and is not effective in elderly patients; however, the former can shorten the operation time and reduce the recovery time of gastrointestinal function by optimizing the learning curve, which is beneficial for patient prognosis. There are several limitations in this study. The surgical efficacy, occurrence of complications, and prognosis of rectal cancer patients can also be affected by other factors, such as the enrollment of a small number of patients and the lack of comprehensive clinical data; moreover, there are several factors that cannot be evaluated, resulting in a certain bias. In the future, further comprehensive collection of clinical data from patients is needed, expanding the sample size of validation studies. The survival rate and quality of life of elderly patients also need to be considered. Future follow-up studies of these patients will continue to observe the long-term efficacy of robot-assisted surgery to enrich the evidence-based basis of robot-assisted TME surgery for elderly patients.