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Asian J Endosc Surg ISSN 1758-5902
R E V I E W A RT I C L E
Laparoscopic surgery for rectal cancer: Current status and future perspective Shigeo Toda & Hiroya Kuroyanagi Department of Gastroenterological Surgery, Toranomon Hospital, Tokyo, Japan
Keywords Laparoscopic surgery; rectal cancer; treatment outcome Correspondence Shigeo Toda, Department of Gastroenterological Surgery, Toranomon Hospital. Toranomon 2-2-2, Minato-ku, Tokyo 105-8470, Japan. Tel: +81 3 3588 1111 Fax: +81 3 3582 7068 Email: [email protected] Received: 13 September 2013; revised 1 October 2013; accepted 4 October 2013 DOI:10.1111/ases.12074
Abstract Although laparoscopic surgery for colon cancer is accepted in the treatment guidelines, the laparoscopic approach for rectal cancer is recommended only in clinical trials. Thus far, several trials have shown favorable short-term results such as early recovery and short hospital stay, but long-term results remain a critical concern for laparoscopic rectal cancer surgery. To date, no randomized control trials have shown an increased local recurrence after laparoscopic surgery for rectal cancer. Additionally, according to previous studies, open conversion, which is more frequent in laparoscopic rectal surgery than in laparoscopic colon surgery, may affect short-term and longterm survival. The evidence on male sexual function has been contradictory. Long-term results from ongoing multicenter trials will be available within several years. Based on accumulated evidence from well-organized clinical trials, laparoscopic surgery will likely be accepted as a treatment choice for rectal cancer. In the future, extended laparoscopic rectal surgery might be feasible for additional procedures such as laparoscopic lateral pelvic lymph node dissection and laparoscopic total pelvic exenteration for rectal cancer invading the adjacent pelvic organ.
Introduction
Data from Major Trials Short-term results
Surgical therapy is essential to treat colorectal cancer, a common malignancy in both Asian and Western countries. Although open surgery is still the standard treatment, laparoscopic surgery has been increasingly performed as a result of improvements in surgical techniques and devices. Laparoscopic surgery for colon cancer is accepted as a treatment option in some treatment guidelines (1,2), as randomized control trials (RCT) and meta-analyses have shown lower morbidity and earlier recovery without impairing long-term cancer control (3–14). In contrast, the laparoscopic approach for rectal cancer is still recommended for use only in clinical trials according to the guidelines due to concerns about long-term cancer control (1,15). Herein, we review the short-term and long-term results from major studies, especially RCT to date, to elucidate the current situation and future perspectives on laparoscopic surgery for rectal cancer.
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Operative time and blood loss Laparoscopic surgery for rectal cancer requires a longer operative time, but it is associated with less blood loss according to previous RCT. The operative time for laparoscopic rectal surgery ranges from 120 to 262 min, which is 14–59 min longer than that for open procedure (Table 1) (4,16–23). Araujo et al. reported a significantly shorter operative time in laparoscopic surgery (16). This result was attributed to the fact that laparoscopic surgery was performed by one surgical team in the study whereas open surgery was performed by several surgical teams. Blood loss in laparoscopic rectal surgery ranges from 20 to 321 mL, which is 17–234 mL less than in open procedure (4,16–23). Because of limited tactile sensations in laparoscopic surgery, maintaining a clear view is extremely important. Surgeons must carefully control all bleeding, which can ruin clear visualization. This is why
Asian J Endosc Surg 7 (2014) 2–10 © 2013 Japan Society for Endoscopic Surgery, Asia Endosurgery Task Force and Wiley Publishing Asia Pty Ltd
Laparoscopic surgery for rectal cancer
S Toda and H Kuroyanagi
Table 1 Operative outcomes of RCT comparing laparoscopic and open rectal surgery Author and Year
Type of study
Patients (n)
Operative time
Blood loss
Araujo et al. (16)
Guillou et al. (4)
Multicenter RCT
Braga et al. (18)
Single-center RCT
Ng et al. (19)
Lujan et al. (21)
Single-center RCT (only APR) Single-center RCT (only AR) Single-center RCT
Kang et al. (22)
Multicenter RCT
van der Pas et al. (23)
Multicenter RCT
L = 13 O = 15 L = 82 O = 89 L = 253 O = 128 L = 83 O = 85 L = 51 O = 48 L = 76 O = 77 L = 101 O = 103 L = 170 O = 170 L = 699 O = 345
L = 228 min O = 284 min* L = 120 min O = 106 min L = 180 min O = 135 min* L = 262 min O = 209 min* L = 213 min O = 163 min* L = 213 min O = 154 min* L = 193 min O = 172 min* L = 244 min O = 197 min* L = 240 min O = 188 min*
NA
Zhou et al. (17)
Single-center RCT (only APR) Single-center RCT
Ng et al. (20)
L = 20 mL O = 92 mL* NA L = 213 mL O = 396 mL* L = 321 mL O = 555 mL L = 280 mL O = 337 mL L = 127 mL O = 234 mL* L = 200 mL O = 217 mL* L = 200 mL O = 400 mL*
Conversion rate 0% NA 34% 7.2% 9.8% 30.3% 7.9% 1.2% 16%
*Significantly different. APR, abdominoperineal resection; AR, anterior resection; L, laparoscopic; NA, not available; O, open; RCT, randomized control trial.
laparoscopic surgery has less blood loss but a longer operative time than open surgery.
Rate of conversion The rate of conversion to open surgery ranges from 0% to 34% (Table 1) (16–23). Conversion is required mainly because of a patient’s anatomy, tumor extension and a surgeon’s experience. Multicenter studies tend to show a higher conversion rate than single-center studies, as there are often differences among the participating centers in terms of surgical experience and the quality of preoperative evaluation for cancer extension. The Medical Research Council Conventional versus LaparoscopicAssisted Surgery in Colorectal Cancer (CLASICC) trial, a multicenter trial in the early laparoscopic era (1996– 2002), had the highest conversion rate (34%) among the RCT comparing laparoscopic surgery and open surgery for rectal cancer. The CLASICC trial had a prerequisite for participating surgeons that required every surgeon to have completed at least prior 20 laparoscopic procedures. The conversion rate gradually decreased year by year during the CLASICC trial (38% in the first year, 16% in sixth year), clearly indicating the existence of a learning curve (4). Park et al. reported on the learning curve for laparoscopic rectal surgery performed by a single surgeon. The experience of a single surgeon was divided into four periods. The conversion rate decreased from 4.3% in the second period to 1.1% in the third period. In this study,
the number of surgeries needed to reduce conversion rate was 146, which was the total number of patients treated in the first and the second periods (24). A recent report from the largest multicenter RCT, the Colorectal Cancer Laparoscopic or Open Resection (COLOR) II trial (2004–2010), showed a lower conversion rate of 16% (23). The COLOR II trial asked surgical teams to submit an unedited video of laparoscopic total mesorectal excision (TME) before participating in the trial. This quality control of surgeons and the more recent study period, during which precise preoperative evaluation for cancer extension was developed and surgical devices and techniques improved, could explain the lower conversion rate. The open versus laparoscopic surgery for mid and low rectal cancer after neoadjuvant chemoradiotherapy (COREAN) trial, another multicenter study, yielded an even lower conversion rate of 1.2%. This trial was undertaken from 2006 to 2009 at three hospitals, each of which treated more than 200 rectal cancer patients annually; the CLASICC trial was undertaken at 27 hospitals and the COLOR II trial at 30 hospitals. The recent study period and the high-quality surgery offered by these three high-volume centers help explain the excellent results in the COREAN trial (22). Poon and Law noted that the definition of conversion varied between trials (25). Conversion is defined as a “vertical abdominal incision greater in size than that needed for specimen retrieval” (4), “requirement of any additional unplanned incision to complete the procedure” (26), “need for conventional midline laparotomy”
Asian J Endosc Surg 7 (2014) 2–10 © 2013 Japan Society for Endoscopic Surgery, Asia Endosurgery Task Force and Wiley Publishing Asia Pty Ltd
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Laparoscopic surgery for rectal cancer
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(27), or “any part of the procedure with an open procedure” (28). The hybrid approach using open technique through a mini-laparotomy for specimen retrieval is not considered a conversion under some of these definitions. Conversion rate cannot be simply compared among the trials because of such differences in definition. Impact of conversion on short-term and long-term results Patients who require conversion are likely to have a higher postoperative morbidity and mortality and worse long-term overall survival than patients who do not (4,8,29). In the CLASICC trial, patients undergoing conversion had a higher morbidity (open vs laparoscopic vs converted group, 37% vs 32% vs 59%; P-value not available) and in-hospital mortality (open vs laparoscopic vs converted group, 5% vs 1% vs 9%; P = 0.34). Furthermore, long-term overall survival of converted patients was significantly lower (open vs laparoscopic vs converted group, 58.5% vs 62.5% vs 49.6%; P = 0.005), while disease-free survival was not significantly different. These results suggest that poor overall survival was attributed not to cancer recurrence but to the higher in-hospital mortality. In the CLASICC study, the overall survival curve for converted patients dropped sharply under the overall survival curve for open and laparoscopic surgery early in the follow-up period, but after the sharp drop, the survival difference appeared almost the same throughout the follow-up period. The survival curve also indicated that the survival difference in the
early follow-up period was caused by the higher in-hospital mortality in the converted group. Thorpe et al. analyzed the data from the CLASICC trial and concluded that high BMI, male gender and peritoneal metastasis were the risk factors for conversion (30). Laurent et al. showed that male gender, stapled anastomosis, and tumor fixity were the independent risk factors for conversion (27). From large multicenter retrospective data in Japan, Yamamoto et al. indicated that the risk factors for conversion were high BMI and low anterior resection (31). Therefore, adequate preoperative evaluation and patient selection based on the experience of the surgical team is essential to minimize the conversion rate. Postoperative morbidity and mortality Postoperative morbidity and mortality were similar between laparoscopic surgery and open surgery. Among several RCT, the morbidity and mortality of laparoscopic rectal surgery ranged from 6.1% to 69% and from 0% to 4%, respectively (Table 2) (4,16–23). However, morbidity differs among trials because of varying definitions of complications. Anastomotic leakage rate The rates of anastomotic leakage were similar between laparoscopic surgery and open surgery. The anastomotic leakage rate in laparoscopic rectal surgery ranged from 1% to 13% (Table 2) (4,16–23). Anastomotic leakage is influenced by various factors, such as low anastomosis, proper transection of the distal rectum, tension to the
Table 2 Postoperative morbidity and mortality of RCT Author
Type of study
Morbidity
Mortality
Anastomotic leakage
Hospital stay
Araujo et al. (16)
NA
Guillou et al. (4)
Multicenter RCT
Braga et al. (18)
Single-center RCT
Ng et al. (19)
Kang et al. (22)
Multicenter RCT
van der Pas et al. (23)
Multicenter RCT
L = 0% O = 0% L = 4% O = 5% L = 1.2% O = 1.2% L = 2.0% O = 2.1% L = 2.6% O = 3.9% L = 1.9% O = 2.9% L = 0% O = 0% L = 1% O = 2%
L = 1.2% O = 3.4% L = 10% O = 7% L = 9.6% O = 10.6% NA
Lujan et al. (21)
Single-center RCT (only APR) Single-center RCT (only AR) Single-center RCT
L = 69% O = 46.7% L = 6.1% O = 12.4%* L = 40% O = 37% L = 28.9% O = 40% L = 45.1% O = 52.1% L = 30.3% O = 31.2% L = 33.0% O = 33.7% L = 21.2% O = 23.5% L = 40% O = 37%
NA
Zhou et al. (17)
Single-center RCT (only APR) Single-center RCT
L = 10.5 days O < 10.5 days L = 8.1 days O = 13.3 days* L = 11 days O = 13 days L = 10 days O = 13.6 days* L = 10.8 days O = 11.5 days L = 8.4 days O = 10.0 days* L = 8.2 days O = 9.9 days L = 8 days O = 9 days L = 8 days O = 9 days*
Ng et al. (20)
L = 1% O = 3% L = 6% O = 12% L = 1.2% O = 0% L = 13% O = 10%
*Significantly different. APR, abdominoperineal resection; AR, anterior resection; L, laparoscopic; NA, not available; O, open; RCT, randomized control trial.
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Asian J Endosc Surg 7 (2014) 2–10 © 2013 Japan Society for Endoscopic Surgery, Asia Endosurgery Task Force and Wiley Publishing Asia Pty Ltd
Laparoscopic surgery for rectal cancer
S Toda and H Kuroyanagi
anastomosis, and blood supply to oral and anal stumps of anastomosis. Particularly in laparoscopic rectal surgery, sufficient rectal mobilization is key to safe anastomosis because it makes rectal transection easy, even in patients undergoing low anastomosis. Multiple firings in distal transection is considered to be potentially hazardous because overlapping or zigzag staple lines may result in incomplete stapling or insufficient blood supply and cause anastomotic leakage. Kuroyanagi et al. reported the standardized technique of laparoscopic rectal transection and double-stapling anastomosis with satisfactory results (2.6% anastomotic leakage, 1.3% rectovaginal fistula). Several practical suggestions were given in this report. A port in the right lower quadrant was placed as low as possible so that an endostapler could be inserted in the port at a right angle toward the long axis of the distal rectum. Rectal mobilization should be distal enough beyond the expected transection line to ensure complete control over the rectal transection. Smooth and coordinated movement between a surgeon and an assistant was essential in transection to complete stapling with two cartridges. The rod of a circular stapler inserted transanally pierced the rectal wall next to the crutch of two staplers (32). Kim et al. analyzed 270 patients who underwent laparoscopic anastomosis by double stapling technique and reported that middle and lower rectal cancer was an independent risk factor for anastomotic leakage (33). Akiyoshi et al. reviewed the data from 363 patients who underwent laparoscopic anterior resection; they concluded that middle and lower rectal cancer and lack of pelvic drain were the independent risk factors for anastomotic leakage (34). Park et al. performed a retrospective analysis of the data from 1609 rectal cancer patients at 11 Korean institutions. Their results showed that male gender, low anastomosis, preoperative chemoradiation, advanced tumor stage, perioperative transfusion, and multiple firings of the stapler increased the risk of anastomotic leakage (35). The results of these large retrospective studies indicate that surgeons should pay special attention during laparoscopic low anterior resection. Postoperative hospital stay The duration of hospital stay after laparoscopic surgery ranges from 8 to 11 days, which is generally 1–2 days shorter than that after open surgery (Table 2) (4,16–23). After laparoscopic rectal surgery, patients tolerate early ambulation, have a bowel movement on postoperative day 3–5, and can resume normal food intake on postoperative day 3–6 (19,26,36–40). These advantages can result in early discharge from the hospital.
Cost of laparoscopic surgery The direct cost of laparoscopic surgery is higher than that of open surgery. The RCT by Ng et al. showed that laparoscopic surgery was $2000 more in direct costs than open surgery (19). Braga et al. performed cost analysis, including postoperative cost and direct cost of surgery. The laparoscopic group was more expensive per patient in terms of surgical instruments ($1194) and longer operative time ($554) (total, $1748), but there were savings as a result of shorter length of hospital stay ($647) and fewer postoperative complications ($749) (total, $1396). Ultimately, it cost $352 more for a patient randomized to laparoscopic surgery (18). Circumferential resection margin (CRM) The incidence of positive CRM was not significantly different between laparoscopic surgery and open surgery (Table 3). However, the CLASSIC trial had a higher incidence of positive CRM in laparoscopic anterior resection group (laparoscopic vs open group, 12% vs 6%; P = 0.19), although it was not significant (4). CRM positivity is known to be a powerful prognostic factor after rectal cancer resection (41–43). Fortunately, there was no significant impairment of local recurrence rate or overall survival at 5 years in the CLASICC trial (8). In the majority of RCT, CRM was considered positive when the distance from the tumor to the resection margin was 1 mm or less (20–22). In the COLOR II trial conducted by van der Pas et al., CRM was defined as positive if the distance was less than 2 mm (23). The study by Nagtegaal et al. showed a significant increase in local recurrence for CRM less than 2 mm compared to CRM 2 mm or more (16% vs. 5.8%; P < 0.0001) (42). The rates of positive CRM in the van der Pas et al. study were 10% in the laparoscopic group and 10% in the open group (P = 0.850), and the positive CRM rate of patients with low rectal cancer was significantly lower in the laparoscopic group than in the open group (9% vs 22%; P = 0.014). Van der Pas et al. speculated that the lower rate of positive CRM after laparoscopic surgery for low rectal cancer could be attributed to improved visualization of the lower pelvis. However, the positive CRM rate of patients with middle rectal cancer was higher in the laparoscopic group than in the open group (10% vs 3%, P = 0.068), although the difference was not significant (23). Long-term outcomes Late morbidity Two single-center RCT reported less late morbidity after laparoscopic surgery than open surgery. Braga et al. reported that late morbidity of the laparoscopic group
Asian J Endosc Surg 7 (2014) 2–10 © 2013 Japan Society for Endoscopic Surgery, Asia Endosurgery Task Force and Wiley Publishing Asia Pty Ltd
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Laparoscopic surgery for rectal cancer
S Toda and H Kuroyanagi
Table 3 Circumferential resection margin positivity and long-term outcomes Author
Type of study
Follow-up period
Positive circumferential resection margin
Araujo et al. (16)
47.2 months
NA
Jayne et al. (8)
Single-center RCT (only APR) Multicenter RCT
56.3 months
Braga et al. (18)
Single-center RCT
53.6 months
Ng et al. (19)
87.2 months
Lujan et al. (21)
Single-center RCT (only APR) Single-center RCT (only AR) Single-center RCT
Kang et al. (22)
Multicenter RCT
NA
van der Pas et al. (23)
Multicenter RCT
NA
L = 16% O = 14% L = 1.2% O = 2.4% L = 5.9% O = 4.2% L = 2.6% O = 1.3% L = 4% O = 2.9% L = 2.9% O = 4.1% L = 10% O = 10%
Ng et al. (20)
112.5 months 32.8 months
Local recurrence
Late morbidity
Overall survival
L = 0% O = 13% L = 9.4% O = 7.6% L = 4% O = 5.2% L = 5% O = 11% L = 7.1% O = 4.9% L = 4.8% O = 5.3% NA
NA
NA
NA
L = 60.3% at 5y O = 52.9% at 5y NA
NA
L = 75.2% at 5y O = 76.5% at 5y L = 63.9% at 10y O = 55.1% at 10y L = 72.1% at 5y O = 75.3% at 5y NA
NA
NA
NA
L = 2.4% O = 10.6% NA L = 10.8% O = 25.7%* NA
*Significantly different. APR, abdominoperineal resection; AR, anterior resection; L, laparoscopic; NA, not available; O, open; RCT, randomized control trial; y, year.
was 2.4% while that of the open group was 10.6% (P = 0.07), and the low late morbidity resulted in cost savings (18). In the study by Ng et al. cumulative probabilities of late morbidity were 13.6% in the laparoscopic group and 25.7% in the open group (P = 0.012) with a long follow-up of 112.5 months. Patients developed adhesion-related bowel obstruction, the most common complication, in the open group more than in the laparoscopic group (19% vs 2.7%) (20).
Bladder and sexual dysfunction
Local recurrence and overall survival To date, there have been no studies that have shown significant deterioration of local recurrence and overall survival after laparoscopic surgery for rectal cancer. Local recurrence and overall survival after laparoscopic surgery at 5 years range from 0% to 9.4% and from 60.3% to 75.2%, respectively (Table 3) (8,16,18–23). In the CLASICC trial, local recurrence and overall survival were similar between the laparoscopic group and the open group, despite the higher positive CRM rate in patients undergoing laparoscopic anterior resection. The rate of local recurrence after anterior resection was 9.4% in the laparoscopic group and 7.6% in the open group (P = 0.74). Overall survival at 5 years was 60.3% in the laparoscopic group and 52.9% in the open group (P = 0.132) (8). Port-site metastasis and wound metastasis The incidences of port-site and wound metastasis were shown to be similar between laparoscopic surgery and open surgery. At the dawn of laparoscopic colorectal
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cancer surgery, port-site metastasis was one of the major concerns about laparoscopic surgery. Recent articles have reported the incidence of port-site metastasis to be 0%–0.69% in laparoscopic surgery (19,44), which is comparable to that of wound recurrence in open surgery (0.6%) (45,46). Port-site metastasis can be prevented by employing standardized cancer surgery, such as the no-touch technique, and routine use of wound protector.
Bladder function after laparoscopic rectal surgery is similar to after open surgery. In contrast, the evidence on male sexual function has been contradictory. Two randomized trials conducted in the early period of laparoscopic era demonstrated more male sexual dysfunction after laparoscopic surgery than after open surgery. However, the rate of bladder dysfunction was not significantly different. In one of the randomized studies, by Quah et al., 111 of the 170 patients (65%) were alive at the time of survey, and 80 of those patients (72%) returned the postal questionnaire on bladder and sexual function. Bladder function was similar after laparoscopic and open rectal operations for rectal cancer. Seven of the 15 sexually active men in the laparoscopic group reported impotence or impaired ejaculation, compared to only 1 of the 22 patients in the open group (P = 0.004). Jayne et al. analyzed the data from 794 patients in the CLASICC trial and, based on additional exclusion criteria for their study on bladder and sexual dysfunction, found that 347 patients (43.7%) were eligible to participate in the study. Of the 347 eligible patients, 247 patients
Asian J Endosc Surg 7 (2014) 2–10 © 2013 Japan Society for Endoscopic Surgery, Asia Endosurgery Task Force and Wiley Publishing Asia Pty Ltd
Laparoscopic surgery for rectal cancer
S Toda and H Kuroyanagi
(71.2%) returned the questionnaire on bladder and sexual function. Overall sexual function and erectile function according to the International Index of Erectile Function tended to be worse in men after laparoscopic rectal surgery than after open rectal surgery (P = 0.063 and P = 0.068, respectively) (47,48). In contrast, recent studies have shown similar or better sexual function in laparoscopic patients, although they were not included in randomized studies. Stamopoulos et al. retrospectively analyzed the data from 56 patients who underwent rectal cancer surgery (38 open, 18 laparoscopic) and concluded that there was no significant difference between the open and laparoscopic groups in International Index of Erectile Function score. The study by Asoglu et al. included 63 patients who underwent rectal cancer surgery (29 open, 34 laparoscopic) for analysis of bladder and sexual function. Sexual dysfunction was observed in 6 of the 17 preoperatively sexually active men after open surgery and in 1 of the 18 men after laparoscopic surgery (P = 0.04); bladder function after laparoscopic surgery was similar to after open surgery. McGrone et al. examined data from 143 patients who underwent rectal surgery (65 open, 78 laparoscopic) and found significant better erectile function after laparoscopic surgery as compared to open surgery (49–51). Despite its technical difficulty, laparoscopic surgery has an advantage in preservation of the autonomic nerves because of the magnified view. One of the reasons for the worse results in the two randomized trials discussed is that a learning curve exists for laparoscopic technique and the recognition of surgical anatomy. The studies by Quah et al. and Jayne et al. received some criticism. Specifically, the number of surviving patients who returned the questionnaire on sexual dysfunction was small, and the techniques and anatomy recognition in laparoscopic rectal surgery were not well established when the trials were undertaken in the early laparoscopic era. The evidence on male sexual function thus remains contradictory. Forthcoming results from RCT are necessary to conclude whether male sexual function after laparoscopic rectal surgery is similar or worse than after open surgery. Learning curve and training surgeons for laparoscopic rectal surgery Park et al. performed an analysis of the learning curve for laparoscopic rectal cancer surgery. The surgical experience of one surgeon was divided into four periods based on the number of operations performed and significant changes in main surgical results. The operative time decreased after 90 operations. The rate of overall anastomotic leakage was 3.7%: 10.3% in the first period; 3.1% in the second period; 1.7% in the third period; and
1.6% in the fourth period. The overall conversion rate was 2.9%: 5.6% in the first period; 4.3% in the second period; 1.1% in the third period; and 1.5% in the fourth period. Anastomotic leakage and conversion rates reached their respective plateaus after 140 surgeries (52). Ogiso et al. reported a training system for laparoscopic low anterior resection for resident surgeons. Before starting laparoscopic rectal surgery, resident surgeons are required to act as an endoscopist in at least 20 surgeries and then perform at least 30 laparoscopic colon surgeries. Ogiso et al. analyzed the short-term outcomes of 137 patients who underwent laparoscopic low anterior resection, of whom 75 had intraperitoneal rectal cancer and 62 had extraperitoneal rectal cancer. Of the 75 patients with intraperitoneal rectal cancer, 40 were operated on by expert surgeons and 35 by resident surgeons. Of the 62 patients with extraperitoneal rectal cancer, 51 were operated on by expert surgeons and 11 by resident surgeons. The operative time for extraperitoneal rectal surgery by resident surgeons was longer than that by expert surgeons. However, the short-term outcomes, including blood loss, anastomotic leakage, conversion to open surgery, and the number of lymph nodes harvested, were similar. Under supervision of expert surgeons, resident surgeons could perform laparoscopic low anterior resection with satisfactory short-term outcomes, which were comparable to those of procedures performed by expert surgeons. Ogiso et al. emphasized the importance of a standardized procedure for maintaining the quality of surgery because the assistant surgeon is always occupied in developing the surgical field and cannot directly help the operating surgeon during surgery. According to this study, the number of surgeries needed to perform appropriate laparoscopic rectal surgery can be reduced with an expert supervision and standardized procedures (53). Future perspectives Ongoing trials Long-term outcomes from three ongoing multicenter trials randomized trials have yet to be released. The trials are the COLOR II trial, the Japan Clinical Oncology Group (JCOG) 0404 trial, and the American College of Surgeons Oncology Group Z6051 trial. Recently, the European COLOR II trial, which compared laparoscopic and open surgery for rectal cancer located within 15 cm of the anal verge, published the short-term outcomes of 1103 enrolled patients. No significant difference was observed in CRM positivity between the laparoscopic and open groups (23). The primary endpoint of this study was the local recurrence rate at 3 years; analysis starts in 2013.
Asian J Endosc Surg 7 (2014) 2–10 © 2013 Japan Society for Endoscopic Surgery, Asia Endosurgery Task Force and Wiley Publishing Asia Pty Ltd
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Laparoscopic surgery for rectal cancer
S Toda and H Kuroyanagi
The JCOG 0404 trial evaluated laparoscopic surgery for colorectal cancer (colon and rectosigmoid cancer except transverse colon cancer) in 1057 patients and found favorable short-term outcomes (less blood loss, shorter hospital stay, less pain, conversion rate of 5.4%) (Nishizawa Y, 2012, unpublished data). The long-term outcomes will be disclosed in 2014. The American College of Surgeons Oncology Group Z6051 trial, which started in 2008, compares laparoscopic and open surgery for rectal cancer within 12 cm of the anal verge. This study will recruit 650 patients. Challenges in laparoscopic rectal cancer surgery Extended laparoscopic rectal surgery, such as laparoscopic lateral pelvic lymph node dissection (LPLD) and laparoscopic total pelvic exenteration for rectal cancer invading the pelvic organ, is feasible. LPLD was established in Japan and is currently performed only in Asian countries. It is not yet accepted in the treatment guidelines because of lack of long-term outcome from randomized trials (1,15). Watanabe et al. reported no significant difference in survival between patients who had neoadjuvant radiotherapy with TME and those undergoing TME plus LPLD (54). Based on the result, there is an opinion that LPLD can be omitted if neoadjuvant radiotherapy is performed. The nationwide, multi-institutional study in Japan by Akiyoshi et al. recently revealed that the prognosis of patients with internal lateral lymph node metastasis does not significantly differ from that of patients with N2a metastasis (according to the American Joint Committee on Cancer staging system). This means that lateral lymph nodes can be considered as regional lymph nodes (55). Kim et al. demonstrated that lateral lymph node metastasis is the most common type of local recurrence after neoadjuvant chemoradiotherapy plus TME alone; it is strongly associated with the preoperative radiographic size of the lateral pelvic lymph node (56). The long-term results from the multicenter randomized trial comparing TME plus LPLD and TME alone for advanced low rectal cancer (JCOG 0212 trial) have yet to be released. One of the problems of TME plus LPLD is an increased amount of blood loss and high morbidity as stated by Fujita et al. (JCOG 0212 trial) (57). Konishi et al. reported the shortterm outcomes and surgical technique of laparoscopic LPLD; the report and accompanying video demonstrated that laparoscopic LPLD is feasible with a small amount of blood loss and low postoperative morbidity (58). Laparoscopy-assisted total pelvic exenteration is technically feasible, although there has been only one reported case until now (59). Our hospital (Toranomon Hospital, Tokyo, Japan) has experienced two cases of laparoscopy-assisted total pelvic exenteration for rectal
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cancer invading the adjacent pelvic organ. This procedure has two technical difficulties: ligation of the periprostatic venous plexus (Santorini’s venous plexus) and urinary diversion. Ligation of the venous plexus has become possible with improved surgical devices such as electric cautery with soft coagulation mode and vessel sealing devices. Urinary diversion is performed using ileal conduit reconstruction through mini-laparotomy.
Conclusion In the near future, laparoscopic surgery will be accepted as the treatment choice for rectal cancer because of its favorable short-term results without deterioration of long-term results. At present, laparoscopic rectal surgery should still be performed only by well-experienced surgeons. However, we expect that laparoscopic rectal surgery will become widespread, in the same manner that TME did.
Acknowledgment The authors have no conflict of interest or financial ties to disclose.
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8. Jayne 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. 9. Abraham NS, Byrne CM, Young JM et al. Meta-analysis of non-randomized comparative studies of the short-term outcomes of laparoscopic resection for colorectal cancer. ANZ J Surg 2007; 77: 508–516. 10. Abraham NS, Young JM, Solomon MJ. Meta-analysis of short-term outcomes after laparoscopic resection for colorectal cancer. Br J Surg 2004; 91: 1111–1124. 11. Chapman AE, Levitt MD, Hewett P et al. Laparoscopicassisted resection of colorectal malignancies: A systematic review. Ann Surg 2001; 234: 590–606. 12. Kuhry E, Schwenk WF, Gaupset R et al. Long-term results of laparoscopic colorectal cancer resection. Cochrane Database Syst Rev 2008; 2 CD003432. 13. Reza MM, Blasco JA, Andradas E et al. Systematic review of laparoscopic versus open surgery for colorectal cancer. Br J Surg 2006; 93: 921–928. 14. Schwenk W, Haase O, Neudecker J et al. Short term benefits for laparoscopic colorectal resection. Cochrane Database Syst Rev 2005; 3 CD003145. 15. Benson AB, 3rd, Bekaii-Saab T, Chan E et al. Rectal cancer. J Natl Compr Canc Netw 2012; 10: 1528–1564. 16. Araujo SE, Sousa AH, Jr, de Campos FG et al. Conventional approach x laparoscopic abdominoperineal resection for rectal cancer treatment after neoadjuvant chemoradiation: Results of a prospective randomized trial. Rev Hosp Clin Fac Med Sao Paulo 2003; 58: 133–140. 17. Zhou ZG, Hu M, Li Y et al. Laparoscopic versus open total mesorectal excision with anal sphincter preservation for low rectal cancer. Surg Endosc 2004; 18: 1211–1215. 18. Braga M, Frasson M, Vignali A et al. Laparoscopic resection in rectal cancer patients: Outcome and cost-benefit analysis. Dis Colon Rectum 2007; 50: 464–471. 19. Ng SS, Leung KL, Lee JF et al. Laparoscopic-assisted versus open abdominoperineal resection for low rectal cancer: A prospective randomized trial. Ann Surg Oncol 2008; 15: 2418–2425. 20. Ng SS, Leung KL, Lee JF et al. Long-term morbidity and oncologic outcomes of laparoscopic-assisted anterior resection for upper rectal cancer: Ten-year results of a prospective, randomized trial. Dis Colon Rectum 2009; 52: 558–566. 21. 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. 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. 23. van der Pas MH, Haglind E, Cuesta MA et al. Laparoscopic versus open surgery for rectal cancer (COLOR II): Short-
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39. Ng SS, Leung KL, Lee JF et al. MRC CLASICC trial. Lancet 2005; 366: 713–714. 40. Pugliese R, Di Lernia S, Sansonna F et al. Laparoscopic resection for rectal adenocarcinoma. Eur J Surg Oncol 2009; 35: 497–503. 41. 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 CO16 randomised clinical trial. Lancet 2009; 373: 821–828. 42. Nagtegaal ID, Marijnen CA, Kranenbarg EK et al. 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 2002; 26: 350–357. 43. Nagtegaal ID & Quirke P. What is the role for the circumferential margin in the modern treatment of rectal cancer? J Clin Oncol 2008; 26: 303–312. 44. Strohlein MA, Grutzner KU, Jauch KW et al. Comparison of laparoscopic vs. open access surgery in patients with rectal cancer: A prospective analysis. Dis Colon Rectum 2008; 51: 385–391. 45. Hughes ES, McDermott FT, Polglase AL et al. Tumor recurrence in the abdominal wall scar tissue after large-bowel cancer surgery. Dis Colon Rectum 1983; 26: 571–572. 46. Reilly WT, Nelson H, Schroeder G et al. Wound recurrence following conventional treatment of colorectal cancer. A rare but perhaps underestimated problem. Dis Colon Rectum 1996; 39: 200–207. 47. Quah HM, Jayne DG, Eu KW et al. Bladder and sexual dysfunction following laparoscopically assisted and conventional open mesorectal resection for cancer. Br J Surg 2002; 89: 1551–1556. 48. Jayne DG, Brown JM, Thorpe H et al. Bladder and sexual function following resection for rectal cancer in a randomized clinical trial of laparoscopic versus open technique. Br J Surg 2005; 92: 1124–1132. 49. Stamopoulos P, Theodoropoulos GE, Papailiou J et al. Prospective evaluation of sexual function after open and laparoscopic surgery for rectal cancer. Surg Endosc 2009; 23: 2665–2674.
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50. Asoglu O, Matlim T, Karanlik H et al. Impact of laparoscopic surgery on bladder and sexual function after total mesorectal excision for rectal cancer. Surg Endosc 2009; 23: 296–303. 51. McGlone ER, Khan O, Flashman K et al. Urogenital function following laparoscopic and open rectal cancer resection: A comparative study. Surg Endosc 2012; 26: 2559–2565. 52. Park IJ, Choi GS, Lim KH et al. Multidimensional analysis of the learning curve for laparoscopic resection in rectal cancer. J Gastrointest Surg 2009; 13: 275–281. 53. Ogiso S, Yamaguchi T, Hata H et al. Introduction of laparoscopic low anterior resection for rectal cancer early during residency: A single institutional study on short-term outcomes. Surg Endosc 2010; 24: 2822–2829. 54. Watanabe T, Tsurita G, Muto T et al. Extended lymphadenectomy and preoperative radiotherapy for lower rectal cancers. Surgery 2002; 132: 27–33. 55. Akiyoshi T, Watanabe T, Miyata S et al. Results of a Japanese nationwide multi-institutional study on lateral pelvic lymph node metastasis in low rectal cancer: Is it regional or distant disease. Ann Surg 2012; 255: 1129–1134. 56. Kim TH, Jeong SY, Choi DH et al. Lateral lymph node metastasis is a major cause of locoregional recurrence in rectal cancer treated with preoperative chemoradiotherapy and curative resection. Ann Surg Oncol 2008; 15: 729–737. 57. Fujita S, Akasu T, Mizusawa J et al. Postoperative morbidity and mortality after mesorectal excision with and without lateral lymph node dissection for clinical stage II or stage III lower rectal cancer (JCOG0212): results from a multicentre, randomised controlled, non-inferiority trial. Lancet Oncol 2012; 13: 616–621. 58. Konishi T, Kuroyanagi H, Oya M et al. Multimedia article. Lateral lymph node dissection with preoperative chemoradiation for locally advanced lower rectal cancer through a laparoscopic approach. Surg Endosc 2011; 25: 2358–2359. 59. Patel H, Joseph JV, Amodeo A et al. Laparoscopic salvage total pelvic exenteration: Is it possible post-chemoradiotherapy. J Minim Access Surg 2009; 5: 111–114.
Asian J Endosc Surg 7 (2014) 2–10 © 2013 Japan Society for Endoscopic Surgery, Asia Endosurgery Task Force and Wiley Publishing Asia Pty Ltd
Asian J Endosc Surg ISSN 1758-5902
R E V I E W A RT I C L E
Laparoscopic surgery for rectal cancer: Current status and future perspective Shigeo Toda & Hiroya Kuroyanagi Department of Gastroenterological Surgery, Toranomon Hospital, Tokyo, Japan
Keywords Laparoscopic surgery; rectal cancer; treatment outcome Correspondence Shigeo Toda, Department of Gastroenterological Surgery, Toranomon Hospital. Toranomon 2-2-2, Minato-ku, Tokyo 105-8470, Japan. Tel: +81 3 3588 1111 Fax: +81 3 3582 7068 Email: [email protected] Received: 13 September 2013; revised 1 October 2013; accepted 4 October 2013 DOI:10.1111/ases.12074
Abstract Although laparoscopic surgery for colon cancer is accepted in the treatment guidelines, the laparoscopic approach for rectal cancer is recommended only in clinical trials. Thus far, several trials have shown favorable short-term results such as early recovery and short hospital stay, but long-term results remain a critical concern for laparoscopic rectal cancer surgery. To date, no randomized control trials have shown an increased local recurrence after laparoscopic surgery for rectal cancer. Additionally, according to previous studies, open conversion, which is more frequent in laparoscopic rectal surgery than in laparoscopic colon surgery, may affect short-term and longterm survival. The evidence on male sexual function has been contradictory. Long-term results from ongoing multicenter trials will be available within several years. Based on accumulated evidence from well-organized clinical trials, laparoscopic surgery will likely be accepted as a treatment choice for rectal cancer. In the future, extended laparoscopic rectal surgery might be feasible for additional procedures such as laparoscopic lateral pelvic lymph node dissection and laparoscopic total pelvic exenteration for rectal cancer invading the adjacent pelvic organ.
Introduction
Data from Major Trials Short-term results
Surgical therapy is essential to treat colorectal cancer, a common malignancy in both Asian and Western countries. Although open surgery is still the standard treatment, laparoscopic surgery has been increasingly performed as a result of improvements in surgical techniques and devices. Laparoscopic surgery for colon cancer is accepted as a treatment option in some treatment guidelines (1,2), as randomized control trials (RCT) and meta-analyses have shown lower morbidity and earlier recovery without impairing long-term cancer control (3–14). In contrast, the laparoscopic approach for rectal cancer is still recommended for use only in clinical trials according to the guidelines due to concerns about long-term cancer control (1,15). Herein, we review the short-term and long-term results from major studies, especially RCT to date, to elucidate the current situation and future perspectives on laparoscopic surgery for rectal cancer.
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Operative time and blood loss Laparoscopic surgery for rectal cancer requires a longer operative time, but it is associated with less blood loss according to previous RCT. The operative time for laparoscopic rectal surgery ranges from 120 to 262 min, which is 14–59 min longer than that for open procedure (Table 1) (4,16–23). Araujo et al. reported a significantly shorter operative time in laparoscopic surgery (16). This result was attributed to the fact that laparoscopic surgery was performed by one surgical team in the study whereas open surgery was performed by several surgical teams. Blood loss in laparoscopic rectal surgery ranges from 20 to 321 mL, which is 17–234 mL less than in open procedure (4,16–23). Because of limited tactile sensations in laparoscopic surgery, maintaining a clear view is extremely important. Surgeons must carefully control all bleeding, which can ruin clear visualization. This is why
Asian J Endosc Surg 7 (2014) 2–10 © 2013 Japan Society for Endoscopic Surgery, Asia Endosurgery Task Force and Wiley Publishing Asia Pty Ltd
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Table 1 Operative outcomes of RCT comparing laparoscopic and open rectal surgery Author and Year
Type of study
Patients (n)
Operative time
Blood loss
Araujo et al. (16)
Guillou et al. (4)
Multicenter RCT
Braga et al. (18)
Single-center RCT
Ng et al. (19)
Lujan et al. (21)
Single-center RCT (only APR) Single-center RCT (only AR) Single-center RCT
Kang et al. (22)
Multicenter RCT
van der Pas et al. (23)
Multicenter RCT
L = 13 O = 15 L = 82 O = 89 L = 253 O = 128 L = 83 O = 85 L = 51 O = 48 L = 76 O = 77 L = 101 O = 103 L = 170 O = 170 L = 699 O = 345
L = 228 min O = 284 min* L = 120 min O = 106 min L = 180 min O = 135 min* L = 262 min O = 209 min* L = 213 min O = 163 min* L = 213 min O = 154 min* L = 193 min O = 172 min* L = 244 min O = 197 min* L = 240 min O = 188 min*
NA
Zhou et al. (17)
Single-center RCT (only APR) Single-center RCT
Ng et al. (20)
L = 20 mL O = 92 mL* NA L = 213 mL O = 396 mL* L = 321 mL O = 555 mL L = 280 mL O = 337 mL L = 127 mL O = 234 mL* L = 200 mL O = 217 mL* L = 200 mL O = 400 mL*
Conversion rate 0% NA 34% 7.2% 9.8% 30.3% 7.9% 1.2% 16%
*Significantly different. APR, abdominoperineal resection; AR, anterior resection; L, laparoscopic; NA, not available; O, open; RCT, randomized control trial.
laparoscopic surgery has less blood loss but a longer operative time than open surgery.
Rate of conversion The rate of conversion to open surgery ranges from 0% to 34% (Table 1) (16–23). Conversion is required mainly because of a patient’s anatomy, tumor extension and a surgeon’s experience. Multicenter studies tend to show a higher conversion rate than single-center studies, as there are often differences among the participating centers in terms of surgical experience and the quality of preoperative evaluation for cancer extension. The Medical Research Council Conventional versus LaparoscopicAssisted Surgery in Colorectal Cancer (CLASICC) trial, a multicenter trial in the early laparoscopic era (1996– 2002), had the highest conversion rate (34%) among the RCT comparing laparoscopic surgery and open surgery for rectal cancer. The CLASICC trial had a prerequisite for participating surgeons that required every surgeon to have completed at least prior 20 laparoscopic procedures. The conversion rate gradually decreased year by year during the CLASICC trial (38% in the first year, 16% in sixth year), clearly indicating the existence of a learning curve (4). Park et al. reported on the learning curve for laparoscopic rectal surgery performed by a single surgeon. The experience of a single surgeon was divided into four periods. The conversion rate decreased from 4.3% in the second period to 1.1% in the third period. In this study,
the number of surgeries needed to reduce conversion rate was 146, which was the total number of patients treated in the first and the second periods (24). A recent report from the largest multicenter RCT, the Colorectal Cancer Laparoscopic or Open Resection (COLOR) II trial (2004–2010), showed a lower conversion rate of 16% (23). The COLOR II trial asked surgical teams to submit an unedited video of laparoscopic total mesorectal excision (TME) before participating in the trial. This quality control of surgeons and the more recent study period, during which precise preoperative evaluation for cancer extension was developed and surgical devices and techniques improved, could explain the lower conversion rate. The open versus laparoscopic surgery for mid and low rectal cancer after neoadjuvant chemoradiotherapy (COREAN) trial, another multicenter study, yielded an even lower conversion rate of 1.2%. This trial was undertaken from 2006 to 2009 at three hospitals, each of which treated more than 200 rectal cancer patients annually; the CLASICC trial was undertaken at 27 hospitals and the COLOR II trial at 30 hospitals. The recent study period and the high-quality surgery offered by these three high-volume centers help explain the excellent results in the COREAN trial (22). Poon and Law noted that the definition of conversion varied between trials (25). Conversion is defined as a “vertical abdominal incision greater in size than that needed for specimen retrieval” (4), “requirement of any additional unplanned incision to complete the procedure” (26), “need for conventional midline laparotomy”
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(27), or “any part of the procedure with an open procedure” (28). The hybrid approach using open technique through a mini-laparotomy for specimen retrieval is not considered a conversion under some of these definitions. Conversion rate cannot be simply compared among the trials because of such differences in definition. Impact of conversion on short-term and long-term results Patients who require conversion are likely to have a higher postoperative morbidity and mortality and worse long-term overall survival than patients who do not (4,8,29). In the CLASICC trial, patients undergoing conversion had a higher morbidity (open vs laparoscopic vs converted group, 37% vs 32% vs 59%; P-value not available) and in-hospital mortality (open vs laparoscopic vs converted group, 5% vs 1% vs 9%; P = 0.34). Furthermore, long-term overall survival of converted patients was significantly lower (open vs laparoscopic vs converted group, 58.5% vs 62.5% vs 49.6%; P = 0.005), while disease-free survival was not significantly different. These results suggest that poor overall survival was attributed not to cancer recurrence but to the higher in-hospital mortality. In the CLASICC study, the overall survival curve for converted patients dropped sharply under the overall survival curve for open and laparoscopic surgery early in the follow-up period, but after the sharp drop, the survival difference appeared almost the same throughout the follow-up period. The survival curve also indicated that the survival difference in the
early follow-up period was caused by the higher in-hospital mortality in the converted group. Thorpe et al. analyzed the data from the CLASICC trial and concluded that high BMI, male gender and peritoneal metastasis were the risk factors for conversion (30). Laurent et al. showed that male gender, stapled anastomosis, and tumor fixity were the independent risk factors for conversion (27). From large multicenter retrospective data in Japan, Yamamoto et al. indicated that the risk factors for conversion were high BMI and low anterior resection (31). Therefore, adequate preoperative evaluation and patient selection based on the experience of the surgical team is essential to minimize the conversion rate. Postoperative morbidity and mortality Postoperative morbidity and mortality were similar between laparoscopic surgery and open surgery. Among several RCT, the morbidity and mortality of laparoscopic rectal surgery ranged from 6.1% to 69% and from 0% to 4%, respectively (Table 2) (4,16–23). However, morbidity differs among trials because of varying definitions of complications. Anastomotic leakage rate The rates of anastomotic leakage were similar between laparoscopic surgery and open surgery. The anastomotic leakage rate in laparoscopic rectal surgery ranged from 1% to 13% (Table 2) (4,16–23). Anastomotic leakage is influenced by various factors, such as low anastomosis, proper transection of the distal rectum, tension to the
Table 2 Postoperative morbidity and mortality of RCT Author
Type of study
Morbidity
Mortality
Anastomotic leakage
Hospital stay
Araujo et al. (16)
NA
Guillou et al. (4)
Multicenter RCT
Braga et al. (18)
Single-center RCT
Ng et al. (19)
Kang et al. (22)
Multicenter RCT
van der Pas et al. (23)
Multicenter RCT
L = 0% O = 0% L = 4% O = 5% L = 1.2% O = 1.2% L = 2.0% O = 2.1% L = 2.6% O = 3.9% L = 1.9% O = 2.9% L = 0% O = 0% L = 1% O = 2%
L = 1.2% O = 3.4% L = 10% O = 7% L = 9.6% O = 10.6% NA
Lujan et al. (21)
Single-center RCT (only APR) Single-center RCT (only AR) Single-center RCT
L = 69% O = 46.7% L = 6.1% O = 12.4%* L = 40% O = 37% L = 28.9% O = 40% L = 45.1% O = 52.1% L = 30.3% O = 31.2% L = 33.0% O = 33.7% L = 21.2% O = 23.5% L = 40% O = 37%
NA
Zhou et al. (17)
Single-center RCT (only APR) Single-center RCT
L = 10.5 days O < 10.5 days L = 8.1 days O = 13.3 days* L = 11 days O = 13 days L = 10 days O = 13.6 days* L = 10.8 days O = 11.5 days L = 8.4 days O = 10.0 days* L = 8.2 days O = 9.9 days L = 8 days O = 9 days L = 8 days O = 9 days*
Ng et al. (20)
L = 1% O = 3% L = 6% O = 12% L = 1.2% O = 0% L = 13% O = 10%
*Significantly different. APR, abdominoperineal resection; AR, anterior resection; L, laparoscopic; NA, not available; O, open; RCT, randomized control trial.
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anastomosis, and blood supply to oral and anal stumps of anastomosis. Particularly in laparoscopic rectal surgery, sufficient rectal mobilization is key to safe anastomosis because it makes rectal transection easy, even in patients undergoing low anastomosis. Multiple firings in distal transection is considered to be potentially hazardous because overlapping or zigzag staple lines may result in incomplete stapling or insufficient blood supply and cause anastomotic leakage. Kuroyanagi et al. reported the standardized technique of laparoscopic rectal transection and double-stapling anastomosis with satisfactory results (2.6% anastomotic leakage, 1.3% rectovaginal fistula). Several practical suggestions were given in this report. A port in the right lower quadrant was placed as low as possible so that an endostapler could be inserted in the port at a right angle toward the long axis of the distal rectum. Rectal mobilization should be distal enough beyond the expected transection line to ensure complete control over the rectal transection. Smooth and coordinated movement between a surgeon and an assistant was essential in transection to complete stapling with two cartridges. The rod of a circular stapler inserted transanally pierced the rectal wall next to the crutch of two staplers (32). Kim et al. analyzed 270 patients who underwent laparoscopic anastomosis by double stapling technique and reported that middle and lower rectal cancer was an independent risk factor for anastomotic leakage (33). Akiyoshi et al. reviewed the data from 363 patients who underwent laparoscopic anterior resection; they concluded that middle and lower rectal cancer and lack of pelvic drain were the independent risk factors for anastomotic leakage (34). Park et al. performed a retrospective analysis of the data from 1609 rectal cancer patients at 11 Korean institutions. Their results showed that male gender, low anastomosis, preoperative chemoradiation, advanced tumor stage, perioperative transfusion, and multiple firings of the stapler increased the risk of anastomotic leakage (35). The results of these large retrospective studies indicate that surgeons should pay special attention during laparoscopic low anterior resection. Postoperative hospital stay The duration of hospital stay after laparoscopic surgery ranges from 8 to 11 days, which is generally 1–2 days shorter than that after open surgery (Table 2) (4,16–23). After laparoscopic rectal surgery, patients tolerate early ambulation, have a bowel movement on postoperative day 3–5, and can resume normal food intake on postoperative day 3–6 (19,26,36–40). These advantages can result in early discharge from the hospital.
Cost of laparoscopic surgery The direct cost of laparoscopic surgery is higher than that of open surgery. The RCT by Ng et al. showed that laparoscopic surgery was $2000 more in direct costs than open surgery (19). Braga et al. performed cost analysis, including postoperative cost and direct cost of surgery. The laparoscopic group was more expensive per patient in terms of surgical instruments ($1194) and longer operative time ($554) (total, $1748), but there were savings as a result of shorter length of hospital stay ($647) and fewer postoperative complications ($749) (total, $1396). Ultimately, it cost $352 more for a patient randomized to laparoscopic surgery (18). Circumferential resection margin (CRM) The incidence of positive CRM was not significantly different between laparoscopic surgery and open surgery (Table 3). However, the CLASSIC trial had a higher incidence of positive CRM in laparoscopic anterior resection group (laparoscopic vs open group, 12% vs 6%; P = 0.19), although it was not significant (4). CRM positivity is known to be a powerful prognostic factor after rectal cancer resection (41–43). Fortunately, there was no significant impairment of local recurrence rate or overall survival at 5 years in the CLASICC trial (8). In the majority of RCT, CRM was considered positive when the distance from the tumor to the resection margin was 1 mm or less (20–22). In the COLOR II trial conducted by van der Pas et al., CRM was defined as positive if the distance was less than 2 mm (23). The study by Nagtegaal et al. showed a significant increase in local recurrence for CRM less than 2 mm compared to CRM 2 mm or more (16% vs. 5.8%; P < 0.0001) (42). The rates of positive CRM in the van der Pas et al. study were 10% in the laparoscopic group and 10% in the open group (P = 0.850), and the positive CRM rate of patients with low rectal cancer was significantly lower in the laparoscopic group than in the open group (9% vs 22%; P = 0.014). Van der Pas et al. speculated that the lower rate of positive CRM after laparoscopic surgery for low rectal cancer could be attributed to improved visualization of the lower pelvis. However, the positive CRM rate of patients with middle rectal cancer was higher in the laparoscopic group than in the open group (10% vs 3%, P = 0.068), although the difference was not significant (23). Long-term outcomes Late morbidity Two single-center RCT reported less late morbidity after laparoscopic surgery than open surgery. Braga et al. reported that late morbidity of the laparoscopic group
Asian J Endosc Surg 7 (2014) 2–10 © 2013 Japan Society for Endoscopic Surgery, Asia Endosurgery Task Force and Wiley Publishing Asia Pty Ltd
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Table 3 Circumferential resection margin positivity and long-term outcomes Author
Type of study
Follow-up period
Positive circumferential resection margin
Araujo et al. (16)
47.2 months
NA
Jayne et al. (8)
Single-center RCT (only APR) Multicenter RCT
56.3 months
Braga et al. (18)
Single-center RCT
53.6 months
Ng et al. (19)
87.2 months
Lujan et al. (21)
Single-center RCT (only APR) Single-center RCT (only AR) Single-center RCT
Kang et al. (22)
Multicenter RCT
NA
van der Pas et al. (23)
Multicenter RCT
NA
L = 16% O = 14% L = 1.2% O = 2.4% L = 5.9% O = 4.2% L = 2.6% O = 1.3% L = 4% O = 2.9% L = 2.9% O = 4.1% L = 10% O = 10%
Ng et al. (20)
112.5 months 32.8 months
Local recurrence
Late morbidity
Overall survival
L = 0% O = 13% L = 9.4% O = 7.6% L = 4% O = 5.2% L = 5% O = 11% L = 7.1% O = 4.9% L = 4.8% O = 5.3% NA
NA
NA
NA
L = 60.3% at 5y O = 52.9% at 5y NA
NA
L = 75.2% at 5y O = 76.5% at 5y L = 63.9% at 10y O = 55.1% at 10y L = 72.1% at 5y O = 75.3% at 5y NA
NA
NA
NA
L = 2.4% O = 10.6% NA L = 10.8% O = 25.7%* NA
*Significantly different. APR, abdominoperineal resection; AR, anterior resection; L, laparoscopic; NA, not available; O, open; RCT, randomized control trial; y, year.
was 2.4% while that of the open group was 10.6% (P = 0.07), and the low late morbidity resulted in cost savings (18). In the study by Ng et al. cumulative probabilities of late morbidity were 13.6% in the laparoscopic group and 25.7% in the open group (P = 0.012) with a long follow-up of 112.5 months. Patients developed adhesion-related bowel obstruction, the most common complication, in the open group more than in the laparoscopic group (19% vs 2.7%) (20).
Bladder and sexual dysfunction
Local recurrence and overall survival To date, there have been no studies that have shown significant deterioration of local recurrence and overall survival after laparoscopic surgery for rectal cancer. Local recurrence and overall survival after laparoscopic surgery at 5 years range from 0% to 9.4% and from 60.3% to 75.2%, respectively (Table 3) (8,16,18–23). In the CLASICC trial, local recurrence and overall survival were similar between the laparoscopic group and the open group, despite the higher positive CRM rate in patients undergoing laparoscopic anterior resection. The rate of local recurrence after anterior resection was 9.4% in the laparoscopic group and 7.6% in the open group (P = 0.74). Overall survival at 5 years was 60.3% in the laparoscopic group and 52.9% in the open group (P = 0.132) (8). Port-site metastasis and wound metastasis The incidences of port-site and wound metastasis were shown to be similar between laparoscopic surgery and open surgery. At the dawn of laparoscopic colorectal
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cancer surgery, port-site metastasis was one of the major concerns about laparoscopic surgery. Recent articles have reported the incidence of port-site metastasis to be 0%–0.69% in laparoscopic surgery (19,44), which is comparable to that of wound recurrence in open surgery (0.6%) (45,46). Port-site metastasis can be prevented by employing standardized cancer surgery, such as the no-touch technique, and routine use of wound protector.
Bladder function after laparoscopic rectal surgery is similar to after open surgery. In contrast, the evidence on male sexual function has been contradictory. Two randomized trials conducted in the early period of laparoscopic era demonstrated more male sexual dysfunction after laparoscopic surgery than after open surgery. However, the rate of bladder dysfunction was not significantly different. In one of the randomized studies, by Quah et al., 111 of the 170 patients (65%) were alive at the time of survey, and 80 of those patients (72%) returned the postal questionnaire on bladder and sexual function. Bladder function was similar after laparoscopic and open rectal operations for rectal cancer. Seven of the 15 sexually active men in the laparoscopic group reported impotence or impaired ejaculation, compared to only 1 of the 22 patients in the open group (P = 0.004). Jayne et al. analyzed the data from 794 patients in the CLASICC trial and, based on additional exclusion criteria for their study on bladder and sexual dysfunction, found that 347 patients (43.7%) were eligible to participate in the study. Of the 347 eligible patients, 247 patients
Asian J Endosc Surg 7 (2014) 2–10 © 2013 Japan Society for Endoscopic Surgery, Asia Endosurgery Task Force and Wiley Publishing Asia Pty Ltd
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(71.2%) returned the questionnaire on bladder and sexual function. Overall sexual function and erectile function according to the International Index of Erectile Function tended to be worse in men after laparoscopic rectal surgery than after open rectal surgery (P = 0.063 and P = 0.068, respectively) (47,48). In contrast, recent studies have shown similar or better sexual function in laparoscopic patients, although they were not included in randomized studies. Stamopoulos et al. retrospectively analyzed the data from 56 patients who underwent rectal cancer surgery (38 open, 18 laparoscopic) and concluded that there was no significant difference between the open and laparoscopic groups in International Index of Erectile Function score. The study by Asoglu et al. included 63 patients who underwent rectal cancer surgery (29 open, 34 laparoscopic) for analysis of bladder and sexual function. Sexual dysfunction was observed in 6 of the 17 preoperatively sexually active men after open surgery and in 1 of the 18 men after laparoscopic surgery (P = 0.04); bladder function after laparoscopic surgery was similar to after open surgery. McGrone et al. examined data from 143 patients who underwent rectal surgery (65 open, 78 laparoscopic) and found significant better erectile function after laparoscopic surgery as compared to open surgery (49–51). Despite its technical difficulty, laparoscopic surgery has an advantage in preservation of the autonomic nerves because of the magnified view. One of the reasons for the worse results in the two randomized trials discussed is that a learning curve exists for laparoscopic technique and the recognition of surgical anatomy. The studies by Quah et al. and Jayne et al. received some criticism. Specifically, the number of surviving patients who returned the questionnaire on sexual dysfunction was small, and the techniques and anatomy recognition in laparoscopic rectal surgery were not well established when the trials were undertaken in the early laparoscopic era. The evidence on male sexual function thus remains contradictory. Forthcoming results from RCT are necessary to conclude whether male sexual function after laparoscopic rectal surgery is similar or worse than after open surgery. Learning curve and training surgeons for laparoscopic rectal surgery Park et al. performed an analysis of the learning curve for laparoscopic rectal cancer surgery. The surgical experience of one surgeon was divided into four periods based on the number of operations performed and significant changes in main surgical results. The operative time decreased after 90 operations. The rate of overall anastomotic leakage was 3.7%: 10.3% in the first period; 3.1% in the second period; 1.7% in the third period; and
1.6% in the fourth period. The overall conversion rate was 2.9%: 5.6% in the first period; 4.3% in the second period; 1.1% in the third period; and 1.5% in the fourth period. Anastomotic leakage and conversion rates reached their respective plateaus after 140 surgeries (52). Ogiso et al. reported a training system for laparoscopic low anterior resection for resident surgeons. Before starting laparoscopic rectal surgery, resident surgeons are required to act as an endoscopist in at least 20 surgeries and then perform at least 30 laparoscopic colon surgeries. Ogiso et al. analyzed the short-term outcomes of 137 patients who underwent laparoscopic low anterior resection, of whom 75 had intraperitoneal rectal cancer and 62 had extraperitoneal rectal cancer. Of the 75 patients with intraperitoneal rectal cancer, 40 were operated on by expert surgeons and 35 by resident surgeons. Of the 62 patients with extraperitoneal rectal cancer, 51 were operated on by expert surgeons and 11 by resident surgeons. The operative time for extraperitoneal rectal surgery by resident surgeons was longer than that by expert surgeons. However, the short-term outcomes, including blood loss, anastomotic leakage, conversion to open surgery, and the number of lymph nodes harvested, were similar. Under supervision of expert surgeons, resident surgeons could perform laparoscopic low anterior resection with satisfactory short-term outcomes, which were comparable to those of procedures performed by expert surgeons. Ogiso et al. emphasized the importance of a standardized procedure for maintaining the quality of surgery because the assistant surgeon is always occupied in developing the surgical field and cannot directly help the operating surgeon during surgery. According to this study, the number of surgeries needed to perform appropriate laparoscopic rectal surgery can be reduced with an expert supervision and standardized procedures (53). Future perspectives Ongoing trials Long-term outcomes from three ongoing multicenter trials randomized trials have yet to be released. The trials are the COLOR II trial, the Japan Clinical Oncology Group (JCOG) 0404 trial, and the American College of Surgeons Oncology Group Z6051 trial. Recently, the European COLOR II trial, which compared laparoscopic and open surgery for rectal cancer located within 15 cm of the anal verge, published the short-term outcomes of 1103 enrolled patients. No significant difference was observed in CRM positivity between the laparoscopic and open groups (23). The primary endpoint of this study was the local recurrence rate at 3 years; analysis starts in 2013.
Asian J Endosc Surg 7 (2014) 2–10 © 2013 Japan Society for Endoscopic Surgery, Asia Endosurgery Task Force and Wiley Publishing Asia Pty Ltd
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The JCOG 0404 trial evaluated laparoscopic surgery for colorectal cancer (colon and rectosigmoid cancer except transverse colon cancer) in 1057 patients and found favorable short-term outcomes (less blood loss, shorter hospital stay, less pain, conversion rate of 5.4%) (Nishizawa Y, 2012, unpublished data). The long-term outcomes will be disclosed in 2014. The American College of Surgeons Oncology Group Z6051 trial, which started in 2008, compares laparoscopic and open surgery for rectal cancer within 12 cm of the anal verge. This study will recruit 650 patients. Challenges in laparoscopic rectal cancer surgery Extended laparoscopic rectal surgery, such as laparoscopic lateral pelvic lymph node dissection (LPLD) and laparoscopic total pelvic exenteration for rectal cancer invading the pelvic organ, is feasible. LPLD was established in Japan and is currently performed only in Asian countries. It is not yet accepted in the treatment guidelines because of lack of long-term outcome from randomized trials (1,15). Watanabe et al. reported no significant difference in survival between patients who had neoadjuvant radiotherapy with TME and those undergoing TME plus LPLD (54). Based on the result, there is an opinion that LPLD can be omitted if neoadjuvant radiotherapy is performed. The nationwide, multi-institutional study in Japan by Akiyoshi et al. recently revealed that the prognosis of patients with internal lateral lymph node metastasis does not significantly differ from that of patients with N2a metastasis (according to the American Joint Committee on Cancer staging system). This means that lateral lymph nodes can be considered as regional lymph nodes (55). Kim et al. demonstrated that lateral lymph node metastasis is the most common type of local recurrence after neoadjuvant chemoradiotherapy plus TME alone; it is strongly associated with the preoperative radiographic size of the lateral pelvic lymph node (56). The long-term results from the multicenter randomized trial comparing TME plus LPLD and TME alone for advanced low rectal cancer (JCOG 0212 trial) have yet to be released. One of the problems of TME plus LPLD is an increased amount of blood loss and high morbidity as stated by Fujita et al. (JCOG 0212 trial) (57). Konishi et al. reported the shortterm outcomes and surgical technique of laparoscopic LPLD; the report and accompanying video demonstrated that laparoscopic LPLD is feasible with a small amount of blood loss and low postoperative morbidity (58). Laparoscopy-assisted total pelvic exenteration is technically feasible, although there has been only one reported case until now (59). Our hospital (Toranomon Hospital, Tokyo, Japan) has experienced two cases of laparoscopy-assisted total pelvic exenteration for rectal
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cancer invading the adjacent pelvic organ. This procedure has two technical difficulties: ligation of the periprostatic venous plexus (Santorini’s venous plexus) and urinary diversion. Ligation of the venous plexus has become possible with improved surgical devices such as electric cautery with soft coagulation mode and vessel sealing devices. Urinary diversion is performed using ileal conduit reconstruction through mini-laparotomy.
Conclusion In the near future, laparoscopic surgery will be accepted as the treatment choice for rectal cancer because of its favorable short-term results without deterioration of long-term results. At present, laparoscopic rectal surgery should still be performed only by well-experienced surgeons. However, we expect that laparoscopic rectal surgery will become widespread, in the same manner that TME did.
Acknowledgment The authors have no conflict of interest or financial ties to disclose.
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