Minimally invasive complete mesocolic excision for right colon cancer

Abstract Complete mesocolic excision (CME) with central vascular ligation (CVL) follows the same principles as the total mesorectal excision (TME) in the rectum of following the embryological planes for right‐sided cancers. The number of lymph nodes yielded increased with a resultant improvement in the oncological outcomes and by reducing local recurrence rates. Hohenberger's radical CME and CVL and the East's modified CME with D3 lymphadenectomy, which traditionally followed the embryological plane dissection for most of its intraabdominal cancer resection, have both shown to harvest significantly higher number of lymph nodes leading to a higher overall survival rate than the traditional right hemicolectomies of the West. To achieve the oncologically superior excision of the CME, awareness of the significant vascular anatomical variation will enhance the precision of the oncosurgery as well as minimize the risk of vascular complications. There has been an increasing body of evidence emerging on the safety of minimally invasive surgery (MIS); both its oncological safety as well as complication rates in the hands of expert and trained surgeons. The surgical technique of a CME right hemicolectomy is described step by step to aid standardization. There is mounting evidence that CME + CVL/ D3 improves survival in patients with colon cancer. Whilst the technical aspect of MIS is more challenging than the left, with a standardized technique and systematic teaching method, safety and benefits for patients can be achieved.

side of the colon arises from the midgut, whilst the left arises from the hindgut. The transverse colon is composed of both structures, although more from the midgut rather than the hindgut. Over the last decade, research and publications are pointing out the differences between cancers arising from the midgut and hindgut. 4 The right colon, arising from the midgut, tends to have more flat polyps than the left, which harbors the typical garden-type polyp.
Right-sided tumors are also more likely to develop in patients with a genetic predisposition, such as those within the Lynch syndrome or microsatellite instability mutation. 5 The differing responses to chemotherapy have been published in various studies, 6,7 with the right side fairing worse than cancers arising from the left side of the colon.
Since the introduction of total mesorectal excision (TME) in the rectum after the landmark paper by Heald in 1987, 8 not only has the excision been standardized worldwide and the lymph nodes yield increased, but there has been significant improvement in oncological outcomes mainly attributed to the reduction in local recurrence rates, which, in turn, has had an impact on overall survival rates. The technique of following the embryological planes has also been adapted to right-sided cancers in the West; in a 2009 paper, Hohenberger 9 coined the term complete mesocolic excision (CME) with central vascular ligation (CVL) for this technique. The significant results from the Erlangen team showed a reduction in the 5-year local recurrence rates from 6.5% down to 3.6%, and an increase in cancer-related 5-year survival rates from 82.1% up to 89.1%. The mounting body of evidence supporting the improved oncological effects of CME cannot be ignored and in some countries, such as Germany, CME has been included in the guidelines for the treatment of colorectal cancer. 10 The Aim of this study is to describe a standardized technique and systematic teaching method to safely undertake a CME + CVL/ D3 lymphadenectomy as mounting evidence suggests its superior benefit for patients with right-sided colon cancers.

| E A S T VS WE S T
The uptake of the CME + CVL method for right-sided cancers has not been as popular in the West as TME has been for rectal cancers; this is perhaps due to its perceived higher risk of complications and technical challenges when resecting around such potentially variable vascular anatomy. 11 Traditionally, in Eastern countries such as South Korea 12 and Japan, the notion of resecting along the embryological planes whilst harvesting the lymph nodes down to its central arterial root has been a longstanding surgical method practiced by the majority of cancer surgeons.
This long-established anatomical classification of the extent of lymph node resection has been used in other intraabdominal cancer surgery, such as gastric cancer resections, 13  Following Hohenberger's 'arcade principle', the greater omentum is removed; however, in the East, only the omentum directly involved with the cancer is removed, en bloc with the tumor. The case of not removing an otherwise intact omentum arises from the fact that the arterial supply of the greater omentum is from the right and left gastroepiploic arteries (also called gastro-omental), which, in turn, arise from the gastroduodenal artery on the right and splenic artery on the left. Both these arteries ultimately derive from the celiac trunk and none of the above vessels and their corresponding draining lymph nodes are known to be associated with colon cancers. 16 Not completely removing an otherwise uninvolved omentum is also down to the important immunological and neovascularization properties of the omentum, which is well described in the literature. 17,18 In the East, the resection of the tumor, its mesentery, and the draining lymph nodes can be described as modified compared to the procedure in the West. The main aim of the operation is the harvesting of D3 lymph nodes and, to a lesser extent, the radical resection of the mesocolon; therefore, neither the duodenum nor the pancreas is mobilized fully as long as adequate lymphadenectomy is achievable. 19 During left colon cancer surgery, the colonic mesentery mobilization is similar in both the East and West. The entire mesocolon of the descending colon and sigmoid, and the splenic flexure (required for an adequate, tension-free length for the distal anastomosis) is mobilized off the retroperitoneal plane. When the surgeon dissects through the correct plane, the prerenal fat, the ureter, and gonadal vessels are not disturbed and left intact, allowing for a bloodless dissection through the intact visceral layer.
Even before the term CME was widespread, a Lancet retrospective observational study of pathologically graded colon cancer resection specimens by the Leeds team 20 published in 2008 pointed out how dissecting along the right plane could improve survival, especially in patients with stage III colon cancers, in the same way that the TME could in the rectum. The paper noted a 15% (95% CI) overall Erlangen from which the original CME and CVL paper 2 was written, compared 49 CME and CVL resection specimens for carcinoma of the colon with a series of 40 standard specimens. The CME + CVL surgery resulted in specimens with greater amounts of tissue such as the distance between the tumor and the high vascular tie was higher, the length of the large bowel as well as the ileum were longer, and the area of the mesentery was greater. The lymph node yield was significantly superior with a mean difference of 30 vs 18 (P < .001) lymph nodes harvested with each specimen. This provides further evidence that grading the plane of dissection in colon cancer may be a valid and reproducible method of specimen assessment.
In Beijing, a paper by Gao et al 22 showed results from a threeyear period on the efficacy and safety of CME. This study showed a statistically greater number of total lymph nodes retrieved in the CME group (24 vs 20, P = .002) as well as a greater area of the mesentery (both in the right colon and sigmoid resections) and tumor to high tie distance (right colon: 129 vs 113 cm; sigmoid colon: 143 vs 121 cm) without a difference in complication rates between the CME and non-CME groups.
There is a dual purpose to the radical harvesting of lymph nodes during a CME and D3 lymphadenectomy down to its arterial root: the process is both for staging and therapeutic intention. The number of lymph nodes analyzed for staging colon cancers has been reported to be an independent prognostic variable outcome in itself.
The improvement in survival of patients undergoing CME has also been attributed by 'stage migration', 23 where patients are moved to a higher cancer stage postoperatively, requiring adjuvant therapy that may have been unforeseen during the preoperative staging.
The high yield of lymph nodes results in a more accurate staging of the disease. Skip lymph node metastasis has been reported to occur in up to 18% of patients, 24 where lymph node metastases do not spread in a step-wise fashion from the paracolic to the intermediate to apical nodes, but can be present in the apical node alone with no presence in the other sites.
Both the West's CME + CVL and the East's D3 lymphadenectomy yield much larger numbers of lymph nodes than standard colectomies, which has been shown to be an independent positive predictor of long-term outcomes. Colon cancer survival has been as- 5-year survival for stage II was 66% on the right compared to 70% on the left, and for stage III, it was 56% for the right and 60% for the left. But when 22 or more lymph nodes were harvested, the survival rate of right-sided cancers was improved by 20%.

| OPER ATIVE AND PERI OPER ATIVE COMPLIC ATIONS
There is significant variation of both the arterial and venous anatomy around the superior mesenteric artery, 27  The use of 3D imaging to delineate the vascular anatomy of the right colon preoperatively can provide surgeons with a precise view of the anatomy, which in turn could reduce the risk of catastrophic bleeding for patients undergoing minimally invasive surgery (MIS). 29,30 The authors agree with the published literature, that the use of preoperative imaging such as 3D-CT could aid planning of CME with D3 lymphadenectomy for right-sided colonic cancers, especially for the novice or training surgeon; however, its routine use is not common place at the authors' institution, and not seen as mandatory. With experience and a systematic approach to the root of the mesenteric vessels, any variation of vascular anatomy can be tackled safely even during MIS as long as a clear view of the operative field is maintained, which in turn allows for secure vessel control in the event of inadvertent bleeding. 5-year disease-specific survival rate (83.7% vs 94.7%, P < .001).

| TECHNIQUE S TANDARDISATION
In the 2018 review article by Hohenberger et al team, the need for teaching programs for minimally invasive CME to facilitate this technique was highlighted. 41 Once the technical challenges have been overcome with thorough education, D3 lymphadenectomy for rightcolon carcinomas will become the standard of care, with the added benefits of MIS and its safe oncological outcome.

| Positioning
The patient is laid supine on a tilt-able operating table over a nonslipping mechanism. anastomosis is to be performed extra-corporeally, only 5 mm ports are necessary; but if an endostapler is to be introduced, a 12 mm port is also required.

| Exposure
After a general laparoscopy of the peritoneal cavity, the patient is positioned head down and right side up to take advantage of the gravitational force for better exposure. The omentum is moved over the liver, pushing the transverse colon away from the SMA root in the midline.

| Vessel ligation
Identification of the ileocolic artery (ICA) root from the SMA in a thin patient is easier by looking at the grooves over the mesentery. In a more well-endowed patient, lifting the ileocecal junction will reveal the ICA tenting posteriorly towards the SMA (Figure 1). Cephalad and anterior traction on the ICA (Figure 1), RCA and MCA (Figure 2) in the midline will reveal the SMA over which the mesentery is opened to reveal the base of each artery. This will allow for the successful harvesting of the lymph nodes around the vessels' roots.   Figure 4 (front) and Figure 5 (back), the whole of the middle colic and its draining lymph nodes are harvested for the maximum oncological benefit that CME and D3 resection offers.

| Medial to lateral dissection
Once the vessels have been divided with at least two endoclips on the patient's side, tunneling under the mesentery laterally takes place by dropping the duodenum and pancreas down and lifting the colon, separating the visceral and parietal fascia along the embryological planes.
Once sufficient medial to lateral dissection has taken place, the omentum is dissected off the proximal transverse colon towards the hepatic flexure.
The terminal ileum, caecum, and ascending colon are dissected off from the lateral peritoneal reflection to meet with the free edge of the hepatic flexure superiorly and the terminal ileum inferiorly.
Caution must be taken during the medial dissection of the caecum and ascending colon as the right ureter has been known to be damaged when the mobilization plane is mistaken by a single layer.

| Division of the colon
The length of bowel to be removed is dictated by the arterial supply of the right colon in parallel with the lymphatic drainage; therefore, enough length either side of the tumor needs to be dissected free and delivered out onto the wound. The current 2019 Japanese Society for Cancer of the Colon and Rectum (JSCCR) guidelines 3 for the treatment of colorectal cancer recommends 10 cm as the optimal length of resection margin, as metastasis of the pericolic/perirectal lymph node at a distance of 10 cm or more from the tumor edge is rare. In the rest of the developed world, 5 cm lateral margins have been acceptable to reduce anastomotic recurrences. 45 If the anastomosis is to be performed extra-corporeally, the tumor is delivered to the skin through a mini laparotomy with the use of a wound protector with a ready-made lid for re-laparoscopy. Once delivered, the ICA vessel division site is identified, and the terminal ileum and transverse colon are divided with enough proximal and distal-free margins. The corresponding mesentery is divided using either an energy device or traditional suture ties to secure hemostasis to the edges while not denuding the bowel edges from its mesenteric blood supply, as this will have an impact on the anastomotic healing.

| Ileocolic anastomosis
The choice of a mechanical stapler or hand-sewn anastomosis is as per surgeon preference as long as there is good supply at the bowel edges without tension. Due to the discrepancy of the diameter between the small and large bowels, a side-to-side anastomosis is favored over an end-to-end anastomosis. Care needs to be taken during bowel handling and its edges checked for bleeding when staplers are used before closure of the lumen. After a watertight anastomosis with a wide enough lumen is performed, the anastomosed bowel is returned to the peritoneum and the lid or glove put on the wound protector to restore the pneumoperitoneum for a re-look laparoscopy.
An intracorporeal anastomosis may require less mobilization and a smaller extraction site wound but a higher level of laparoscopic technique. Both bowel ends are divided with the use of the endostapler to free the bowel containing the tumor. A small entrance is made in each arm of the terminal ileum and colon through which each arm of the endostapler is introduced, and a side-to-side ileocolic anastomosis is performed. The resulting defect requires endoscopic suture closure whilst minimizing spillage of gut content into the peritoneal cavity. A two-layer continuous full thickness suture is recommended starting at the bottom of the wound to minimize spilling of bowel contents into the peritoneum.
A Cochrane systematic review on transverse vs midline incisions for abdominal surgery, 46 as well as a systematic review and meta-analysis examining the impact of incision on outcomes after abdominal surgery, 47 showed evidence to suggest that a transverse incision was superior to a vertical incision in the short-term pulmonary function as well as in long-term incisional hernia rates. During an intracorporeal anastomosis, after the specimen is freed, the extraction site can be placed on the most cosmetically suitable site, such as a Pfannenstiel or either iliac fossa transverse incisions.
Once the specimen has been delivered through a wound protector, the lid is put back on to restore the pneumoperitoneum. A final laparoscopy is performed to suction any free fluid and check for hemostasis as well as any malrotation of the returned anastomosed bowel.

| Closure
The sheath of the extraction mini-laparotomy site and the 12 mm port site are closed with strong dissolvable sutures. The wound through which the bowel was delivered is washed with saline and the skin closed with either interrupted or subcuticular dissolvable undyed sutures. A long-acting local anesthetic to all wounds will improve the pain score when the patient wakes up from the general anesthesia.

| CON CLUS ION
Both in the East and West the evidence is mounting for the radical dissection of the mesocolon along its embryological planes together with widespread lymphadenectomy to improve survival of colon cancer patients. The minimally invasive approach is not only proving to be a safe and feasible approach, but one with better shortterm recovery profiles and as oncologically beneficial as the open approach for right-sided colon cancer.
The technical aspect of the minimally invasive approach is more challenging than the left and is exposed to operator variability; however, with a standardized technique and systematic teaching method, the safety and benefits for the patient can be achieved as successfully as in the open surgical approach.

D I SCLOS U R E
Conflict of Interest: The authors certify that they have no affiliations with or involvement in any organization or entity with any financial interest (such as honoraria; educational grants; participation in speakers' bureaus; membership, employment, consultancies, stock ownership, or other equity interest; and expert testimony or patent-licensing arrangements), or non-financial interest (such as personal or professional relationships, affiliations, knowledge, or beliefs) in the subject matter or materials discussed in this manuscript.