The tunnel approach versus medial approach in laparoscopic radical right hemicolectomy for colon cancer: A retrospective cohort study

Background: Although Multiple studies showed that the median approach is nowadays the most widely accepted approach according to the “no-touch” principle and safety. However, this approach is a demanding procedure with a steep learning curve and has a high rate of conversion to laparotomy. This aim is to explore the feasibility and safety of tunnel approach in laparoscopic radical right hemicolectomy for colon cancer. Methods From July 2016 to October 2018, a total of 106 consecutive patients with colon cancer who were subjected to the laparoscopic radical right hemicolectomy in the affiliated cancer hospital of zhengzhou university were enrolled. The patients underwent either tunnel approach (TA) (n=56) or traditional medial approach (MA) (n=50) according to the surgical maneuver performed. The patients' baseline demographics and perioperative results were compared between the two groups. Results: The baseline characteristics did not differ between groups. The blood loss was significantly less [20.0(5.0-40.0) vs. 100(50.0-150.0) , p < 0.001] and operation time was significantly shorter [128.4±16.7 vs. 145.6±20.3min, p < 0.001]in the TA group than those in MA group. Time to first flatus and postoperative hospital stay were similar [3.0(2.0-4.0) vs. 3.0(3-4.0)dp=0.329; 10.4±2.6 vs. 10.7±3.0dp=0.506] in both groups. The conversion to laparotomy and complication rates were similar between the groups(0 vs. 6.0%, p = 0.203; 14.3% vs. 18.0%, p =0.603,respectively). There was no treatment-related death in both groups. Conclusions: The tunnel approach in laparoscopic radical right hemicolectomy for colon cancer is a technically feasible and safe procedure as a preferable approach at present compared to those of medial approach, meanwhile this method is easier for beginners to master. Hence this tunnel approach right hemicolectomy is worth recommended.


Introduction
Laparoscopic right hemicolectomy was first recommended by Since Jacobs et al [1] in 1990s, laparoscopic radical right hemicolectomy has become the standard procedure for the treatment of right-sided colon cancer with better short-term outcomes and comparable effectivity and safety compared with laparotomy [2][3][4] . Hohenberger et al [5] also recommended the concept of complete mesocolic excision (CME) with high arterial ligation in 2009. Recent studies have confirmed that CME approach can obtain more thorough lymph node dissection and better oncological outcomes, without increasing the risk of complications [6][7][8] .
Although Multiple studies showed that the various approach being acceptable currently achieve different advantages respectively, the median approach is nowadays the most widely accepted approach according to the "no-touch" principle and safety [9][10][11][12][13] . However, the medial-to-lateral approach laparoscopic right hemicolectomy is a demanding procedure with a steep learning curve and has a high rate of conversion to laparotomy, the main reason is anatomic complexity numerous variation of right colonic vessels [14,15] . Thus, we design the tunnel type lower right approach to finish the complete mesocolic excision (CME) based on the operation idea of "Easier surgery" and have achieved satisfactory clinical results [16] . The aim of this study is to compare the surgical feasibility and safety with this new surgical approach performed.

Search strategy
A total of 106 consecutive patients with colonic cancer who underwent the laparoscopic radical right hemicolectomy were included in the affiliated cancer hospital of zhengzhou university from July 2016 to October 2018. The patients underwent either tunnel approach (TA) (n=56) or traditional medial approach (MA) (n=50) according to the surgical maneuver performed at that time. Inclusion criteria: 1)Eligible patients were diagnosis as right-sided colonic cancer with clinical stage I-III at preoperative examination by colonoscopy and abdominal enhanced computed tomography (CT); 2)Single tumor in ileocecum, ascending colon, hepatic flexure or right transverse colon; 3)Tumor size ≤10 cm in the intraoperative laparoscopic exploration; 4) Diagnosis with adenocarcinoma of the colon were considered; 5) The tumor did not invade adjacent organs. Exclusion criteria: 1) Patients have received the neoadjuvant therapy; 2) Patients with distant metastases confirmed by imaging; 3) Preoperative symptoms of intestinal obstruction; 4) Laparoscopy cannot be tolerated due to the other organ dysfunction. We used the NCCN guidelines for colon cancer (v.1.2019) [17] to evaluate TNM staging.
The study was conducted in accordance with the principles of the Declaration of Helsinki, and the study protocol was approved by the ethics committee of affiliated cancer hospital of zhengzhou university. Because of the retrospective nature of the study, patient consent statement is waived.

Fourth: expose and incise the blood vessels along trunk of the superior mesenteric artery and vein
The ileocolic mesenteric avascular zone was incised below the ileocolic vessel, the root of ileocolic vessel was exposed from the right side of the superior mesenteric vein. Then the ileocolic artery and vein, right colonic artery and vein, middle colonic artery(or its right branch) and vein and gastric colon vein trunk (or its colonic branch) were exposed and divided along the trunk of the superior mesenteric artery and vein(Each patient may has the different vascular variant) figure 4 and 5

Last: remove the specimen completely and digestive tract reconstruction
The lateral peritoneum was dissociated sharply along the paracolic sulcus of ascending colon, then the specimen was removed completely. An approximate 6 cm incision was made approximately 2 cm

MA Group: 50 patients underwent the traditional medial-to-lateral approach (1) Expose and incise the mesenteric vessels
The ascending mesocolon is incised along the left side of the superior mesenteric vein at the root of the ileocolic vascular to enter Toldt's gap. Then dissected cephalad along the superior mesenteric vein until the lower edge of pancreatic neck with crossing the front of the horizontal segment of duodenum and pancreatic uncinate. Then the ileocolic artery and vein, right colonic artery and vein, middle colonic artery (or its right branch) and vein and gastric colon vein trunk (or its colonic branch) were exposed and divided along the trunk of the superior mesenteric artery and vein. So far, the dissection of the right mesenteric vessel and surrounding lymph nodes has been completed.

(2) Dissociate of mesocolon completely
The ascending mesentery was incised close to the right side of the mesenteric vein to enter the Toldt's gap. then dissociated Toldt's gap rightwards until the right white line of Toldt, cephalad until the root of transverse mesocolon with crossing the junction of duodenal descending and horizontal segments, caudalwards until the root of the ileal mesentery. Thus, the right colonic mesentery was separated from retroperitoneum completely.

(3) Dissociate colonic lateral peritoneum
The gastrocolic omentum was incised at the place where the transverse colon is pre-resected, the hepatic flexure was dissociated rightwards (Notices are the same as TA Group). The right white line of Toldt was incised caudalwards from the hepatic flexure to the cecum, the right colon and its corresponding mesentery were dissociated completely.

(4) remove the specimen completely and digestive tract reconstruction
The operation was performed as the same as the procedures in the TA group.

Statistical analysis
All statistical data was analyzed with SPSS 22.0. The continuous variables were expressed as the mean ± standard deviation (SD) with using the t test or the median ( interquartile range (IQR)) with using the rank-sum test between groups according to Whether they fit the normal distribution. Chi-square test or Fisher's exact test was used for categorical variables. We define the p value < 0.05 as a statistically significant difference.

Operative outcomes
All 106 cases were completed laparoscopic radical right hemicolectomy successfully and confirmed R0 resection by postoperative pathology results. The mean operative time had a significant advantage in the TA group compared with MA group (128.4±16.7 vs. 145.6±20.3min, p 0.001).
Meanwhile, intraoperative blood loss was significantly lower in the TA group than in the MA group [20.0(5.0-40.0) vs 100(50.0-150.0) ml, p < 0.001]. There was no statistically significant difference in tumor size and lymph node yield. There were three patients (6.0%) required conversion to laparotomy only in the MA group, the reasons were severe adhesion in one patient and intraoperative uncontrolled intraoperative bleeding in two patients. (Table 2) Postoperative recovery

Discussion
In the 1980s, proximal and distal margins of the colonic tumor should be resected at least 5-10cm long with corresponding mesenterium according to JGR [18] . Hohenberger et al [5] also recommended the concept of complete mesocolic excision (CME) in 2009, CME has become a standard procedure as a novel concept for colectomy.
Laparoscopic right hemicolectomy could be performed with less bleeding, less trauma, rapider recovery of gastrointestinal function and shorter postoperative hospital stay compared with traditional laparotomy [19] . But mastery of the laparoscopic approach demanded a steep learning curve [20] . Therefore, numerous studied explored different surgical approaches and tried to find a better one. Jie Ding et al shown that the medial approach is a preferable approach at present [21] .
Kuzu et al [22] showed different variation of right colonic vessels is an important reason for the long learning curve of laparoscopic approach. For experienced surgeon, it is not difficult to expose the superior mesenteric vein completely, but it is hard for beginners to master. Dissecting the root of the right gastroepiploic artery is very difficult in the medial approach with causing the hemorrhage and more serious consequences. During the laparoscopic right hemicolectomy, it is the key that how to enter the anatomical plane faster and more accurately to expose the gastrocolic trunk. We summarize the tunnel operation method on the basis of various clinical procedures [23,24] . The tunnel method starts from the attachment of ileocecal region and the retroperitoneal, so that Toldt's gap can be entered easily the regardless of their bodily form. This approach can also prevent beginners from dissociating superior mesenteric vessels at first. This tunnel approach is to convert the anatomy from two-dimensional to three-dimensional, so the superior mesentery vessels were exposed more easily after dissociating right mesentery completely, which reduces the risk of bleeding and conversion rate and is easier for beginners to master.
In the present study, intraoperative blood loss and operation time in TA group were Significantly better than those in MA group. Although there was no statistical significance, the conversion and postoperative major complication rates were lower in the TA group compared with the MA group in the present study. Reduced risk of severe complications and conversion is potential advantages of tunnel approach laparoscopic colectomy compared with medial approach. Meanwhile the difference may be caused by a small sample size, which needs to be further confirmed by large sample studies.
Conversion rates in randomized controlled trials comparing laparoscopic with other approaches colectomy ranged from 0% to 18.1% [25][26] . The cause of conversion in laparoscopic colectomy for cancer included tumor invasion, abdominal adhesions, intraoperative bleeding, anatomical complexity and so on [27][28][29] . Tarnowski et al [30] showed the main cause of conversion is local tumor progression.
In the present study, two of the three conversions due to uncontrolled bleeding occurred during dissection of superior mesenteric artery, which is considered a complicated operation in laparoscopic procedure. The difference between the results of the study and the results of previous studies may also be caused by insufficient sample size.
We should pay attention to the following points during the operation: 1. Don't dissociate too deeply to avoid injuring ureter and gonad vessels in the procedure; 2. After entering the Toldt's gap, the ultrasonic scalpel dissociates the complete anatomical plane close to the mesocolon. 3. Adopt the blunt dissociation mainly and sometimes sharp dissociation to protect duodenum carefully. 4. When dissociating liver flexure, avoid entering Gerota fascia to injure the right kidney by putting a gauze at the root of the transverse mesocolon.
Meanwhile, this study is subject to several limitations. Firstly, observation or nonexperimental method are the inherent weaknesses of retrospective design. Secondly, the findings may lack generalizability due to the relatively small number of cases. The long-term outcomes of randomized clinical trials require further confirmation with large number of cases and multicenter studies.

Conclusion
This study suggests that the tunnel approach in laparoscopically assisted radical right hemicolectomy is a technically feasible and safe procedure. It can significantly reduce the operation time and intraoperative blood loss, and has the advantages of lower conversion and complication rates and shorter learning curve compared with traditional middle approach in laparoscopic right hemicolectomy. Therefore, this new surgical approach in right hemicolectomy is recommended.

Ethics approval and consent to participate
The study was conducted in accordance with the principles of the Declaration of Helsinki, and the study protocol was approved by the ethics committee of affiliated cancer hospital of zhengzhou university. Because of the retrospective nature of the study, patient consent statement is waived.

Availability of data and materials
Data are available on reasonable request from the authors.

Competing interests
The authors declare that they have no competing interests

Funding/Support
We have received no funding for this study. 28  TA tunnel approach, MA medial approach.   TA tunnel approach, MA medial approach, IQR inter-quartile range. Figure 1 separate the attachment of the terminal ileum from the posterior peritoneum