ORIGINAL ARTICLE
Laparoscopic Total Mesorectal Excision With Coloanal Anastomosis for Rectal Cancer Quentin Denost, MD, PhD, Jean-Philippe Adam, MD, Arnaud Pontallier, MD, Bertrand Celerier, MD, Christophe Laurent, MD, PhD, and Eric Rullier, MD
Objective: Oncologic and functional outcomes were compared between transanal and transabdominal specimen extraction after laparoscopic coloanal anastomosis for rectal cancer. Background: Laparoscopic coloanal anastomosis is an attractive new surgical option in patients with low rectal cancer because laparotomy is not necessary due to transanal specimen extraction. Risks of tumor spillage and fecal incontinence induced by transanal extraction are not known. Methods: Between 2000 and 2010, 220 patients with low rectal cancer underwent laparoscopic rectal excision with hand-sewn coloanal anastomosis. The rectal specimen was extracted transanally in 122 patients and transabdominally in 98 patients. End points were circumferential resection margin, mesorectal grade, local recurrence, survival, and functional outcome. Results: The mortality rate was 0.5% and surgical morbidity rate was 17%. The rate of positive circumferential resection margin was 9% and the mesorectum was graded complete in 79%, subcomplete in 12%, and incomplete in 9%. After a follow-up of 51 months (range, 1–151), the local recurrence rate was 4% and overall survival and disease-free survival rates were 83% and 70% at 5 years, respectively. The continence score was 6 (range, 0–20). There was no difference of mortality rate, morbidity rate, circumferential resection margin, mesorectal grade, local recurrence (4% vs 5%, P = 0.98), and disease-free survival rate (72% vs 68%, P = 0.63) between transanal and transabdominal extraction groups. Continence score was also similar (6 vs 6, P = 0.92). Conclusions: Transanal extraction of the rectal specimen did not compromise oncologic and functional outcome after laparoscopic surgery for low rectal cancer and seems as a safe option to preserve the abdominal wall. Keywords: coloanal anastomosis, laparoscopy, low rectal cancer, sphincter preservation, transanal extraction (Ann Surg 2015;261:138–143)
L
aparoscopic surgery is validated in treatment of colon cancer.1–5 The advantages are improved short-term outcome with no difference of survival at 5 years. In contrast, the laparoscopic approach in rectal cancer is still debated. Only 1 randomized trial is available for long-term outcome, suggesting similar survival rates between laparoscopic and open surgery at 5 years,6 but a higher morbidity rate7 and a lower survival rate in the subgroup of converted patients.6 One of the main restrictions for developing laparoscopic surgery in rectal cancer are the difficulties for stapling the distal rectum to achieve a low anterior resection.8,9 This may translate to
From the Department of Surgery, Colorectal Unit, CHU Bordeaux, Saint-Andre Hospital, France; and Universit´e Bordeaux Segalen, Bordeaux, France. Disclosure: The authors report no financial or other conflicts of interest relevant to the subject of this article. Presented at the Congress of European Society of Coloproctology (ESCP), as oral communication, September 26–28, 2012, Vienne, France. Reprints: Eric Rullier, MD, Service de Chirurgie Digestive, Hopital Saint-Andre, 33075 Bordeaux, France. E-mail: [email protected]. C 2014 by Lippincott Williams & Wilkins Copyright ISSN: 0003-4932/14/26101-0138 DOI: 10.1097/SLA.0000000000000855
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a higher rate of APR in laparoscopic procedures,10 the necessity to use hybrid procedures for rectal transection11 or to perform a hand-sewn coloanal anastomosis. There are few data of full laparoscopic coloanal anastomosis for rectal cancer,12–14 including small series12 and short follow-up.13,14 Moreover, the risk of anastomotic or perineal recurrence induced by transanal extraction of the rectal specimen is not known. In the United Kingdom trial comparing laparoscopic versus open colorectal surgery, 9 extraction-site recurrences have been reported in the laparoscopic group compared with one in the open group.6 Moreover, functional outcomes of laparoscopic coloanal anastomosis have never been reported, and therefore the potential risk of anal incontinence related to transanal specimen extraction has never been discussed. The objective of our large monocenter series was to report long-term outcome of laparoscopic coloanal anastomosis for rectal cancer, with the aim to solve the oncologic and functional impact of transanal extraction.
METHODS Patients All patients operated on between 2000 and 2010 at Saint-Andre Hospital by laparoscopic total mesorectal excision with hand-sewn coloanal anastomosis for low rectal cancers were considered. During this period, 871 patients were treated for rectal cancer, 244 received open surgery for T4 (tumor fixation) or M1 (metastatic disease) lesions, 277 had a laparoscopic low anterior resection with endoscopic rectal stapling for high and midrectal tumors, 30 were treated by laparoscopic abdominoperineal excision for a very low rectal cancer infiltrating the external sphincter or the levator ani muscles, and 100 underwent local excision for early (T1) low rectal cancer or downstaged T2–T3 after radiochemotherapy.15 The population study included 220 patients with laparoscopic total mesorectal excision and coloanal anastomosis for rectal cancer. There were 139 males and 81 females with a median age of 64 (range, 20–90) years. The ASA score was 1 in 136 patients, 2 in 73 patients, and 3 in 11 patients. The body mass index was 25 (range, 17–38). Tumors were staged after colonoscopy, CT scan, endorectal ultrasound and pelvic magnetic resonance imaging according to the TNM/UICC classification16 as follows: uT1 in 13 patients, uT2 in 26 patients, uT3 in 175 patients, and uT4 in 6 patients; 130 were uN+ and 13 M1 (synchronous metastases). The tumors were 4 cm (range, 1–6 cm) from the anal verge and 1 cm (range, −2 to 3 cm) from the anal ring.
Neoadjuvant and Adjuvant Treatments Neoadjuvant radiochemotherapy was used in patients with locally advanced disease, that is, T3 and T4 or N1 disease. Preoperative radiotherapy consisted in 45 Gy during 5 weeks and was given in 192 patients (87%), in association with concomitant neoadjuvant chemotherapy (5 fluorouracil and capecitabine) in 164 patients. Postoperative adjuvant chemotherapy (5 fluorouracil and capecitabine and oxaliplatine) was given for 6 months in patients Annals of Surgery r Volume 261, Number 1, January 2015
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Annals of Surgery r Volume 261, Number 1, January 2015
with positive lymph nodes at the specimen (pN1 disease). This included 84 patients after laparoscopic coloanal anastomosis (38%).
Surgical Procedure Surgery was performed 6 weeks after radiotherapy. All patients had a mechanic bowel preparation the day before surgery and antibioprophylaxia the day of surgery. Patients were operated on by a team trained in both colorectal and laparoscopic surgery. All patients had curative surgery. Patients with synchronous metastases had surgery of the secondaries 2 months after rectal surgery. A 5-port technique was used. A high ligation of the inferior mesenteric artery and a full mobilization of the left colon, including the splenic flexure, were systematically performed. This was to achieve a tension-free low anastomosis and also to permits transanal extraction of the specimen. During this step, care was taken to open enough window into the mesentery to optimize left colon mobilization, but avoiding injury of the marginal colonic artery. Exposure of the pelvis was facilitated by the previous mobilization of the colon. The pelvic dissection was performed by using harmonic scalpel (Ultracision; Ethicon Endosurgery, Cincinnati, OH), thermal fusion (Ligasure Advance; Covidien, Mansfield, MA), or conventional scissors with monopolar coagulation. It included total mesorectal excision with preservation of the pelvic autonomic nerves. The dissection began posteriorly to continue laterally first on the right then on the left and finished anteriorly. The hypogastric nerves, inferior hypogastric plexuses, and presacral nerves were identified and preserved, except in case of fixed tumor. In males, the Denonvilliers fascia was removed, except in case of posterior tumors. The laparoscopic dissection continued along the pelvic floor toward the top of the anal canal anteriorly and the puborectalis sling posteriorly. The distal level of the laparoscopic dissection was confirmed by digital rectal examination. In case of juxta or intraanal tumors suitable for intersphincteric resection, the aponeurosis of the levator ani muscles (sheath of the pelvic floor) was incised to enter into the intersphincteric plane. This steep was enhanced by the optimal view of the laparoscopic approach and facilitated the connection with the perineal dissection. During the perineal phase, the anal canal was then exposed by a self-holding retractor (Lone Star Retractor; Lone Star Medical Products Inc., Houston, TX). A mesh was introduced into the rectum to limit the risk of spillage. In case of supraanal tumors (>1 cm from the anal ring), rectal transection was at the top of the anal canal and a mucosectomy was performed above the dentate line. In case of juxta- or intraanal tumors, a partial or total intersphincteric resection was carried out, transecting the anal canal at least 1 cm below the tumor.17 Then, the rectum was closed transanally by suture to avoid intraoperative tumor seeding, and was carefully dissected free of the levator ani muscle until the level of the pelvic dissection was reached. Then, rectal specimen was removed transanally or via a small (5–6 cm) suprapubic incision at the discretion of the surgeon. Reconstruction included a colonic pouch, when feasible, and a handsewn coloanal anastomosis. A loop ileostomy and a presacral suction drain were systematically used.
Laparoscopic Coloanal Anastomosis for Rectal Cancer
and disease-free survivals were measured from the date of operation to death, recurrence, and last follow-up evaluation. Patients with M1 disease (synchronous metastases) were excluded from disease-free survival analysis. Functional outcome was evaluated in patients alive with 12 months of follow-up after ileostomy closure and without recurrence. A questionnaire was send to the patients in March 2012, asking for stool frequency, fragmentation, urgency, dyschezia, feces/flatus discrimination, and anal incontinence. Score of the study by Jorge and Wexner20 was used to assess fecal continence. Patients who did not respond to the questionnaire were contacted by telephone.
Statistical Analysis Data were expressed as median with range. Comparison between groups was assessed by Mann-Whitney tests and by χ 2 tests or the Fisher exact tests when appropriate. Recurrence and survival were evaluated by the Kaplan-Meier method and compared with the log-rank test. Predictive factors of survival were analyzed by using a stepwise Cox proportional hazards regression model. P < 0.05 was considered as statistically significant.
RESULTS Surgical Technique and Postoperative Morbidity Of the 220 laparoscopic restorative rectal resections for low rectal cancer, a conventional or Parks coloanal anastomosis was performed in 68 patients and an intersphincteric resection with low coloanal anastomosis in 152 patients. The anastomosis was 2 cm (range, 0.5–4) from the anal verge. A colonic pouch was associated with the coloanal anastomosis in 151 patients (69%). The specimen extraction site was transanal in 122 cases, through a 6-cm suprapubic incision in 66 cases and through a converted midline laparotomy in 32 cases. Overall, the extraction site was transanal in 55% of the cases and transabdominal in 45% of the cases. Postoperative mortality rate (60 days) was 0.5% (1 of 220). Conversion to a laparotomy occurred in 32 patients (15%). Reasons for conversion are in Table 1. The overall morbidity rate was 38% (n = 84) and significant surgical morbidity rate, that is, stage III– IV of Dindo classification,21 was 17% (n = 38) (Table 2). The rate of pelvic sepsis (anastomotic leakage, pelvic abscess and/or colonic ischemia) was 10% (n = 24). Medical morbidity included cardiorespiratory insufficiency (n = 3), renal insufficiency (n = 2), pancreatitis (n = 1), and temporary urinary dysfunction (n = 10). Hospital stay was 9 days (range, 5–57 days).
TABLE 1. Reasons for Conversion During Laparoscopic Coloanal Anastomosis N = 32
End Points We analyzed quality of surgery, oncologic and functional outcomes. Quality of surgery included circumferential resection margin and the mesorectal excision grade. The circumferential resection margin was considered as negative, if more than 1 mm.18 Assessment of the mesorectum used the Quirke classification19 : grade 1 was incomplete mesorectum showing the muscularis propria, grade 2 was subcomplete mesorectum with irregularities of the mesorectal surface and grade 3 was complete mesorectum with no defect more than 5 mm. Local recurrence was defined as any recurrence occurring in the pelvis or at the perineum, with or without metastases. Overall C 2014 Lippincott Williams & Wilkins
Pelvic causes Adhesions Tumor fixation Difficulty for low pelvic dissection Hemorrhage Abdominal causes Difficulty for splenic flexure mobilization Difficulty for exploration Difficulty of dissection Technical problem Pneumoperitoneum intolerance
5 4 6 4 4 5 2 1 1
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TABLE 2. Surgical Morbidity N = 61∗ Bowel obstruction Anastomotic leak and/or pelvic abscess† Distal colonic ischemia Pelvic hematoma Small bowel perforation Wound dehiscence Ileostomy prolapse or stenosis
25 18 6 5 3 2 2
∗
Some patients may have had several complications. †Includes 1 colovaginal fistula and 1 leak from the colonic pouch.
Pathologic Data and Quality of Surgery The pathologic assessment of rectal specimen was performed by a single colorectal pathologist by using the pathologic checklist for colorectal cancer recommended by the US guidelines.18 To optimize assessment, the whole of the residual tumor was included in irradiated specimen. Of 220 patients treated for low rectal cancer, 17 (8%) were stage 0 (pT0-N0, complete response after radiochemotherapy), 87 (40%) were stage I (pT1-2N0), 43 (20%) were stage II (pT3-4N0), and 73 (33%) were stage III (pT1-4N1-2). The tumor size was 3.5 cm (range, 1–15). The median number of lymph nodes analyzed was 13 (range, 1–40). The distal resection margin was 15 mm (range, 0–40 mm) and the circumferential resection margin was 5 mm (range, 0–20 mm). The rate of positive circumferential resection margin (≤1 mm) was 9% (20 of 220). Overall, the rate of R0 resection was 89%. Macroscopic pathologic assessment of the mesorectum showed grade 3 (complete mesorectum) in 174 patients, grade 2 (subcomplete mesorectum) in 26 patients, and grade 1 (incomplete mesorectum) in 20 patients, including perforation in 4 cases. Overall, the mesorectum was complete or subcomplete in 91% of the specimen.
Recurrence and Survival The median follow-up was 51 months (range, 1–151 months). The local recurrence rate was 4.5% (n = 10) and the rate of distant metastases was 21.8% (n = 48). The delay of overall recurrence was 12 months (range, 3–88 months). There was no anastomotic, perineal, or port-site recurrence. The 5-year overall and disease-free survival rates were 83% and 70%, respectively (Fig. 1).
FIGURE 1. Overall and disease-free survival rates after coloanal anastomosis for low rectal cancer. OS indicates overall survival; DFS, disease-free survival.
TABLE 3. Patient Characteristics According to Type of Extraction Transanal
Age, median (range), yr Sex, male, n (%) BMI, median (range), kg/m2 Tumor stage T1–T2, n (%) T3–T4, n (%) Tumor size, median (range), cm Tumor height from anal verge, median (range), cm Preoperative radiotherapy, n (%)
Transabdominal
(N = 122)
(N = 98)
P
63 (20–90) 70 (57) 24.3 (17.3–33.6)
65 (25–85) 69 (70) 25.8 (18.8–38.3)
0.083 0.046 0.010
26 (21) 96 (79) 3.9 (1–10)
0.120 13 (13) 85 (87) 4 (1–15)
0.309
4 (1.5–6)
0.282
4 (1–6) 104 (85)
88 (90)
0.314
Functional Outcome Among the 220 patients receiving a laparoscopic coloanal anastomosis for low rectal cancer, 134 were eligible for functional outcome. Reasons for exclusion were death (n = 31), follow-up less than 12 months (n = 25), recurrence (n = 20), definitive stoma for complications, or temporary stoma not reversed (n = 10). Overall, 131 of the 134 eligible patients (98%) responded to the questionnaire or the phone call. The median number of stools per 24 hours was 3 (range, 1–10), stool fragmentation was present in 81 patients (62%), and urgency noted in 64 patients (49%). Dyschezia was present in 30% of the cases (n = 39) and feces/flatus discrimination was possible in 73 patients (56%). The median anal continence score was 6 (range, 0–20).
Comparison Between Transanal and Transabdominal Extraction Characteristics of the patients according to the extraction site are presented in Table 3. Patients treated by transabdominal extraction were more likely to be male and obese. Tumor characteristics and neoadjuvant treatment were similar in both groups. We observed 140 | www.annalsofsurgery.com
no difference in mortality and morbidity rates between transanal and transabdominal extraction groups (Table 4). Quality of surgery was not influenced by the extraction site. The rate of positive circumferential margin was 7% after transanal extraction versus 11% after transabdominal extraction (P = 0.32). Similarly, a complete mesorectum was observed in 83% of patients with transanal extraction, compared with 75% after transabdominal extraction (P = 0.22). There was no difference in long-term oncologic outcome due to the rectum extraction site. The local recurrence rate was 4% and 5% after transanal and transabdominal extraction, respectively (Table 4). There was no perineal recurrence in both groups. At 5 years, the overall survival rate was 86% versus 80% (P = 0.37) and the diseasefree survival rate was 72% versus 68% (P = 0.63) between patients with transanal and transabdominal extraction, respectively (Figs. 2 and 3). Functional outcome after laparoscopic coloanal anastomosis for low rectal cancer showed no difference in term of stool frequency, fragmentation, urgency, dyschezia, and feces/flatus discrimination C 2014 Lippincott Williams & Wilkins
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Annals of Surgery r Volume 261, Number 1, January 2015
TABLE 4. Outcome After Laparoscopic Coloanal Anastomosis According to Type of Extraction
Mortality, n (%) Overall morbidity, n (%) Surgical morbidity (Dindo III–V) , n (%) Positive circumferential margin, n (%) Mesorectum grade (19) 1 incomplete, n (%) 2 subcomplete, n (%) 3 complete, n (%) Local recurrence, n (%)
Laparoscopic Coloanal Anastomosis for Rectal Cancer
TABLE 5. Functional Results of Laparoscopic Coloanal Anastomosis According to Extraction Site (N = 131)
Transanal
Transabdominal
(N = 122)
(N = 98)
P
Transanal Transabdominal
1 (0.8) 42 (34) 18 (15)
0 (0) 42 (43) 21 (21)
1.000 0.201 0.198
9 (7)
11 (11)
0.324
6 (5) 15 (12) 101 (83) 5 (4)
0.056 14 (14) 11 (11) 73 5 (5)
(75) 0.976
Stool frequency, median (range) Stool fragmentation, n (%) Fecal urgency, n (%) Dyschezia, n (%) Feces/flatus discrimination, n (%) Wexner score, median (range) Follow-up, median (range), mo
(N = 73)
(N = 58)
P
3 (1–10) 43 (59) 36 (49) 18 (25) 38 (52) 6 (0–20) 46 (3–137)
3 (2–10) 38 (66) 28 (48) 21 (36) 35 (60) 6 (0–20) 50 (13–107)
0.322 0.439 0.906 0.151 0.343 0.919 0.486
between patients with transanal specimen extraction and those with transabdominal extraction (Table 5). The anal continence score was also similar in both groups: 6 versus 6 (P = 0.92) after a median follow-up of 48 months. Independent predictive factors of fecal incontinence (continence score ≥7) were preoperative radiotherapy and tumor height from the anal verge 4 cm or less. The site of extraction and patient characteristics did not influence continence.
DISCUSSION
FIGURE 2. Overall survival rate according to rectum extraction site. Transabdo. indicates transabdominal.
FIGURE 3. Disease-free survival rate according to rectum extraction site. Transabdo. indicates transabdominal. C 2014 Lippincott Williams & Wilkins
The aim of the study was to demonstrate the safety and the efficacy of the laparoscopic approach for sphincter-preserving surgery in low rectal cancer. First, we observed a low local recurrence rate and a good survival rate in the overall population of patients treated by laparoscopic coloanal anastomosis. Second, we demonstrated no difference of morbidity rate, quality of specimen, positive circumferential resection margin, local recurrence, and survival rate between transanal and transabdominal extraction groups. Finally, gastrointestinal function and anal continence were similar in both groups. Our results therefore suggest that laparoscopic coloanal anastomosis is efficient in low rectal cancer and that removing the rectal specimen through the anus that is, avoiding a minilaparotomy, did not affect long-term oncologic and functional outcome. Some randomized trials6,22,23 have suggested the feasibility of the laparoscopic approach in the treatment of rectal cancer and one6 has demonstrated the efficacy with similar 5 years survival rate between open and laparoscopic surgery. However, the technical problems for ultralow sphincter preservation have never been discussed in these trials. The reason is probably because most patients with rectal cancer of the lower third are treated by abdominoperineal excision.24 Only 2 retrospective series have challenged the issue of laparoscopic sphincter preservation in low rectal cancer.13,14 Marks et al13 reported on 79 patients with T2–T3 rectal tumors at 1.2 cm from the anal ring and treated by laparoscopic coloanal anastomosis after radiochemotherapy. The distal rectum was dissected transanally first and the laparoscopic approach was used for the mesorectal dissection and the colonic mobilization. The specimen was extracted either transabdominally or transanally. Major and minor morbidity rates were 11% and 19%, respectively. A permanent colostomy was required in 10% of the patients for inadequate surgical margin, postoperative complications, or recurrence. After a mean follow-up of 34 months, the local recurrence rate was 2.5% and the distant metastases rate was 10% with an overall survival rate of 97%. Similarly Park et al14 analyzed 130 patients with low rectal cancer at 3.6 cm from the anal verge treated by laparoscopic intersphincteric resection. The laparoscopic approach was carried out first, whereas the perineal approach was used at the end of the procedure for rectal transection and specimen extraction. They reported a shorter bowel recovery and hospital stay, but similar morbidity rate and surgical margin, compared with an open controlled group. After www.annalsofsurgery.com | 141
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a median follow-up of 32 months, the local recurrence was 2.6% and the 3-year survival rate was 77%. In both series, the feasibility of the laparoscopic restorative surgery for low rectal cancer is well documented. However, there is no long-term oncologic data and functional outcome that have been reported. Furthermore, the impact of transanal extraction of the specimen has never been evaluated. In the CLASICC UK trial comparing laparoscopic and open surgery for colorectal cancer, a total of 10 patients presented wound/port site recurrence after 5 years of follow-up.6 The risk of wound/port site recurrence was 0.5% in the open group, which was similar to the 0.6% reported in 1711 open colorectal procedures from US trials.25 By contrast, the risk of wound/port site recurrence was 2.4% in the laparoscopic group, which seemed 5 times higher than after open surgery. Moreover, among the 10 patients presenting recurrence, 1 was a true port-site recurrence, whereas 9 were extractionsite recurrence. Thus, the laparoscopic approach may increase the rate of recurrence related to the extraction-site, although this risk decreases with experience and volume. The reasons are not clear and probably multifactorial: direct wound implantation, tumor perforation, excessive tumor manipulation, small incision, large specimen, no wound protector, poor surgical technique, or inadequate surgical experience.26 In our study including 220 laparoscopic coloanal anastomoses for low rectal cancer, we observed 4.5% of local recurrence with zero wound/port site recurrence after a median follow-up of 51 months. Moreover, the 122 patients with transanal specimen extraction, where wound protector were not used, had similar mesorectal grade and outcome than those with conventional transabdominal extraction (Table 4). Our results suggest, first the efficacy of the laparoscopic ultralow sphincter-preserving surgery in low rectal cancer, second the safety of the transanal extraction site. We believe that neoadjuvant radiochemotherapy (downstaging effect), the technique of total mesorectal excision (protector effect of the preserved fascia recti), the full laparoscopic approach (protector against improper tumor handling manipulation), and patient selection for extraction site (transabdominal for obese) have participated to validate our results. The functional outcome of the laparoscopic restorative surgery for low rectal cancer has never been evaluated. We reported, for the first time, a careful long-term gastrointestinal outcome in patients receiving a hand-sewn coloanal anastomosis by using a full laparoscopic approach. The results were obtained by a questionnaire sent to patients free of disease with at least 1 year of follow-up after stoma closure. The median stools frequency per day was 3; and half the number of patients had stool fragmentation and urgency. These results were similar to those of patients treated in the same institution by open surgery.27 More interesting is the fact that patients treated by transanal extraction had the same anal continence score than those treated by transabdominal extraction, suggesting that removing the rectal specimen through the anus is functionally safe. Our conclusion are limited by the fact that the BMI was slightly lower in the transanal group (24.3 vs 25.8; P = 0.01), suggesting that some obese patients probably received transabdominal instead of transanal extraction. Therefore, as we recommend preventing excessive stretching of the anal sphincter during rectal extraction, we also recommend to be cautious when performing transanal extraction in obese patients with wide mesorectal specimen, especially to avoid mesorectal injury and tumor spillage.
CONCLUSIONS We reported long-term outcome in 220 patients operated by laparoscopic coloanal anastomosis for low rectal cancer and observed that pelvic control and survival were not compromised by the association between mini invasive surgery and ultralow sphincter preservation. Moreover, we demonstrated the safety and efficacy of transanal 142 | www.annalsofsurgery.com
extraction of the rectal specimen with similar oncologic and functional outcome than the conventional abdominal extraction. Because of the wound advantages of transanal extraction, in term of abdominal wall preservation, transanal extraction can be recommended in laparoscopic surgical management of low rectal cancer.
REFERENCES 1. Lacy AM, Garcia-Valdecasas JC, Delgado S, et al. Laparoscopy-assisted colectomy versus open colectomy for treatment of non-metastatic colon cancer: a randomised trial. Lancet. 2002;359:2224–2229. 2. Leung KL, Kwok SP, Lam SC, et al. Laparoscopic resection of rectosigmoid carcinoma: prospective randomised trial. Lancet. 2004;363:1187–1192. 3. Clinical Outcomes of Surgical Therapy (COST) Study Group. A comparison of laparoscopically assisted and open colectomy for colon cancer. N Engl J Med. 2004;350:2050–2059. 4. Jayne DG, Guillou PJ, Thorpe H, et al. UK MRC CLASICC Trial Group. Randomized trial of laparoscopic-assisted resection of colorectal carcinoma: 3-year results of the UK MRC CLASICC Trial Group. J Clin Oncol. 2007;25:3061– 3068. 5. The COlon Cancer Laparoscopic or Open Resection Study Group. Survival after laparoscopic surgery versus open surgery for colon cancer: long-term outcome of a randomised clinical trial. Lancet Oncol. 2009;10:44–52. 6. Jahne DG, Thorpe HC, Copeland J, et al. Five-year follow-up of the Medical Research Council CLASICC trial of laparoscopically assisted versus open surgery for colorectal cancer. Br J Surg. 2010;97:1638–1645. 7. Guillou PJ, Quirke P, Thorpe H, et al. Short-term end points of conventional versus laparoscopic-assisted surgery in patients with colorectal cancer (MRC CLASICC trial): multicentre, randomised controlled trial. Lancet. 2005;365:1718–1726. 8. Laurent C, Leblanc F, Gineste C, et al. Laparoscopic approach in surgical treatment of rectal cancer. Br J Surg. 2007;94:1555–1561. 9. Ito M, Sugito M, Kobayashi A, et al. Relationship between multiple numbers of stapler firings during rectal division and anastomotic leakage after laparoscopic rectal resection. Int J Colorectal Dis. 2008;23:703–707. 10. Scheidbach H, Schneider C, Konradt J, et al. Laparoscopic abdominoperineal resection and anterior resection with curative intent for carcinoma of the rectum. Surg Endosc. 2002;16:7–13. 11. Akamatsu H, Omori T, Oyama T, et al. Totally laparoscopic low anterior resection for lower rectal cancer: combination of a new technique for intracorporeal anastomosis with prolapsing technique. Dig Surg. 2009;26:446–450. 12. Fujimoto Y, Akiyoshi T, Kuroyanagi H, et al. Safety and feasibility of laparoscopic intersphincteric resection for very low rectal cancer. J Gastrointest Surg. 2010;14:645–650. 13. Marks J, Mizrahi B, Dalane S, et al. Laparoscopic transanal abdominal transanal resection with sphincter preservation for rectal cancer in the distal 3 cm of the rectum after neoadjuvant therapy. Surg Endosc. 2010;24:2700– 2707. 14. Park JS, Choi G-S, Jun SH, et al. Laparoscopic versus open intersphincteric resection and coloanal anastomosis for low rectal cancer. Ann Surg. 2011;254:941–46. 15. Rullier E, Vendrely V. Can mesorectal lymph nodes excision be avoided in rectal cancer surgery? Colorectal Dis. 2011;13(suppl 7):37–42. 16. Edge SB, Byrd DR, Carducci MA, et al. AJCC Cancer Staging Manual. 7th ed. New York, NY: Springer; 2009. 17. Rullier E, Laurent C, Bretagnol F, et al. Sphincter-saving resection for all rectal carcinomas: the end of the 2-cm distal rule. Ann Surg. 2005;241:465–469. 18. Washington MK, Berlin F, Branton P, et al. Protocol for examination of specimens from patients with primary carcinoma of the colon and rectum. Arch Pathol Lab Med. 2009;133:1539–1551. 19. Quirke P, Steele R, Monson J, et al. Effect of the plane of surgery achieved on local recurrence in patients with operable rectal cancer: a prospective study using data from the MRC CR07 and NCIC-CTG C016 randomised clinical trial. Lancet. 2009;373:821–828. 20. Jorge JM, Wexner SD. Etiology and management of fecal incontinence. Dis Colon Rectum. 1993;36:77–96. 21. Dindo D, Demartines N, Clavien PA. 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. 22. Kang SB, Park JW, Jeong SY, et al. Open versus laparoscopic surgery for mid or low rectal cancer after neoadjuvant chemoradiotherapy (COREAN trial): short-term outcomes of an open-label randomised controlled trial. Lancet Oncol. 2010;11:637–645.
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23. Lujan J, Valero G, Hernandez Q, et al. Randomized clinical trial comparing laparoscopic and open surgery in patients with rectal cancer. Br J Surg. 2009;96:982–989. 24. Ricciardi R, Roberts PL, Read TE, et al. Variability in reconstructive procedures following cancer surgery in the United States. Dis Colon Rectum. 2010;53: 874–880. 25. Reilly WT, Nelson H, Schroeder G, et al. Wound recurrence following conventional treatment of colorectal cancer. A rare but
C 2014 Lippincott Williams & Wilkins
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perhaps underestimated problem. Dis Colon Rectum. 1996;39:200– 207. 26. Seow-Choen F, Wan WH, Tan KY. The use of a wound protector to prevent port site recurrence may not be totally logical. Colorectal Dis. 2009;11: 123–125. 27. Bretagnol F, Rullier E, Laurent C, et al. Comparison of functional results and quality of life between intersphincteric resection and conventional coloanal anastomosis for low rectal cancer. Dis Colon Rectum. 2004;47:832–838.
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Laparoscopic Total Mesorectal Excision With Coloanal Anastomosis for Rectal Cancer Quentin Denost, MD, PhD, Jean-Philippe Adam, MD, Arnaud Pontallier, MD, Bertrand Celerier, MD, Christophe Laurent, MD, PhD, and Eric Rullier, MD
Objective: Oncologic and functional outcomes were compared between transanal and transabdominal specimen extraction after laparoscopic coloanal anastomosis for rectal cancer. Background: Laparoscopic coloanal anastomosis is an attractive new surgical option in patients with low rectal cancer because laparotomy is not necessary due to transanal specimen extraction. Risks of tumor spillage and fecal incontinence induced by transanal extraction are not known. Methods: Between 2000 and 2010, 220 patients with low rectal cancer underwent laparoscopic rectal excision with hand-sewn coloanal anastomosis. The rectal specimen was extracted transanally in 122 patients and transabdominally in 98 patients. End points were circumferential resection margin, mesorectal grade, local recurrence, survival, and functional outcome. Results: The mortality rate was 0.5% and surgical morbidity rate was 17%. The rate of positive circumferential resection margin was 9% and the mesorectum was graded complete in 79%, subcomplete in 12%, and incomplete in 9%. After a follow-up of 51 months (range, 1–151), the local recurrence rate was 4% and overall survival and disease-free survival rates were 83% and 70% at 5 years, respectively. The continence score was 6 (range, 0–20). There was no difference of mortality rate, morbidity rate, circumferential resection margin, mesorectal grade, local recurrence (4% vs 5%, P = 0.98), and disease-free survival rate (72% vs 68%, P = 0.63) between transanal and transabdominal extraction groups. Continence score was also similar (6 vs 6, P = 0.92). Conclusions: Transanal extraction of the rectal specimen did not compromise oncologic and functional outcome after laparoscopic surgery for low rectal cancer and seems as a safe option to preserve the abdominal wall. Keywords: coloanal anastomosis, laparoscopy, low rectal cancer, sphincter preservation, transanal extraction (Ann Surg 2015;261:138–143)
L
aparoscopic surgery is validated in treatment of colon cancer.1–5 The advantages are improved short-term outcome with no difference of survival at 5 years. In contrast, the laparoscopic approach in rectal cancer is still debated. Only 1 randomized trial is available for long-term outcome, suggesting similar survival rates between laparoscopic and open surgery at 5 years,6 but a higher morbidity rate7 and a lower survival rate in the subgroup of converted patients.6 One of the main restrictions for developing laparoscopic surgery in rectal cancer are the difficulties for stapling the distal rectum to achieve a low anterior resection.8,9 This may translate to
From the Department of Surgery, Colorectal Unit, CHU Bordeaux, Saint-Andre Hospital, France; and Universit´e Bordeaux Segalen, Bordeaux, France. Disclosure: The authors report no financial or other conflicts of interest relevant to the subject of this article. Presented at the Congress of European Society of Coloproctology (ESCP), as oral communication, September 26–28, 2012, Vienne, France. Reprints: Eric Rullier, MD, Service de Chirurgie Digestive, Hopital Saint-Andre, 33075 Bordeaux, France. E-mail: [email protected]. C 2014 by Lippincott Williams & Wilkins Copyright ISSN: 0003-4932/14/26101-0138 DOI: 10.1097/SLA.0000000000000855
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a higher rate of APR in laparoscopic procedures,10 the necessity to use hybrid procedures for rectal transection11 or to perform a hand-sewn coloanal anastomosis. There are few data of full laparoscopic coloanal anastomosis for rectal cancer,12–14 including small series12 and short follow-up.13,14 Moreover, the risk of anastomotic or perineal recurrence induced by transanal extraction of the rectal specimen is not known. In the United Kingdom trial comparing laparoscopic versus open colorectal surgery, 9 extraction-site recurrences have been reported in the laparoscopic group compared with one in the open group.6 Moreover, functional outcomes of laparoscopic coloanal anastomosis have never been reported, and therefore the potential risk of anal incontinence related to transanal specimen extraction has never been discussed. The objective of our large monocenter series was to report long-term outcome of laparoscopic coloanal anastomosis for rectal cancer, with the aim to solve the oncologic and functional impact of transanal extraction.
METHODS Patients All patients operated on between 2000 and 2010 at Saint-Andre Hospital by laparoscopic total mesorectal excision with hand-sewn coloanal anastomosis for low rectal cancers were considered. During this period, 871 patients were treated for rectal cancer, 244 received open surgery for T4 (tumor fixation) or M1 (metastatic disease) lesions, 277 had a laparoscopic low anterior resection with endoscopic rectal stapling for high and midrectal tumors, 30 were treated by laparoscopic abdominoperineal excision for a very low rectal cancer infiltrating the external sphincter or the levator ani muscles, and 100 underwent local excision for early (T1) low rectal cancer or downstaged T2–T3 after radiochemotherapy.15 The population study included 220 patients with laparoscopic total mesorectal excision and coloanal anastomosis for rectal cancer. There were 139 males and 81 females with a median age of 64 (range, 20–90) years. The ASA score was 1 in 136 patients, 2 in 73 patients, and 3 in 11 patients. The body mass index was 25 (range, 17–38). Tumors were staged after colonoscopy, CT scan, endorectal ultrasound and pelvic magnetic resonance imaging according to the TNM/UICC classification16 as follows: uT1 in 13 patients, uT2 in 26 patients, uT3 in 175 patients, and uT4 in 6 patients; 130 were uN+ and 13 M1 (synchronous metastases). The tumors were 4 cm (range, 1–6 cm) from the anal verge and 1 cm (range, −2 to 3 cm) from the anal ring.
Neoadjuvant and Adjuvant Treatments Neoadjuvant radiochemotherapy was used in patients with locally advanced disease, that is, T3 and T4 or N1 disease. Preoperative radiotherapy consisted in 45 Gy during 5 weeks and was given in 192 patients (87%), in association with concomitant neoadjuvant chemotherapy (5 fluorouracil and capecitabine) in 164 patients. Postoperative adjuvant chemotherapy (5 fluorouracil and capecitabine and oxaliplatine) was given for 6 months in patients Annals of Surgery r Volume 261, Number 1, January 2015
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Annals of Surgery r Volume 261, Number 1, January 2015
with positive lymph nodes at the specimen (pN1 disease). This included 84 patients after laparoscopic coloanal anastomosis (38%).
Surgical Procedure Surgery was performed 6 weeks after radiotherapy. All patients had a mechanic bowel preparation the day before surgery and antibioprophylaxia the day of surgery. Patients were operated on by a team trained in both colorectal and laparoscopic surgery. All patients had curative surgery. Patients with synchronous metastases had surgery of the secondaries 2 months after rectal surgery. A 5-port technique was used. A high ligation of the inferior mesenteric artery and a full mobilization of the left colon, including the splenic flexure, were systematically performed. This was to achieve a tension-free low anastomosis and also to permits transanal extraction of the specimen. During this step, care was taken to open enough window into the mesentery to optimize left colon mobilization, but avoiding injury of the marginal colonic artery. Exposure of the pelvis was facilitated by the previous mobilization of the colon. The pelvic dissection was performed by using harmonic scalpel (Ultracision; Ethicon Endosurgery, Cincinnati, OH), thermal fusion (Ligasure Advance; Covidien, Mansfield, MA), or conventional scissors with monopolar coagulation. It included total mesorectal excision with preservation of the pelvic autonomic nerves. The dissection began posteriorly to continue laterally first on the right then on the left and finished anteriorly. The hypogastric nerves, inferior hypogastric plexuses, and presacral nerves were identified and preserved, except in case of fixed tumor. In males, the Denonvilliers fascia was removed, except in case of posterior tumors. The laparoscopic dissection continued along the pelvic floor toward the top of the anal canal anteriorly and the puborectalis sling posteriorly. The distal level of the laparoscopic dissection was confirmed by digital rectal examination. In case of juxta or intraanal tumors suitable for intersphincteric resection, the aponeurosis of the levator ani muscles (sheath of the pelvic floor) was incised to enter into the intersphincteric plane. This steep was enhanced by the optimal view of the laparoscopic approach and facilitated the connection with the perineal dissection. During the perineal phase, the anal canal was then exposed by a self-holding retractor (Lone Star Retractor; Lone Star Medical Products Inc., Houston, TX). A mesh was introduced into the rectum to limit the risk of spillage. In case of supraanal tumors (>1 cm from the anal ring), rectal transection was at the top of the anal canal and a mucosectomy was performed above the dentate line. In case of juxta- or intraanal tumors, a partial or total intersphincteric resection was carried out, transecting the anal canal at least 1 cm below the tumor.17 Then, the rectum was closed transanally by suture to avoid intraoperative tumor seeding, and was carefully dissected free of the levator ani muscle until the level of the pelvic dissection was reached. Then, rectal specimen was removed transanally or via a small (5–6 cm) suprapubic incision at the discretion of the surgeon. Reconstruction included a colonic pouch, when feasible, and a handsewn coloanal anastomosis. A loop ileostomy and a presacral suction drain were systematically used.
Laparoscopic Coloanal Anastomosis for Rectal Cancer
and disease-free survivals were measured from the date of operation to death, recurrence, and last follow-up evaluation. Patients with M1 disease (synchronous metastases) were excluded from disease-free survival analysis. Functional outcome was evaluated in patients alive with 12 months of follow-up after ileostomy closure and without recurrence. A questionnaire was send to the patients in March 2012, asking for stool frequency, fragmentation, urgency, dyschezia, feces/flatus discrimination, and anal incontinence. Score of the study by Jorge and Wexner20 was used to assess fecal continence. Patients who did not respond to the questionnaire were contacted by telephone.
Statistical Analysis Data were expressed as median with range. Comparison between groups was assessed by Mann-Whitney tests and by χ 2 tests or the Fisher exact tests when appropriate. Recurrence and survival were evaluated by the Kaplan-Meier method and compared with the log-rank test. Predictive factors of survival were analyzed by using a stepwise Cox proportional hazards regression model. P < 0.05 was considered as statistically significant.
RESULTS Surgical Technique and Postoperative Morbidity Of the 220 laparoscopic restorative rectal resections for low rectal cancer, a conventional or Parks coloanal anastomosis was performed in 68 patients and an intersphincteric resection with low coloanal anastomosis in 152 patients. The anastomosis was 2 cm (range, 0.5–4) from the anal verge. A colonic pouch was associated with the coloanal anastomosis in 151 patients (69%). The specimen extraction site was transanal in 122 cases, through a 6-cm suprapubic incision in 66 cases and through a converted midline laparotomy in 32 cases. Overall, the extraction site was transanal in 55% of the cases and transabdominal in 45% of the cases. Postoperative mortality rate (60 days) was 0.5% (1 of 220). Conversion to a laparotomy occurred in 32 patients (15%). Reasons for conversion are in Table 1. The overall morbidity rate was 38% (n = 84) and significant surgical morbidity rate, that is, stage III– IV of Dindo classification,21 was 17% (n = 38) (Table 2). The rate of pelvic sepsis (anastomotic leakage, pelvic abscess and/or colonic ischemia) was 10% (n = 24). Medical morbidity included cardiorespiratory insufficiency (n = 3), renal insufficiency (n = 2), pancreatitis (n = 1), and temporary urinary dysfunction (n = 10). Hospital stay was 9 days (range, 5–57 days).
TABLE 1. Reasons for Conversion During Laparoscopic Coloanal Anastomosis N = 32
End Points We analyzed quality of surgery, oncologic and functional outcomes. Quality of surgery included circumferential resection margin and the mesorectal excision grade. The circumferential resection margin was considered as negative, if more than 1 mm.18 Assessment of the mesorectum used the Quirke classification19 : grade 1 was incomplete mesorectum showing the muscularis propria, grade 2 was subcomplete mesorectum with irregularities of the mesorectal surface and grade 3 was complete mesorectum with no defect more than 5 mm. Local recurrence was defined as any recurrence occurring in the pelvis or at the perineum, with or without metastases. Overall C 2014 Lippincott Williams & Wilkins
Pelvic causes Adhesions Tumor fixation Difficulty for low pelvic dissection Hemorrhage Abdominal causes Difficulty for splenic flexure mobilization Difficulty for exploration Difficulty of dissection Technical problem Pneumoperitoneum intolerance
5 4 6 4 4 5 2 1 1
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TABLE 2. Surgical Morbidity N = 61∗ Bowel obstruction Anastomotic leak and/or pelvic abscess† Distal colonic ischemia Pelvic hematoma Small bowel perforation Wound dehiscence Ileostomy prolapse or stenosis
25 18 6 5 3 2 2
∗
Some patients may have had several complications. †Includes 1 colovaginal fistula and 1 leak from the colonic pouch.
Pathologic Data and Quality of Surgery The pathologic assessment of rectal specimen was performed by a single colorectal pathologist by using the pathologic checklist for colorectal cancer recommended by the US guidelines.18 To optimize assessment, the whole of the residual tumor was included in irradiated specimen. Of 220 patients treated for low rectal cancer, 17 (8%) were stage 0 (pT0-N0, complete response after radiochemotherapy), 87 (40%) were stage I (pT1-2N0), 43 (20%) were stage II (pT3-4N0), and 73 (33%) were stage III (pT1-4N1-2). The tumor size was 3.5 cm (range, 1–15). The median number of lymph nodes analyzed was 13 (range, 1–40). The distal resection margin was 15 mm (range, 0–40 mm) and the circumferential resection margin was 5 mm (range, 0–20 mm). The rate of positive circumferential resection margin (≤1 mm) was 9% (20 of 220). Overall, the rate of R0 resection was 89%. Macroscopic pathologic assessment of the mesorectum showed grade 3 (complete mesorectum) in 174 patients, grade 2 (subcomplete mesorectum) in 26 patients, and grade 1 (incomplete mesorectum) in 20 patients, including perforation in 4 cases. Overall, the mesorectum was complete or subcomplete in 91% of the specimen.
Recurrence and Survival The median follow-up was 51 months (range, 1–151 months). The local recurrence rate was 4.5% (n = 10) and the rate of distant metastases was 21.8% (n = 48). The delay of overall recurrence was 12 months (range, 3–88 months). There was no anastomotic, perineal, or port-site recurrence. The 5-year overall and disease-free survival rates were 83% and 70%, respectively (Fig. 1).
FIGURE 1. Overall and disease-free survival rates after coloanal anastomosis for low rectal cancer. OS indicates overall survival; DFS, disease-free survival.
TABLE 3. Patient Characteristics According to Type of Extraction Transanal
Age, median (range), yr Sex, male, n (%) BMI, median (range), kg/m2 Tumor stage T1–T2, n (%) T3–T4, n (%) Tumor size, median (range), cm Tumor height from anal verge, median (range), cm Preoperative radiotherapy, n (%)
Transabdominal
(N = 122)
(N = 98)
P
63 (20–90) 70 (57) 24.3 (17.3–33.6)
65 (25–85) 69 (70) 25.8 (18.8–38.3)
0.083 0.046 0.010
26 (21) 96 (79) 3.9 (1–10)
0.120 13 (13) 85 (87) 4 (1–15)
0.309
4 (1.5–6)
0.282
4 (1–6) 104 (85)
88 (90)
0.314
Functional Outcome Among the 220 patients receiving a laparoscopic coloanal anastomosis for low rectal cancer, 134 were eligible for functional outcome. Reasons for exclusion were death (n = 31), follow-up less than 12 months (n = 25), recurrence (n = 20), definitive stoma for complications, or temporary stoma not reversed (n = 10). Overall, 131 of the 134 eligible patients (98%) responded to the questionnaire or the phone call. The median number of stools per 24 hours was 3 (range, 1–10), stool fragmentation was present in 81 patients (62%), and urgency noted in 64 patients (49%). Dyschezia was present in 30% of the cases (n = 39) and feces/flatus discrimination was possible in 73 patients (56%). The median anal continence score was 6 (range, 0–20).
Comparison Between Transanal and Transabdominal Extraction Characteristics of the patients according to the extraction site are presented in Table 3. Patients treated by transabdominal extraction were more likely to be male and obese. Tumor characteristics and neoadjuvant treatment were similar in both groups. We observed 140 | www.annalsofsurgery.com
no difference in mortality and morbidity rates between transanal and transabdominal extraction groups (Table 4). Quality of surgery was not influenced by the extraction site. The rate of positive circumferential margin was 7% after transanal extraction versus 11% after transabdominal extraction (P = 0.32). Similarly, a complete mesorectum was observed in 83% of patients with transanal extraction, compared with 75% after transabdominal extraction (P = 0.22). There was no difference in long-term oncologic outcome due to the rectum extraction site. The local recurrence rate was 4% and 5% after transanal and transabdominal extraction, respectively (Table 4). There was no perineal recurrence in both groups. At 5 years, the overall survival rate was 86% versus 80% (P = 0.37) and the diseasefree survival rate was 72% versus 68% (P = 0.63) between patients with transanal and transabdominal extraction, respectively (Figs. 2 and 3). Functional outcome after laparoscopic coloanal anastomosis for low rectal cancer showed no difference in term of stool frequency, fragmentation, urgency, dyschezia, and feces/flatus discrimination C 2014 Lippincott Williams & Wilkins
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Annals of Surgery r Volume 261, Number 1, January 2015
TABLE 4. Outcome After Laparoscopic Coloanal Anastomosis According to Type of Extraction
Mortality, n (%) Overall morbidity, n (%) Surgical morbidity (Dindo III–V) , n (%) Positive circumferential margin, n (%) Mesorectum grade (19) 1 incomplete, n (%) 2 subcomplete, n (%) 3 complete, n (%) Local recurrence, n (%)
Laparoscopic Coloanal Anastomosis for Rectal Cancer
TABLE 5. Functional Results of Laparoscopic Coloanal Anastomosis According to Extraction Site (N = 131)
Transanal
Transabdominal
(N = 122)
(N = 98)
P
Transanal Transabdominal
1 (0.8) 42 (34) 18 (15)
0 (0) 42 (43) 21 (21)
1.000 0.201 0.198
9 (7)
11 (11)
0.324
6 (5) 15 (12) 101 (83) 5 (4)
0.056 14 (14) 11 (11) 73 5 (5)
(75) 0.976
Stool frequency, median (range) Stool fragmentation, n (%) Fecal urgency, n (%) Dyschezia, n (%) Feces/flatus discrimination, n (%) Wexner score, median (range) Follow-up, median (range), mo
(N = 73)
(N = 58)
P
3 (1–10) 43 (59) 36 (49) 18 (25) 38 (52) 6 (0–20) 46 (3–137)
3 (2–10) 38 (66) 28 (48) 21 (36) 35 (60) 6 (0–20) 50 (13–107)
0.322 0.439 0.906 0.151 0.343 0.919 0.486
between patients with transanal specimen extraction and those with transabdominal extraction (Table 5). The anal continence score was also similar in both groups: 6 versus 6 (P = 0.92) after a median follow-up of 48 months. Independent predictive factors of fecal incontinence (continence score ≥7) were preoperative radiotherapy and tumor height from the anal verge 4 cm or less. The site of extraction and patient characteristics did not influence continence.
DISCUSSION
FIGURE 2. Overall survival rate according to rectum extraction site. Transabdo. indicates transabdominal.
FIGURE 3. Disease-free survival rate according to rectum extraction site. Transabdo. indicates transabdominal. C 2014 Lippincott Williams & Wilkins
The aim of the study was to demonstrate the safety and the efficacy of the laparoscopic approach for sphincter-preserving surgery in low rectal cancer. First, we observed a low local recurrence rate and a good survival rate in the overall population of patients treated by laparoscopic coloanal anastomosis. Second, we demonstrated no difference of morbidity rate, quality of specimen, positive circumferential resection margin, local recurrence, and survival rate between transanal and transabdominal extraction groups. Finally, gastrointestinal function and anal continence were similar in both groups. Our results therefore suggest that laparoscopic coloanal anastomosis is efficient in low rectal cancer and that removing the rectal specimen through the anus that is, avoiding a minilaparotomy, did not affect long-term oncologic and functional outcome. Some randomized trials6,22,23 have suggested the feasibility of the laparoscopic approach in the treatment of rectal cancer and one6 has demonstrated the efficacy with similar 5 years survival rate between open and laparoscopic surgery. However, the technical problems for ultralow sphincter preservation have never been discussed in these trials. The reason is probably because most patients with rectal cancer of the lower third are treated by abdominoperineal excision.24 Only 2 retrospective series have challenged the issue of laparoscopic sphincter preservation in low rectal cancer.13,14 Marks et al13 reported on 79 patients with T2–T3 rectal tumors at 1.2 cm from the anal ring and treated by laparoscopic coloanal anastomosis after radiochemotherapy. The distal rectum was dissected transanally first and the laparoscopic approach was used for the mesorectal dissection and the colonic mobilization. The specimen was extracted either transabdominally or transanally. Major and minor morbidity rates were 11% and 19%, respectively. A permanent colostomy was required in 10% of the patients for inadequate surgical margin, postoperative complications, or recurrence. After a mean follow-up of 34 months, the local recurrence rate was 2.5% and the distant metastases rate was 10% with an overall survival rate of 97%. Similarly Park et al14 analyzed 130 patients with low rectal cancer at 3.6 cm from the anal verge treated by laparoscopic intersphincteric resection. The laparoscopic approach was carried out first, whereas the perineal approach was used at the end of the procedure for rectal transection and specimen extraction. They reported a shorter bowel recovery and hospital stay, but similar morbidity rate and surgical margin, compared with an open controlled group. After www.annalsofsurgery.com | 141
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Annals of Surgery r Volume 261, Number 1, January 2015
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a median follow-up of 32 months, the local recurrence was 2.6% and the 3-year survival rate was 77%. In both series, the feasibility of the laparoscopic restorative surgery for low rectal cancer is well documented. However, there is no long-term oncologic data and functional outcome that have been reported. Furthermore, the impact of transanal extraction of the specimen has never been evaluated. In the CLASICC UK trial comparing laparoscopic and open surgery for colorectal cancer, a total of 10 patients presented wound/port site recurrence after 5 years of follow-up.6 The risk of wound/port site recurrence was 0.5% in the open group, which was similar to the 0.6% reported in 1711 open colorectal procedures from US trials.25 By contrast, the risk of wound/port site recurrence was 2.4% in the laparoscopic group, which seemed 5 times higher than after open surgery. Moreover, among the 10 patients presenting recurrence, 1 was a true port-site recurrence, whereas 9 were extractionsite recurrence. Thus, the laparoscopic approach may increase the rate of recurrence related to the extraction-site, although this risk decreases with experience and volume. The reasons are not clear and probably multifactorial: direct wound implantation, tumor perforation, excessive tumor manipulation, small incision, large specimen, no wound protector, poor surgical technique, or inadequate surgical experience.26 In our study including 220 laparoscopic coloanal anastomoses for low rectal cancer, we observed 4.5% of local recurrence with zero wound/port site recurrence after a median follow-up of 51 months. Moreover, the 122 patients with transanal specimen extraction, where wound protector were not used, had similar mesorectal grade and outcome than those with conventional transabdominal extraction (Table 4). Our results suggest, first the efficacy of the laparoscopic ultralow sphincter-preserving surgery in low rectal cancer, second the safety of the transanal extraction site. We believe that neoadjuvant radiochemotherapy (downstaging effect), the technique of total mesorectal excision (protector effect of the preserved fascia recti), the full laparoscopic approach (protector against improper tumor handling manipulation), and patient selection for extraction site (transabdominal for obese) have participated to validate our results. The functional outcome of the laparoscopic restorative surgery for low rectal cancer has never been evaluated. We reported, for the first time, a careful long-term gastrointestinal outcome in patients receiving a hand-sewn coloanal anastomosis by using a full laparoscopic approach. The results were obtained by a questionnaire sent to patients free of disease with at least 1 year of follow-up after stoma closure. The median stools frequency per day was 3; and half the number of patients had stool fragmentation and urgency. These results were similar to those of patients treated in the same institution by open surgery.27 More interesting is the fact that patients treated by transanal extraction had the same anal continence score than those treated by transabdominal extraction, suggesting that removing the rectal specimen through the anus is functionally safe. Our conclusion are limited by the fact that the BMI was slightly lower in the transanal group (24.3 vs 25.8; P = 0.01), suggesting that some obese patients probably received transabdominal instead of transanal extraction. Therefore, as we recommend preventing excessive stretching of the anal sphincter during rectal extraction, we also recommend to be cautious when performing transanal extraction in obese patients with wide mesorectal specimen, especially to avoid mesorectal injury and tumor spillage.
CONCLUSIONS We reported long-term outcome in 220 patients operated by laparoscopic coloanal anastomosis for low rectal cancer and observed that pelvic control and survival were not compromised by the association between mini invasive surgery and ultralow sphincter preservation. Moreover, we demonstrated the safety and efficacy of transanal 142 | www.annalsofsurgery.com
extraction of the rectal specimen with similar oncologic and functional outcome than the conventional abdominal extraction. Because of the wound advantages of transanal extraction, in term of abdominal wall preservation, transanal extraction can be recommended in laparoscopic surgical management of low rectal cancer.
REFERENCES 1. Lacy AM, Garcia-Valdecasas JC, Delgado S, et al. Laparoscopy-assisted colectomy versus open colectomy for treatment of non-metastatic colon cancer: a randomised trial. Lancet. 2002;359:2224–2229. 2. Leung KL, Kwok SP, Lam SC, et al. Laparoscopic resection of rectosigmoid carcinoma: prospective randomised trial. Lancet. 2004;363:1187–1192. 3. Clinical Outcomes of Surgical Therapy (COST) Study Group. A comparison of laparoscopically assisted and open colectomy for colon cancer. N Engl J Med. 2004;350:2050–2059. 4. Jayne DG, Guillou PJ, Thorpe H, et al. UK MRC CLASICC Trial Group. Randomized trial of laparoscopic-assisted resection of colorectal carcinoma: 3-year results of the UK MRC CLASICC Trial Group. J Clin Oncol. 2007;25:3061– 3068. 5. The COlon Cancer Laparoscopic or Open Resection Study Group. Survival after laparoscopic surgery versus open surgery for colon cancer: long-term outcome of a randomised clinical trial. Lancet Oncol. 2009;10:44–52. 6. Jahne DG, Thorpe HC, Copeland J, et al. Five-year follow-up of the Medical Research Council CLASICC trial of laparoscopically assisted versus open surgery for colorectal cancer. Br J Surg. 2010;97:1638–1645. 7. Guillou PJ, Quirke P, Thorpe H, et al. Short-term end points of conventional versus laparoscopic-assisted surgery in patients with colorectal cancer (MRC CLASICC trial): multicentre, randomised controlled trial. Lancet. 2005;365:1718–1726. 8. Laurent C, Leblanc F, Gineste C, et al. Laparoscopic approach in surgical treatment of rectal cancer. Br J Surg. 2007;94:1555–1561. 9. Ito M, Sugito M, Kobayashi A, et al. Relationship between multiple numbers of stapler firings during rectal division and anastomotic leakage after laparoscopic rectal resection. Int J Colorectal Dis. 2008;23:703–707. 10. Scheidbach H, Schneider C, Konradt J, et al. Laparoscopic abdominoperineal resection and anterior resection with curative intent for carcinoma of the rectum. Surg Endosc. 2002;16:7–13. 11. Akamatsu H, Omori T, Oyama T, et al. Totally laparoscopic low anterior resection for lower rectal cancer: combination of a new technique for intracorporeal anastomosis with prolapsing technique. Dig Surg. 2009;26:446–450. 12. Fujimoto Y, Akiyoshi T, Kuroyanagi H, et al. Safety and feasibility of laparoscopic intersphincteric resection for very low rectal cancer. J Gastrointest Surg. 2010;14:645–650. 13. Marks J, Mizrahi B, Dalane S, et al. Laparoscopic transanal abdominal transanal resection with sphincter preservation for rectal cancer in the distal 3 cm of the rectum after neoadjuvant therapy. Surg Endosc. 2010;24:2700– 2707. 14. Park JS, Choi G-S, Jun SH, et al. Laparoscopic versus open intersphincteric resection and coloanal anastomosis for low rectal cancer. Ann Surg. 2011;254:941–46. 15. Rullier E, Vendrely V. Can mesorectal lymph nodes excision be avoided in rectal cancer surgery? Colorectal Dis. 2011;13(suppl 7):37–42. 16. Edge SB, Byrd DR, Carducci MA, et al. AJCC Cancer Staging Manual. 7th ed. New York, NY: Springer; 2009. 17. Rullier E, Laurent C, Bretagnol F, et al. Sphincter-saving resection for all rectal carcinomas: the end of the 2-cm distal rule. Ann Surg. 2005;241:465–469. 18. Washington MK, Berlin F, Branton P, et al. Protocol for examination of specimens from patients with primary carcinoma of the colon and rectum. Arch Pathol Lab Med. 2009;133:1539–1551. 19. Quirke P, Steele R, Monson J, et al. Effect of the plane of surgery achieved on local recurrence in patients with operable rectal cancer: a prospective study using data from the MRC CR07 and NCIC-CTG C016 randomised clinical trial. Lancet. 2009;373:821–828. 20. Jorge JM, Wexner SD. Etiology and management of fecal incontinence. Dis Colon Rectum. 1993;36:77–96. 21. Dindo D, Demartines N, Clavien PA. 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. 22. Kang SB, Park JW, Jeong SY, et al. Open versus laparoscopic surgery for mid or low rectal cancer after neoadjuvant chemoradiotherapy (COREAN trial): short-term outcomes of an open-label randomised controlled trial. Lancet Oncol. 2010;11:637–645.
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23. Lujan J, Valero G, Hernandez Q, et al. Randomized clinical trial comparing laparoscopic and open surgery in patients with rectal cancer. Br J Surg. 2009;96:982–989. 24. Ricciardi R, Roberts PL, Read TE, et al. Variability in reconstructive procedures following cancer surgery in the United States. Dis Colon Rectum. 2010;53: 874–880. 25. Reilly WT, Nelson H, Schroeder G, et al. Wound recurrence following conventional treatment of colorectal cancer. A rare but
C 2014 Lippincott Williams & Wilkins
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perhaps underestimated problem. Dis Colon Rectum. 1996;39:200– 207. 26. Seow-Choen F, Wan WH, Tan KY. The use of a wound protector to prevent port site recurrence may not be totally logical. Colorectal Dis. 2009;11: 123–125. 27. Bretagnol F, Rullier E, Laurent C, et al. Comparison of functional results and quality of life between intersphincteric resection and conventional coloanal anastomosis for low rectal cancer. Dis Colon Rectum. 2004;47:832–838.
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