Introduction
Total mesorectal excision (TME) and multimodal approach have incredibly changed the long-term outcome of the patients with mid-low rectal cancer.1 Open or laparoscopic trans-abdominal (up-to-down) TME represents the gold-standard approach to rectal cancer.2 However, up-to-down TME is technically demanding, especially in male patients with narrow pelvis, in obese patients, or in patients with low rectal cancer.3 Increased risks of positive circumferential resection margin (CRM) are reported.4,5
In 2012, De Lacy et al6 reported the first case of transanal laparoscopic TME (taTME). Since then, this new technique has gained popularity. Approaching the mesorectal dissection transanally seems to exceed the limits of the gold-standard up-to-down approach with better short-term oncological results.2 However, taTME approach has also shown some pitfalls like a long learning curve and worse short-term results at the beginning of a taTME program.7
In 2015, after a training made of courses, cadaver-labs, and proctored cases, we started to approach transanally all the patients with mild-low rectal cancer.
Aim of the present paper is to report our initial experience with this new technique.
Methods
At the General Surgery Department of the Civil Hospital of Lentini (Siracusa, Italy), between May 2015 and December 2020, 33 patients with rectal cancer underwent a laparoscopic transanal total mesorectal excision (taTME).
All the perioperative clinical data were collected prospectively both on a hospital database and on the International Transanal Total Mesorectal Excision (TATME) registry (https://www.pelicancancer.org/).
All the taTME procedures were performed by a single surgeon (C.P.) with a single-team approach. The first three procedures were performed under the supervision of an experienced tutor (M.A.).
Eligibility criteria for TaTME were patients with mid-low rectal cancer requiring a sphincter-saving low anterior resection (LAR). Patients with cT4 cancer at the preoperative staging were considered not eligible.
Colonscopy, thoraco-abdominal computed tomography (CT), and lower abdomen high-resolution magnetic resonance imaging (MRI) were routinely used to stage patients with rectal cancer. Endorectal ultrasound was used only in cT1–2. Tumor height was measured by MRI, depending on the distance between the distal end of the tumor and the anal margin, and classified as low (up to 5 cm), medium (5.1–10 cm), or high (10.1–15 cm).8 Tumor and nodes distance to the mesorectal fascia of ≤1 mm was recorded as an MRI-involved CRM.9
Indication for neoadjuvant radiotherapy was according to European Society for Medical Oncology (ESMO) guidelines.8
At the end of neoadjuvant chemoradiotherapy protocol (CTRT), all patients were submitted to diagnostic restaging work-up (DRW) with proctoscopy, digital rectal examination (DRE), computer tomography (CT), MRI, or endorectal ultrasound (EUS).
A critical assessment of the surgical approach and of the anastomosis technique was performed for each patient in relation to the tumor’s distance from the anorectal junction, according to Rullier’s classification.10
Postoperative complications were recorded and classified according to the Clavien-Dindo classification for surgical complications.11
Anastomotic leak was defined according to the International Study Group of Rectal Cancer classification.12
Surgical technique
Preoperative mechanical bowel preparation with a polyethylene glycol electrolyte solution was given 2 days before surgery. Systemic antibiotics were administered less than 30 minutes before the induction of anesthesia.
The patient was placed in the modified lithotomy position (Lloyd-Davis), with legs apart thanks to adjustable stirrups and head-down lithotomy. Rectal enema with diluted iodine solution was routinely performed before starting the operation. Sequential pneumatic compression devices were placed and activated before induction of general anesthesia to avoid venous thromboembolism.
The first time of the operation was always the laparoscopic transanal TME followed by the abdominal time.
Laparoscopic transanal TME
A Lone Star Retractor (Lone Star Medical Products Inc, Stafford, TX, United States) is always placed to have a better exposure of the anal canal.
In cases when we decide to perform an intersphinteric resection or an anal sleeve mucosectomy, we perform an initial intersphinteric rectal dissection before making the circumferential purse string, which will be used to tightly close the distal rectal lumen, avoiding the proximal distension of the colon. These procedures are performed with short traditional instruments, under direct vision and without carbon dioxide insufflation.
In mid-high rectal cancers, after placement of the transanal Platform SILS Port (Covidien, Mansfield, MA) or GelPOINT Path (Applied Medical, Inc. Rancho Santa Margarita, CA), the distal purse-string suture is placed and tied. The CO2 is insufflated using the AirSeal iFS insufflator (Conmed Corp, Largo, FL, United States). We started to use this insufflator from the 15th patient and we immediately realized the benefit of perform the rectal dissection without smokes.
The 10-mm, 30-degree videolaparoscope is introduced through the inferior trocar, the grasper or the suction-irrigation cannulas is placed through the left superior trocar, whereas the monopolar electrocautery trough the right superior trocar.
To stitch the purse string, we are used to utilize a monofilament suture such as 0 Polypropylene with a swaged and tapered small-half circle (SH) needle. The purse string is performed about 1 cm below the distal margin of the rectal cancer and it is started posteriorly, at 6 o’clock and continued clockwise. The purse-string suture must be closed tight to have a sealed working environment. Care must be taken to have symmetric suture bites which do not incorporate surrounding tissue. The application of the initial purse string is one of the most important steps because it maintains the “pneumopelvis” making possible the most appropriate pelvic dissection.
Once the purse string suture is tightly closed, the rectal mucosa is circumferentially marked with an electric hook, about 1 cm distal to the purse-string suture and a full-thickness circumferential equally rectotomy is performed.
Instead the dissection of the mesorectal “holy” plane is usually started posterolaterally at the 5 o’clock position and continues circumferentially and evenly.
We avoid to start the dissection form the 6 o’clock position (posterior midline) because the presence of the rectosacral ligament may compromise the identification of the correct plane and make more difficult the dissection. The anterior plane of dissection is conduct anteriorly to the Denonvillier’s fascia only when the rectal cancer is located on the anterior wall. The bottom-up TME dissection continues in accordance with Heald’s principles.
During the dissection, the “bat wings” is a very frequent sign of a correct technique and it is important to pay attention to the recognition and preservation of the inferior hypogastric plexus and the erigentes nerves.
The transanal approach stopped once landmarks were reached, the anterior one is the pelvic peritoneum and posteriorly the sacral promontory and with the section of the double layer of the pelvic peritoneum of the Douglas pouch and the entry into the abdominal cavity.
Then the transabdominal approach started from the top to down until the reunification with the plan obtained during the transanal phase.
Laparoscopic abdominal phase
The patient is placed in Trendelenburg position with moderate right lateral tilt.
When the multiport technique is used, four trocars are placed: a para-umbilical 12-mm port for a 30-degree videolaparoscope, a 11-mm port on the site of the future planned right-sided ileostomy, a 5-mm port in the right hypochondrium, and a 5-mm port on the left flank on the site of the drainage. When a single-port technique is used, The SILS Port (Covidien) is placed on the site of the future planned right-sided ileostomy.
The laparoscopic procedure is performed following the standard steps of laparoscopic anterior TME resection: medial to lateral mesocolic mobilization, releasing of splenic flexure, complete mobilization of the mid-distal transverse colon, and high tie of the inferior mesenteric vessels.
We usually perform a transanal specimen extraction. In case of bulky rectal cancer, the specimen is removed through a Pfannenstiel incision with a wound protector.
Anastomosis
Depending on the location of the tumor, the anastomosis is fashioned either by hand sewing or a double purse-string stapled technique.
When we perform an hand-sewn anastomosis, we usually realize an end-to-end coloanal anastomosis using 2–0 polyglactin (V586H Vicryl, 2-0, FSL needle, 70cm purple filament, pkg=36) sutures.
Rather, when we performed a stapled anastomosis, we realize an end-to-end or side-to-end anastomoses were performed using a EEA 33-mm stapler (Autosuture, Covidien).
The long anvil of hemorrhoidal stapler is placed into the lumen of the proximal bowel and secured using a 2–0 polypropylene purse-string suture. The circular stapler is advanced through the anorectal ring and the trocar of the circular stapler is placed into the anvil. A diverting loop ileostomy is usually performed.
Results
Clinical parameters
Thirty-three patients with rectal cancer were included in this study: 19 males (57.6%) and 14 females (42.4%). The median age and body mass index (BMI) were 67 years (mean 66.87; range 43–86 years) and 27 kg/m2 (mean 26.78 range 19.8–38.1 kg/m2), respectively. According to the classification of the American Society of Anaesthesiologists (ASA), 13 patients (39.4%) were class II, 18 (54.5%) class III, and two (6.1%) class IV (Table 1).
Table 1 -
Preoperative characteristics of the 33 patients undergone taTME.
Characteristic |
Data |
Age, mean |
67 years (mean 66.87; range 43–86 years) |
Sex, n (%) |
|
Male |
19 (57.6%) |
Female |
14 (42.4%) |
BMI, kg/m2; mean |
27 (mean 26.78; range 19.8–38.1 kg/m2) |
American Society of Anesthesiologists score, n (%) |
I |
0 |
II |
13 (39.4%) |
III |
18 (54.5%) |
IV |
2 (6.1%) |
MRI tumor location (30 pt), n (%) |
Upper rectum |
3 (10%) |
Middle rectum |
12 (40%) |
Lower rectum |
15 (50%) |
Preoperative T stage, n (%) |
|
T1 |
1 (3) |
T2 |
7 (21.2) |
T3 |
23 (69.6) |
T4 |
2 (6) |
Preoperative N stage, n (%) |
|
N− |
14 (42.4) |
N+ |
19 (57.5) |
Preoperative staging and neoadjuvant therapy
The median distance of the rectal cancer from anal verge was 6.5 cm (mean: 6.46; range: 3–11 cm): low rectal cancer in 15 patients (50%), mid rectal cancer in 12 (40%), and high rectal cancer in three patients (10%). For three patients, it has not been possible to make an MRI local staging and these patients underwent rectal EUS preoperative staging.
At pretreatment MRI, performed before the neoadjuvant chemoradiation, MRF was positive in 10 patients (30.3%).
At the primary diagnosis, 30 patients (90.9 %) were staged as cT2-3 and 19 (57.5%) as cN+.
Overall, 23 patients (69.7%) underwent long-course neoadjuvant therapy (50 Gy; capecetabine 6 weeks). Up-front surgery was performed in the remaining 10 patients (30.3%).
Rectal cancer restaging was performed about 10 weeks (mean:12; range: 6–51) after the end of neoadjuvant chemoradiation course.
Surgery was performed about 13 weeks after the end of the neoadjuvant therapy course (mean 15.59; range: 8–53 weeks).
Surgical results
All the 33 patients underwent a taTME approach. No conversions occurred.
Of the 33 patients in the study, 20 patients (60.6%) underwent a LAR, and 13 (39.4%) an ultra low anterior resection (ULAR). A partial intersphincteric resection (PISR) was performed in seven patients (53.8%), and a anal sleeve mucosectomy in the remaining six.
As transanal access platform, the COVIDIEN SILS Port, Watford, United Kingdom was used in the first 18 patients (54.6%), whereas the GelPOINTPath, Rancho Santa Margarita, CA, United States was used in the remaining 15 patients.
The CONMED’s AirSeal System Utica, NY, United States was used for the final 17 (51.5%) patients.
During the transanal time of the operation, there were eight (24.2%) intraoperative complications, immediately resolved without conversion to open surgery. There were no urethral or vaginal injury during transanal TME; however there were five (15.1%) cases of failure of purse-string suture which occurred all during the initial phase of the learning curve.
Even with a meticulous suture we could not get a complete lumen closure with an air-tight purse-string suture, with a consequent air spillage.
The abdominal phase of the operation was laparoscopic in 25 patients (75.8%), and open in the remaining eight patients (24.2%). The conversion rate to an open approach was needed in five patients (20%).
Among the patients whose abdominal time of the operation was concluded laparoscopically, specimen extraction was transanal in 10 patients (50 %), through a Pfannestiel incision in eight (40%), and through the SILS site in two (10%).
A loop ileostomy was performed in 30 patients, and a ghost-ileostomy in two patients. An anastomosis was performed in 32 of the 33 patients undergone a LAR, because one patient underwent to Hartmann procedure with end colostomy.
A hand-sewn coloanal anastomosis was performed in 13 patients (40.6%), end-to-end in 12 patients, and side-to-end in one patient, whereas a stapled colorectal anastomosis was performed in 19 (59.4%), end-to-end in 13 patients, and side-to-end in six patients.
The overall operative time was 368 minutes (mean) and the blood loss was less than 200 cc.
Thirty-day morbidity was minor (Clavien-Dindo I + II) in 36% (12 patients) and major (Clavien-Dindo III + IV) in 18.8% (6 patients). One patient died within the first 30 days postsurgery (Clavien-Dindo V).
Short-term outcome
Median hospital stay was 8 days (mean: 10.1; range: 4–29). Postoperative mortality was 3%: one patient died of multiorgan failure. Death occurred among patients ASA IV and cirrotic Child B.
The overall morbidity rate was 36% (12 patients). Overall, four patients (12.5%) had an anastomotic leak, but only two patients (6.2%) have become symptomatic.
Six patients (18.18%) needed a reoperation: two for the anastomotic leak, one for bowel occlusion (torsion of the ileostomy), one for hemoperitoneum, and two for ischemia of the left colon. The remaining two anastomotic leaks were asymptomatic and were treated conservatively (Table 2).
Table 2 -
Early postoperative complications.
Early postoperative complications, 30 postoperative days |
n (%) |
Overall morbidity |
12 (36) |
Conservative treatment |
6 |
Reoperation (2 anastomotic leak, 1 bowel occlusion, 1 hemoperitoneum, 2 ischemia left colon) |
6 |
Anastomotic leakage |
4 (12.5) |
Conservatively treatment |
2 |
Operative treatment (Ileostomy - Hartmann) |
2 |
Postoperative mortality |
1 (3) |
Histopathological results
All the patients had a R0 resection. The median distal resection margin (DRM), CRM were 1.94 cm (range: 0.2–6 cm) and 6.52 mm (range 4–18 mm), respectively. No patients had a positive CRM at final pathology.
The median number of harvested lymph nodes was 12 (mean: 11.5; range: 4–20); the median number of positive lymph nodes was 2 (mean:2.5; range 1–4). The quality of mesorectal excision was complete in 33 cases (100%).
pTNM stage was: pT0 in eight patients (24.2%), pT1 in two (6%) patients, pT2 in11 patients (33.3%), and pT3 in 12 patients (36.3%). Metastatic lymph nodes were present in nine patients (27.3%): pN1 in seven patients and pN2 in two patients (Table 3).
Table 3 -
Histopathologic characteristics of surgical specimens.
Characteristic |
Data |
T stage, n (%) |
|
pT0 |
8 (24.2) |
pT1 |
2 (6) |
pT2 |
11 (33.3) |
pT3 |
12 (36.3) |
N positive stage (%) |
9 patients (27.3) |
Lymph nodes, n, median |
12 |
Tumor size, median (range) |
2 cm (1–5.03 cm) |
DRM; median (range) |
1.94 cm (0.2–6 cm) |
CRM; median (range) |
6.52 mm (4–18 mm) |
Quality of mesorectum, n (%) |
Grade 3: complete |
33 (100) |
Discussion
Rectal cancer is one of the most common malignancies worldwide with an incidence of about 704,000 new cases of rectal cancer to be diagnosed in 2018.13
Sir Bill Heald has incredibly changed the history of rectal cancer surgery. In 1982, he first introduced the concept of TME.1 He recognized that by using meticulous, sharp dissection, under direct vision, staying between the visceral and parietal pelvic fascia down to the level of the levators, or upper aspect of the anal canal, the rectum and its mesentery could be removed as an intact unit. This new surgical approach has allowed great improvements in terms of local recurrence and survival rate.1 Since then, despite an initial skepticism of the surgical community, TME became the gold-standard treatment of rectal cancer.
Technological advances have pushed the surgeons toward laparoscopic and robotic TME procedures. All over the world, laparoscopic approach to rectal cancer is becoming the gold-standard despite the lack of clear scientific evidences in terms of superior short- and long-term outcome.14–16
Moreover, the noninferiority of laparoscopic procedure in terms of oncological outcomes has not been still demonstrated. Up-to-down TME, both open and laparoscopic, has been associated with higher rates of anastomotic leak, conversion to open surgery, incomplete mesorectal excision, and positive CRM,13,15 especially in male patients, in high-BMI patients, or in patients with a narrow pelvis and a low bulky rectal cancer.17 An incomplete mesorectal excision is associated with higher local recurrence rates.18
To overcome these difficulties, the taTME approach was introduced for the first time by Sylla et al.19 Laparoscopic taTME is a new minimally invasive alternative to conventional transabdominal laparoscopic surgery for patients with mid-low rectal cancer.6
Since then several studies has been carried out and taTME appears to be safe in terms of complications and of oncological outcome.20
However, the transanal approach has peculiar challenges, mainly associated with the change in anatomic perspective. Recognizing correct landmarks and know how to orient during the dissection are at the heart of a safe surgical procedure. It is crucial that the surgeon develops the correct plane around the tumor and stays within it. Improved recognition may prevent injury of pelvic nerve, protect the function of pelvic organs and potentially improve outcomes.
The taTME is an advanced and complex technique that requires dedicated training and experience in TME surgery. Before starting this technique, surgeons need to undergo didactic learning, observation of live surgery sessions of taTME procedures, and hands-on courses and local proctoring.21
The international St. Gallen consensus statement suggested that proper training should consist of hands-on courses, proctoring program, and proper supervision in the first 1–5 cases. The learning curve is estimated to be around 20 cases.22
As asserted by Koedam et al,23 the learning curve for taTME would appear to be of 40 cases, indeed at 40 patients, the amount of major surgical complications decreases for the next 60 patients operated on by the primary surgeon.
Extensive training, careful monitoring, and a strict patient selection are the most important factors to keep in mind at the beginning of the experience.
The taTME technique can safely be introduced even in a low-volume hospital only by complying with a defined surgeon population in a controlled fashion using a taTME training, proctoring, and audit pathway.24
A systematic review of published taTME outcomes confirmed that higher volume surgeons (>30 cases) were associated with higher TME quality compared with lower volume surgeons.21,25
We believe that, with proper training and proctoring, the benefits of this technique can be delivered to both colorectal surgeons and patients at medium volume colorectal units like ours.
The key elements of taTME implementation according to Adamina et al22 are: patient selection, perioperative optimization, operating room set up, achieve a correct surgical technique, know very well the transanal pelvic anatomy, have performed a taTME training and constant monitoring of the surgical and functional outcomes.
Once understood the different anatomy point of view, the taTME offers clear visualization of the dissection plane, especially in narrow pelvis and this leads to improve the quality of the TME specimen.26
The pathological specimen is often thought to be an important predictor of the quality of surgery and to predict the prognosis and decrease positive resection margins. De Lacy et al7 reported on the high TME quality with this approach in their experience with 186 patients with mid and low rectal cancers, TME was complete or near-complete in 97.3%. In our hands, we have a rate of 100% complete TME.
In Veltcamp study, two groups of patients with cT1–T3 rectal cancer who underwent TME surgery with LapTME and TaTME with primary anastomosis were included. Postoperative T2-weighted MRI of the pelvis was performed at least 6 months after TME surgery and evaluated by two radiologists. Residual mesorectal tissue was detected in 3.1% of TaTME patients and of 46.9% in LapTME patients (P < 0.001). Multivariate analysis identified only type of surgery as a significant risk factor for leaving residual mesorectum.27
The CRM is a most significant prognostic factor for local recurrences. The average involved CRM rate after laparoscopic abdominal rectal resection in large randomized trials including TME is approximately 6%–8%. In the COLOR II study, using the limit of 1 mm for comparison, positive margins were seen in 7% of laparoscopic and 9% of open resections.16
The taTME had higher success rate with resecting complete mesorectum, longer CRM, and less positive CRM. In taTME series by Veltcamp-Helbach et al,5 the rate of CRM positivity (<2 mm) was 2.5%. De Lacy et al’s7 group also reported CRM positivity (<1 mm) and DRM positivity in only 8.1% (mean of 15.4 mm) and 3.2% (mean of 2.1 cm) of patients, respectively. In taTME series by Burke et al,4 the rate of DRM positivity (<1 mm) was 2% (median 10 mm) and the CRM positivity (<1 mm) was 4% (median 7 mm), respectively.
In our hands, we have achieved a DRM less than 1 cm in only six patients (rate of 18 %), on average the median was of 19 mm. Our results in term of CRM were satisfactory, we never got a CRM positivity, they were all superior to 4 mm, median of 6.52 mm.
Adherence to the oncologic principles of TME directly impacts oncologic outcomes. The taTME offers the benefit of enhanced visualization of the deep pelvis, preservation of the distal mesorectum, control of the distal margin, and preservation of the nerves leading to reports on improvement of quality.26,28
In the absence of clinical trials, the evidence is based on the results of meta-analysis comparing taTME versus laparoscopic TME (LapTME). A recently published meta-analysis included 14 studies (10 of them prospective series) comparing 495 patients in the taTME group versus 547 in the LapTME group. The data showed significant differences in terms of less major comorbidities, less percentage of anastomotic leakage, and less length of hospital stay and readmission rates in the TaTME group.28
In the end, there are no randomized controlled studies comparing taTME and LapTME, several comparative retrospective studies have been reported. There are two ongoing large randomized controlled trials comparing taTME and LapTME. Results of these studies, including long-term outcomes, are awaited for accurately evaluating the efficacy of taTME.29,30
In our opinion, the taTME has technical advantages over the LapTME approach for oncological resections of low rectal tumors that require a TME. These advantages are most striking when the taTME is performed in a difficult narrow male pelvis or to remove bulky and very low tumors.30
The total morbidity of the taTME procedure is comparable with the conventional LapTME as published in the large randomized trials which display 37%–54% total complications.31,32 Our results are overlapping with the literature results.
Fernandez-Hevia et al33 showed a decrease in morbidity including decreased rate of anastomotic leakage compared the taTME to conventional TME surgery. A low incidence of anastomotic leak rate following taTME has been reported by several authors in large TaTME series and meta-analyses. In particular, data from the two largest meta-analyses currently available in the literature including 510 and 794 patients report figures of 5.7% and 6.1%, respectively. Moreover, recent data from the International taTME registry on 1594 patients operated over a 30-month period in 107 surgical centers reported an overall 30-day anastomotic leak rate of 7.8% and a delayed leak rate of 2.0%. According to published data from international trials, our study present an “real” anastomotic leak rate of 6.2%.
The total operative time from the International Registry was 277 minutes, and the reported operative time ranged from 62 to 685 minutes. In our study, the total operative time for taTME was longer compared to our laparoscopic cases, given the taTME was performed by a single surgeon. However, our operative times are comparable with those from centers with one-surgeon teams, 368 minutes compared to 303 minutes.34 In other hands, the operative time ranged from 180 to 480 minutes with a weighted mean of 315 minutes with one operating team.35 The operating time can be further reduced if the procedure can be performed using a two-team simultaneous approach. Unfortunately, for a medium volume colorectal unit like ours with limited number of specialist surgeons available, a two-team approach is not always possible.
There are several potential benefits of the Cecil approach over the one-team approach, including assistance with exposure of the operative field and/or enhanced comprehension of the surgical anatomy.7 However, the two-team approach requires extra human and device resources that might not always be available with the exception of in specialized centers.36 However the single-team approach is recommend for the beginner taTME surgeon and low-volume hospital.37
In our series, we have performed taTME by a one-surgeon team, it is oncologically adequate, safe, feasible, and morbidities are comparable with existing literature data from two-surgeon teams. In addition, resection margins, mesorectal integrity, and proper linfadenectomy are also comparable or superior to some of the existing studies.
Conclusion
In our experience, the initial results of taTME are encouraging and promising. This surgical technique is especially attractive in male patients with a narrow and irradiated pelvis and with a tumor in the lower third of the rectum.
The taTME permits a better visualization of the distal rectum and an easier identification of the plan of dissection, this could to result in a higher quality of TME specimens, and in a reduction of CRM and DRM positive rate.
The most important benefit of the taTME approach is the significant increase of the sphincter-saving rectal surgery with reduced use of abdominal perineal resection surgery (APR) and decrease in the length of stay for our patients.
We believe, in accordance with the literature, that taTME, with a single-surgeon team is a feasible and safe technique even if practiced in a suburban hospital with a medium volume of colorectal surgery activity, but only after completion of appropriate training.
Conflicts of interest statement
The authors declare that they have no conflicts of interest with regard to the content of this report.
References
1. Heald RJ, Ryall RD. Recurrence and survival after total mesorectal excision for rectal cancer. Lancet (London, England). 1986;1:1479–1482.
2. Wexner SD, Berho M, et al. Transanal total mesorectal excision of rectal carcinoma. Ann Surg. 2015;261:234–236.
3. Ma B, Gao P, Song Y, et al. Transanal total mesorectal excision (taTME) for rectal cancer: a systematic review and meta-analysis of oncological and perioperative outcomes compared with laparoscopic total mesorectal excision. BMC Cancer. 2016;16:380.
4. Burke JP, Martin-Perez B, Khan A, et al. Transanal total mesorectal excision for rectal cancer: early outcomes in consecutive patients. Colorectal Dis. 2016;18:570–577.
5. Veltcamp Helbach M, Deijen CL, Velthuis S, et al. Transanal total mesorectal excision for rectal carcinoma: short-term outcomes and experience after 80 cases. Surg Endosc. 2016;30:464–470.
6. De Lacy AM, Rattner DW, Adelsdorfer C, et al. Transanal natural orifice transluminal endoscopic surgery (NOTES) rectal resection: “down-to-up” total mesorectal excision (TME)--short-term outcomes in the first 20 cases. Surg Endosc. 2013;27:3165–3172.
7. de Lacy FB, van Laarhoven JJEM, Pena R, et al. Transanal total mesorectal excision: pathological results of 186 patients with mid and low rectal cancer. Surg Endosc. 2018;32:2442–2447.
8. Glynne-Jones R, Wyrwicz L, Tiret E, et al.; ESMO Guidelines Committee. Rectal cancer: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2018;29(Suppl 4):iv263iv 263.
9. Quirke P, West NP, Nagtegaal ID, et al. EURECCA consensus conference highlights about colorectal cancer clinical management: the pathologists expert review. Virchows Arch. 2014;464:129129e–1291134.
10. Rullier E, Denost Q, Vendrely V, et al. Low rectal cancer: classification and standardization of surgery. Dis Colon Rectum. 2013;56:560–567.
11. Dindo C, Demartines N, Clavien PA, et al. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg. 2004;240:205–213.
12. Rahbari NN, Weitz J, Hohenberger W, et al. Definition and grading of anastomotic leakage following anterior resection of the rectum: a proposal by the ISGRC. Surgery. 2010;147:339339 e–33933351.
13. Bray F, Ferlay J, Soerjomataram I, et al. Global cancer statistics GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68:394–424.
14. Fleshman J, Branda M, Sargent DJ, et al. Effect of laparoscopic- assisted resection vs open resection of stage II or III rectal cancer on pathologic outcomes: the ACOSOG Z6051 randomized clinical trial. JAMA. 2015;314:1346–1355.
15. Stevenson AR, Solomon MJ, Lumley JW, et al.; ALaCaRT Investigators. Effect of laparoscopic-assisted resection vs open resection on pathological outcomes in rectal cancer: the ALaCaRT randomized clinical trial. JAMA. 2015;314:1356–1363.
16. VanderPas MH, Haglind E, Cuesta MA, et al. COlorectal cancer Laparoscopic or Open Resection II (COLOR II) Study Group. Laparoscopic versus open surgery for rectal cancer (COLOR II): short-term outcomes of a randomised, phase 3 trial. Lancet Oncol. 2013;14:210–212.
17. Penna M, Hompes R, Arnold S, et al.; TaTME Registry Collaborative. Transanal total mesorectal excision: international registry results of the first 720 cases. Ann Surg. 2017;266:111–117.
18. Syk E, Torkzad MR, Blomqvist L, et al. Local recurrence in rectal cancer: anatomic localization and effect on radiation target. Int J Radiat Oncol Biol Phys. 2008;72:658–664.
19. Sylla P, Rattner DW, Delgado S, et al. NOTES transanal rectal cancer resection using transanal endoscopic microsurgery and laparoscopic assistance. Surg Endosc. 2010;24:1205–1210.
20. Penna M, Cunningham C, Hompes R. Transanal total mesorectal excision: why, when, and how. Clin Colon Rectal Surg. 2017;30:339–345.
21. McLemore E, Lavi P, Attaluri V. Learning transanal total mesorectal excision. Clin Colon Rectal Surg. 2020;33:168–172.
22. Adamina M, Buchs NC, Penna M, et al.; St. Gallen Colorectal Consensus Expert Group. St. Gallen consensus on safe implementation of transanal total mesorectal excision. Surg Endosc. 2018;32:1091–1103.
23. Koedam TWA, Veltcamp Helbach M, van de Ven PM, et al. Transanal total mesorectal excision for rectal cancer: evaluation of the learning curve. Tech Coloproctol. 2018;22:279–287.
24. Abbott SC, Stevenson ARL, Bell SW, et al. An assessment of an Australasian pathway for the introduction of transanal total mesorectal excision (taTME). Colorectal Dis. 2018;20:O1–O6.
25. Deijen CL, Tsai A, Koedam TW, et al. Clinical outcomes and case volume effect of transanal total mesorectal excision for rectal cancer: a systematic review. Tech Coloproctol. 2016;20:811–824.
26. Ren J, Luo H, Liu S, et al. Short and mid-term outcomes of transanal versus laparoscopic total mesorectal excision for low rectal cancer: a meta-analysis. Ann Surg Treat Res. 2021;100:86–99.
27. Veltcamp Helbach M, Koedam TWA, Knol JJ, et al. Residual mesorectum on postoperative magnetic resonance imaging following transanal total mesorectal excision (TaTME) and laparoscopic total mesorectal excision (LapTME) in rectal cancer. Surg Endosc. 2019;33:94–102.
28. Aubert M, Mege D, Panis Y. Total mesorectal excision for low and middle rectal cancer: laparoscopic versus transanal approach-a meta-analysis. Surg Endosc. 2020;34:3908–3919.
29. Lelong B, de Chaisemartin C, Meillat H, et al.; French Research Group of Rectal Cancer Surgery (GRECCAR). A multicentre randomised controlled trial to evaluate the efficacy, morbidity and functional outcome of endoscopic transanal proctectomy versus laparoscopic proctectomy for low-lying rectal cancer (ETAP-GRECCAR 11 TRIAL): rationale and design. BMC Cancer. 2017;17:253.
30. Muratore A, Mellano A, Marsanic P, et al. Transanal total mesorectal excision (taTME) for cancer located in the lower rectum: short- and mid-term results. Eur J Surg Oncol. 2015;41:478–483.
31. Guillou PJ, Quirke P, Thorpe H, et al.; MRC CLASICC trial group. Short-term endpoints of conventional versus laparoscopic-assisted surgery in patients with colorectal cancer (MRC CLASICC trial): multicentre, randomised controlled trial. Lancet. 2005;365:1718–1726.
32. Peeters KC, Marijnen CA, Nagtegaal ID, et al.; Dutch Colorectal Cancer Group. The TME trial after a median follow-up of 6 years: increased local control but no survival benefit in irradiated patients with resectable rectal carcinoma. Ann Surg. 2007;246:693–701.
33). Fernandez-Hevia M, Delgado S, Castells A, et al. Transanal total mesorectal excision in rectal cancer: short-term outcomes in comparison with laparoscopic surgery. Ann Surg. 2015;261:221–227.
34. Caycedo-Marulanda A, Jiang HY, Kohtakangas EL. Outcomes of a Single Surgeon-Based Transanal-Total Mesorectal Excision (TATME) for rectal cancer. J Gastrointest Cancer. 2018;49:455–462.
35. Buchs NC, Nicholson GA, Yeung T, et al. Transanal rectal resection: an initial experience of 20 cases. Colorectal Dis. 2016;18:45–50.
36. Albert M, Lee L. Tips and tricks. Clin Colon Rectal Surg. 2020;33:173–179.
37. Deijen CL, Velthuis S, Tsai A, et al. COLOR III: a multicentre randomised clinical trial comparing transanal TME versus laparoscopic TME for mid and low rectal cancer. Surg Endosc. 2016;30:3210–3215.