Transanal down-to-up dissection of the distal rectum as a viable approach to achieve total mesorectal excision in laparoscopic sphincter-preserving surgery for rectal cancer near the anus: a study of short- and long-term outcomes of 127 consecutive patients from a single Japanese institution

doi:10.21203/rs.3.rs-1980972/v1

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Research Article

Transanal down-to-up dissection of the distal rectum as a viable approach to achieve total mesorectal excision in laparoscopic sphincter-preserving surgery for rectal cancer near the anus: a study of short- and long-term outcomes of 127 consecutive patients from a single Japanese institution

https://doi.org/10.21203/rs.3.rs-1980972/v1

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Purpose

In laparoscopic sphincter-preserving surgery (lap-SPS) for rectal cancer (RC), total mesorectal excision (TME) in low RC patients is difficult. This study aimed to evaluate the short- and long-term outcomes of transanal down-to-up dissection of the distal rectum to achieve TME in lap-SPS for RC near the anus.

Methods

A total of 137 consecutive patients with RC near the anus underwent lap-SPS, with either transanal rectal dissection under direct vision (TARD), which mobilized the most difficult portion of TME via the anus, or trans-anal TME (TaTME), which used an endoscopic system, between January 2006 and February 2021.

Results

A total of 127 consecutive patients (87 men), with a median age of 66 years (range: 33–86 years), were included. TARD and TaTME were performed in 51 (40.2%) and 76 (59.8%) patients, respectively. Preoperative treatment was performed in 41 (32.3%) patients. Although operative time in the transanal portion in the TaTME group was longer (p < 0.001), total operative time was unaffected. Median blood loss was lower in the TaTME group (p < 0.001). Postoperative complications developed in 56 (44.1%) patients. TME quality was good for almost all the patients and recurrence occurred in 18 patients (14.2%). The five-year overall survival and disease-free survival rates in the 127 patients were 90.4% and 83.2%, respectively.

Conclusion

Our data suggest that a transanal down-to-up dissection of the distal rectum might be a viable approach in lap-SPS for RC near the anus. Further studies are needed to examine the differences between TARD and TaTME.

Rectal cancer near the anus

laparoscopic sphincter preserving surgery

trans-anal down-to-up dissection of the distal rectum

transanal total mesorectal excision

transanal rectal dissection

Total mesorectal excision (TME) is the standard procedure for reducing local recurrence after rectal cancer (RC) surgery. Although laparoscopic surgery is beneficial in RC surgery, the difficulty of achieving TME in laparoscopic sphincter-preserving surgery (lap-SPS), especially for RC patients with a narrow pelvis, is a critical issue. Improving visualization at the bottom of the pelvis is very useful for achieving complete TME in lap-SPS in RC patients with a narrow pelvis. In addition, improving visualization at the bottom of the pelvis could lead to short-term clinical advantages, including a lower conversion rate to open surgery and less anastomotic leakage [1–5] when compared with conventional abdominal approaches. Technical assistance via the anus for complete TME in lap-SPS is available and includes transanal abdominal transanal (TATA) proctosigmoidectomy with a hand-sewn coloanal anastomosis and transanal TME (TaTME) mobilization of the rectum under endoscopy [6]. We began lap-SPS combined with the transanal rectal dissection (TARD) for RC near the anus, wherein the most difficult portion of TME is mobilized down-to-up (“under direct vision”) via the anus, since January 2006 [7–9]. Since, we have performed TaTME, wherein the most difficult portion of TME is mobilized down-to-up via the anus, using an endoscopic system instead of direct vision, since January 2014. In this study, we aimed to evaluate the surgical and oncological outcomes of transanal down-to-up rectal dissection, including TARD and TaTME, when lap-SPS was performed for RC near the anus.

Patients

This study was approved by the Ethics Committee of the Toho University Omori Medical Center (clearance number: M 21325). We performed lap-SPS combined with TARD or TaTME, to achieve TME in 137 patients with rectal tumors near the anus, between January 2006 and February 2021. In this study, 10 patients have excluded: five patients who required rectal amputation, two patients with gastrointestinal stromal tumors, two patients with neuroendocrine tumors, and one patient with missing data. Thus, we retrospectively evaluated surgical and oncological outcomes in 127 patients. The study population consisted of 51 patients who underwent lap-SPS combined with TARD mobilizing the distal rectum (under direct vision) via the anus, between January 2006 and December 2013 (TARD group) and 76 patients who underwent lap-SPS combined with TaTME (using an endoscopic system instead of direct vision) via the anus, between January 2014 and February 2021 (TaTME group), respectively (Fig. 1).

Outcomes

As for surgical outcomes, we evaluated total operation time, blood loss, the number of dissected lymph nodes, the period to catheter removal, and postoperative complications. Postoperative complications were reported according to the Clavien–Dindo classification. Anastomotic leakage was determined by evaluating a combination of symptoms, imaging and/or radiological findings. Degree of urinary dysfunction was determined by the incidence of re-indwelling urinary catheter, requiring of medicine and/or clean intermittent catheterization after surgery. As for oncological outcomes, we evaluated the pathological quality of the specimen including the mesorectum, circumferential resection margin (CRM), and distal resection margin from the rectal stump (DM); the incidence of recurrence; the overall survival; and the disease-free survival. Specimens were assessed by gastrointestinal pathologists. The quality of the mesorectum was defined according to the method defined by Quirke et al. [10]. The patients were followed up after surgery as follows: blood tests including carcinoembryonic antigen (CEA) and carbohydrate antigen (CA 19 − 9) were performed every 3 months. Computed tomography (CT) and/or abdominal ultrasonography were performed every 3 months in the first 3 years and every 6 months thereafter to check for cancer recurrence. Local recurrence was defined as any recurrence that was diagnosed or suspected in the pelvis.

Indication of transanal down-to-up rectal dissection combined with lap-SPS for RC near the anus

We chose transanal down-to-up rectal dissection to perform lap-SPS for RC near the anus. Inter-sphincteric resection (ISR) was indicated for lesions < 5 cm from the anal verge, excluding cases of clinical stage IV cancer. According to the UICC TNM classification of malignant tumors, we first evaluated clinical TNM staging using enhanced CT and magnetic resonance imaging (MRI). For locally-advanced tumors with clinical stage N2-3 and/or suspected direct invasion to adjacent organs (including the prostate, vagina, and levator ani muscle), we administered chemoradiation therapy (CRT) with S-1 or neoadjuvant chemotherapy (NAC) before surgery. Subsequently, we evaluated the final TNM staging using enhanced CT and MRI. Patients with obvious findings of direct invasion to adjacent organs were excluded from the indication of lap-SPS with transanal mobilization, and instead underwent rectal amputation.

Surgical procedure

The surgical technique for TARD has been previously described [7]. First, division of the rectum was initiated at the posterior side: ≥ 2 cm for clinical T2 and 3 cancers or ≥ 1 cm for clinical T1 cancer, distal to the tumor margin. As for the goal of TARD, division and mobilization of the distal rectum (including the mesorectum) is performed “under direct vision”, both anteriorly (until the peritoneal reflection is identified) and posteriorly (until the sacral promontory beyond the rectosacral ligament is nearly reached), using an electronic scalpel and a pusher. However, we dissected both anterolateral sides of the rectum, where the neurovascular bundle was located transabdominally. We immediately converted to rectal amputation if we suspected any findings of direct invasion of the external anal sphincter or levator ani muscles during dissection of the internal and external anal sphincter muscles.

Contrastingly, for TaTME, division and mobilization of the rectum (including the mesorectum) is performed using an electric scalpel under an endoscope, instead of under direct vision. In this series, because all RCs were located ≤ 5 cm from the anal verge, we dissected the distal rectum under direct vision, beyond the anorectal ring, to access the E Z ACCESS (Hakko. Co., Ltd. Medical Division, Japan) as a platform for the TaTME.

Second, we initiated the laparoscopic procedure. The sigmoid colon mesentery was mobilized, preserving the superior hypogastric plexus. The lymph nodes around the inferior mesenteric artery were dissected with a harmonic scalpel. The inferior mesenteric artery was ligated at a high level, using an endoclip. The sigmoid and descending colons were mobilized completely from the sub-retroperitoneal fascia to ensure that the subsequent coloanal anastomosis was free of tension. During peritoneal reflection, exposing the seminal vesicles and prostate gland or the posterior of the vagina is relatively easy. On the posterior of the rectum, we mobilized the lower rectum with the mesorectum from the sacrum towards gauze, which was placed at the separated plane between the visceral and parietal endopelvic fascia, via the anus, as a landmark. The lateral ligaments of the rectum are gradually divided with an electric and/or harmonic scalpel, from the inner limit of the inferior hypogastric nerve fibers. The rectum, including the total mesorectum, could thus be removed from the pelvic floor. Finally, the colon and rectum were removed from the umbilical wound and resected. Coloanal anastomosis was transanally performed by hand suturing. A diverting ileostoma was created for each procedure. All the procedures were performed by a single team (Fig. 2).

Statistical analysis

Comparisons between the two groups were performed using Chi-square (χ²) or Fisher’s exact tests for categorical variables and Mann–Whitney U tests for continuous variables. Tests of significance were two-sided, and p values < 0.05 were considered statistically significant. All data were entered into a computer database and analyzed using EZR version 1.55 [11], which is for R. EZR is a modified version of the R commander designed to add statistical functions frequently used in biostatistics.

Patient characteristics

The characteristics of 127 patients are presented in Table 1. The study population consisted of 87 men, with a median age of 66 years. Preoperative treatments were administered to 41 (32.3%) of the 127 patients, including 29 patients who received CRT and 12 patients who received NAC. Five (12.2%) of the 41 patients showed a complete pathological response. TARD and TaTMEs were performed in 51 (40.2%) and 76 (59.8%) patients, respectively. Among the 51 patients with TARD and 76 patients with TaTME, significantly more men were present in the TaTME group (p = 0.031). In addition, all 16 patients who received CRT as preoperative treatment were included in the TARD group. No significant differences in age, body mass index, preoperative treatments, TNM factors, or pathological stage (pStage) were observed between the groups. Ultra-low anterior resection with coloanal anastomosis by hand suturing and ISR were performed in 79 (62.2%) and 48 (37.8%) patients, respectively. ISR was performed more frequently in the TARD group than in the TaTME group (56.9% versus 25.0%; p < 0.001).

Table 1. Patient characteristics

	Total (n = 127)	TARD (n = 51)	TaTME (n = 76)	P value[A1]
Sex, n (%)				0.031**
Male	87 (68.5)	29 (56.9)	58 (76.3)
Female	40 (31.5)	22 (43.1)	18 (23.7)
Age*	66 (33-86)	64 (33-77)	67 (41-86)	0.237
Body mass index*	21.9 (16.7-41.8)	21.6 (16.7-37.2)	22.4 (16.8-41.8)	0.592
Preoperative treatment, n (%)				1.000
Positive	41 (32.3)	16 (31.4)	25 (32.9)
CRT	29 (22.8)	16 (31.4)	13 (17.1)
NAC	12 (9.5)	0	12 (15.8)
Negative	86 (67.7)	35 (68.6)	51 (67.1)
Resection of the AIS
ISR	48 (37.8)	29 (56.9）	19 (25.0)	<0.001**
Ultra-LAR with CAA	79 (62.2)	22 (43.1)	57 (75.0)
Tumor related factor
T, n (%)				0.231
1b	22 (17.3)	10 (19.6)	12 (15.8)
2	38 (29.9)	14 (27.5)	24 (31.6)
3	56 (44.2)	24 (47.1)	32 (42.1)
4a	6 (4.7)	0 (0)	6 (7.9)
pCR	5 (3.9)	3 (5.8)	2 (2.6)
N, n (%)				1.000
Positive	33 (26.0)	13 (25.5)	20 (26.3)
Negative	94 (74.0)	38 (74.5)	56 (73.7)
M, n (%)				1.000
Positive	0 (0)	0 (0)	0 (0)
Negative	127 (100)	51 (100)	76 (100)
pStage, n (%)				0.804
I	53 (41.7)	22 (43.1)	31 (40.9)
II	35 (27.6)	13 (25.5)	22 (28.9)
III	34 (26.8)	13 (25.5)	21 (27.6)
pCR	5 (3.9)	3 (5.9)	2 (2.6)
: median (range) *: p<0.05 when comparing patients who underwent TARD to patients who underwent TaTME CRT: chemoradiation therapy, NAC: neoadjuvant therapy, AIS: the anal internal sphincter muscle, ISR: intersphincteric resection, Ultra-LAR: ultra-low anterior resection, CAA: coloanal anastomosis, pCR: pathological complete response, pStage: pathological stage, TARD: transanal rectal dissection, TaTME: transanal total mesorectal excision,

Surgical outcomes

Table 2 shows the surgical outcomes of the patients. Median operative time of the perineal portion was significantly longer in the TaTME group than in the TARD group (95 versus 145 minutes; p < 0.001), but total operation time was not significantly different between the groups. Median blood loss was significantly lower in the TaTME group than in the TARD group (278 versus 83.5 ml; p < 0.001) and the median number of dissected lymph nodes was significantly higher in the TaTME group compared to that of the TARD group (9 nodes versus 10 nodes; p = 0.024). The median period for urinary catheter removal following surgery was five days (ranging from 3–16 days) in the TaTME group, which was significantly longer than the four days (ranging from 2–18 days) of the TARD group (p < 0.001). Postoperative complications (Clavien–Dindo classification grade ≥ 2) occurred in 56 (44.1%) of the 127 patients: 19 (37.3%) patients in the TARD group and 37 (48.7%) patients in the TaTME group (p = 0.502). In addition, severe postoperative complications (Clavien–Dindo classification grade ≥ 3) occurred in 25 (19.7%) of the 127 patients: 10 (19.6%) patients in the TARD group and 15 (19.7%) patients in the TaTME group (p = 1.000).

Table 2

Surgical outcomes
	Total (n = 127)	TARD (n = 51)	TaTME (n = 76)	P-value
Total operative time, minutes*	431 (291–906)	419 (291–625)	445.5 (309–906)	0.133
Perineal portion	123 (26–261)	95 (26–174)	145(62–178)	< 0.001**
Abdominal portion	316 (163–589)	319 (214–528)	302 (163–589)	0.189
Blood loss, ml*	110 (0-1097)	278 (0-1097)	83.5 (0-765)	< 0.001**
Number of dissected LN, n*	10 (0–38)	9 (2–38)	10 (0–36)	0.274
Period to catheter removal*, day	5 (2–18)	4 (2–18)	5 (3–16)	< 0.001**
Postoperative complication (C-D ≧ grade 2), n (%)				0.502
Positive	56 (44.1)	19 (37.3)	37 (48.7)
Negative	71 (55.9)	32 (62.7)	39 (51.3)
Postoperative severe complication (C-D ≧ grade 3), n (%)
Positive	25 (19.7)	10 (19.6)	15 (19.7)	1.000
Negative	102 (80.3)	41 (80.4)	61 (80.3)
: median, (range) *: p < 0.05 when comparing patients who underwent TARD to patients who underwent TaTME LN: lymph node, C-D: the Clavien-Dindo classification,. TARD: transanal rectal dissection, TaTME: transanal total mesorectal excision,

No cases of mortality occurred in our cohort. Urinary dysfunction was the most frequent complication, occurring in 17 (13.4%) of the 127 patients, followed by stoma-related complications (occurring in 16 [12.6%] of the 127 patients) and leakage (occurring in 12 [9.4%] of the 127 patients, including one patient in the TARD group requiring reoperation because of major anastomotic leakage). As for urinary dysfunction, 14 (11.0%) patients required urinary catheter re-indwelling, including one (0.8%) patient who required clean intermittent catheterization. Finally, 11 patients (8.7%) required medication for urinary dysfunction. Outlet obstruction and high-output stoma, as stoma-related complications, developed most frequently. No significant differences in postoperative complications were observed between the groups (Table 3).

Table 3

Postoperative complications (Clavien-Dindo classification grade ≥ 2)
	Total (n = 127)	TARD (n = 51)	TaTME (n = 76)	P-value
Leakage, n (%)	12 (9.4)	3 (5.9)	10 (11.8)	0.359
Pelvic abscess, n (%)	9 (7.1)	3 (5.9)	6 (7.9)	0.739
Stoma-related complication, n (%)	16 (12.6)	6 (11.8)	10 (13.2)	1.000
Outlet obstruction	7 (5.5)	2 (3.9)	5 (6.6)
High output	8 (6.3)	3 (9.8)	5 (6.6)
Parastomal abscess	2 (1.6)	1 (2.0)	1 (1.3)
Collapse	1 (0.8)	1 (2.0)	0 (0)
Gangrenous pyoderma	1 (0.8)	0 (0)	1 (1.3)
Ileus, n (%)	10 (7.9)	6 (11.8)	4 (5.3)	0.199
Urinary dysfunction	17 (13.4)	6 (11.8)	11 (14.5)	0.793
Urinary catheter re-indwelling, n (%)	14 (11.0)	6 (11.8)	8 (10.5)	1.000
Medication, n (%)	11 (8.7)	6 (11.8)	5 (6.6)	0.347
CIC, n (%)	1 (0.8)	1 (2.0)	0 (0)	1.000
Others, n (%)	3 (2.4)	1 (2.0)	2 (2.6)	1.000
CIC: clean intermittent catheterization, TARD: transanal rectal dissection, TaTME: transanal total mesorectal excision,

Oncological outcomes

We achieved complete or nearly complete TME in all patients in this study. In addition, we identified a negative circumferential margin in all the patients. As for DM, the median distance of the distal resection margin from a tumor was longer in the TARD group than in the TaTME group (20.0 versus 15.0 mm; p < 0.01). Five (3.9%) patients had a complete pathological response to preoperative treatment. Finally, excluding the five patients with complete pathological responses, the number of patients with pathological Stage I, II, and III was 53 (41.7%), 35 (27.6%), and 34 (26.8%), respectively (Table 4).

Table 4

Oncological outcomes
	Total (n = 127)	TARD (n = 51)	TaTME (n = 76)	P-value
TME, n (%)				1.000
Complete	123 (96.9)	49 (96.1)	74 (97.4)
Nearly complete	4 (3.1)	2 (3.9)	2 (2.6)
Incomplete	0 (0)	0 (0)	0 (0)
CRM, n (%)				0.439
Positive	4 (3.1)	3 (5.9)	1 (1.3)
Negative	123 (96.9)	48 (94.1)	75 (98.7)
DM				0.516
Positive, n (%)	2 (1.6)	0 (0)	2 (2.6)
Negative, n (%)	125 (98.4)	51 (100)	74 (97.4)
Distance* mm (range)		20 (3–59)	15.0 (0.5–85)
Final stage, n (%)				0.804
0	0	0 (0)	0 (0)
Ⅰ	53 (41.7)	22 (43.1)	31 (40.8)
Ⅱ	35 (27.6)	13 (25.5)	22 (28.9)
Ⅲ	34 (26.8)	13 (25.5)	21 (27.6)
Ⅳ	0 (0)	0 (0)	0 (0)
pCR	5 (3.9)	3 (5.9)	2 (2.7)
Final stage, n (%)		0		0.711
I	53 (41.7)	22 (43.1)	31 (40.8)
II + III	69 (54.3)	26 (51.0)	43 (56.6)
*: median, TME:: total mesorectalexcision, CRM: circumferential resection margin, DM: distal resection margin, pCR: pathological complete response, TARD: transanal rectal dissection, TaTME: transanal total mesorectal excision

Recurrence developed in 18 (14.2%) of 127 patients, with a median observation time of 1425 (ranging from 69-4975 days) days: one patient with a complete pathological response, four patients with pStage I, three patients with pStage II, and 10 patients with pStage III. Recurrence rates in pStage I, II, and III were 7.5% (4/53 patients), 8.6% (3/35 patients), and 29.4% (10/34 patients), respectively, and a high recurrence rate was found in locally-advanced cancers, such as pStage III cancers. Lung metastases (6.7%) developed most frequently, followed by pelvic lymph nodes (3.9%) and local recurrence (0.8%). The median period until recurrence was 18.5 (ranging from 4–41 months) months. No significant differences in each of the recurrence patterns and the median period until recurrence were observed between the groups (Table 5). Overall survival (OS) and disease-free survival (DFS) are shown in Fig. 3. The five-year OS and DFS rates in the 127 patients who underwent transanal down-to-up dissection of the distal rectum were 90.4% and 83.2%, respectively. Although the five-year OS rates between the two groups were comparable (93.8% in the TARD group versus 85.7% in the TaTME group; p = 0.261), the five-year DFS rates were significantly lower in the TaTME group than in the TARD group (92.0 versus 69.0%; p = 0.024) (Fig. 4).

Table 5

Recurrence rates
	Total (n = 127)	TARD (n = 51)	TaTME (n = 76)	P-value
Recurrence, n (%)				1.000
Negative	109 (85.8)	45 (88.2)	64 (84.2)
Positive	18 (14.2)	6 (11.8)	12 (15.8)
Lung	6 (4.7)	2 (3.9)	4 (5.3)
Liver	1 (0.8)	0 (0)	1 (1.3)
Liver + local	1 (0.8)	0 (0)	1 (1.3)
Lung + liver	1 (0.8)	1 (2.0)	0 (0)
Bone	1 (0.8)	0 (0)	1 (1.3)
Para-aorta lymph node	1 (0.8)	0 (0)	1 (1.3)
Lymph nodes in the pelvis	5 (3.9)	2 (3.9)	3 (3.9)
Local	1 (0.8)	1 (2.0)	0 (0)
Wound	1 (0.8)	0 (0)	1 (1.3)
Period until recurrence*, month (range)	18.5 (4–41)	17.5 (4–41)	19 (4–32)	0.908
Median observation time, day (range)	1425 (69-4975)	2894 (670–4975)	1047 (69-2361)	< 0.001**
**: p < 0.05 when comparing patients who underwent TARD to patients who underwent TaTME TARD: transanal rectal dissection, TaTME: transanal total mesorectal excision,

Achieving complete TME in lap-SPS for mid- and low-RC is a significant oncological issue. Therefore, various strategies to achieve complete TME have been developed. Marks et al. [12] first reported favorable outcomes of cancer of the distal 3 cm of the true rectum by TATA with a hand-sewn coloanal anastomosis. Marks et al. [13,14] then reported the usefulness of TATA in lap-SPS for rectal cancer. Kanso et al. [15] evaluated the short- and long-term outcomes of 138 patients treated with the primary perineal approach, compared to the primary abdominal approach, in ISR for low RC. The researchers concluded that a primary perineal approach could be considered the standard strategy for lap-SPS for low RC, because of reduced operative time and similar short- and long-term outcomes. In addition, a randomized trial by Denost et al. [16] suggested that perineal rectal dissection was a new standard in lap-SPS for low RC, since perineal rectal dissection reduced the risk of positive CRM in low RC.

In 2006, we started TARD combined with lap-SPS as a strategy to achieve complete TME in lap-SPS for RC near the anus — a procedure that mobilizes the most different portion of TME, “under direct vision”, in a down-to-up manner via the anus. We have been performing TaTME, using an endoscopic system, in lap-SPS for RC near the anus since January of 2014. Recently, TaTMEs have been extensively studied, worldwide. In this study, we aimed to evaluate the feasibility of transanal down-to-up dissection of the distal rectum, including TARD, to assist in achieving complete TME in lap-SPS for RC near the anus, assessing the surgical and oncological outcomes of these two procedures.

Regarding surgical outcomes, TaTME significantly reduced blood loss when compared with TARD. In contrast, using TARD to dissect the distal rectum under direct vision might be a simpler procedure, because operative time of the perineal portion in TARD was shorter than that of TaTME; however, the shorter operative time of the perineal portion did not affect total operative times of either procedure, in this study.

Second, in this study, no cases of mortality occurred; however, we experienced relatively high rates of postoperative complications, with 44.1% of patients displaying Clavien–Dindo classification grade ≥ 2 and 19.7% of patients displaying Clavien–Dindo classification grade ≥ 3. Urinary dysfunction was the most common postoperative complication, followed by stoma-related complications and leakage. According to previous studies, the incidence of postoperative complications in the TARD group is nearly equivalent. Kanso et al. [15] reported overall morbidity and severe morbidities in ISR with a primary perineal approach in 47% and 16% of patients, respectively. Also, Denost et. al. [16] reported that surgical morbidity occurred in 12% of lap-SPS cases.

In a study by Roodbeen et al. [17], postoperative complications (Clavien–Dindo classification grade ≥ 2 and ≥ 3) developed in 13 (31.7%) and 9 (22.0%) patients (out of 41 patients) with TaTME, respectively. In another study by Munini et al. [18], the frequency of Clavien–Dindo classification grade ≥ 2 was 28.9% in TaTME patients, while grade ≥ 3 classifications were absent. In contrast, Hallam et al. [19] reported more favorable outcomes: postoperative complications (Clavien–Dindo classification grades ≥ 2 and ≥ 3) occurred in 14% (10/70 patients) and 11% (8/70 patients) of patients, respectively. In a recent systematic review and meta-analysis by An et al. [20], the overall morbidity of TaTME was 30%, including leakage at 6.8%.

Colorectal surgeons are aware that urinary morbidity is an important clinical issue during down-to-up dissection of the rectum via the anus. In other studies, the rate of urinary injury has been reported to be 1–11%. Klein et al. [21] reported that, although urinary function was preserved in 89% of 115 patients, urethral injury occurred in one patient, while six (5%) patients required permanent urinary catheterization. In addition, Sylla et al. [22] analyzed urologic injuries in TaTME patients and reported 34 urethral, two ureteral, and three bladder injuries occurring during TaTME, performed over seven years, by 32 surgical teams.

In this study, although none of our patients incurred urethral injury, urinary dysfunction developed in 17 (13.4%) patients, including 11 (8.7%) patients who required medication for urinary dysfunction. In general, a transanal down-to-up approach to the rectum, including TARD and TaTME, is likely to injure the urethra and its associated neurovascular bundle. In particular, anterior dissection of the distal rectum is, technically, very difficult because of anatomical complexity, where attention must be paid to the neurovascular bundle located at the anterolateral side of the rectum, to avoid urinary morbidity after surgery. In TARD, we performed dissection not transanally, but abominably, for the anterolateral side of the rectum — where the neurovascular bundle is located. In contrast, taking advantage of good vision under endoscopy in TaTME, we aggressively attempted transanal dissection around the neurovascular bundle. For these reasons, urinary morbidity might have occurred more frequently in the TaTME group than in the TARD group. In addition, 11.8% (6 patients) of patients in the TARD group required medication for urinary dysfunction. This was thought to be due to blind dissection under direct vision, at the anterior side of the rectum.

Leakage is a critical issue in transanal down-to-up rectal dissection procedures. Previous studies have reported an anastomotic leakage rate of between 5.5%- 17.9% [17–21, 23].

The international TaTME registry reports a morbidity rate of 35.4%, including an anastomotic failure rate of 15.7%, a pelvic abscess rate of 4.7%, an anastomotic fistula rate of 0.8%, a chronic sinus rate of 0.9%, and an anastomotic stricture rate of 3.6%. The registry also reported that male sex, obesity, smoking, diabetes mellitus, tumors > 25 mm, excessive intraoperative blood loss, manual anastomosis, and prolonged perineal operative time were independent risk factors for anastomotic failure [24].

In this study, anastomotic leakage occurred in 9.4% of patients, including one patient who required reoperation because of ischemia at the anastomotic site [25]. However, for other patients with leakage, we could only treat the patients conservatively, with interventional radiological drainage. The reason for this might be because diverting ileostomas were created in all patients. In addition, in this study, stoma-related complications occurred more frequently than expected, where most patients had outlet obstruction and/or a high-output stoma. Stoma-related complications could be associated with the fact that we created a stoma at the ileum, and not at the transverse colon, for all patients.

Third, to clarify the feasibility of down-to-up dissection for RC, focusing on oncological outcomes is also important. In particular, local recurrence is of great concern. We achieved complete or nearly complete TME in all patients. In addition, we obtained safe surgical margins, including the CRM and DMs in both groups. Jiang et al. conducted a systematic review and meta-analysis [26] showing that TaTME had more advantages in terms of a positive CRM and DM than laparoscopic did TME. We believe that transanal down-to-up dissections have some benefits. First, we could convert the procedure to rectal amputation whenever any direct invasion of the adjacent organs (such as the vagina, prostate, and seminal vesicle) was suspected during mobilization of the distal rectum [27]. Second, with down-to-up dissections under direct vision, we could obtain an adequate distant margin from the end of the tumor. For patients who needed ISR to preserve the anus for RC near the anus, we obtained an adequate distance from the end of the RC. For five patients in whom the tumor was suspected to invade the external sphincter muscle or the adjacent organs (such as the prostate and vagina), we could choose an adequate surgery for rectal amputation, from an oncological perspective.

In this study, recurrence developed in 14.2% (18/127) of patients. Although no significant difference in recurrent organs was found between the two groups, we observed a high recurrence rate of 29.4% even in pStage III, compared with 7.5% in pStage I and 8.6% in pStage II. Metastasis to the lungs and local recurrence, including the lymph nodes of the pelvis, was frequent. Wasmuth et al. [28] reported a high local recurrence rate of 7.6% (12/157 patients) at a median follow-up of 20 months, including eight expected patterns of multifocal or extensive local recurrences, resulting in the abandonment of TaTME in Norway. van Oostendorp et al. [29] reported the short-term outcomes of 120 patients with TaTME performed at 12 centers. The overall local recurrence rate was 10%, with a mean interval to recurrence of 15.2 months. Multifocal local recurrence was present in eight of 12 patients. In a prolonged cohort (266 patients), overall multifocal local recurrence rate was 5–6%. The researchers stated that multifocal local recurrence may be closely associated with suboptimal TaTME execution. In both studies, most local recurrences were multifocal or extensive. In our study, we did not experience the same degree of multifocal or extensive local recurrence, as reported in the literature.

In a prospective multicenter study in Denmark [2], the plane of dissection was mesorectal in 60% of the cases, intra-mesorectal in 28%, and muscularis in 12%. Non-micro-radicality was observed in 8% of cases, although microscopic and macroscopic residual tumors were observed in 6% and 2%, respectively. Although local recurrence rate was 3.5% (4/115 patients), one patient had multifocal recurrence at a median follow-up of 23 months. A systematic review with meta-analysis by Jiang et al. [26], examining pathological outcomes of transanal versus laparoscopic TME for RC, reported that TaTME had better outcomes for positive CRM than did laparoscopic TME. However, Caycedo-Marulanda et al. [30] reported that a positive CRM increased the risk of local recurrence 4.2 times more than did a negative CRM. Local recurrence is likely closely associated with positive CRM. Therefore, we emphasize cognizance regarding the development of multifocal or extensive local recurrence in a transanal down-to-up dissection of the rectum, which could be closely associated with a positive CRM. Preoperative treatment is important for patients with locally-advanced RC.

Finally, in this study, a favorable survival rate was found, with a five-year OS rate of 90.4% and a five-year DFS rate of 83.2%. In comparing the two groups, although no difference in five-year OS was found between the groups (93.8% in the TARD group versus 85.7% in the TaTME group), the five-year DFS in the TaTME group (69.0%) was significantly lower than that of the TARD group (92.0%), though we could not identify why this result was obtained.

Marks et al. [15] reported a five-year OS rate of 90% (regarding long-term outcomes) after a transanal approach to TME for RC. In addition, Denost et al. [31] reported that the five-year OS and DFS rates of transanal low rectal dissection were 87.0% and 72%, respectively. Recently, we found studies evaluating long-term outcomes of TaTME. Hol et al. [32] reported that the five-year DFS and OS rates in 159 consecutive patients with TaTME were 81% and 77.3%, respectively. In addition, Ourô et al. [33] reported that the five-year DFS and OS rates in 44 patients with TaTME were 87.0% and 81%, respectively.

Recent meta-analyses [34–39] suggest that transanal down-to-up dissection procedures, including TARD and TaTME, might be an acceptable procedure in lap-SPS for mid-and low-RC. However, at present, we reason that oncological safety in a transanal down-to-up dissection for RC is still controversial. We must wait for the results of the COLOR III [40] and ETAP-GRECCAR 11 TRIAL [41] studies to further evaluate the efficacy and safety of TaTME.

Limitation

This study had some limitations. First, this study was conducted at a single institution in Japan, and the data were retrospectively analyzed using a small sample size. As a transanal down-to-up dissection of the distal rectum to achieve complete TME is considered to be a difficult technique even for colorectal surgeons, the quality of the techniques could improve with increasing surgical experience. These experiences might affect the surgical and oncological outcomes. However, we could not evaluate the outcomes of 127 patients, especially for the TARD group, in which only 51 patients could be evaluated in this study. The small sample size of the TARD group may cause some bias in surgical and oncology outcomes. Second, in this study, a one-team approach was used for all patients. If the surgery was performed by two teams, we may have reduced both operative time and blood loss, because of improved visualization of the anterior side of the distal rectum. Finally, we should have evaluated functional outcomes following surgery to further evaluate the efficacy and safety of the procedures we performed.

Our data suggest that transanal down-to-up rectal dissections, including TARD, might be an acceptable procedure for achieving TME in lap-SPS for RC near the anus, from both a surgical and an oncological perspective. However, to further confirm the possible superiority of TaTME for advanced RC, large-scale multicenter randomized controlled trials are warranted.

Author’s contributions: Kimihiko Funahashi conceived the idea of the study. Satoru Kagami collected and analyzed the data. Satoru Kagami wrote the manuscript text under supporting of Kimihiko Funahashi. Toshimitsu Ushigome conducted the statistical analysis. Satoru Kagami, Tomoaki Kaneko, Takayuki Suzuki, and Yasuyuki Miura contributed to the interpretation of the results. Takamaru Koda, Yasuo Nagashima, Kimihiko Yoshida, and Akiharu Kurihara contributed to collecting the references related to the study. All authors reviewed the manuscript draft and revised it critically on intellectual content. All authors approved the final version of the manuscript to be published.

Funding: None of the authors have funding to declare.

Compliance with ethical standards

Conflicts of Interest: The authors have no competing interests to declare relevant to this article’s content.

Ethics approval: This study was approved by the Ethics Committee of the Toho University Omori Medical Center (clearance number: M 21325)

Consent to participate: We applied the opt-out method on the home page of Toho University Omori Medical Center to obtain consent for this study.

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No competing interests reported.

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Transanal down-to-up dissection of the distal rectum as a viable approach to achieve total mesorectal excision in laparoscopic sphincter-preserving surgery for rectal cancer near the anus: a study of short- and long-term outcomes of 127 consecutive patients from a single Japanese institution

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Background

Patients And Methods

Patients

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Indication of transanal down-to-up rectal dissection combined with lap-SPS for RC near the anus

Surgical procedure

Statistical analysis

Results

Patient characteristics

Surgical outcomes

Oncological outcomes

Discussion

Limitation

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