Since its introduction, laparoscopy has gained more and more consent in colorectal surgery, becoming the Gold Standard for the surgical treatment of colon cancer (1). On the contrary, its role in rectal cancer surgery is still controversial and widely debated. In fact rectal cancer surgery results more technically difficult than the colonic one, due to the narrow space of the pelvis, which gets laparoscopic surgery particularly challenging. For this reason laparoscopic rectal surgery gets performed only in specialized centers worldwide.
In the last decade accumulating evidence has demonstrated that recovery after laparoscopy is faster and better, moreover laparoscopic rectal resection has been proven equivalent to the traditional technique in terms of short-terms outcomes. Nevertheless, its oncologic safety remains unclear and doubts about pathologic outcomes are still open and worsened by new evidence reported by the most recent international studies. With this study we aim to present the ongoing situation of laparoscopic treatment for rectal cancer by reviewing the current literature.
Materials and methods
To identify all possible studies regarding the comparison between laparoscopic and open rectal resection for rectal cancer and to make the state of art of laparoscopic rectal resection, we performed a systematic search in the electronic databases (PubMed, Web of Science, Scopus, EMBASE) according to preferred reporting items for systematic reviews and meta-analyses (PRISMA) guidelines (2). We limited the search until 31 March 2017 and used the following search terms in all possible combinations: rectal cancer, laparoscopy, minimally invasive and open surgery. We included only English-written articles comparing laparoscopic surgery to the open technique for rectal cancer treatment.
The search produced 402 articles; 143 were duplicates and were removed. Two independent Authors evaluated the remaining articles excluding the ones that were not pertinent (not comparing laparoscopy to the traditional technique in rectal cancer treatment) or not English-written. Reviews were excluded too resulting in 66 articles, of which 38 are non-randomized trials, 8 are randomized controlled trials (RCTs) performed in a single center, 5 are multicentric RCTs and 15 are meta-analyses (Figure 1).
Articles included in this review have been divided in four categories: non RCTs, single-center RCT, multicentric RCTs, meta-analyses; and chronologically ordered in Tables 1-4.
Rectal cancer is a worldwide disease that constitutes one-third of colorectal cancers (67) and whose incidence has increased significantly in the last decades (68). The main treatment for rectal cancer is the surgical resection, which results have drastically improved since the introduction of total mesorectal excision (TME).
Thanks to accumulating evidence indicating that laparoscopic treatment of colon carcinoma is considered equivalent to the open technique, the laparoscopic technique is widely accepted and performed in the treatment of colon carcinoma. On the contrary, the role of laparoscopy in the treatment of rectal cancer is still not clear. Laparoscopic rectal surgery is more difficult than colonic one, due to the narrow space of pelvic cavity and the oncological safety remains unclear. Therefore, laparoscopy in rectal cancer is still not recommended as the gold standard treatment by international guidelines.
Anyhow the open approach too presents several limitations, especially in terms of oncologic outcomes, as it has been demonstrated by Rickles et al. (69) who reported a 22% less risk of positive circumferential resection margin (CRM) after laparoscopic surgery compared to an open approach.
All these reasons led to the current interest of surgeons towards new techniques, such as the use of robotics, transanal approach (taTME) or the combination of laparoscopy and transanal approach for rectal cancer surgery.
During the last decade many studies have been performed to prove the safety and feasibility of laparoscopic-assisted resection for rectal cancer. In order to demonstrate the non-inferiority of the laparoscopic approach against the open surgery, Authors all over the world have compared the two techniques in terms of short- and long-term outcomes.
Most of these studies are non-randomized comparative (3-20) trials (NRCTs) (21-38). The findings of these studies were extremely encouraging, showing the non-inferiority of laparoscopy compared to the open technique in terms of oncological outcomes (like disease-free survival and local recurrence) and intraoperative and postoperative factors. Moreover the laparoscopic group presented advantages regarding antibiotic and analgesic therapy, early mobilization, hospital stay, intraoperative blood loss, resuming oral nutrition, bowel transit resumption, postoperative complications and wound complications, concluding that laparoscopic resection for rectal cancer is feasible, safe and effective.
To collect more accurate evidence about short- and long-term outcomes after laparoscopic surgery for rectal cancer compared to open surgery, a large number of randomized control trials (RCTs) have been produced in the last few years (39-47). Most of these studies focused on postoperative morbidity, length of hospital stay, quality of life, long-term survival, and local recurrences, finding no significant difference between the groups.
For an example, a recent study was developed by Ng et al. (43) who performed a single-center, prospective, randomized trial on 80 patients with mid and low rectal cancer, focusing on oncologic outcomes (in particular quality of the TME specimen, circumferential resection margin (CRM) involvement, and number of lymph nodes removed), which were found similar between both groups.
The results assessed with these randomized trials seem to suggest that laparoscopic surgery for rectal cancer could improve short-term results while not jeopardizing the oncological outcomes compared with open surgery. The major limitation of these studies is that, being single-centered they are based on an exiguous number of patients.
To reach a wider number of patients multicentric studies have been designed and performed all over the world in the last 20 years (Figure 2).
In the CLASICC trial (48) 794 patients with colorectal cancer from 27 UK centers were enrolled to be treated by either laparoscopic or open surgery. Primary short-term end-points were positivity rates of circumferential and longitudinal resection margins and in-hospital mortality. In the CLASICC trial, regarding the cancer of the rectum, no significant difference in CRM positivity was detected in patients who underwent a rectal resection in both laparoscopic and open group. CRM positivity, instead, was significantly greater in laparoscopic than in the open surgery group for patients who underwent anterior resection. It is important to highlight that positive CRM is a strong predictor of both local recurrence and overall survival, since it is associated with a high rate of local recurrence and poor morbidity and mortality for rectal cancer patients (69). As a first conclusion, at the time of its first publication, the impair short-term outcomes after a laparoscopic approach in an anterior resection of the rectum did not justify its routine use. Further studies about long-term outcomes of patient enrolled in the CLASICC trial, have been recently published focusing on the local recurrence, overall survival and disease-free survival (70,71). No significant differences between the laparoscopic and open approach were found in local recurrence, overall survival and disease-free survival after 3, 5 and 10 years follow-up. However, it is worth mentioning that the CLASICC trial (48) enrolled not only patients with rectal cancer but also patients with colon cancer, which may cause confusion on conclusions about rectal cancer.
Two other multicentric studies, aimed to compare laparoscopic and open surgery in patients with rectal cancer, were the COLOR II trial (49) and the COREAN trial (50), enrolling respectively 1,103 patients with rectal cancer within 15 cm from the anal verge and 340 patients with II and III mid- and low rectal cancer. Both studies demonstrated similar results in oncologic outcomes, disease-free survival and recurrence, confirming the safety and feasibility of the laparoscopic approach for rectal cancer. COLOR II trial was performed in 30 centers and hospitals from eight countries from 2004 to 2010. As expected, blood loss and recovery resulted better after the laparoscopic approach, even if it was connected to longer operative time. In terms of safety, completeness of the resection, positive CM (<2 mm) and median tumor distance to distal resection margin did not differ significantly between the groups. Also morbidity and mortality within 28 days after surgery were similar. So the authors concluded that laparoscopic surgery resulted in similar safety to open surgery and associated to a better recovery, if performed in selected patients treated by skilled surgeons.
The COREAN trial (50) was performed in three centers from 2006 to 2009 in South Korea. Its conclusions were similar to the COLOR II trial (49): although surgery time was longer in the laparoscopic group, no significant difference was found in the involvement of the CRM, macroscopic quality of the TME specimen, number of harvested lymph nodes, and perioperative morbidity, once again stating the efficacy and safety of laparoscopic rectal resection.
More recently, two multicentric studies have been published, introducing controversial conclusions about the non-inferiority of laparoscopic surgery compared with open surgery. In the ALaCaRT Randomized Clinical Trial conducted between 2010 and 2014, 475 randomized patients with T1–T3 rectal adenocarcinoma, underwent either laparoscopic  or open  rectal resection (52). The primary end point was several oncological factors selected to an adequate surgical resection. A successful resection was achieved in 194 patients (82%) who underwent laparoscopic surgery and 208 patients (89%) who received open surgery. CRM was clear in 93% of patients in the laparoscopy group and in 97% who underwent open surgery. Distal margin was clear in 99% of cases in both groups, and TME was complete in 87% of patients in the laparoscopic surgery group and 92% in the open surgery group. Based on these findings the Authors concluded that, among patients with T1–T3 rectal tumors, there was not sufficient evidence to establish the non-inferiority of laparoscopic surgery compared to open surgery, so the choice of a laparoscopic approach for a patient with rectal cancer should be made with caution.
Similar evidence was found by Fleshman et al. in the ACOSOG Z6051 randomized clinical trial (51). A multicenter randomized trial enrolling patients from 35 institutions across United States and Canada, between 2008 and 2013. A total of 486 patients with a stage II or III rectal cancer within 12 cm from the anal verge were randomized after neoadjuvant therapy to receive a laparoscopic  or an open  resection. The aim of the study was to assess whether laparoscopic resection was not inferior to open resection, based on pathologic and histologic evaluation of the resected specimen. Successful resection occurred in 81.7% of laparoscopic resection cases and 86.9% of open resection cases and did not support the non-inferiority. These results too do not support the use of laparoscopic resection in patients with stage II or III rectal cancer.
It’s important to notice that the chosen outcome to assess the efficacy of laparoscopic surgery in rectal cancer was a composite of a CRM greater than 1 mm, distal margin without tumor, and completeness of TME. This combination of short-terms outcomes has been arbitrarily chosen by the Authors and it still has to be proven its real impact on recurrence and long-term survival. So, both studies share the main limitation: the non-inferiority of laparoscopy compared to open surgery is based on the combination of completeness of TME and the positivity of CRM which, as short-terms outcomes, are only predictors of local recurrence. Long-terms outcomes are needed to define laparoscopy inferior compared to the traditional approach.
Moreover, although the results of the comparison between laparoscopy and open technique in terms of successful resection do not support the non-inferiority of laparoscopy, taken singularly, CRM and TME in the ALaCaRT trial are very close to be significant (P=0.06) and then equivalent in open and laparoscopic surgery.
Finally both studies do not take under consideration short-terms outcomes, like recovery, which has been worldwide demonstrated faster and associated with a lower rate of incidence of complications after laparoscopic surgery.
In the past 10 years meta-analytic studies have been performed to be able to give definitive results by pooling together a wide number of patients. Studies before the publication of ACOSOG and ALaCaRT protocols (51,52) stated the non-inferiority of laparoscopy compared to the open approach for rectal resection. Although their optimistic conclusions, we must underline how these studies share some limitations. Many of them, in fact, included non-RCT studies in the analysis that can lead to misleading results due to a selection bias.
Including ALaCaRT e ACOSOG (51,52) the Authors came to the conclusion that the risk for achieving an incomplete mesorectal excision is significantly higher in patients undergoing laparoscopic rectal resection compared to the open technique, dampening the enthusiasm in support of laparoscopy for rectal surgery.
In conclusion, due to its impressing outcomes in terms of post-operative recovery and low rate of complication, laparoscopy has been seen for many years as the answer for rectal surgery. For the first time, after decades of certain advantages of laparoscopy, we are now witnessing the questioning of its equivalence to the traditional technique in terms of oncologic outcomes (Table 5). So the answers is yet to be found: to assess if the results of ongoing multicentric RCTs have a real impact on the disease-free and overall survival of patients undergoing rectal surgery performed with laparoscopic technique, thus we will have to wait for their long-term results. Only in the next future, in fact, we will be able to assess if the failure of laparoscopy in these trials in terms of pathologic outcomes will bring to an actual increase of recurrence and mortality, alongside a shortage of the disease-free survival. This should give the rationale to perform new meta-analyses based on the new evidence produced. Moreover, even more multicentric RCTs studies, hypothetically designed on new pathological outcomes, should be performed to finally assess if laparoscopy is a valid choice for the treatment of rectal cancer.
Furthermore, the controversial findings we are facing could be explained by the fact that TME is challenging at baseline, working in the deep pelvis, with rigid instruments, from angles that require complicated maneuvers results even more difficult. It is possible that future developing of instruments, the introduction of different technologies such as robotics and the introduction of new techniques like taTME will improve efficacy of minimally invasive techniques and exceed the limitations of laparoscopy (12).
Conflicts of Interest: The authors have no conflicts of interest to declare.
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Cite this article as: Milone M, Manigrasso M, Burati M. Rectal cancer—state of art of laparoscopic versus open surgery. Ann Laparosc Endosc Surg 2017;2:147.