Robotic Male and Laparoscopic Female Sphincter-Preserving Total Mesorectal Excision of Mid-Low Rectal Cancer Share Similar Specimen Quality, Complication Rates and Long-Term Oncological Outcomes

Materials And Methods

Study population

This retrospective study evaluated a consecutive series of F-Lap-TME and M-Rob-TME RC patients performed between January 2011 and January 2020. Data were extracted from a prospectively maintained surgical database. Informed consent was obtained from each patient. Inclusion criteria were (Fig. 1): 1) rectal adenocarcinoma; 2) mid-low RC (below 10 cm from the anal verge); 3) no distant metastases (clinical TNM stage I, II, III); 4) minimally-invasive sphincter-preserving TME. Exclusion criteria were: 1) Open surgery; 2) Transanal minimally invasive surgery (TAMIS); 3) Abdominoperineal resections (APR); 4) Metastatic disease.

All resections (robotic and laparoscopic) were performed by a single surgeon (O.A.) at three centers: 1) Istanbul University Faculty of Medicine, Department of General Surgery, Istanbul, Turkey; 2) Liv Hospital, Department of General Surgery, Istanbul, Turkey; 3) Maslak Acibadem Hospital, Istanbul, Turkey. Surgical approach was discussed with each patient and decided according to surgeon’s indication, patient’s opinion, and surgical cost. Preoperative staging included chest X-ray, assessment of carcinoembryonic antigen (CEA) levels, total colonic examination with flexible colonoscopy, thoracoabdominal computed tomography (CT), pelvic-phased array magnetic resonance imaging (MRI), and/or endorectal ultrasound.

Patients with clinical T3, T4, or node-positive disease (stage II and III) were initially treated with either neoadjuvant long-course chemoradiotherapy (5,080 cGy administered in 28 fractions and 5-fluorouracil based chemotherapy). The waiting period was eight-to-twelve weeks for long-course radiotherapy. The performed Lap-TME and Rob-TME technique was previously described [19, 20]. Perioperative outcomes included operation time, conversion to an open procedure, time to first flatus, time to soft diet, and length of postoperative hospital stay. Conversion was defined as any unplanned laparotomy at any time during surgery, regardless of the incision length.

Pathological staging was modified according to the American Joint Committee on Cancer (AJCC) 8th edition staging system during data review [21]. All pathology specimens were examined to determine tumor size, number of lymph nodes harvested, microscopic proximal resection margin (PRM), DRM, CRM, and the integrity of the mesorectum. Quality of mesorectum was assessed according to Quirke et al. [22].

A positive CRM was defined as a direct tumor extension within 1mm of the radial, non-peritonealized surface of the resection specimen [23].

Postoperative complications were defined as adverse events occurring within 30 days from surgery and were assessed according to Clavien-Dindo’s classification [24].

Long-term oncological outcomes were compared between F-Lap-TME and M-Rob-TME groups. Follow-up included control of oncological markers (CEA, Carbohydrate antigen 19 − 9) every three months, evaluation with thoracoabdominal CT annually, and colonoscopy examination on the first, third, fifth, and tenth year from primary surgery.

Overall survival (OS) was measured from date of surgery to that of death/last follow-up, disease-free survival (DFS) to that of tumor recurrence. Recurrence was diagnosed through radiological detection of enlarging lesions or by histological confirmation. This study follows the STROBE statement for cohort studies [25].

Statistical Analysis

Patient characteristics were summarized using basic descriptive statistics. Continuous variables were presented as median (interquartile range, IQR) or mean ± standard deviation accordingly, and compared using the Mann-Whitney U test. Categorical variables were expressed as proportions and analyzed using the Chi-squared or Fisher’s exact test. Statistical analysis was performed using the STATA software package version 9.0 (StataCorp, College Station, TX, USA). Survival and recurrence rates were estimated through the Kaplan-Meier model, and compared by the log-rank test. P values < 0.05 were considered statistically significant.

Results

Clinical Outcomes

A total of 170 consecutive patients were selected for the study: 60 F-Lap-TME and 110 M-Rob-TME. Patient’s demographic and clinical details are listed in Table 1. Both groups were comparable in demographics, BMI, ASA score, tumor location, clinical TNM stage, and neoadjuvant treatment. Perioperative outcomes are summarized in Table 2. There was no conversion to open surgery in both groups. Protective ileostomy was created in 48 (80%) patients from F-Lap-TME and 97 (94%) patients from the M-Rob-TME group (p = 0.494). The mean operation time was significantly longer in the M-Rob-TME group than in the F-Lap-TME group 185.3 ± 28.4 versus 124.5 ± 35.8 minutes (p < 0.001). There was no difference regarding blood loss, bowel activity, or postoperative hospital stay.

Table 1

Demographic and clinical characteristics of the patients. Data are expressed as mean ± standard deviation or n (%). ASA: American Society of Anesthesiologists; BMI: body mass index; CRM: circumferential resection margin; CRT: chemoradiotherapy; CT: chemotherapy
	F-Lap-TME n = 60	M-Rob-TME n = 110	p
Age, years	59.2 ± 11.7	57.5 ± 12.3	0.760
BMI, kg/m2	23.9 ± 1.63	24.7 ± 1.81	0.507
ASA class 1–2 3	56 (93.3) 4 (6.7)	106 (96.4) 4 (3.6)	0.100
Tumor location Mid (5-10cm) Low (< 5cm)	22 (36.7) 38 (63.3)	38 (34.5) 72 (64.6)	0.174
cTNM stage I II III	12 (20.0) 23 (38.3) 25 (41.7)	23 (20.9) 39 (35.5) 48 (43.6)	0.768
Clinical CRM status Clear Involved	58 (96.7) 2 (3.3)	106 (96.4) 4 (3.6)	0.186
Neoadjuvant CRT Yes No	44 (73.3) 16 (26.7)	79 (71.8) 31 (28.2)	0.472
Adjuvant CT Yes No	27 (45.0) 33 (55.0)	47 (42.7) 63 (57.3)	0.214

Table 2

Perioperative outcomes. Data are expressed as mean ± standard deviation, median (interquartile range), or n (%). ISR: intersphincteric resection; LAR: low anterior resection.
	F-Lap-TME n = 60	M-Rob-TME n = 110	p
Surgical technique LAR ISR	46 (76.7) 14 (23.3)	38 (34.5) 72 (65.5)	< 0.001
Anastomosis type Double stapled Handsewn	46 (76.7) 14 (23.3)	43 (39.1) 67 (60.9)	< 0.001
Diverting ileostomy	48 (80.0)	97 (94.0)	0.492
Conversion rate	0	0
Operative time, min	124.5 ± 35.8	185.3 ± 28.4	< 0.001
Estimated blood loss, ml	152.8 ± 24.5	126.3 ± 18.5	0.076
Time to 1st flatus, days	1.6 ± 1.2	1.8 ± 1.4	0.325
Oral re-intake, days	2.1 ± 1.7	2.4 ± 1.5	0.230
Postoperative stay, days	4.3 ± 3.2	4.6 ± 2.8	0.226
Follow up, months	62 (24–120)	64 (24–120)	0.128

Histopathologic outcomes

The histopathological findings are shown in Table 3. The mean number of retrieved lymph nodes (F-Lap-TME vs. M-Rob-TME) were: 26.3 ± 10.4 versus 29.6 ± 8.2 nodes (p = 0.714). The mean length of DRM was 14.50 ± 1.8 mm and 15.7 ± 1.2 mm (p = 0.065), in F-Lap-TME and M-Rob-TME groups, respectively. CRM involvement was observed in two (3.3%) and three (2.9%) in F-Lap-TME and M-Rob-TME patients, respectively (p = 0.210). Incomplete mesorectum was observed in two (3.3%) and three (2.8%) patients of F-Lap-TME and M-Rob-TME groups, respectively (p = 0.508). Other histopathological outcomes, including tumor size, grade of tumor differentiation, and pathological T and N stage, were not significantly different between the two groups.

Table 3

Histopathological outcomes. Data are expressed as mean ± standard deviation or n (%). CRM: circumferential resection margin; ypTNM: Pathological staging according to the American Joint Committee on Cancer (AJCC) 8th edition staging system.
	F-Lap-TME n = 60	M-Rob-TME n = 110	p
Tumor diameter, mm	35.6 ± 20.5	33.8 ± 18.2	0.470
Harvested lymph nodes, n	26.3 ± 10.4	29.6 ± 8.2	0.714
Involved lymph nodes, n	1.8 ± 1.9	1.6 ± 2.2	0.166
Distal margin, mm	14.5 ± 1.8	15.7 ± 1.2	0.065
Involved CRM	2 (3.3)	3 (2.9)	0.210
Integrity of mesorectum Complete/near complete Incomplete	58 (96.7) 2 (3.3)	107 (97.3) 3 (2.7)	0.508
(y)pTNM stage 0 I II III	3 (5.0) 6 (10.0) 23 (38.3) 28 (46.7)	8 (7.8) 30 (27.8) 24 (21.8) 48 (43.6)	0.890
Tumor differentiation Well Moderate Poor	16 (26.7) 38 (63.3) 6 (10.0)	24 (21.8) 68 (61.8) 18 (16.4)	0.745

Postoperative Complications

The overall complication rate was 21.7% (n = 13) for the F-Lap-TME group and 19.1% (n = 21) for the M-Rob-TME group (p = 0.420) Table 4). Postoperative morbidity based on a Clavien-Dindo classification was not significantly different between F-Lap-TME and M-Rob-TME groups (p = 0.650). Incidence of AL was 6.7% (n = 4) and 7.3% (n = 8) in F-Lap-TME and M-Rob-TME patients, respectively. All patients with leakage were treated conservatively by maintaining a pelvic drain until the existing collection was clinically resolved, and postponing the ileostomy closing time. Rectovaginal fistula developed in two (3.3%) patients from the F-Lap-TME group, which further underwent a Martius labial flap interposition procedure. Rectourethral fistula occurred in one (0.9%) patient from the M-Rob-TME group, which was managed with colostomy opening and fistula repairing, and closed after the no evidence of fistula.

Table 4

Postoperative complications. Data are expressed as n (%).
	F-Lap-TME n = 60	M-Rob-TME n = 110	p
Overall complications, n	13 (21.7)	21 (19.1)	0.420
Clavien-Dindo classification I-II III-IV	9 (15.0) 4 (6.7)	14 (12.7) 7 (6.4)	0.650
Anastomotic leakage, n	4 (6.7)	8 (7.3)	0.085
Rectourethral fistula, n	0	1 (0.9)
Ileus, n	2 (3.3)	4 (3.6)	0.660
Colonic ischemia, n	0	1 (0.9)
Rectovaginal fistula, n	2 (3.3)	0
Pelvic abscess, n	2 (3.3)	3 (2.7)	0.240
Wound infection, n	3 (5.0)	4 (3.6)	0.125

Oncological Outcomes

With a mean follow-up of 62 months (range, 24–108) in F-Lap-TME and 64 months (range, 24–108) in M-Rob-TME, the 5-y DFS was 87.5% and 86.5%, respectively. The 5-y OS rates for the F-Lap-TME and M-Rob-TME groups were 90.5% and 89.6%, respectively. Kaplan-Meier OS and DFS curves are reported in Fig. 2. LR occurred in three (5%) patient in the F-Lap-TME and six (5.5%) patients in the M-Rob-TME group. Distant metastasis developed in five (8.3%) and ten (9.1%) patients, respectively in the F-Lap-TME and M-Rob-TME groups.

Discussion

The adoption of minimally invasive surgery in patients with RC has gained tremendous popularity due to its benefits, especially for low lying rectal cancers [26]. Results of the two major randomized trials demonstrated non-inferiority of laparoscopic RC surgery compared to the open approach [27, 28]. The ROLARR randomized clinical trial demonstrated no significant differences between the robotic and conventional laparoscopic TME in terms of conversion rates (adjusted OR = 0.61 [95% CI, 0.31 to 1.21]; p = 0.16). However, the multivariate analysis demonstrated that male (adjusted OR = 2.44 [95% CI, 1.05 to 5.71]; p = 0.04) and obese (adjusted OR = 4.69 [95% CI, 2.08 to 10.58]; p < 0.001) patients were prone to significantly higher conversion rates in the laparoscopic group [29]. Additionally, our recent study showed that obese and male patients with mid-low RC undergoing Lap-TME had a higher conversion rate and poorer specimen integrity and long-term local control compared to those undergoing Rob-TME [17]. The 10-year follow-up of 217 standardized Lap-TME cases performed by a single surgeon (O.A.) between 2005 and 2012, showed that oncological outcomes were adversely affected in open surgery converted patients [19]. In the conversion group (6.5%), DFS was 50.0%, whereas it was 78.3% in the laparoscopic group (p < 0.001). Chan et al. also reported higher rates of LR (9.8% vs. 2.8%; p < 0.001) and reduced cumulative DFS in colorectal cancer patients who had a conversion from laparoscopic to open procedures [30]. In contrast, compared to laparoscopy, robotic RC surgery provided lower conversion rates, better preservation of sexual function, and oncological outcomes [31, 32]. Also, the robotic approach has a shorter learning curve [33] and provides higher camera navigation quality than laparoscopy [34]. If the robotic approach could be theoretically advantageous for male patients with mid-low RC, for female patients both robotic and laparoscopic approach could provide similar results. The aim of the present study was to compare the laparoscopic approach in anatomically easier patients (females) with the robotic approach in anatomically challenging patients (males). Sex differences in pelvic anatomy and reflection on surgical outcomes as well as pathological metrics in RC surgery were widely described previously [35–38].

A female-wide pelvis is beneficial for the maneuverability of laparoscopic instruments during TME for RC. In contrast, it is challenging to perform Lap-TME in male patients with mid-low RC without damaging the mesorectal envelope and obtaining negative DRM and CRM. This was confirmed in our previous study, comparing Lap-TME (n = 84) and Rob-TME (n = 103) techniques in male patients with mid-low RC [17]. Rob-TME provides improved mesorectum specimen compared to Lap-TME (complete mesorectum, 93.2% vs. 44.1%) in male patients with mid-low RC. Additionally, we found differences in conversion rates in male patients with RC concerning laparoscopic and robotic approaches (Lap-TME 3.5% versus Rob-TME 0%) [17]. Also, Rob-TME decreases the local recurrence rate (LRR) and improves OS (LRR: 3.8% vs. 7.1%, OS: 87.0% vs. 85.7%) [17].

Multiple studies have been conducted on comparative analysis of laparoscopic and robotic approaches for RC surgery [17, 20, 29, 39, 40]. The effects of both techniques on perioperative (conversion to open surgery, amount of bleeding, operative time), postoperative (complication rates, length of postoperative hospital stay, pathological parameters), and oncologic outcomes (LRR, DFS, OS) were investigated. However, most of these studies included mixed-sex (male/female) patients. Due to the distinct difference in pelvic anatomy between male and female individuals, questions on superiority of laparoscopic or robotic approaches were made. The effects of these approaches on TME quality in both sex and its reflection on long-term oncological results have not been evaluated yet.

The adult male pelvis is more technically challenging during sphincter-preserving Lap-TME because of its anatomical features: narrow space, oval-shaped pelvic inlet, angle of the public arch less than 90 degrees, and the insertion level of the levator ani muscle which is lower [35]. Limited space restricts maneuverability of laparoscopic instruments, which translates into a decreased quality of mesorectal dissection, associated with higher conversion rate, and particularly impaired local control. Additionally, it becomes challenging to perform division of the rectum, requiring multiple number of staples in the depths of the pelvis which can increase the AL rates [41].

Pathological evaluation is essential for predicting the prognosis of patients after TME. Therefore, CRM, DRM, and mesorectal integrity are pathological metrics that play a crucial role in assessing TME quality and local control [4–6, 23]. Furthermore, the precise dissection provided through the robotic platform may be expected to improve the pathological metrics. Standardized TME procedures performed by experienced surgeons reduced the risk of obtaining CRM-positive specimens [19]. The high rate of CRM positivity reported in the Colorectal Cancer Laparoscopic or Open Resection (COLOR II) trial in the laparoscopic group has raised concerns regarding the feasibility of the laparoscopic approach for rectal cancer [27]. In the prospective study conducted by Baek et al., the CRM involvement was not statistically different between Lap-TME and Rob-TME groups [16].

A recent study showed that the rate of positive CRM was lower in the Rob-TME group than in the Lap-TME group [29]. Aliyev et al. found significant differences in CRM-positive rates between the Lap-TME (7.1%) and Rob-TME (3.0%) groups, including only male patients [17]. The authors concluded that Rob-TME allowed to achieve complete and oncological adequate resection of the specimen with lower CRM involvement than the Lap-TME in male patients [17].

On the contrary, the current study demonstrated that mesorectal integrity, CRM, and DRM results are similar if the TME is performed laparoscopically in females and robotically in male patients with mid-low rectal cancer. Moreover, long-term oncologic outcomes (OS, DFS, and LRR) are comparable in the two groups of patients. There was no conversion to open surgery in both groups of patients. Rob-TME in male patients provided more harvested lymph nodes than Lap-TME in female patients. M-Rob-TME was associated with a more extended operation time than the Lap-TME group. The postoperative complications rates were also comparable among the two groups of patients. Therefore, this study shows that performing Lap-TME in females is as good as Rob-TME in males on perioperative and oncological outcomes. This study could lead to a sex-based analysis between Lap-TME and Rob-TME on a wider scale in order to confirm these results. The possible outcome is to indicate Rob-TME especially to male patients, or generally complex pelvic anatomies, optimizing the implementation of the robotic platform for RC.

This study has several limitations. First of all, it was a retrospective analysis of prospectively collected data from a single surgeon's experience. Second, the number of Lap-TME procedures is lower than Rob-TME. A large prospective randomized study is needed to confirm our results. Third, side of the recurrences was not revealed in this study. Fourth, comparative functional outcomes (urinary, sexual, and overall quality of life) were not evaluated. Fifth, molecular and genetic data were unavailable in this study, and tumor behavioral biology may differ between the two sex, which may have affected the oncological outcomes. And finally, cost-effectiveness was not investigated in this study.

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