Has the open surgical approach in colorectal cancer really become uncommon?

Abstract

Colorectal cancer is the third most common cancer in the world. Surgery is mandatory to treat patients with colorectal cancer. Can colorectal cancer be treated in laparoscopy? Scientific literature has validated the oncological quality of laparoscopic approach for the treatment of patients with colorectal cancer. Randomized non-inferiority trials with good remote control have answered positively to this long-debated question. Early as 1994, first publications demonstrated technical feasibility and compliance with oncological imperatives and, as far as short-term outcomes are concerned, there is no difference in terms of mortality and post-operative morbidity between open and minimally invasive surgical approaches, but only longer operating times at the beginning of the experience. Subsequently, from 2007 onwards, long-term results were published that demonstrated the absence of a significant difference regarding overall survival, disease-free survival, quality of life, local and distant recurrence rates between open and minimally invasive surgery. In this editorial, we aim to summarize the clinical and technical aspects which, even today, make the use of open surgery relevant and necessary in the treatment of patients with colorectal cancer.

Key Words: Colorectal cancer, Laparoscopy, Laparoscopic colorectal resection, Bowel obstruction, Bowel perforation, Advanced colorectal cancer

Core Tip: In terms of oncological outcomes and quality of resection, laparoscopic approach allows to do just as well as open surgery, in particular the number of the lymph nodes removed is identical, regardless of the access. However, the laparoscopic approach is not recommended when the neoplasm presents with urgency, in the occlusive or perforated phase, as well as it is not recommended for locally advanced tumors. When the tumor involved the serosal layer or invades an adjacent organ, open “en-bloc” excision is recommended.

INTRODUCTION

Colorectal cancer is the third most common cancer in the world. In 2019, new cases of colorectal cancer in the world were 1931590, corresponding to 10% of new cancer diagnoses, and is responsible for approximately 750000 cancer-related deaths annually[1]; in Italy there are estimated around 51000 cases/year, representing overall the 15% of new cancer diagnoses[2]. Surgery is mandatory to treat patients with colorectal cancer. In the case of primary non-metastatic disease, surgery guarantees a better long-term prognosis, both in terms of overall survival, disease-free survival and patient quality of life[3-5].

Curative resection aims to radically remove the segment of intestine in which the tumor is located. The resection must include at least 5 cm of healthy colon upstream and downstream of the lesion[6,7]. Furthermore, lymphadenectomy is fundamental for a systematic lymph node dissection and for removing all potentially metastatic lymph nodes[8-11]. International guidelines have established that a number equal or greater than 12 lymph nodes must be removed to guarantee an adequate lymphadenectomy and, at the same time, the possibility of staging the neoplastic disease more accurately[9,10,12]. It is therefore established as an oncologically appropriate resection influences the prognosis of patients with colorectal cancer.

In recent decades, the traditional surgical approach via laparotomy and direct access to the patient’s abdominal cavity has been joined by new minimally invasive surgical techniques. Laparoscopic surgery has now been validated through large randomized controlled studies conducted throughout the world. In this editorial, we aim to summarize the clinical and technical aspects which, even today, make the use of laparotomy relevant and necessary in the treatment of patients with colorectal cancer.

LAPAROSCOPIC TREATMENT

Laparoscopic surgery in colorectal cancer represents a correct alternative to open surgery, if performed by surgeons with adequate training in this specific procedure[13]. Even in laparoscopic surgery the proximal and distal resection margins are appropriate and proximal vessel ligation is performed safely. Curative resections are therefore obtained, with en-bloc removals and tumor-free radial margins (R0)[14].

The United Kingdom Medical Research Counsel (MRC) trial of conventional vs laparoscopic assisted surgery in colorectal cancer, published in 2005, which included patients with both colon and rectal cancer was the first randomized controlled trial to investigate the role of laparoscopy in colorectal cancer[15]. After this trial there were four subsequent randomized controlled trials comparing laparoscopy to open surgery in colorectal cancer. All these studies - the Comparison of Open vs Laparoscopic Surgery for Mid and Low Rectal Cancer After Neoadjuvant Chemoradiotherapy[16], the Colorectal Cancer Laparoscopic or Open (COLOR II)[17], the American College of Surgeons Oncology Group Z6051[18], and the Australasian Laparoscopic Cancer of the Rectum Randomized Clinical Trial (ALaCart)[19] - were designed to assess the non-inferiority of laparoscopic surgery compared to open surgery. In all these studies, patients with T4 tumors were excluded from inclusion. The COLOR II study also excluded T3 tumors within 2 mm of the endopelvic fascia. The laparoscopic approach was associated with longer operative times, lower estimated blood loss, and faster recovery of bowel function in all of these studies. These randomized trials evaluating the oncologic outcomes of laparoscopic colectomy showed no significant differences in proximal and distal margins, number of lymph nodes retrieved, and perpendicular length of the primary vascular pedicle compared with open surgery[14,15,17,20-22]. Furthermore, long-term survival and recurrence were no different for patients treated with open and laparoscopic surgery in these studies[15,21,23,24].

Recently, the short-term results of a multicenter prospective randomized trial conducted in China comparing laparoscopic and open resection have been published[20]. The Laparoscopy-Assisted Surgery for Carcinoma of the Low Rectum study was conducted on a population of over 1000 patients. Specifically, 685 patients in the laparoscopic surgery group and 350 patients in the open surgery group were included. No significant differences in morbidity rate were observed between the two groups. Higher rates of sphincter preservation and shorter length of stay were observed in patients undergoing laparoscopic surgery.

Extraperitoneal rectal carcinoma presents peculiar aspects. While the approach to carcinoma of high rectum does not differ from that of the recto-sigmoid junction and the sigmoid carcinoma, surgery of the mid-lower rectum presents technical difficulties that are best managed in high-volume specialist centers. The cornerstones of this surgery concern the total excision of the mesorectum (Figure 1), the preservation of the sympathetic and parasympathetic innervation (nerve-sparing technique), the distal and circumferential section margin free from neoplasia and, in locally advanced forms (T3-T4 and/or regional lymph node metastases) the use of neoadjuvant therapies. In these patients, laparoscopic total mesorectal excision can be performed safely and adequately as demonstrated in prospective studies and retrospective series[25-29]. Mid and long-term oncological outcomes appear similar between open and laparoscopic approaches[30]. We can therefore conclude that oncologic results of the laparoscopic surgery for rectal cancer are generally comparable to open surgery. Currently, the results reported by numerous studies in the literature highlight that laparoscopic surgery is the therapeutic option of choice for the surgical treatment of rectal cancer.

Figure 1 Surgical specimen of anterior resection of the rectum with complete removal of the mesorectum (personal observations).

THE ROLE OF OPEN SURGERY

In colorectal cancer patients, laparoscopic surgery has some controversial aspects. A learning curve appears fundamental in the laparoscopic field. Both the surgeon and the operating room auxiliary staff are required to acquire advanced laparoscopic skills in well-defined time intervals[31,32]. Laparoscopic surgery is very demanding, and can be performed with low morbidity and mortality rates only by a surgeon with above-average experience with this type of surgery and a large caseload of laparoscopic colorectal procedures. The learning curve for such procedures is appreciably longer than for other laparoscopic operations. With increasing experience, technically more demanding operations, including radical oncologic rectal laparoscopic procedures, can be performed with appreciably reduced operating times and conversion rates, but with no increase in morbidity or mortality. At least 20 laparoscopic procedures for colon cancer are required for the individual surgeon to be included in multicenter clinical trials. Studies more carefully examining the learning curve for laparoscopic colectomy have suggested that full surgical autonomy and competence is acquired with at least 50 colorectal resection procedures in a defined time interval[31-33]. Advanced laparoscopic training during residency or fellowship and training on simulators may shorten the learning curve toward proficiency. Mentoring, proctoring, and working with an experienced assistant have each been shown effective in the adoption of techniques new to a surgeon’s skill set[34-37].

Furthermore, aspects of laparoscopic surgery have raised some initial concerns in the scientific community. The risk of a potential violation of oncological principles, the possible spread of neoplastic cells linked to carbon dioxide insufflation and the possibility of tumor recurrence in the access sites of the trocars have represented some of the controversial aspects[38,39]. However, it seems right to emphasize that these fears and these controversial aspects were found to be completely unjustified, both by evaluating some aspects of basic scientific research and by analyzing the results of large randomized and controlled studies.

T4 tumors show an incidence of up to 15% in patients with colon cancer. Among patients with rectal cancer, 5% to 12% of patients have tumors adherent to adjacent organs[40-42]. In these patients, is recommended en-bloc resection to manage locally advanced colorectal cancer[43,44]. Thus is T4 colorectal cancer still an absolute contraindication to laparoscopic surgery? The answer is that T4 colon cancer is not an absolute contraindication. Obviously, the possibility of treating T4 colorectal cancer laparoscopically depends on local circumstances (e.g., organs involved in the enlarged demolition and factors related to the surgeon (e.g., skill and experience of the individual surgeon in performing a laparoscopic en-bloc resection). Intraoperative observation of a T4 lesion often requires conversion to open surgery, especially if the goal of the therapeutic approach is curative resection. This eventuality is necessary because en-bloc demolition in the presence of a T4 lesion is not always effective in laparoscopic surgery. However, en-bloc resection may not be possible using either technique or, therefore, the surgeon must decide whether conversion is likely to allow curative resection. To date, there have been no randomized trials comparing laparoscopic and open approaches to T4 colonic or rectal cancers.

In the UK MRC-CLASSIC trial, 34% of the patients randomized to the laparoscopic group underwent conversion to an open procedure. In this group of patients, a higher post-operative morbidity rate (P = 0.002) and a worsened overall survival have been observed[45,46]. Furthermore, in patients undergoing laparoscopic low anterior resection or abdominoperineal resection (Figure 2), there was a higher rate of positive circumferential margins, although this did not impact local recurrence or survival[47]. Overall, male sexual and erectile function was worse in the laparoscopic group[46].

Figure 2 Clinical case of adenocarcinoma of the low rectum treated with laparoscopic abdominoperineal resection sec. Miles after neoadjuvant treatment. A: Surgical specimen of abdominoperineal resection; B: Photo of the abdomen; C: Perineal wound (personal observations).

In rectal cancer, when using the minimally invasive approach, particularly for tumors in low rectum, a further challenge is represented by the anatomical conformation of the pelvis. Elements that can hinder the execution of an oncological adequate resection for rectal cancer laparoscopically are the size and location of the tumor. Additional clinical-anatomical factors such as narrow pelvis, obesity, large uterus and preoperative radiation effects are of particular importance. The inability to conduct demolition in accordance with oncological principles should lead to conversion to open surgery. Similar considerations must guide the choice of the type of colorectal anastomosis or the creation of a temporary or permanent stoma.

Complications of large bowel diseases account for 47% of gastrointestinal emergencies. Colorectal cancer presents as emergency in a wide range of patients (from 7% to 40% of the total). Large bowel obstruction represents almost 80% of the emergencies related to colorectal cancer, while perforation accounts for the remaining 20%. The most common location of bowel obstruction is the sigmoid colon, with 75% of the tumors located distal to the splenic flexure. Perforation occurs at the tumor site in almost 70% of cases and proximal to the tumor site in around 30% of cases[48]. The management of colon and rectal obstruction and perforation is challenging in terms of clinical severity, diagnostic and therapeutic options, and management of septic (Figure 3) and oncological issues. As a general rule, the principles of oncological resection should be followed. It should be emphasized that in these conditions it is important to consider the role of medical comorbidities, sarcopenia and local or systemic septic status. Even in these patients, the main objective is to optimize the postoperative course, avoiding and preventing complications, especially anastomotic leakage, to allow the completion of oncological staging and the start of integrated chemotherapy and/or radiotherapy treatments[48].

Figure 3 Intraoperative photo of diffuse fecal peritonitis due to perforation of the cecum in a patient with neoplastic stenosis of the sigmoid colon (personal observations).

In case of colonic obstruction due to tumor of the right colon or proximal transverse colon, right hemicolectomy, classic or extended, with subsequent primary ileocolic anastomosis represents the most appropriate treatment. The general condition of the patient strongly affects the choice to perform an anastomosis. The patient’s condition, including hemodynamic stability, the extent of abdominal distention, the resectability of the carcinoma and the surgeon’s ability to perform a curative resection represent the elements that must be taken into consideration when choosing a possible laparoscopic approach in the presence of an occlusive colorectal carcinoma[49]. Although there have been some retrospective studies demonstrating feasibility of laparoscopic resection with benefits in short-term outcomes, a prospective randomized controlled trial has not yet been published[50-52].

In case of obstructing cancer of the left colon, a variety of options have been advocated[53]. Resection and primary anastomosis, with or without protective stoma, resection according to Hartmann, intraabdominal subtotal colectomy with ileostomy or ileorectal anastomosis are the most frequently used procedures. More recently, endoscopically placed colonic stents are used in selected patients. These endoscopic procedures, allowing the decompression of the colon and favoring the clinical stabilization of the patient, allow urgent surgery to be postponed and elective colectomies with primary anastomosis to be performed in a re-balanced patient. In this way, such an approach allows the decrease in colostomy creation rates in patients with occluding cancer of the left colon.

The use of laparoscopy in the emergency treatment of colorectal cancer cannot be recommended and should be reserved to selected favorable cases and in specialized centers[54]. Emergency presentation has been considered an absolute contraindication to laparoscopy, due to the profile of the patient at high septic risk and the level of technical operative difficulties due to the dilated and vulnerable intestine. However, with the spread of colorectal laparoscopy and the increase in experience, favorable results have been published[55], but no randomized trials.

Risk factors for conversion for different populations have been widely reported in the literature. A recent meta-analysis documented an average conversion rate of 17.9%. An evaluation of the factors that negatively influence the completion of the laparoscopic surgical procedure has shown that the factors that are most responsible for the conversion to open surgery are male sex, a tumor localized in the extraperitoneal rectum, the T3/T4 stage and the presence of metastases to locoregional lymph nodes[56]. With increasing laparoscopic hospital volume, conversion decreases below 10% with only minimal impact of conversion on short-term postoperative outcome. To perform an early conversion can be an appropriate decision, for which reason this type of conversion should not be considered a failure[57-59].

CONCLUSION

Laparoscopy is a safe and effective surgical technique for the treatment of colorectal cancer. Laparoscopy remains an acceptable minimally invasive option in well trained hands. Surgeon represents a significant prognostic factor: His operative volume and that of the team with which he works is linked to surgical mortality, peri-operative complications and prognosis. Locally advanced disease and emergency presentation are relative contraindications to the laparoscopic approach. Highly predictive factors of conversion are the lower and left site of the tumor, obesity as well as previous major abdominal surgery.

Laparoscopic surgery for low rectal cancer, when performed by experienced surgeons, could produce pathological outcomes comparable to those of open surgery. In large surgical series and multicenter studies, no differences are observed regarding complete excision of the mesorectum and the appropriateness of the resection margins. In the population of patients undergoing laparoscopic demolition, a higher rate of sphincter preservation and a favorable postoperative recovery are documented. While no differences in short-term oncological outcomes have been observed, long-term oncological outcomes in homogeneous patient populations are currently being evaluated.