Surg Endosc DOI 10.1007/s00464-014-3636-1
and Other Interventional Techniques
Transanal versus traditional laparoscopic total mesorectal excision for rectal carcinoma Simone Velthuis • Dorothee H. Nieuwenhuis T. Emiel G. Ruijter • Miguel A. Cuesta • H. Jaap Bonjer • Colin Sietses
•
Received: 17 December 2013 / Accepted: 16 May 2014 Ó Springer Science+Business Media New York 2014
Abstract Background After total mesorectal excision (TME) surgery, patients with an incomplete mesorectum have an increased risk of local and overall recurrence. With the introduction of laparoscopic TME, an improved quality of the specimen was expected. However, the quality-related results were comparable to the results after traditional open surgery. Transanal TME is a new technique in which the rectum is mobilised by using a single-port and endoscopic instruments through the so called ‘down to up’ procedure. This new technique potentially leads to an improved specimen quality. This study was designed to investigate the pathological quality of specimens after transanal (TME) and to compare these with specimens after traditional laparoscopic TME. Methods This matched case control study compared the specimens of a cohort of consecutive patients who underwent transanal TME with the specimens after traditional laparoscopic TME. The pathological quality of the mesorectum was determined by the definitions of Quirke as ‘complete’, ‘nearly complete’, or ‘incomplete’. Results From June 2012 until July 2013, 25 consecutive patients underwent transanal TME because of a rectum carcinoma. Within the transanal TME group, 96 % of the
S. Velthuis (&) C. Sietses Department of Surgery, Gelderse Vallei Hospital, 6716 RP Ede, The Netherlands e-mail: [email protected] D. H. Nieuwenhuis M. A. Cuesta H. J. Bonjer C. Sietses Department of Surgery, Vrije Universiteit Medical Center, Amsterdam, The Netherlands T. E. G. Ruijter Department of Pathology, Rijnstate Hospital, Arnhem, The Netherlands
specimens had a complete mesorectum, while in the traditional laparoscopic group, 72 % was deemed complete (p \ 0.05). Other pathological characteristics, such as the circumferential resection margin, were comparable between the two groups. Conclusions Transanal TME appears associated with a significant higher rate of completeness of the mesorectum. Further studies are necessary to evaluate this novel technique. Keywords Colorectal cancer TME Minimally invasive surgery Transanal TME NOTES Pathology The importance of the radicality of surgery in the treatment of rectal cancer has been stressed ever since Heald and Ryall [1, 2] first described the total mesorectal excision (TME). Since then, a significant reduction in local recurrence rate has been achieved. A further reduction in local recurrence rate was demonstrated by the Dutch TME trial. They reported an increased risk of local tumour recurrence for patients who underwent a potentially curative procedure, but had an incomplete mesorectal excision, as compared to patients in whom the specimen showed a complete or nearly complete mesorectum [3, 4]. In time, TME has changed from the traditional open technique to an endoscopic approach with clear short-term clinical benefits [5]. Laparoscopy offers better visualisation of the pelvic cavity and therefore facilitates mobilisation of the rectum. Unfortunately, this approach is not always possible and 10–30 per cent of the procedures have to be converted to an open approach [5–7]. This mainly concerns male patients with a small pelvis in which there is limited space to mobilise the rectum distal from the tumour, potentially resulting in a damaged mesorectum.
123
Surg Endosc
During open and laparoscopic surgery, dissection of the rectum is started proximally, the ‘top to bottom’ TME. Recently, we have published our results concerning a new transanal TME approach to mobilise the rectum transanally by using a single-port and traditional endoscopic instruments. This ‘down to up’ procedure potentially gives new options in difficult cases and may therefore improve the quality of surgery [8]. In this study, the pathological quality of transanal TME specimens will be compared with specimens from matched traditional laparoscopic procedures.
Methods Subjects Between June 2012 and July 2013, patients with histologically proven distal (0–5 cm from the dentate line) or mid rectum (5–10 cm from the dentate line) carcinomas, without evidence of distant metastases, were included and underwent transanal TME for rectal cancer in Gelderse Vallei Hospital. The ethical committee of the Vrije Universiteit Medical Center (VUmc) approved the feasibility study for transanal TME. Patients with T4 tumours or previous abdominal surgery were excluded. This cohort was matched for gender and type of procedure with a cohort of patients who underwent traditional laparoscopic low anterior resection (LAR) or an abdominoperineal resection (APR) by TME principles. Perioperative assessment The preoperative assessment for both groups included magnetic resonance imaging for local staging, and computed tomography of the thorax and abdomen to rule out or to detect distant metastases. All patients were treated according to the Dutch guidelines for the treatment of rectal cancer. Patients with T2–3 N0–1 tumours underwent preoperative radiotherapy with a total dose of 25 Gy and a daily dose of 5 Gy. Surgery was performed in the week following cessation of radiotherapy. Patients with T2–3 N2 tumours underwent chemoradiotherapy with a total dose of 50 Gy, with a daily dose of 2 Gy combined with 5-fluorouracil. In this case, surgery was performed 6 weeks after the end of the neoadjuvant treatment. Patients received mechanical bowel preparation before surgery with Moviprep (Norgine, Amsterdam, The Netherlands). For postoperative pain control, they received epidural analgesia. Prophylactic antibiotics were administered according to protocol. Patients were treated according to enhanced recovery after surgery (ERAS) guidelines [9].
123
Surgical procedures Both transanal and standard laparoscopic TMEs were performed by two experienced laparoscopic surgeons. Transanal TME Transanal TME was performed as previously described by Velthuis et al. [8]. Patients were placed in the lithotomy position with the arms parallel to the body. In the first five patients, dissection was started with the transanal phase. A Scott retractor (Lone Star Medical Products, Houston, Texas, USA) facilitated the full-thickness circumferential transection. A minimum of 3 cm distal to the tumour was used. After full-thickness transection, the rectal stump was closed with a purse-string suture to prevent spillage of tumour cells and bacteria. After closure of the rectal stump, the cavity was rinsed with a povidone-iodine solution as a cytocidal agent. Subsequently, a SILS Port (Covidien, Mansfield, Massachusetts, USA) was introduced into the anus. A pneumorectum was created with carbon dioxide at a pressure of 14 mmHg. The avascular presacral plane was developed by gently pushing against the tissue, starting at the dorsal side. According to TME principles, the plane of dissection was first extended posteriorly, then anteriorly, and then laterally. After circumferential mobilisation of the rectum, the peritoneal reflection was exposed and opened, thereby entering the peritoneal cavity. The laparoscopic part of the procedure was performed with a second SILS Port introduced at the future ileostomy site in the right lower abdomen. The descending colon and sigmoid were mobilised from medial to lateral using the single-incision laparoscopic surgery technique described previously [10] or through traditional laparoscopic technique. The splenic flexure was mobilised in all patients. To avoid rotation of the colon, the rectosigmoid was exteriorised transanally under direct visualisation by using the camera in the abdominal port. Anal retrieval of the specimen was performed under the protection of an Alexis wound protector (Applied Medical, Rancho Santa Margarita, California, USA) to avoid any wound contamination by bacteria or tumour cells. After dividing the sigmoid, a coloanal anastomosis was made either by hand or by using an EEA Hemorrhoid stapler (Covidien, Mansfield, Massachusetts, USA). An ileostomy was created in all patients. Because of nuisance due to pneumatosis of the retroperitoneum while performing the abdominal phase after the transanal phase, the sequence of phases was reversed after the first five procedures. Currently, the technique has been standardised, starting with the abdominal phase. After full mobilisation of the sigmoid and in most cases the splenic flexure, the proximal rectum was mobilised. The transanal is phase started after localisation of the hypogastric nerves. The rectum was thoroughly rinsed with a betadine solution. The
Surg Endosc Table 1 Quality of the mesorectum Complete
Intact mesorectum with only minor irregularities of smooth mesorectal surface. No defect is deeper than 5 mm, and there is no coning toward the distal margin of the specimen. There is a smooth circumferential resection margin at slicing
Nearly complete
Moderate bulk to the mesorectum, but irregularity of the mesorectal surface. Moderate coning of the specimen is allowed. At no site is the muscularis propria visible, except for the insertion of the levator muscles
Incomplete
Low bulk mesorectum with defects down onto the muscularis propria and/or a very irregular circumferential resection margin
transanal port was introduced, and a pneumorectum was created. Two different ports were used, the previously mentioned SILS Port and the GelPOINT Path Transanal Access Platform (Applied Medical, Rancho Santa Margarita, California, USA). The rectum was closed endoscopically with a purse-string suture. A full-thickness transection of the mucosa was performed. Thereafter, the avascular plane was developed as described above. In case of distal tumours which needed an APR, an intersphinteric dissection was performed before closure of the rectal stump. In these patients, the SILS Port was sutured to the perineal skin. Traditional laparoscopic TME The traditional four trocar laparoscopic TME was performed using standard medial to lateral approach, as described in previous studies [11]. The specimens were extracted through a small transumbilical incision after placement of a wound protector. An anastomosis was created by using an EEA stapler (Covidien, Mansfield, Massachusetts, USA), after which an ileostomy was created. Pathological analysis Pathological examination was performed through a standardised procedure as described by Quirke et al. [12], and assessed with the sixth edition of the TNM classification system. The pathologist was not informed about the performed type of surgery. The depth of the tumour spread in relation to the circumferential resection margin (CRM), and the presence of discontinuous tumour deposits and lymph nodes involved by tumour were evaluated and described. Additionally, the maximum diameter and the location of the tumour were recorded. CRM tumour involvement of 2 mm or more was considered a positive resection margin, as defined by Nagtegaal et al. [13]. The quality of the mesorectum was scored using three grades, as defined by the Quirke, and depicted in Table 1.
was performed to compare the baseline characteristics between the groups. A v2 test (Pearson’s chi-squared test) was used to analyse the data regarding the pathological quality of the specimen. A p \ 0.05 was considered statistically significant.
Results A total of 25 consecutive patients underwent a transanal TME in the period June 2012 until July 2013 and were included in this study. This group was compared with a group of patients who underwent a traditional laparoscopic TME in the period from June 2011 until June 2012. Neoadjuvant therapy was given according to protocol and comparable between the two groups. Patient and tumour characteristics are depicted in Table 2. The groups were matched for gender and type of surgery. Both groups were comparable for BMI. The mean age of the patients in the transanal TME group was 64 years with a range from 49 to 86 years. In the traditional laparoscopic TME group, the mean age was 65 years with a range from 38 to 81 years. No significant differences in tumour characteristics between the groups were seen. The mean distance of the tumour to the anal verge was comparable in both groups. Specimen characteristics are depicted in Tables 3 and 4. No differences between the groups were seen in length of specimen, CRM, or distal margin. A significant difference was, however, seen in the macroscopic quality of the specimens. In the transanal TME group, the mesorectum of all specimens was classified as complete (94 %) except one (4 %), which was assessed as nearly complete. Within the traditional laparoscopic TME group, 18 (72 %) specimens were classified as complete, 2 (8 %) as nearly complete, and 5 (20 %) as incomplete (p \ 0.05). The mesorectal defects were localised in the distal part of the specimen, both on the anterior and posterior site.
Statistical analysis
Discussion
The statistical analysis was performed using SPSS 20.0 (SPSS Inc., Chicago, Illinois, USA). An independent T test
TME is considered the standard of care for rectal cancer. In TME, the rectum and mesorectum are excised through
123
Surg Endosc Table 2 Patients, treatment, and tumour characteristics Transanal TME N = 25
Laparoscopic TME N = 25
Table 3 Resection and staging characteristics Transanal TME N = 25
p value
Laparoscopic TME N = 25
Length of resected specimen Gender 1.0a
Median (cm)
18
20
Range
12–28
10–80
Male
18
18
Female BMI
7
7
Mean
25
27
Median
25
28
Range
20–36
21–34
5 9 5 Gy radiotherapy
19
20
0.73a
Median (mm)
23
25
25 9 2 Gy radiotherapy ? 5-FU
6
5
1.0b
Range
5–80
0–55
Circumferential resection margin involvement Positive (\2 mm) 0.07b
1 (4 %)
Mean (mm) Range
Neoadjuvant therapy
2 (8 %)
Circumferential resection margin 13 1.5–30
12 0–25
Distal resection margin
TME total mesorectal excision
Type of resection LAR
19
19
APR
6
6
Tumour distance to anal verge (cm) Mean 8
6
Median
8
7
Range
0–16
0–15
Table 4 Macroscopic quality of mesorectum Transanal TME N = 25
Laparoscopic TME N = 25
p value
Complete
24 (96 %)
18 (72 %)
\0.05a
0.29b Mesorectum total
Tumour status (T) 1
1
1
Nearly complete
1 (4 %)
2 (8 %)
2
11
9
Incomplete
0
5 (20 %)
3
13
15
Mesorectum LAR
4
0
0
Complete
19 (100 %)
16 (84 %)
Nearly complete Incomplete
0 0
1 (5 %) 2 (11 %)
Lymph nodes status (N) 0.60a
0
17
15
1
5
8
Mesorectum APR
2
3
2
Complete
5 (83 %)
2 (33 %)
Nearly complete
1 (17 %)
1 (17 %)
Incomplete
0
3 (50 %)
Number of lymph nodes Mean
14
13
7–24
1–36
Well differentiated
2
2
Moderately differentiated
22
21
Poorly differentiated
1
2
Mean (mm)
33
33
Range
18–90
9–60
Range Type of adenocarcinoma
0.42b
TME total mesorectal excision, LAR low anterior resection, APR abdominoperineal resection 0.84a
Tumour size 0.98a
TME total mesorectal excision, BMI body mass index, Gy grey, 5-FU 5-fluorouracil, LAR low anterior resection, APR abdominoperineal resection a
v2 test (Pearson’s chi-squared test)
b
Independent T test
sharp dissection under direct vision of the avascular plane between the visceral and parietal pelvic fascia, separating the mesorectal fat from the pelvic structures. The introduction of TME surgery reduced local recurrence rates
123
a
v2 test (Pearson’s chi-squared test)
from 20 to 45 % to around 10 % [14]. The most important predictor of local recurrence is the involvement of the CRM. A CRM of \2 mm is shown to be a strong predictor of local recurrence. However, local recurrence may also develop in patients with an uninvolved CRM [4, 13]. Several studies suggest that the quality of the surgery, reflected in the quality of the mesorectum after TME surgery as determined by pathological evaluation, may influence prognosis. Bosch and Nagtegaal recently published a pooled meta-analysis of the quality of the specimen after open TME.4 The total percentage of complete, nearly complete, and incomplete mesorectum was 56.4, 29.0, and 14.6 %. Furthermore, they showed an increased risk of local and overall recurrence in patients with incomplete specimens (muscularis propria resection plane).
Surg Endosc
Transabdominal endoscopic techniques were expected to improve the quality of surgery by improving visualisation of the pelvic cavity and therefore facilitating mobilisation of the rectum. However, laparoscopy has its limitations. Bulky tumours and a small male pelvis will make dissection distally of the tumour often difficult. Furthermore, it is often difficult to place endoscopic staplers distally from the tumour. Both may cause damage to the specimen. A metaanalysis showed no significant difference in the quality of the specimens between laparoscopic or open TME.4 To further improve the quality of surgery, it may be necessary to change the surgical strategy. In current laparoscopic technique, the rectum is always mobilised transabdominally. In 2012, Zorron et al. [15] described a new approach, the perirectal NOTES access, the ‘down to up’ TME. In this technique, the rectal carcinoma is approached transanally. They described two different transanal endoscopic techniques in which the whole rectum is mobilised. The first patient was operated using a flexible colonoscope. The second using a transanally placed SILS Port and standard endoscopic instruments. These preliminary data showed that it was possible to perform an oncologic resection in a selected group of patients. Recently, we published our initial experience with the transanal TME for the treatment of rectal carcinoma [8]. In 5 unselected patients, the rectum was mobilised using the transanal TME technique, comparable to standard laparoscopy remains to be proven. In this study, the specimens of the first 25 patients operated through the transanal TME in our clinic were compared with an equally large group of patients who had undergone traditional laparoscopic LAR or APR because of rectal carcinoma. The study is small, retrospective and non-randomised and therefore subject to bias. However, to minimise the differences, the groups were matched for gender and type of resection. Secondly, the pathologist who performed the macroscopic evaluation was not aware of the performed type of surgery. The data in this study suggest that the quality of the specimen improves when the TME is performed transanally, when compared with the standard laparoscopic technique. All specimens but one were considered complete. Only one specimen was judged as nearly complete. In the laparoscopic group, 20 % of the specimens were considered as incomplete, a percentage comparable with those in the known literature [16]. To emphasise the difference between both approaches, it is important to notice that these were the first transanal TMEs performed by this team, having extensive experience with laparoscopic colorectal procedures. Even though there are currently few other published data available, Heald already stressed the importance of this new technique in his editorial ‘a new solution to some old problems’ [17].
Recently, De Lacy et al. [18] published their data on the largest group of patients who underwent transanal TME. They described their experience with the first 20 patients and showed feasibility and safety of the transanal TME in experienced hands. They also reported that the quality of the mesorectal plane was satisfactory in all patients. Other research groups also confirmed safety [19].
Conclusions Transanal TME is a new approach in the treatment of rectal cancer in patients with a poorly accessible pelvis for traditional laparoscopic TME. Transanal TME seems to improve the mesorectal quality of the specimen. This improvement in the quality of rectal surgery may reduce local recurrence rate and improves overall survival in patients with rectal carcinoma. Disclosures Drs. Velthuis S, Drs. Nieuwenhuis DH, Dr. Ruijter TEG, Prof. Dr. Cuesta MA, Prof. Dr. Bonjer HJ, and Dr. Sietses C have no conflicts of interest or financial ties to disclose.
References 1. Heald RJ, Husband EM, Ryall RD (1982) The mesorectum in rectal cancer surgery—the clue to pelvic recurrence? Br J Surg 69:613–616 2. Heald RJ, Ryall RD (1986) Recurrence and survival after total mesorectal excision for rectal cancer. Lancet 1:1479–1482 3. Nagtegaal ID, van de Velde CJ, van der Worp E, Kapiteijn E, Quirke P, van Krieken JH (2002) Macroscopic evaluation of rectal cancer resection specimen: clinical significance of the pathologist in quality control. J Clin Oncol 20:1729–1734 4. Bosch SL, Nagtegaal ID (2012) The importance of the pathologist’s role in assessment of the quality of the mesorectum. Curr Colorectal Cancer Rep 8:90–98 5. van der Pas MH, Haglind E, Cuesta MA, Furst A, Lacy AM, Hop WC, Bonjer HJ (2013) Laparoscopic versus open surgery for rectal cancer (COLOR II): short-term outcomes of a randomised, phase 3 trial. Lancet Oncol 14:210–218 6. Penninckx F, Kartheuser A, Van de Stadt J, Pattyn P, Mansvelt B, Bertrand C, Van Eycken E, Jegou D, Fieuws S (2013) Outcome following laparoscopic and open total mesorectal excision for rectal cancer. Br J Surg 100:1368–1375 7. Jayne DG, Thorpe HC, Copeland J, Quirke P, Brown JM, Guillou PJ (2010) Five-year follow-up of the medical research council CLASICC trial of laparoscopically assisted versus open surgery for colorectal cancer. Br J Surg 97:1638–1645 8. Velthuis S, van den Boezem PB, van der Peet DL, Cuesta MA, Sietses C (2013) Feasibility study of transanal total mesorectal excision. Br J Surg 100: 828–831; discussion 831 9. Kehlet H (1997) Multimodal approach to control postoperative pathophysiology and rehabilitation. Br J Anaesth 78:606–617 10. van den Boezem PB, Sietses C (2011) Single-incision laparoscopic colorectal surgery, experience with 50 consecutive cases. J Gastrointest Surg 15:1989–1994 11. Furst A, Schwandner O, Heiligensetzer A, Iesalnieks I, Agha A (2010) Laparoscopic TME in rectal cancer–electronic supplementary: op-video. Langenbecks Arch Surg 395:181–183
123
Surg Endosc 12. Quirke P, Durdey P, Dixon MF, Williams NS (1986) Local recurrence of rectal adenocarcinoma due to inadequate surgical resection. Histopathological study of lateral tumour spread and surgical excision. Lancet 2:996–999 13. Nagtegaal ID, Marijnen CA, Kranenbarg EK, van de Velde CJ, van Krieken JH (2002) Circumferential margin involvement is still an important predictor of local recurrence in rectal carcinoma: not one millimeter but two millimeters is the limit. Am J Surg Pathol 26:350–357 14. van Gijn W, Marijnen CA, Nagtegaal ID, Kranenbarg EM, Putter H, Wiggers T, Rutten HJ, Pahlman L, Glimelius B, van de Velde CJ (2011) Preoperative radiotherapy combined with total mesorectal excision for resectable rectal cancer: 12-year follow-up of the multicentre, randomised controlled TME trial. Lancet Oncol 12:575–582 15. Zorron R, Phillips HN, Coelho D, Flach L, Lemos FB, Vassallo RC (2012) Perirectal NOTES access: ‘‘down-to-up’’ total mesorectal excision for rectal cancer. Surg Innov 19:11–19
123
16. Breukink SO, Grond AJ, Pierie JP, Hoff C, Wiggers T, Meijerink WJ (2005) Laparoscopic versus open total mesorectal excision for rectal cancer: an evaluation of the mesorectum’s macroscopic quality. Surg Endosc 19:307–310 17. Heald RJ (2013) A new solution to some old problems: transanal TME. Tech Coloproctol 17:257–258 18. de Lacy AM, Rattner DW, Adelsdorfer C, Tasende MM, Fernandez M, Delgado S, Sylla P, Martinez-Palli G (2013) Transanal natural orifice transluminal endoscopic surgery (NOTES) rectal resection: ‘‘down-to-up’’ total mesorectal excision (TME)-shortterm outcomes in the first 20 cases. Surg Endosc 27:3165–3172 19. Sylla P, Bordeianou LG, Berger D, Han KS, Lauwers GY, Sahani DV, Sbeih MA, Lacy AM, Rattner DW (2013) A pilot study of natural orifice transanal endoscopic total mesorectal excision with laparoscopic assistance for rectal cancer. Surg Endosc 27:3396–3405
and Other Interventional Techniques
Transanal versus traditional laparoscopic total mesorectal excision for rectal carcinoma Simone Velthuis • Dorothee H. Nieuwenhuis T. Emiel G. Ruijter • Miguel A. Cuesta • H. Jaap Bonjer • Colin Sietses
•
Received: 17 December 2013 / Accepted: 16 May 2014 Ó Springer Science+Business Media New York 2014
Abstract Background After total mesorectal excision (TME) surgery, patients with an incomplete mesorectum have an increased risk of local and overall recurrence. With the introduction of laparoscopic TME, an improved quality of the specimen was expected. However, the quality-related results were comparable to the results after traditional open surgery. Transanal TME is a new technique in which the rectum is mobilised by using a single-port and endoscopic instruments through the so called ‘down to up’ procedure. This new technique potentially leads to an improved specimen quality. This study was designed to investigate the pathological quality of specimens after transanal (TME) and to compare these with specimens after traditional laparoscopic TME. Methods This matched case control study compared the specimens of a cohort of consecutive patients who underwent transanal TME with the specimens after traditional laparoscopic TME. The pathological quality of the mesorectum was determined by the definitions of Quirke as ‘complete’, ‘nearly complete’, or ‘incomplete’. Results From June 2012 until July 2013, 25 consecutive patients underwent transanal TME because of a rectum carcinoma. Within the transanal TME group, 96 % of the
S. Velthuis (&) C. Sietses Department of Surgery, Gelderse Vallei Hospital, 6716 RP Ede, The Netherlands e-mail: [email protected] D. H. Nieuwenhuis M. A. Cuesta H. J. Bonjer C. Sietses Department of Surgery, Vrije Universiteit Medical Center, Amsterdam, The Netherlands T. E. G. Ruijter Department of Pathology, Rijnstate Hospital, Arnhem, The Netherlands
specimens had a complete mesorectum, while in the traditional laparoscopic group, 72 % was deemed complete (p \ 0.05). Other pathological characteristics, such as the circumferential resection margin, were comparable between the two groups. Conclusions Transanal TME appears associated with a significant higher rate of completeness of the mesorectum. Further studies are necessary to evaluate this novel technique. Keywords Colorectal cancer TME Minimally invasive surgery Transanal TME NOTES Pathology The importance of the radicality of surgery in the treatment of rectal cancer has been stressed ever since Heald and Ryall [1, 2] first described the total mesorectal excision (TME). Since then, a significant reduction in local recurrence rate has been achieved. A further reduction in local recurrence rate was demonstrated by the Dutch TME trial. They reported an increased risk of local tumour recurrence for patients who underwent a potentially curative procedure, but had an incomplete mesorectal excision, as compared to patients in whom the specimen showed a complete or nearly complete mesorectum [3, 4]. In time, TME has changed from the traditional open technique to an endoscopic approach with clear short-term clinical benefits [5]. Laparoscopy offers better visualisation of the pelvic cavity and therefore facilitates mobilisation of the rectum. Unfortunately, this approach is not always possible and 10–30 per cent of the procedures have to be converted to an open approach [5–7]. This mainly concerns male patients with a small pelvis in which there is limited space to mobilise the rectum distal from the tumour, potentially resulting in a damaged mesorectum.
123
Surg Endosc
During open and laparoscopic surgery, dissection of the rectum is started proximally, the ‘top to bottom’ TME. Recently, we have published our results concerning a new transanal TME approach to mobilise the rectum transanally by using a single-port and traditional endoscopic instruments. This ‘down to up’ procedure potentially gives new options in difficult cases and may therefore improve the quality of surgery [8]. In this study, the pathological quality of transanal TME specimens will be compared with specimens from matched traditional laparoscopic procedures.
Methods Subjects Between June 2012 and July 2013, patients with histologically proven distal (0–5 cm from the dentate line) or mid rectum (5–10 cm from the dentate line) carcinomas, without evidence of distant metastases, were included and underwent transanal TME for rectal cancer in Gelderse Vallei Hospital. The ethical committee of the Vrije Universiteit Medical Center (VUmc) approved the feasibility study for transanal TME. Patients with T4 tumours or previous abdominal surgery were excluded. This cohort was matched for gender and type of procedure with a cohort of patients who underwent traditional laparoscopic low anterior resection (LAR) or an abdominoperineal resection (APR) by TME principles. Perioperative assessment The preoperative assessment for both groups included magnetic resonance imaging for local staging, and computed tomography of the thorax and abdomen to rule out or to detect distant metastases. All patients were treated according to the Dutch guidelines for the treatment of rectal cancer. Patients with T2–3 N0–1 tumours underwent preoperative radiotherapy with a total dose of 25 Gy and a daily dose of 5 Gy. Surgery was performed in the week following cessation of radiotherapy. Patients with T2–3 N2 tumours underwent chemoradiotherapy with a total dose of 50 Gy, with a daily dose of 2 Gy combined with 5-fluorouracil. In this case, surgery was performed 6 weeks after the end of the neoadjuvant treatment. Patients received mechanical bowel preparation before surgery with Moviprep (Norgine, Amsterdam, The Netherlands). For postoperative pain control, they received epidural analgesia. Prophylactic antibiotics were administered according to protocol. Patients were treated according to enhanced recovery after surgery (ERAS) guidelines [9].
123
Surgical procedures Both transanal and standard laparoscopic TMEs were performed by two experienced laparoscopic surgeons. Transanal TME Transanal TME was performed as previously described by Velthuis et al. [8]. Patients were placed in the lithotomy position with the arms parallel to the body. In the first five patients, dissection was started with the transanal phase. A Scott retractor (Lone Star Medical Products, Houston, Texas, USA) facilitated the full-thickness circumferential transection. A minimum of 3 cm distal to the tumour was used. After full-thickness transection, the rectal stump was closed with a purse-string suture to prevent spillage of tumour cells and bacteria. After closure of the rectal stump, the cavity was rinsed with a povidone-iodine solution as a cytocidal agent. Subsequently, a SILS Port (Covidien, Mansfield, Massachusetts, USA) was introduced into the anus. A pneumorectum was created with carbon dioxide at a pressure of 14 mmHg. The avascular presacral plane was developed by gently pushing against the tissue, starting at the dorsal side. According to TME principles, the plane of dissection was first extended posteriorly, then anteriorly, and then laterally. After circumferential mobilisation of the rectum, the peritoneal reflection was exposed and opened, thereby entering the peritoneal cavity. The laparoscopic part of the procedure was performed with a second SILS Port introduced at the future ileostomy site in the right lower abdomen. The descending colon and sigmoid were mobilised from medial to lateral using the single-incision laparoscopic surgery technique described previously [10] or through traditional laparoscopic technique. The splenic flexure was mobilised in all patients. To avoid rotation of the colon, the rectosigmoid was exteriorised transanally under direct visualisation by using the camera in the abdominal port. Anal retrieval of the specimen was performed under the protection of an Alexis wound protector (Applied Medical, Rancho Santa Margarita, California, USA) to avoid any wound contamination by bacteria or tumour cells. After dividing the sigmoid, a coloanal anastomosis was made either by hand or by using an EEA Hemorrhoid stapler (Covidien, Mansfield, Massachusetts, USA). An ileostomy was created in all patients. Because of nuisance due to pneumatosis of the retroperitoneum while performing the abdominal phase after the transanal phase, the sequence of phases was reversed after the first five procedures. Currently, the technique has been standardised, starting with the abdominal phase. After full mobilisation of the sigmoid and in most cases the splenic flexure, the proximal rectum was mobilised. The transanal is phase started after localisation of the hypogastric nerves. The rectum was thoroughly rinsed with a betadine solution. The
Surg Endosc Table 1 Quality of the mesorectum Complete
Intact mesorectum with only minor irregularities of smooth mesorectal surface. No defect is deeper than 5 mm, and there is no coning toward the distal margin of the specimen. There is a smooth circumferential resection margin at slicing
Nearly complete
Moderate bulk to the mesorectum, but irregularity of the mesorectal surface. Moderate coning of the specimen is allowed. At no site is the muscularis propria visible, except for the insertion of the levator muscles
Incomplete
Low bulk mesorectum with defects down onto the muscularis propria and/or a very irregular circumferential resection margin
transanal port was introduced, and a pneumorectum was created. Two different ports were used, the previously mentioned SILS Port and the GelPOINT Path Transanal Access Platform (Applied Medical, Rancho Santa Margarita, California, USA). The rectum was closed endoscopically with a purse-string suture. A full-thickness transection of the mucosa was performed. Thereafter, the avascular plane was developed as described above. In case of distal tumours which needed an APR, an intersphinteric dissection was performed before closure of the rectal stump. In these patients, the SILS Port was sutured to the perineal skin. Traditional laparoscopic TME The traditional four trocar laparoscopic TME was performed using standard medial to lateral approach, as described in previous studies [11]. The specimens were extracted through a small transumbilical incision after placement of a wound protector. An anastomosis was created by using an EEA stapler (Covidien, Mansfield, Massachusetts, USA), after which an ileostomy was created. Pathological analysis Pathological examination was performed through a standardised procedure as described by Quirke et al. [12], and assessed with the sixth edition of the TNM classification system. The pathologist was not informed about the performed type of surgery. The depth of the tumour spread in relation to the circumferential resection margin (CRM), and the presence of discontinuous tumour deposits and lymph nodes involved by tumour were evaluated and described. Additionally, the maximum diameter and the location of the tumour were recorded. CRM tumour involvement of 2 mm or more was considered a positive resection margin, as defined by Nagtegaal et al. [13]. The quality of the mesorectum was scored using three grades, as defined by the Quirke, and depicted in Table 1.
was performed to compare the baseline characteristics between the groups. A v2 test (Pearson’s chi-squared test) was used to analyse the data regarding the pathological quality of the specimen. A p \ 0.05 was considered statistically significant.
Results A total of 25 consecutive patients underwent a transanal TME in the period June 2012 until July 2013 and were included in this study. This group was compared with a group of patients who underwent a traditional laparoscopic TME in the period from June 2011 until June 2012. Neoadjuvant therapy was given according to protocol and comparable between the two groups. Patient and tumour characteristics are depicted in Table 2. The groups were matched for gender and type of surgery. Both groups were comparable for BMI. The mean age of the patients in the transanal TME group was 64 years with a range from 49 to 86 years. In the traditional laparoscopic TME group, the mean age was 65 years with a range from 38 to 81 years. No significant differences in tumour characteristics between the groups were seen. The mean distance of the tumour to the anal verge was comparable in both groups. Specimen characteristics are depicted in Tables 3 and 4. No differences between the groups were seen in length of specimen, CRM, or distal margin. A significant difference was, however, seen in the macroscopic quality of the specimens. In the transanal TME group, the mesorectum of all specimens was classified as complete (94 %) except one (4 %), which was assessed as nearly complete. Within the traditional laparoscopic TME group, 18 (72 %) specimens were classified as complete, 2 (8 %) as nearly complete, and 5 (20 %) as incomplete (p \ 0.05). The mesorectal defects were localised in the distal part of the specimen, both on the anterior and posterior site.
Statistical analysis
Discussion
The statistical analysis was performed using SPSS 20.0 (SPSS Inc., Chicago, Illinois, USA). An independent T test
TME is considered the standard of care for rectal cancer. In TME, the rectum and mesorectum are excised through
123
Surg Endosc Table 2 Patients, treatment, and tumour characteristics Transanal TME N = 25
Laparoscopic TME N = 25
Table 3 Resection and staging characteristics Transanal TME N = 25
p value
Laparoscopic TME N = 25
Length of resected specimen Gender 1.0a
Median (cm)
18
20
Range
12–28
10–80
Male
18
18
Female BMI
7
7
Mean
25
27
Median
25
28
Range
20–36
21–34
5 9 5 Gy radiotherapy
19
20
0.73a
Median (mm)
23
25
25 9 2 Gy radiotherapy ? 5-FU
6
5
1.0b
Range
5–80
0–55
Circumferential resection margin involvement Positive (\2 mm) 0.07b
1 (4 %)
Mean (mm) Range
Neoadjuvant therapy
2 (8 %)
Circumferential resection margin 13 1.5–30
12 0–25
Distal resection margin
TME total mesorectal excision
Type of resection LAR
19
19
APR
6
6
Tumour distance to anal verge (cm) Mean 8
6
Median
8
7
Range
0–16
0–15
Table 4 Macroscopic quality of mesorectum Transanal TME N = 25
Laparoscopic TME N = 25
p value
Complete
24 (96 %)
18 (72 %)
\0.05a
0.29b Mesorectum total
Tumour status (T) 1
1
1
Nearly complete
1 (4 %)
2 (8 %)
2
11
9
Incomplete
0
5 (20 %)
3
13
15
Mesorectum LAR
4
0
0
Complete
19 (100 %)
16 (84 %)
Nearly complete Incomplete
0 0
1 (5 %) 2 (11 %)
Lymph nodes status (N) 0.60a
0
17
15
1
5
8
Mesorectum APR
2
3
2
Complete
5 (83 %)
2 (33 %)
Nearly complete
1 (17 %)
1 (17 %)
Incomplete
0
3 (50 %)
Number of lymph nodes Mean
14
13
7–24
1–36
Well differentiated
2
2
Moderately differentiated
22
21
Poorly differentiated
1
2
Mean (mm)
33
33
Range
18–90
9–60
Range Type of adenocarcinoma
0.42b
TME total mesorectal excision, LAR low anterior resection, APR abdominoperineal resection 0.84a
Tumour size 0.98a
TME total mesorectal excision, BMI body mass index, Gy grey, 5-FU 5-fluorouracil, LAR low anterior resection, APR abdominoperineal resection a
v2 test (Pearson’s chi-squared test)
b
Independent T test
sharp dissection under direct vision of the avascular plane between the visceral and parietal pelvic fascia, separating the mesorectal fat from the pelvic structures. The introduction of TME surgery reduced local recurrence rates
123
a
v2 test (Pearson’s chi-squared test)
from 20 to 45 % to around 10 % [14]. The most important predictor of local recurrence is the involvement of the CRM. A CRM of \2 mm is shown to be a strong predictor of local recurrence. However, local recurrence may also develop in patients with an uninvolved CRM [4, 13]. Several studies suggest that the quality of the surgery, reflected in the quality of the mesorectum after TME surgery as determined by pathological evaluation, may influence prognosis. Bosch and Nagtegaal recently published a pooled meta-analysis of the quality of the specimen after open TME.4 The total percentage of complete, nearly complete, and incomplete mesorectum was 56.4, 29.0, and 14.6 %. Furthermore, they showed an increased risk of local and overall recurrence in patients with incomplete specimens (muscularis propria resection plane).
Surg Endosc
Transabdominal endoscopic techniques were expected to improve the quality of surgery by improving visualisation of the pelvic cavity and therefore facilitating mobilisation of the rectum. However, laparoscopy has its limitations. Bulky tumours and a small male pelvis will make dissection distally of the tumour often difficult. Furthermore, it is often difficult to place endoscopic staplers distally from the tumour. Both may cause damage to the specimen. A metaanalysis showed no significant difference in the quality of the specimens between laparoscopic or open TME.4 To further improve the quality of surgery, it may be necessary to change the surgical strategy. In current laparoscopic technique, the rectum is always mobilised transabdominally. In 2012, Zorron et al. [15] described a new approach, the perirectal NOTES access, the ‘down to up’ TME. In this technique, the rectal carcinoma is approached transanally. They described two different transanal endoscopic techniques in which the whole rectum is mobilised. The first patient was operated using a flexible colonoscope. The second using a transanally placed SILS Port and standard endoscopic instruments. These preliminary data showed that it was possible to perform an oncologic resection in a selected group of patients. Recently, we published our initial experience with the transanal TME for the treatment of rectal carcinoma [8]. In 5 unselected patients, the rectum was mobilised using the transanal TME technique, comparable to standard laparoscopy remains to be proven. In this study, the specimens of the first 25 patients operated through the transanal TME in our clinic were compared with an equally large group of patients who had undergone traditional laparoscopic LAR or APR because of rectal carcinoma. The study is small, retrospective and non-randomised and therefore subject to bias. However, to minimise the differences, the groups were matched for gender and type of resection. Secondly, the pathologist who performed the macroscopic evaluation was not aware of the performed type of surgery. The data in this study suggest that the quality of the specimen improves when the TME is performed transanally, when compared with the standard laparoscopic technique. All specimens but one were considered complete. Only one specimen was judged as nearly complete. In the laparoscopic group, 20 % of the specimens were considered as incomplete, a percentage comparable with those in the known literature [16]. To emphasise the difference between both approaches, it is important to notice that these were the first transanal TMEs performed by this team, having extensive experience with laparoscopic colorectal procedures. Even though there are currently few other published data available, Heald already stressed the importance of this new technique in his editorial ‘a new solution to some old problems’ [17].
Recently, De Lacy et al. [18] published their data on the largest group of patients who underwent transanal TME. They described their experience with the first 20 patients and showed feasibility and safety of the transanal TME in experienced hands. They also reported that the quality of the mesorectal plane was satisfactory in all patients. Other research groups also confirmed safety [19].
Conclusions Transanal TME is a new approach in the treatment of rectal cancer in patients with a poorly accessible pelvis for traditional laparoscopic TME. Transanal TME seems to improve the mesorectal quality of the specimen. This improvement in the quality of rectal surgery may reduce local recurrence rate and improves overall survival in patients with rectal carcinoma. Disclosures Drs. Velthuis S, Drs. Nieuwenhuis DH, Dr. Ruijter TEG, Prof. Dr. Cuesta MA, Prof. Dr. Bonjer HJ, and Dr. Sietses C have no conflicts of interest or financial ties to disclose.
References 1. Heald RJ, Husband EM, Ryall RD (1982) The mesorectum in rectal cancer surgery—the clue to pelvic recurrence? Br J Surg 69:613–616 2. Heald RJ, Ryall RD (1986) Recurrence and survival after total mesorectal excision for rectal cancer. Lancet 1:1479–1482 3. Nagtegaal ID, van de Velde CJ, van der Worp E, Kapiteijn E, Quirke P, van Krieken JH (2002) Macroscopic evaluation of rectal cancer resection specimen: clinical significance of the pathologist in quality control. J Clin Oncol 20:1729–1734 4. Bosch SL, Nagtegaal ID (2012) The importance of the pathologist’s role in assessment of the quality of the mesorectum. Curr Colorectal Cancer Rep 8:90–98 5. van der Pas MH, Haglind E, Cuesta MA, Furst A, Lacy AM, Hop WC, Bonjer HJ (2013) Laparoscopic versus open surgery for rectal cancer (COLOR II): short-term outcomes of a randomised, phase 3 trial. Lancet Oncol 14:210–218 6. Penninckx F, Kartheuser A, Van de Stadt J, Pattyn P, Mansvelt B, Bertrand C, Van Eycken E, Jegou D, Fieuws S (2013) Outcome following laparoscopic and open total mesorectal excision for rectal cancer. Br J Surg 100:1368–1375 7. Jayne DG, Thorpe HC, Copeland J, Quirke P, Brown JM, Guillou PJ (2010) Five-year follow-up of the medical research council CLASICC trial of laparoscopically assisted versus open surgery for colorectal cancer. Br J Surg 97:1638–1645 8. Velthuis S, van den Boezem PB, van der Peet DL, Cuesta MA, Sietses C (2013) Feasibility study of transanal total mesorectal excision. Br J Surg 100: 828–831; discussion 831 9. Kehlet H (1997) Multimodal approach to control postoperative pathophysiology and rehabilitation. Br J Anaesth 78:606–617 10. van den Boezem PB, Sietses C (2011) Single-incision laparoscopic colorectal surgery, experience with 50 consecutive cases. J Gastrointest Surg 15:1989–1994 11. Furst A, Schwandner O, Heiligensetzer A, Iesalnieks I, Agha A (2010) Laparoscopic TME in rectal cancer–electronic supplementary: op-video. Langenbecks Arch Surg 395:181–183
123
Surg Endosc 12. Quirke P, Durdey P, Dixon MF, Williams NS (1986) Local recurrence of rectal adenocarcinoma due to inadequate surgical resection. Histopathological study of lateral tumour spread and surgical excision. Lancet 2:996–999 13. Nagtegaal ID, Marijnen CA, Kranenbarg EK, van de Velde CJ, van Krieken JH (2002) Circumferential margin involvement is still an important predictor of local recurrence in rectal carcinoma: not one millimeter but two millimeters is the limit. Am J Surg Pathol 26:350–357 14. van Gijn W, Marijnen CA, Nagtegaal ID, Kranenbarg EM, Putter H, Wiggers T, Rutten HJ, Pahlman L, Glimelius B, van de Velde CJ (2011) Preoperative radiotherapy combined with total mesorectal excision for resectable rectal cancer: 12-year follow-up of the multicentre, randomised controlled TME trial. Lancet Oncol 12:575–582 15. Zorron R, Phillips HN, Coelho D, Flach L, Lemos FB, Vassallo RC (2012) Perirectal NOTES access: ‘‘down-to-up’’ total mesorectal excision for rectal cancer. Surg Innov 19:11–19
123
16. Breukink SO, Grond AJ, Pierie JP, Hoff C, Wiggers T, Meijerink WJ (2005) Laparoscopic versus open total mesorectal excision for rectal cancer: an evaluation of the mesorectum’s macroscopic quality. Surg Endosc 19:307–310 17. Heald RJ (2013) A new solution to some old problems: transanal TME. Tech Coloproctol 17:257–258 18. de Lacy AM, Rattner DW, Adelsdorfer C, Tasende MM, Fernandez M, Delgado S, Sylla P, Martinez-Palli G (2013) Transanal natural orifice transluminal endoscopic surgery (NOTES) rectal resection: ‘‘down-to-up’’ total mesorectal excision (TME)-shortterm outcomes in the first 20 cases. Surg Endosc 27:3165–3172 19. Sylla P, Bordeianou LG, Berger D, Han KS, Lauwers GY, Sahani DV, Sbeih MA, Lacy AM, Rattner DW (2013) A pilot study of natural orifice transanal endoscopic total mesorectal excision with laparoscopic assistance for rectal cancer. Surg Endosc 27:3396–3405
![[Transanal total mesorectal excision].](/assets/img/hold.png)
