Results of Neoadjuvant Short-Course Radiation Therapy Followed by Transanal Endoscopic Microsurgery for T1-T2 N0 Extraperitoneal Rectal Cancer

doi:10.1016/j.ijrobp.2015.01.024

International Journal of Radiation OncologyBiologyPhysics

Volume 92, Issue 2, 1 June 2015, Pages 299-306

https://doi.org/10.1016/j.ijrobp.2015.01.024 Get rights and content

Purpose

This study was undertaken to assess the short-term outcomes of neoadjuvant short-course radiation therapy (SCRT) followed by transanal endoscopic microsurgery (TEM) for T1-T2 N0 extraperitoneal rectal cancer. Recent studies suggest that neoadjuvant radiation therapy followed by TEM is safe and has results similar to those with abdominal rectal resection for the treatment of extraperitoneal early rectal cancer.

Methods and Materials

We planned a prospective pilot study including 25 consecutive patients with extraperitoneal T1-T2 N0 M0 rectal adenocarcinoma undergoing SCRT followed by TEM 4 to 10 weeks later (SCRT-TEM). Safety, efficacy, and acceptability of this treatment modality were compared with historical groups of patients with similar rectal cancer stage and treated with long-course radiation therapy (LCRT) followed by TEM (LCRT-TEM), TEM alone, or laparoscopic rectal resection with total mesorectal excision (TME) at our institution.

Results

The study was interrupted after 14 patients underwent SCRT of 25 Gy in 5 fractions followed by TEM. Median time between SCRT and TEM was 7 weeks (range: 4-10 weeks). Although no preoperative complications occurred, rectal suture dehiscence was observed in 7 patients (50%) at 4 weeks follow-up, associated with an enterocutaneous fistula in the sacral area in 2 cases. One patient required a colostomy. Quality of life at 1-month follow-up, according to European Organization for Research and Treatment of Cancer QLQ-C30 survey score, was significantly worse in SCRT-TEM patients than in LCRT-TEM patients (P=.0277) or TEM patients (P=.0004), whereas no differences were observed with TME patients (P=.604). At a median follow-up of 10 months (range: 6-26 months), we observed 1 (7%) local recurrence at 6 months that was treated with abdominoperineal resection.

Conclusions

SCRT followed by TEM for T1-T2 N0 rectal cancer is burdened by a high rate of painful dehiscence of the suture line and enterocutaneous fistula, compared to TEM alone and TEM following LCRT, which forced us to stop the study.

Introduction

With the widespread introduction of population-based screening programs, the rate of rectal cancers diagnosed at an early stage has progressively raised during the last 2 decades, leading to an increasing debate around the potential role of local treatment of early rectal cancer (1). In 1983, Buess et al (2) introduced a novel surgical approach for the resection of large rectal adenomas, namely transanal endoscopic microsurgery (TEM). Since its introduction, many centers have adopted TEM as the new standard surgical approach to treating both large rectal adenomas and early rectal cancer (3). Supporters of the TEM technique praise the excellent exposure of the rectum and the minimal invasiveness, as opposed to conventional surgical techniques (1). In addition, recurrence rates after TEM appear to be lower than with conventional surgical transanal excision (4). The TEM technique has been shown to be highly effective in several retrospective and prospective case series with reported recurrence rates of 0% to 19% and complication rates of 2% to 21% 5, 6, 7, 8, 9, 10.

Even if TEM provides excellent outcomes, diffusion of the technique among colorectal surgeons has been limited by the considerable cost of the instrumentation and the steep learning curve required to master the TEM technique. In 2007, the transanal endoscopic operation device was introduced (Karl Storz GmbH, Tuttlingen, Germany), and 2 years later, the device for transanal minimally invasive surgery was introduced, adopting the use of a simplified rectoscope in the first case and use of a disposable, single-port device in the second case, with the intent of making this technique available to a wider population of surgeons (11).

More recently, TEM has been proposed in a multimodality treatment strategy of highly selected T2 N0 rectal cancers. In these series, including a randomized controlled trial (12), patients underwent neoadjuvant long-course chemoradiation therapy: 50.4 Gy in 28 fractions associated with a continuous infusion of 5-fluorouracil, 200 mg/m²/day. Although this schedule showed great efficacy in terms of control of the disease, it is quite uncomfortable for patients, who often are elderly. Moreover, there are concerns regarding the wound healing process after neoadjuvant long-course chemoradiation therapy 13, 14.

Two randomized European clinical trials have shown that short-course preoperative radiation therapy (SCRT) reduces local recurrence and improves survival in locally advanced rectal cancer 15, 16. In selected T1-T2 N0 rectal cancers it could represent a more comfortable alternative therapy, ensuring results comparable to long-course chemoradiation therapy in terms of control of the disease.

The aim of this pilot study was to assess short-term outcomes of SCRT followed by TEM for selected T1-T2 N0 extraperitoneal rectal cancers.

Section snippets

Study design

The study is a prospective case series pilot study including consecutive patients undergoing neoadjuvant SCRT followed by TEM (SCRT-TEM) for T₁ to T₂, N₀, or G_1-2 rectal cancer.

Preoperative results, morbidity, quality of life (QoL), and oncologic outcomes of SCRT-TEM patients were compared with the outcomes of patients who had undergone TEM following 46-Gy long-course radiation therapy (LCRT-TEM), TEM alone (TEM), or laparoscopic rectal resection with total mesorectal excision (TME) for

Results

Recruitment of consecutive patients eligible for this study started on June 1, 2011. The study was interrupted in January 2014 after enrolment of 14 SCRT-TEM patients for the high rate of complications observed.

Although no preoperative complication was reported, 7 patients (50%) showed a complete dehiscence of the suture line at endoscopy 4 weeks after surgery. All 7 patients with suture dehiscence presented with severe pelvic pain within 2 weeks after surgery. This was treated in all cases

Discussion

The introduction of colorectal cancer screening programs has led to an increased detection of early rectal cancers, which has stimulated research focused on assessing the most appropriate treatment in terms of efficacy, safety, and QoL. We recently reported our series of rectal cancers treated by TEM, which demonstrates once more that submucosal invasion when extended to >1 mm in depth is associated with a non-negligible risk of lymph node metastases and local recurrence (24). Several groups

Conclusions

The present pilot study of SCRT followed by TEM aimed to verify at a minimum follow-up of 3 years the good oncologic results previously reported with LCRT followed by TEM, reducing discomfort for the patient. Unfortunately the very high complication rate, consisting of suture dehiscence and severity of 2 cases of enterocutaneous fistula, convinced us to stop the recruitment. The high complication rate severely affected QoL of patients whose QoL score was similar to that in TME and much worse

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Cited by (37)

Whether the watch-and-wait strategy has application value for rectal cancer with clinical complete response after neoadjuvant chemoradiotherapy? A network meta-analysis
2024, Asian Journal of Surgery
The aim was to evaluate the efficacy and safety between the watch-and-wait strategy (WW), radical surgery (RS), and local excision (LE) for rectal cancer with clinical complete response (cCR) after neoadjuvant radiotherapy (nCRT). We searched MEDLINE, EMBASE, the Cochrane Library, and clinical trials to compare WW with RS and LE for patients with cCR until March 2023 and collected the following data: local recurrence (LR), distant metastasis (DM), cancer-related death (CRD), overall survival (OS), and disease-free survival (DFS). In total, 2240 patients from 21 studies were included. Pairwise meta-analysis revealed no statistically significant differences between the three groups in terms of CRD and 2-, 3-, and 5-year OS (P < 0.05). The RS group was significantly better than the WW group in terms of the LR rate (odds ratio [OR] = 0.12, 95 % confidence interval [CI]: 0.06–0.21, P < 0.001, I² = 0 %], 3-year DFS (OR = 1.56, 95 % CI: 1.10–2.21, P = 0.01, I² = 38 %), and 5-year DFS (OR = 2.30, 95 % CI: 1.53–3.46, P < 0.001, I² = 34 %). The results of network meta-analysis were also similar. After sensitivity analysis, the 5-year OS of the RS group was significantly better than that of the WW group (OR = 2.77, 95 % CI: 1.28–6.00, P = 0.009, I² = 33 %). Nevertheless, neither regression analysis nor subgroup analysis provided meaningful results. However, the cumulative meta-analysis of LR, DM, and 3- and 5-year DFS revealed significant turning points (P < 0.05). Our meta-analysis recommends using the WW strategy for patients with cCR having poor underlying conditions and high surgical risk; however, there is a risk of higher LR and worse survival after 3 years.
Short-term outcomes of chemoradiotherapy and local excision versus total mesorectal excision in T2-T3ab,N0,M0 rectal cancer: a multicentre randomised, controlled, phase III trial (the TAU-TEM study)
2023, Annals of Oncology
Citation Excerpt :
The vast majority of these pCRs published in the literature have been obtained with long CRT courses, similar to the one described in our study. Short courses of CRT do not achieve the same results, and are associated with higher post-operative morbidity.33 The multicentre prospective studies TREC,17 Italian,14 ACOSOGZ604115 and GRECCAR 216 obtained rates of pCR of 30%, 66.7%, 49% and 20%, respectively, also applying different CRT regimens.
The standard treatment of T2-T3ab,N0,M0 rectal cancers is total mesorectal excision (TME) due to the high recurrence rates recorded with local excision. Initial reports of the combination of pre-operative chemoradiotherapy (CRT) and transanal endoscopic microsurgery (TEM) have shown reductions in local recurrence. The TAU-TEM study aims to demonstrate the non-inferiority of local recurrence and the improvement in morbidity achieved with CRT-TEM compared with TME. Here we describe morbidity rates and pathological outcomes.
This was a prospective, multicentre, randomised controlled non-inferiority trial including patients with rectal adenocarcinoma staged as T2-T3ab,N0,M0. Patients were randomised to the CRT-TEM or the TME group. Patients included, tolerance of CRT and its adverse effects, surgical complications (Clavien–Dindo and Comprehensive Complication Index classifications) and pathological results (complete response in the CRT-TEM group) were recorded in both groups. Patients attended follow-up controls for local and systemic relapse. Trial registration: NCT01308190.
From July 2010 to October 2021, 173 patients from 17 Spanish hospitals were included (CRT-TEM: 86, TME: 87). Eleven were excluded after randomisation (CRT-TEM: 5, TME: 6). Modified intention-to-treat analysis thus included 81 patients in each group. There was no mortality after CRT. In the CRT-TEM group, one patient abandoned CRT, 1/81 (1.2%). The CRT-related morbidity rate was 29.6% (24/81). Post-operative morbidity was 17/82 (20.7%) in the CRT-TEM group and 41/81 (50.6%) in the TME group (P < 0.001, 95% confidence interval 42.9% to 16.7%). One patient died in each group (1.2%). Of the 81 patients in the CRT-TEM group who received the allocated treatment, 67 (82.7%) underwent organ preservation. Pathological complete response in the CRT-TEM group was 44.3% (35/79). In the TME group, pN1 were found in 17/81 (21%).
CRT-TEM treatment obtains high pathological complete response rates (44.3%) and a high CRT compliance rate (98.8%). Post-operative complications and hospitalisation rates were significantly lower than those in the TME group. We await the results of the follow-up regarding cancer outcomes and quality of life.
Quality-of-life outcomes in older patients with early-stage rectal cancer receiving organ-preserving treatment with hypofractionated short-course radiotherapy followed by transanal endoscopic microsurgery (TREC): non-randomised registry of patients unsuitable for total mesorectal excision
2022, The Lancet Healthy Longevity
Citation Excerpt :
The authors later concluded that SCRT and delayed surgery should be considered the recommended schedule in older or frailer patients, who might struggle to tolerate the additional toxicity of concomitant chemotherapy, in the setting of locally advanced rectal cancer.36 In the setting of early-stage rectal cancer, few studies have explored this novel organ-preservation approach of SCRT with or without local excision in older and frailer patients.37–40 The largest of these studies, with TEM 8–10 weeks following SCRT, found this approach to be well tolerated, with no mortality associated, and that 48 (77%) of 62 patients were disease-free at a median follow-up of 13 months.37
Older patients with early-stage rectal cancer are under-represented in clinical trials and, therefore, little high-quality data are available to guide treatment in this patient population. The TREC trial was a randomised, open-label feasibility study conducted at 21 centres across the UK that compared organ preservation through short-course radiotherapy (SCRT; 25 Gy in five fractions) plus transanal endoscopic microsurgery (TEM) with standard total mesorectal excision in adults with stage T1–2 rectal adenocarcinoma (maximum diameter ≤30 mm) and no lymph node involvement or metastasis. TREC incorporated a non-randomised registry offering organ preservation to patients who were considered unsuitable for total mesorectal excision by the local colorectal cancer multidisciplinary team. Organ preservation was achieved in 56 (92%) of 61 non-randomised registry patients with local recurrence-free survival of 91% (95% CI 84–99) at 3 years. Here, we report acute and long-term patient-reported outcomes from this non-randomised registry group.
Patients considered by the local colorectal cancer multidisciplinary team to be at high risk of complications from total mesorectal excision on the basis of frailty, comorbidities, and older age were included in a non-randomised registry to receive organ-preserving treatment. These patients were invited to complete questionnaires on patient-reported outcomes (the European Organisation for Research and Treatment of Cancer Quality of Life [EORTC-QLQ] questionnaire core module [QLQ-C30] and colorectal cancer module [QLQ-CR29], the Colorectal Functional Outcome [COREFO] questionnaire, and EuroQol-5 Dimensions-3 Level [EQ-5D-3L]) at baseline and at months 3, 6, 12, 24, and 36 postoperatively. To aid interpretation, data from patients in the non-randomised registry were compared with data from those patients in the TREC trial who had been randomly assigned to organ-preserving therapy, and an additional reference cohort of aged-matched controls from the UK general population. This study is registered with the ISRCTN registry, ISRCTN14422743, and is closed.
Between July 21, 2011, and July 15, 2015, 88 patients were enrolled onto the TREC study to undergo organ preservation, of whom 27 (31%) were randomly allocated to organ-preserving therapy and 61 (69%) were added to the non-randomised registry for organ-preserving therapy. Non-randomised patients were older than randomised patients (median age 74 years [IQR 67–80] vs 65 years [61–71]). Organ-preserving treatment was well tolerated among patients in the non-randomised registry, with mild worsening of fatigue; quality of life; physical, social, and role functioning; and bowel function 3 months postoperatively compared with baseline values. By 6–12 months, most scores had returned to baseline values, and were indistinguishable from data from the reference cohort. Only mild symptoms of faecal incontinence and urgency, equivalent to less than one episode per week, persisted at 36 months among patients in both groups.
The SCRT and TEM organ-preservation approach was well tolerated in older and frailer patients, showed good rates of organ preservation, and was associated with low rates of acute and long-term toxicity, with minimal effects on quality of life and functional status. Our findings support the adoption of this approach for patients considered to be at high risk from radical surgery.
Cancer Research UK.
Radical surgery versus organ preservation via short-course radiotherapy followed by transanal endoscopic microsurgery for early-stage rectal cancer (TREC): a randomised, open-label feasibility study
2021, The Lancet Gastroenterology and Hepatology
Citation Excerpt :
Despite the small patient numbers, the patient-reported outcomes data reveal that an organ preservation approach is associated with consistent improvements in multiple symptom and function items 3 months after treatment, with longer-term benefits for overall QOL, social function, body image, and less embarrassment about bowel function. We found no evidence of acute deterioration in HRQOL or patient-reported toxicity with organ preservation versus total mesorectal excision.10,15,24 This exploratory analysis supports favourable longer-term patient-reported outcome scores seen at 1-year, 2-year, and 5-year follow-ups after organ preservation in various trials.10,33
Radical surgery via total mesorectal excision might not be the optimal first-line treatment for early-stage rectal cancer. An organ-preserving strategy with selective total mesorectal excision could reduce the adverse effects of treatment without substantially compromising oncological outcomes. We investigated the feasibility of recruiting patients to a randomised trial comparing an organ-preserving strategy with total mesorectal excision.
TREC was a randomised, open-label feasibility study done at 21 tertiary referral centres in the UK. Eligible participants were aged 18 years or older with rectal adenocarcinoma, staged T2 or lower, with a maximum diameter of 30 mm or less; patients with lymph node involvement or metastases were excluded. Patients were randomly allocated (1:1) by use of a computer-based randomisation service to undergo organ preservation with short-course radiotherapy followed by transanal endoscopic microsurgery after 8–10 weeks, or total mesorectal excision. Where the transanal endoscopic microsurgery specimen showed histopathological features associated with an increased risk of local recurrence, patients were considered for planned early conversion to total mesorectal excision. A non-randomised prospective registry captured patients for whom randomisation was considered inappropriate, because of a strong clinical indication for one treatment group. The primary endpoint was cumulative randomisation at 12, 18, and 24 months. Secondary outcomes evaluated safety, efficacy, and health-related quality of life assessed with the European Organisation for Research and Treatment of Cancer (EORTC) QLQ C30 and CR29 in the intention-to-treat population. This trial is registered with the ISRCTN Registry, ISRCTN14422743.
Between Feb 22, 2012, and Dec 19, 2014, 55 patients were randomly assigned at 15 sites; 27 to organ preservation and 28 to radical surgery. Cumulatively, 18 patients had been randomly assigned at 12 months, 31 at 18 months, and 39 at 24 months. No patients died within 30 days of initial treatment, but one patient randomly assigned to organ preservation died within 6 months following conversion to total mesorectal excision with anastomotic leakage. Eight (30%) of 27 patients randomly assigned to organ preservation were converted to total mesorectal excision. Serious adverse events were reported in four (15%) of 27 patients randomly assigned to organ preservation versus 11 (39%) of 28 randomly assigned to total mesorectal excision (p=0·04, χ² test). Serious adverse events associated with organ preservation were most commonly due to rectal bleeding or pain following transanal endoscopic microsurgery (reported in three cases). Radical total mesorectal excision was associated with medical and surgical complications including anastomotic leakage (two patients), kidney injury (two patients), cardiac arrest (one patient), and pneumonia (two patients). Histopathological features that would be considered to be associated with increased risk of tumour recurrence if observed after transanal endoscopic microsurgery alone were present in 16 (59%) of 27 patients randomly assigned to organ preservation, versus 24 (86%) of 28 randomly assigned to total mesorectal excision (p=0·03, χ² test). Eight (30%) of 27 patients assigned to organ preservation achieved a complete response to radiotherapy. Patients who were randomly assigned to organ preservation showed improvements in patient-reported bowel toxicities and quality of life and function scores in multiple items compared to those who were randomly assigned to total mesorectal excision, which were sustained over 36 months’ follow-up. The non-randomised registry comprised 61 patients who underwent organ preservation and seven who underwent radical surgery. Non-randomised patients who underwent organ preservation were older than randomised patients and more likely to have life-limiting comorbidities. Serious adverse events occurred in ten (16%) of 61 non-randomised patients who underwent organ preservation versus one (14%) of seven who underwent total mesorectal excision. 24 (39%) of 61 non-randomised patients who underwent organ preservation had high-risk histopathological features, while 25 (41%) of 61 achieved a complete response. Overall, organ preservation was achieved in 19 (70%) of 27 randomised patients and 56 (92%) of 61 non-randomised patients.
Short-course radiotherapy followed by transanal endoscopic microsurgery achieves high levels of organ preservation, with relatively low morbidity and indications of improved quality of life. These data support the use of organ preservation for patients considered unsuitable for primary total mesorectal excision due to the short-term risks associated with this surgery, and support further evaluation of short-course radiotherapy to achieve organ preservation in patients considered fit for total mesorectal excision. Larger randomised studies, such as the ongoing STAR-TREC study, are needed to more precisely determine oncological outcomes following different organ preservation treatment schedules.
Cancer Research UK.
Transanal Approaches to Early Rectal Cancer: Transanal Endoscopic Microsurgery and Conventional Transanal Excision
2019, Shackelford's Surgery of the Alimentary Tract: 2 Volume Set
Conventional transanal excision (TAE) and transanal endoscopic microsurgery (TEM) are two established minimally invasive surgical options for the treatment of early rectal cancer (ERC). Nowadays, TEM should be considered the procedure of choice for local excision (LE) of ERC because it is associated with significantly higher rates of en bloc full-thickness excision and better oncologic outcomes than TAE. Postoperative morbidity and functional outcomes after TEM alone for selected T1N0M0 rectal cancers are better than those achieved after radical resection by total mesorectal excision (TME), with similar long-term oncologic outcomes. The role of neoadjuvant chemoradiation therapy (CRT) followed by TEM in selected T1-2 N0 is under evaluation.
Preoperative radiotherapy and local excision of rectal cancer: Long-term results of a randomised study
2018, Radiotherapy and Oncology
Citation Excerpt :
Thus, it is possible that the difference in efficacy between the two radiotherapy schedules has been revealed in the LE setting but has not in the TME setting. Remarkably, this trial and other studies have demonstrated that when surgery is delayed, short-course radiotherapy causes substantial cCR, pCR and local control rates [7,15–17,21]. Thus, for elderly patients who cannot tolerate chemotherapy, short-course radiotherapy with long interval to LE remains a valuable option.
It is uncertain whether local control is acceptable after preoperative radiotherapy and local excision (LE). An optimal preoperative dose/fractionation schedule has not yet been established.
In a phase III study, patients with cT1-2N0M0 or borderline cT2/T3N0M0 < 4 cm rectal adenocarcinomas were randomised to receive either 5 × 5 Gy plus 1 × 4 Gy boost or chemoradiation: 50.4 Gy in 28 fractions plus 3 × 1.8 Gy boost and 5-fluorouracil with leucovorin bolus. LE was performed 6–8 weeks later. Patients with ypT0–1R0 disease were observed. Completion total mesorectal excision (CTME) was recommended for poor responders, i.e. ypT1R1/ypT2-3.
Of 61 randomised patients, 10 were excluded leaving 51 for analysis; 29 in the short-course group and 22 in the chemoradiation group. YpT0–1R0 was observed in 66% of patients in the short-course group and in 86% in the chemoradiation group, p = 0.11. CTME was performed only in 46% of patients with ypT1R1/ypT2-3. The median follow-up was 8.7 years. Local recurrence incidences and overall survival at 10 years were respectively for the short-course group vs. the chemoradiation group 35% vs. 5%, p = 0.036 and 47% vs. 86%, p = 0.009. In total, local recurrence at 10 years was 79% for ypT1R1/T2-3 without CTME.
This trial suggests that in the LE setting, both local recurrence and survival are worse after short-course radiotherapy than after chemoradiation. Because of the risk of bias, a confirmatory study is desirable. Lack of CTME is associated with an unacceptably high local recurrence rate.

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Clinical InvestigationResults of Neoadjuvant Short-Course Radiation Therapy Followed by Transanal Endoscopic Microsurgery for T1-T2 N0 Extraperitoneal Rectal Cancer

Purpose

Methods and Materials

Results

Conclusions

Introduction

Section snippets

Study design

Results

Discussion

Conclusions

Dig Liver Dis

Radiother Oncol

Radiother Oncol

Quality of life after transanal endoscopic microsurgery and total mesorectal excision in early rectal cancer

Colorectal Dis

A system for a transanal endoscopic rectum operation

Chirurg

TEM/local excision: Indications, techniques, outcomes, and the future

J Surg Oncol

Transanal endoscopic microsurgery: A systematic review

Dis Colon Rectum

Local excision of rectal tumours by transanal endoscopic microsurgery

Br J Surg

Giant adenomas of the rectum: Complete resection by transanal endoscopic microsurgery (TEM)

Int J Colorectal Dis

Factors predicting early recurrence after transanal endoscopic microsurgery excision for rectal adenoma

Colorectal Dis

Transanal endoscopic microsurgery: Risk factors for local recurrence of benign rectal adenomas

Colorectal Dis

Transanal endoscopic excision of rectal adenomas

Surg Endosc

A systematic review of transanal minimally invasive surgery (TAMIS) from 2010 to 2013

Tech Coloproctol

Randomized clinical trial of endoluminal locoregional resection versus laparoscopic total mesorectal excision for T2 rectal cancer after neoadjuvant therapy

Br J Surg

Transanal endoscopic microsurgery for the treatment of rectal cancer: Comparison of wound complication rates with and without neoadjuvant radiation therapy

Surg Endosc

Clinical Investigation
Results of Neoadjuvant Short-Course Radiation Therapy Followed by Transanal Endoscopic Microsurgery for T1-T2 N0 Extraperitoneal Rectal Cancer