Complete Mesocolic Excision for Colon Cancer: The New Standard of Care?

Abstract

Complete mesocolic excision (CME) for colorectal cancer builds on the success of total mesorectal excision (TME), the international gold standard for rectal cancer. In TME, removal of the primary tumor along with associated mesocolon and accompanying structures as single intact specimen allows in toto excision of all structures that could potentially lead to dissemination. Recent meta-analysis has confirmed that CME results in better disease-free survival (DFS) and overall survival (OS) rates. CME can be done in three ways—open, laparoscopic, and robotic-assisted. We conducted a survey to identify the real-world situation with the use of CME by surgical oncologists. A total of 116 responders shared their experiences and thoughts. The benefit of CME was primarily thought to be for both OS and DFS by 78/116 (67%). The majority of CMEs are being conducted by the open method (74/116; 64%). A total of 52/116 (45%) were of the opinion that 6 to 10 surgeries constitute the learning curve for new surgeons for this technique. Based on our survey results, as well as two recently published systematic reviews and meta-analysis, it is time to consider CME as one of the standards of care in colorectal surgery.

Keywords

gastrointestinal malignancy - survey - optimal surgery

Shyam Aggarwal

Introduction

Resection of colorectal cancer by operating along the embryologic tissue planes has been described more than a century back.[1] Over the past three decades, the standardization of total mesorectal excision (TME) technique in the management of rectal cancer has shown excellent outcomes. TME, currently considered the international gold standard surgery for treatment of rectal cancer, was first standardized in 1982 by Professor Heald.[2] It involves dissection along the embryological planes of the dorsal mesentery and complete removal of the rectum along with the mesorectal envelope. This revolutionary surgery yields an uninjured clear specimen that includes the vascular and lymphatic pathways and lymph nodes. TME has been associated with reduction of local recurrence to 6 to 12% and a 53 to 87% improvement in the 5-year survival.[3]

Hohenberger et al[4] applied the same concept to colon cancer surgery in the form of complete mesocolic excision (CME). Over the years, sufficient data has been generated to allow meta-analysis that objectively shows its benefit—cancer-related 5-year survival rates improved from 82.1 to 89.1% and the local 5-year recurrence rates reduced from 6.5 to 3.6%. We therefore decided to survey and document the practices and utility of CME in the real-world setting among surgical oncologists who were performing this surgical technique.

Methods

The authors discussed online regarding the current challenges and advantages of CME in real-world practice. We agreed upon the most important aspects and finalized a list of 10 multiple-choice questions ([Table 1]) with appropriate options. These questions were circulated on WhatsApp groups of surgical oncologists (as a Google Form link) and the oncologists interested in the subject were invited to share their real-world experience. Data was collected on this Google Form over a period of 7 days. The answers were evaluated, duplicate/incomplete submissions deleted, and the remaining data was analyzed.

Table 1 Survey of real-world practice questions and answer choices

Question no.	Question description	Options
1	In your real-world practice, for operable colon cancer, is complete mesocolic excision (CME) standard of care?	Yes, No
2	In your real-world practice, what do you believe CME improves	OS, DFS, both, neither
3	In your practice, what is your preferred method for CME	Open, laparoscopic, robotic
4	In your real-world practice, in what percentage of patients could you not complete the CME (removal of the primary tumor along with associated mesocolon and accompanying structures as single intact specimen allows in toto excision of all structures that could potentially lead to dissemination)	Less than 2%, 3–6%, 7–10%, more than 11%
5	In your practice, which is the most difficult part in performing successful CME	Dissection of loop of Henle, right colic artery ligation, resection of adequate length of bowel, dealing with Toldt fascia, none
6	In your real-world practice, for CME do you follow the Japanese technique of bowel being resected 5 cm beyond the feeding arterial branch in the direction of the lymph flow and 10 cm beyond the tumor in the opposite direction	Yes, No
7	In your real-world practice, while doing CME, what do you do first?	Central ligation, colon mobilization, omentectomy followed by entry into omental bursa
8	In your real-world practice, in CME, your preferred choice is	Intracorporeal anastomosis, extracorporeal anastomosis
9	In your real-world practice, in CME, your preferred choice is placement of a drain	Yes, No
10	In your real-world practice, for a new surgeon, how much time is required to complete the learning curve and master the techniques of CME	Less than 5, 6–10, 11–15, more than 15 surgeries

Abbreviations: DFS, disease-free survival; OS, overall survival.

Results

A total of 116 surgical oncologists responded online. There were no incomplete or duplicate responses. CME was considered as standard of care by 111/116 (96%). The benefit of CME was thought to be for overall survival (OS) by 6/116 (5%), for disease-free survival (DFS) by 23/116 (23%), for both by 78/116 (67%), and neither by 5/116 (4%). The preferred method for doing CME in the real world is show in [Fig. 1]. The majority of CMEs are being conducted by the open method (74/116; 64%). CME could not be completed in less than 2% (63/116; 54%) of instances ([Fig. 2]) and in 3 to 6% of cases in 29/116 (25%).

Fig. 1 Preferred method (real world) for complete mesocolic excision (CME) (N = 116).

Fig. 2 Percentage of patients in which complete mesocolic excision (CME) could not be completed in real-world practice (N = 116).

The most difficult technical part in performing a successful CME was dissection of the loop of Henle (52/116; 45%) followed by the right colic artery (RCA) ligation (13/116; 11%), resection of adequate length of the bowel (9/116; 5%), and dealing with Toldt's fascia (3/116 (3%) ([Fig. 3]). No difficulty was faced by 39/116 (34%) of responders. The Japanese technique (of bowel being resected 5 cm beyond the feeding arterial branch in the direction of the lymph flow and 10 cm beyond the tumor in the opposite direction) was followed by 54/116 (47%). The first step in the CME procedure was central ligation in 58/116 (50%), colon mobilization in 54/116 (47%), and omentectomy followed by entry into omental bursa in 4/116 (3%). Intracorporeal anastomosis was preferred by 51/116 (44%) and extracorporeal anastomosis was the choice in the remaining 56% (65/116). Drain utilization was preferred by 100/116 (86%) and the remaining 16/116 (14%) preferred not using the same. [Fig. 4] shows existence of a learning curve in successful practice of CME in the real world. A total of 52/116 (45%) were of the opinion that 6 to 10 surgeries constitutes the learning curve whereas 29/116 (25%) felt that the learning curve required 11 to 15 or more than 15 surgeries each. A total of 6/116 (5%) thought that up to five surgeries were sufficient to learn the technique of CME.

Fig. 3 Most difficultly in performing successful complete mesocolic excision (CME) in real-world practice (N = 116).

Fig. 4 Learning curve—how many surgeries are required to master the techniques of complete mesocolic excision (CME).

Discussion

While the CME technique was introduced in the West in 2008, in the far East (Japan, China, Korea, and Taiwan) surgeons have used D3 lymphadenectomy (defined as the dissection of the paracolic, intermediate, and central lymph nodes), a procedure equivalent to CME resections for colon cancer, since decades.[5]

The three essential steps for optimal surgical technique in CME include[6]: (1) dissection between the mesenteric plane and the parietal fascia to remove the mesentery within a complete envelope of mesenteric fascia and visceral peritoneum that contains all lymph nodes draining the area, (2) central vascular ligation to completely remove all apical lymph nodes, and (3) resection of an adequate length of bowel to remove involved pericolic lymph nodes in the longitudinal direction. Actual practices differ significantly, especially between the far East (e.g., Japan) and the Western World (e.g., Western Europe, the United States).[6] The Japanese follow a more systematic and extensive dissection—the bowel being resected 5 cm beyond the feeding arterial branch in the direction of the lymph flow and 10 cm beyond the tumor in the opposite direction.[6]

Option 1: Open Surgery

The colectomy is performed through an open midline laparotomy. In open surgery, a “lateral to medial” approach is common. For right-sided colon, the lateral peritoneal fold is first identified to facilitate mesofascial and retrofascial separation. Dissection is continued in the mesofascial interface. After mobilizing the mesenteric root up to the origin of the superior mesenteric pedicle, dissection is continued over the duodenum and pancreatic uncinate process. The entire bowel can easily be twisted clockwise. This exposes the superior mesenteric vein (SMV) and the superior mesenteric artery (SMA). At this point, Hohenberger et al[4] originally added a duodenal kocherization but it is not performed routinely.[7] The small intestinal mesentery, ileocecal junction, right colon, right mesocolon, and mesenteric confluence are fully mobilized from the underlying fascia and retroperitoneum. The autonomic nervous plexus is preserved.

After complete mobilization of the right colon, the supplying vessels are ligated. The ileocolic vein (ICV) and ileocolic artery (ICA) are identified. ICV is first suture-ligated as it drains the SMV.[7] Then, the ICA is ligated. As there may be aberrant vasculature here, caution must be taken. Sharp dissection is then performed along the SMA and all associated lymph nodes are cleared.

For cancers of the cecum or ascending colon, the omentum caudal to the gastroepiploic arcade is breached and the lesser sac is entered. The omentum is then divided and only the right branch of the middle colic vein (MCV) and middle colic artery (MCA) are divided and ligated.[7] [8] The surgeon needs to be aware of the variability in vascularity in this region. The transverse mesocolon dissection is continued vertically to meet the dissection near the superior mesenteric vascular pedicle. A rectangular specimen is formed with an intact mesocolic envelope containing all the central lymph nodes. Colon is divided at the level of the middle colic vessels.[4]

For cancers of the hepatic flexure or proximal transverse colon, the lesser sac is entered by dividing the right gastric artery to allow retrieval of the peripancreatic lymph nodes.[7] For cancers on the left of the MCA, left gastroepiploic arcade and lymph nodes along the inferior aspect of the left side of the pancreas are resected.[6] If they are involved, the lymph nodes over the head of the pancreas should be removed with central ligation of the right gastroepiploic artery. The superior pancreaticoduodenal artery and the autonomic nerve plexus are preserved.[8]

Resection of the left-sided tumors involves mobilization of the splenic flexure, division of the inferior mesenteric vein at the inferior border of the pancreas, and division of the inferior mesenteric artery on the aorta. The “lateral to medial” dissection begins at the lateral peritoneal fold and continues in the mesofascial interface.[8] The mesocolon of the descending and sigmoid colon is dissected, omentum is separated from the transverse colon, and the lesser sac is exposed. The two layers of the transverse mesocolon are divided at the inferior border of the pancreas. The splenic flexure is mobilized if needed. If the cancer is in the descending colon, the ascending branch of the left colic artery is ligated. The lymph nodes at the origin of the SMA are dissected without damaging the superior hypogastric plexus. If the cancer is in the middle of the descending colon down to the sigmoid colon, the root of the inferior mesenteric vessels below the pancreas is divided. Depending on the site of the tumor, the colon is dissected proximally between the left transverse colon and the distal descending colon. Distal transection is, however, always in the upper third of the rectum.

Option 2: Laparoscopic Surgery

A “medial to lateral” approach is preferred in laparoscopic surgery. In right hemicolectomy, the mesocolon is incised along the mesenteric axis and the ileocolic vessels are divided close to the SMV.[8] The surgical plane composed of the Toldt's fascia and the prerenal fascia is exposed. This uncovers the head of the pancreas and the duodenum can be mobilized. Some surgeons prefer not to mobilize the duodenum.[9] Dissection continues along the plane between the intact dorsal mesocolon of the hepatic flexure and the Fredet's pre-duodenopancreatic fascia. At the lateral aspect of the right colon the dissection stops, exposing the colo-fascial interface.

For cecal or ascending colon cancers, the transverse colon is transected with central ligation of the middle colic vessels. Colon is stapled 10 cm from the tumor.[9] For hepatic flexure or proximal colon transversum cancers, central ligation of the middle colic and right gastroepiploic vessels is done, subplyoric lymph nodes are removed, 10 to 15 cm of the greater omentum off the tumor is excised, and colon is stapled proximal to the splenic flexure.[6] However, laparoscopic CME for cancers close to the flexures and the transverse colon is somewhat controversial. Many surgeons prefer the open approach.[8]

There are several variations to laparoscopic classic CME and central ligation. In their modified CME, Cho et al[10] did not perform the kocherization as described by Hohenberger et al. They cleared the prerenal soft tissue behind Gerota's fascia for T3/4 cancer and customized the resection of the mesentery and mesocolon as per the location of the tumor.

Feng et al[11] proposed two variations. The hybrid medial approach blends both top-to-bottom and bottom-to-top dissection. The intermesenteric space (IMS) is entered by incision of the gastrocolonic ligament. The section of the gastrocolic ligament and dissection of the middle colic vessels and Henle's trunk is blended with a subsequent medial-to-lateral bottom-to-top approach and the inferior edge of the pancreas is dissected. The completely medial approach (CMA) involves bottom-to-top approach throughout. The IMS is entered through the transverse retrocolic space. The middle colic vessels and Henle's trunk are dissected and then the inferior edge of pancreas is dissected. CMA was the preferred approach as it took less time and reduced vessel-related complications.

Matsuda et al[12] proposed a different approach. They first opened the omental bursa wide and exposed Henle's trunk. After dividing the accessory right colic vein (ARCV), they divided the MCV at its root and dissected the lymph nodes along the SMV in a cranial-to-caudal approach. They suggested a caudal traction of the mesocolon to detect the origin of the middle colic vessels. This is suitable for easily detecting variations in the MCV branching and helps reduce vessel injury. It provides easy access to the pancreas, early division of the ARCV and middle colic vessels at origin, and easy dissection along the SMV.[12]

Option 3: Robotic Surgery

Robotic CME is another minimally invasive option available. Three 8-mm trocars carry a monopolar cautery hook/scissors in the left upper quadrant port (R1), bipolar forceps in the suprapubic port (R2), and Cadiere's fenestrated forceps in the subxyphoid port (R3).[13] A 12-mm trocar carries the camera and a 15-mm trocar has the assistant port.

R2 and R3 are used to keep the superior mesenteric axis in traction. The monopolar cautery hook/scissors in R1 is used for dissection. Through the grasp in R3, a cephalad traction of the transverse mesocolon is done. The ileocolic vessels are lifted up with R2. The peritoneum is opened just below the prominence of the ileocolic vessels and along the left side of the anterior aspect of the SMV. The ileocolic vessels, right colic vessel (if present), the MCV, and the right branch of the MCA are ligated at their roots. CME is performed by sharp dissection of the posterior visceral fascial layer, exposing the duodenum and pancreatic head so that a specimen with intact visceral fascial layers on both sides can be removed. A side-to-side isoperistaltic mechanical anastomosis is then done.

Schulte amEsch et al[14] proposed a 4-step bottom-to-up approach in robotic CME. In step 1, they initiated CME with caudolateral mobilization of the right colon guided by the fascia of Toldt across the duodenum and up to the trunk of Henle. In step 2, bottom-to-up dissection was done right of the middle supramesenteric vessels and central ligation of the ileocolic vessels was done. In step 3, the transverse retromesenteric space was separated and the hepatic flexure was mobilized. In step 4, the transverse mesocolon was transected right of the middle colic vessels.

Thus, CME requires sharp dissection that avoids any breech in the visceral fascia and minimizes the risk of tumor spread within the peritoneal cavity. The colonic arteries are exposed and ligated centrally as near their origin as possible—also allowing more comprehensive lymph node harvesting.

There is an extrafascial plane between the mesocolon and the retroperitoneum, called the “Toldt fascia,” which is an important part of the strategy in CME. The upper part of the Toldt fascia fuses closely with the mesothelial layer of the overlying mesocolon and the lower part with the mesothelial layer of the underlying retroperitoneum. It therefore becomes a natural embryonic dissection plane for successful CME for colorectal cancer.

Culligan et al[15] showed that (1) the mesocolon continues from the ileocecal to rectosigmoid level, (2) the mesocolon of the transverse colon and the mobile sigmoid colon does not include Toldt's fascia, and (3) Toldt's fascia is defined in the rest of the mesocolon that is connected to the retroperitoneum, that is, the ascending, descending, and the nonmobile part of the sigmoid colon.

Three surgical interfaces have been described: (1) mesofascial, (2) retrofascial, and (3) colofascial.[9] The mesofascial interface is the confluence of Toldt's fascia and the mesocolon. The retrofascial interface is the confluence of the Toldt's fascia and the retroperitoneum. The colofascial interface is the confluence of the Toldt's fascia and the colonic surface.

Immunohistochemical analysis of the mesocolon reveals a rich lymphatic network within both the submesothelial connective tissue and the septations, in all regions of the mesocolon.[16] Dissection that breaches the mesocolic surface can extensively disrupt the lymphovascular network and cause spillage of tumor tissue.

Identification and ligation of important blood vessels close to their origin requires attention to the RCA and ICA, the latter being the terminal part of the SMA.[17] [18] It is prudent to identify these vessels and their anatomic variations preoperatively using three-dimensional (3D) computed tomographic scans.[19]

Value of CME in the Real World ([Table 2])

Table 2 Surgical treatment options in colorectal cancer

Approach	5-year survival	Recurrence	Mortality	Complications
Endoscopic resection	90–100%	13.6–18.7% (5-year)	1.6–3.8% (5-year)	0–9%
Laparoscopic resection	94.2%	16% (3-year)	< 1% (30-day)	19%
Open colectomy	89.17%	18% (3-year)	1% (30-day)	19%
Total mesorectal excision	91.4%	7.3% (5-year)	0.8% (30-day)	15–20%

Interinstitutional comparisons report that in comparison to traditional surgery, when CME and central venous ligation are done, the surgeries are more often in the correct anatomical plane, resection specimen have larger mesenteric surface, and higher number of lymph nodes is harvested.[20] [21] In a single hospital, Bertelsen et al[22] found that the induction of CME led to significant increase in the length of vascular ligation (p < 0.0001) and the mean number of lymph nodes harvested (p = 0.0095). The plane of mesocolic resection, the rate of R0 resection, and the risk of complications were equivalent. The median length of hospitalization increased from 4 to 5 days (p = 0.04). Among patients who had undergone laparoscopic left-sided colectomies, CME was technically more challenging and required significantly longer operation time than non-CME surgeries.[23] However, there was no increase in short-term complications.

A meta-analysis of 8,586 patients from 12 studies suggested that compared with non-CME surgeries, CME was more effective for improving specimen quality and survival but had a higher complication rate.[24] It was associated with greater intraoperative blood loss, more postoperative surgical complications, longer large bowel resection, greater distance from the tumor to the vascular tie, larger area of mesentery, and more lymph node harvest. The CME group also showed better 5-year survival, 3-year survival, and 3-year survival for stage II as compared with the non-CME group. However, Alhassan et al[25] say that the data are currently limited and does not consistently support the superiority of CME. Therefore, it is too early to recommend CME as the standard treatment.

Although CME is technologically challenging and appropriate training is required, several studies show good oncological outcomes with CME. In a recently published study, Gao et al[26] report a more number of total lymph nodes harvested (24 vs. 20, p = 0.002), and significantly better 3-year local recurrence-free survival (100.0% vs. 90.2%) in patients who underwent CME rather than a non-CME procedure. There was no difference in the postoperative complications. Earlier, Agalianos et al[27] had shown similar results. More number of lymph nodes was harvested (27 vs. 18) and the 5-year OS (81.3% vs. 70.9%) and DFS (84.6% vs. 76.4%) were better in patients who underwent CME rather than a non-CME procedure.

Laparoscopic CME offers outcomes comparable to open CME surgeries, with regard to intraoperative blood loss and immediate postoperative morbidity and mortality rates.[28] Specimen quality is also similar in both open and laparoscopic CME for right or left colon cancers.[9] [28] Laparoscopic surgery offers the added advantages of minimally invasive surgery in terms of faster recovery and better immune competence due to less surgical stress.[9]

Robotic surgery offers the advantage of 3D visualization and improved instrument dexterity.[29] It gives superior oncological and postoperative outcomes than open surgery.[29] However, robotic techniques are not available in all centers and practitioners are slow to adopt the technique where it is available. There are still many surgeons who have no experience with robotic surgery. During the learning curve, longer operative times are required. The procedure is also costlier. Despite these challenges, robotic-assisted CME provides greater lymph node yield, superior oncological resection, and longer DFS.

Some researchers believe the improved outcomes in CME, whether by open surgery, laparoscopy, or robotic-assisted surgery, may be related to the mesocolic plane of surgery.[5] [28] [30] Others relate it to the high ligation of vessels draining the tumor.[4] [31] Some researchers, however, believe the complete removal of an intact mesocolonic envelope (CME) along with central vascular ligation and apical node dissection are each essential to improve outcomes in colon cancer patients.[8]

Hohenberger et al demonstrated that a lymph node yield of ≥ 28 was an independent association with an improved 5-year cancer-related survival (96.3% vs. 90.7%, p = 0.018) in node-negative patients[4] [6] [32]

The ratio of lymph node metastases to the total number of harvested lymph nodes, regards as the lymph node ratio, has been shown to be a better prognostic indicator than the actual N-stage, with the greater the number of negative nodes relative to metastatic nodes, the better the prognosis.[33] [34] [35] [36]

Technical Challenges

CME remains a technically challenging procedure, especially on the right side where the anatomical variability is greater. Damage to the SMV remains the biggest fear, occurring in up to 1.6% of all surgeries.[37]

Excessive retraction of the hepatic flexure may lead to avulsion injury of the MCV, usually at its origin from the SMV. Other potential complications include genitourinary dysfunction, chyle leak and increased inpatient days. Since the optimal time for high-risk (stage II and III colon cancer) patients to begin adjuvant chemotherapy is 4 to 6 weeks after surgery, complications will lead to delay and compromise final oncological outcome.

Operating time for CME is also longer, and associated with higher blood loss. This delayed the wide acceptance of CME in daily practice. However, we have more robust data today.

When compared with non-CME resections, about five different studies, between 2007 to 2013, have also showed that the local 5-year recurrence rates have almost halved.[31] [37] [38] [39] [40] Han et al reported an improved 5-year OS of 70.4% compared with 53.5% for the non-CME patients, these findings were consistently replicated in other studies.[37] [38] [39] Storli et al and Le Voyer et al have shown an increased DFS from 82 to 89% for stage I to II colon cancers.[21] [40] [41] [42] [43]

The Final Verdict

A recent population cohort study by Bertelsen et al presented 5-year survival after CME for right side colon cancer.[44] This included data from four hospitals in Denmark and followed up for 5.2 years following surgery. A total of 1,069 patients (813 in the control group and 256 in the CME cohort) underwent elective surgery with curative intent for right-sided colon cancer. The 5.2-year recurrence rate was 9.7% (95% CI 6.3–13.1) in the CME cohort as compared with 17.9% (15.3–20.5) in the control group. The control group had 145/813 (18%) patients with recurrence and 281 (35%) died during follow-up. In the CME cohort, only 25/256 (10%) patients had a recurrence and 75 (29%) died during follow-up.

In the recent systematic review and meta-analysis, De Simoni et al evaluated eight studies that met their criteria for inclusion.[45] Data was from a total of 1,871 patients. They showed that the CME group had significantly higher number of lymph nodes retrieved (mean difference 9.17, CI 4.67–13.68, p < 0.001), better 3-year OS (odds ratio [OR] 1.57, 95% CI 1.17–2.11, p = 0.003), better 5-year OS (OR 1.41, 95% CI 1.06–1.89, p = 0.02), as well as better 5-year DFS (OR 1.99, 95% CI 1.29–3.07, p = 0.002).

The same journal also subsequently published another meta-analysis by Ferri et al that included 17 studies and 3,918 patients.[46] Their objective was to look at 5-year OS and DFS. They not only confirmed better DFS and OS with the CME group but also reported that there was no difference in hospital stay or blood loss in the two groups. Similar oncological results were found in a prospective study from Norway that compared laparoscopic to open CME. The 3-year OS rate (80.4% vs. 88.2%, p = 0.152) and DFS rate (74.8% vs. 80.0%, p = 0.405) were similar.[47] And a Korean study comparing the outcome of laparoscopic right to open right CME showed a better 5-year OS rate in the laparoscopic group compared with the open group (77.8% vs. 90.3%, p = 0.028) and a similar 5-year DFS rate (71.8% vs. 83.3%, p = 0.578).[48] Yamamoto et al's randomized trial confirmed that the laparoscopic group has a lower complication rate as well as shorter hospital stay.[49]

For proximal right- and left-sided tumors, laparoscopic CME can be performed with safety and good oncological outcome. However, for tumors located near the flexures or in the transverse colon, the open approach is still the standard.[50] The bottom line is that the outcome benefits are dependent on accuracy and completeness of the surgical procedure. Learning curve continues to be long, as evident from data on the need to convert from laparoscopic surgery to open surgery. A focus on better training is key to replicating study results in the real world.

Conflict of Interest

None declared.

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Artikel online veröffentlicht:
02. Januar 2025