Dorsal approach for advanced gastric cancer invading the transverse mesocolon

Abstract

Minimally invasive gastrectomy is increasingly performed for advanced gastric cancer, but the indication for this procedure for a tumor invading adjacent structures is still limited. In cases with tumors invading the transverse mesocolon, a large tumor together with the involved mesocolon blocks the surgical view, which prevents evaluation of the extent of invasion and makes it difficult to ensure oncologically adequate resection. To solve these technical issues, we established a novel method that uses a dorsal approach. By approaching the transverse mesocolon from the dorsal side, tumor penetration and involvement of the colic vessels or pancreas can be evaluated, and margin‐free resection of the tumor becomes easier. In a series of 13 patients with mesocolon invasion, a dorsal approach enabled minimally invasive margin‐free resection in 11 cases by resection of the anterior layer of the mesocolon (n = 6); enucleation of the mesocolon (n = 4); or enucleation plus distal pancreato‐splenectomy (n = 1). Two patients with broad invasion that obstructed the view underwent combined colectomy by open conversion. A major postoperative complication of pancreatic fistula following distal pancreatectomy occurred in one case. These results suggest that a dorsal approach may be useful for minimally invasive combined resection of gastric cancer invading the transverse mesocolon.

In advanced gastric cancer invading the transverse mesocolon, a large tumor together with the involved mesocolon blocks the surgical view, which prevents evaluation of the extent of invasion and makes it difficult to ensure oncologically adequate resection. A novel method that uses a dorsal approach is useful to evaluate tumor penetration and involvement of the colic vessels or pancreas and perform minimally invasive combined resection.

1. BACKGROUND

Gastrectomy with D2 lymphadenectomy and perioperative chemotherapy is a recommended treatment for advanced gastric cancer (AGC). ¹ , ² In terms of the surgical method, minimally invasive gastrectomy is becoming common, based on recent positive results in randomized controlled trials in East Asia. ³ , ⁴ , ⁵ However, these trials excluded highly advanced cases such as large type 3 or type 4 tumors, those with bulky lymph node metastasis, and tumors invading adjacent structures. Therefore, in these cases technical issues remain to be overcome for safe curative resection using a minimally invasive approach.

In invasion of gastric cancer in adjacent organs, the involved organ depends on the tumor location. An upper AGC often invades the pancreatic body or tail and can be resected with distal pancreatectomy plus splenectomy, whereas a middle or distal AGC may invade the transverse mesocolon, sometimes together with the pancreas. In cases with invasion of the mesocolon, it is important to determine the depth of invasion and if the major colic vessels or pancreas are involved. This information is needed to determine whether curative resection is possible with or without combined resection. However, accurate evaluation of the extent of invasion can be difficult laparoscopically because a large tumor and the mesocolon block the surgical view.

We showed favorable outcomes of minimally invasive gastrectomy for AGC in the KUGC04 clinical trial, ⁶ , ⁷ and we have subsequently accumulated experience in such cases. This article describes our novel technique combining an approach from the dorsal side of the transverse mesocolon with the standard approach under a ventral view. This technique allows the surgeon to obtain a better surgical view and orientation to facilitate safe resection of AGC invading the transverse mesocolon.

2. SURGICAL TECHNIQUE

The first surgical step for AGC is omentectomy to enter the omental bursa. Tumor invasion to the transverse mesocolon is usually identified during this step. After division of the omentum, the left gastroepiploic artery is divided unless the tumor has not invaded the pancreas tail. This procedure allows surgeons to roll up the stomach and widely expose its posterior side. Lifting of the stomach with the assistant's forceps, with caution not to contact the tumor directly, allows observation of tight adhesion of the anterior layer of the mesocolon to the serosal surface of the tumor (Figures 1A and 2A). At this point, the mesocolon is flipped over to expose its dorsal side and to determine if the tumor has penetrated the posterior layer. In cases with such penetration, the location relative to anatomical landmarks such as the middle colic vessels and the pancreas is also evaluated (Figure 1B,C).

FIGURE 1.

Intraoperative views of a representative case of gastric cancer invading the mesocolon. (A) Ventral view. The mesocolon is strongly adhered to the serosal invasion site of the tumor (white arrows). (B) View in the dorsal approach. The whitish scar shows that the tumor has invaded and penetrated the posterior surface of the mesocolon (black arrow). Middle colic vessels (dotted line) are spared, but invasion of the pancreas cannot be excluded at this point. (C) Anatomical landmarks for location of the tumor invasion site in a dorsal approach. The dotted circle indicates the tumor site. ARCV, accessory right colic vein

FIGURE 2.

Schematic illustrations of the dorsal approach. (A) The stomach is rolled up to expose the tumor site on the posterior wall where the mesocolon is tightly adhered. (B) Dorsal view of the tumor invasion site. The mesocolon is divided to secure a margin from the tumor on the distal side. The stomach wall is seen from the opened window. (C) Ventral view after partial division of the mesocolon. The tumor penetration site can be seen from the window. (D) The proximal side of the mesocolon is divided with an appropriate margin to complete enucleation. The anterior layer of the mesocolon is dissected to expose the posterior layer on the right side of the tumor invasion site. (E) The pancreas body is exposed after completion of enucleation of the involved mesocolon

If tumor invasion is limited and the colic vessels are spared, curative resection can be achieved with enucleation of the involved mesocolon. The mesocolon is first divided at the distal part of the tumor‐invaded area under a dorsal view (Figures 2B and 3A). The standard ventral view improves after this procedure because the mesocolon is half taken down (Figures 2C and 3B). For a tumor located in the lower third of the stomach, the anterior layer of the mesocolon on the right side is resected to expose the posterior layer and middle colic vessels. Then, the proximal part of the mesocolon is divided with appropriate margins to complete enucleation of the mesocolon (Figures 2D and 3C,D). After enucleation, the stomach can be lifted with the resected mesocolon, unless the tumor has also invaded the pancreas (Figure 2E, Video S1). After the tumor is separated, infrapyloric lymph nodes (#6) are dissected. Superior mesenteric vein (SMV) lymph nodes are also dissected in cases with clinical lymph node metastasis at the #6 station or with lower‐third gastric cancer. The details of the subsequent D2 lymphadenectomy have been described elsewhere. ⁶ , ⁸

FIGURE 3.

Intraoperative views of a case undergoing enucleation of the mesocolon. (A) The mesocolon is partially divided on the distal side of the tumor invasion site in a dorsal approach (dotted circle). The posterior wall of the stomach is seen through the opening. (B) Ventral view. A gauze inserted into the opened window (dotted circle) from the dorsal side is pulled out. The posterior side of the mesocolon is seen through the window. (C) The mesocolon is divided on the proximal side of the tumor invasion site with an appropriate margin. (D) Enucleation is completed. The anterior layer (*) of the mesocolon is resected while the posterior layer (**) is preserved

If a dorsal approach reveals that the tumor has infiltrated a large area, including the distal pancreas, combined distal pancreatectomy is required to accomplish curative resection (Figure 4A,B). In these cases, the pancreas tail is mobilized using a dorsal approach after dividing the inferior mesenteric vein (Figure 4C). Following opening of the mesocolon at an intact area, the mesocolon is further divided with an appropriate margin to identify the pancreas under a ventral view (Figure 4D). Enucleation of the mesocolon together with the distal pancreas frees the transverse colon. Following mobilization of the spleen, curative resection is performed by total gastrectomy plus distal pancreato‐splenectomy with enucleation of the mesocolon.

FIGURE 4.

A case with invasion of both the mesocolon and distal pancreas. (A) A dorsal approach revealed that the tumor invaded a broad area of the mesocolon and involved the distal pancreas. (B) Anatomical landmarks in a dorsal approach. The dotted circle indicates the area of infiltration of the tumor. (C) The mesocolon is divided at an intact part of the mesocolon (dotted line). The stomach can be seen through the incision. (D) Operative view after division of the mesocolon and mobilization of the distal pancreas. The dotted line indicates the site of distal pancreatectomy. ARCV, accessory right colic vein

Partial colectomy is necessary in cases with involvement of the middle colic vessels. Minimally invasive combined resection of the involved colon is still possible, but a large tumor invading a broad area blocks the surgical view and accurate evaluation of the extent of invasion is difficult. In such cases, we consider open conversion. A tumor that does not penetrate the mesocolon usually only invades the anterior layer of the mesocolon. Curative resection is possible with combined resection of the involved anterior layer unless the tumor has invaded the middle colic vessels.

3. RESULTS

Among 238 patients who underwent minimally invasive surgery for gastric cancer in New Tokyo Hospital from October 2018 to September 2022, tumor invasion in the transverse mesocolon was identified in 13 cases during surgery (Table 1). The dorsal approach identified no tumor penetration in six of these patients, who underwent R0 resection with combined resection of the anterior layer of the mesocolon only. In the other seven patients, tumor penetration was observed at the dorsal surface of the mesocolon. Five of these seven cases underwent minimally invasive margin‐free resection: four by enucleation of the involved mesocolon; and one by enucleation of the mesocolon with distal pancreato‐splenectomy. The other two patients underwent open conversion to total gastrectomy with combined colectomy for involvement of the colic vessels. The surgical approaches and short‐term outcomes are summarized in Table 1. A postoperative complication of Grade 3a or higher in the Clavien–Dindo classification occurred in one patient: pancreatic fistula following combined distal pancreatomy. The median postoperative hospital stay was 12 days.

TABLE 1.

Characteristics and surgical outcomes of patients

Number of patients	13
Age, median (range)	80 (70–92)
Sex (male/female)	9/4
Performance status (0/1/2)	8/4/1
Body mass index	23.9 (19.6–29.3)
Preoperative chemotherapy (no/yes)	11/2
Approach (laparoscopic/robotic)	8/5
Operation time (min)	382 (244–482)
Estimated blood loss (g)	100 (0–595)
Complications (≥Grade 3a)	1
Open conversion	2
Postoperative hospital stay (days)	12 (8–40)

4. DISCUSSION

It is difficult to diagnose invasion of gastric cancer in the mesocolon in preoperative computed tomography (CT), even with the use of multiplanar reconstruction. ⁹ Therefore, it is important to anticipate and be prepared for mesocolon invasion in surgery for patients with large tumors in the posterior wall of the stomach. There are three surgical options in such cases: anterior layer resection of the mesocolon; enucleation of the mesocolon; and combined colectomy. A dorsal approach has several advantages in selection and performance of the most appropriate option. First, the surgeon can evaluate the depth of invasion; that is, whether the tumor does or does not penetrate to the posterior layer. This information is crucial to determine the need for enucleation or colectomy. Actually, observation from the dorsal side is mandatory when T4b to mesocolon is suspected. Second, it is easier to evaluate the proximity of invasion to colic vessels because the running course of these vessels is better observed from the dorsal side. It may be difficult in very obese patients, but the roots of middle colic vessels were identified in all cases, including a patient with a body mass index of 29.3. Third, the surgeon can initiate division of the mesocolon in a distal region safely under a dorsal view, while avoiding injury to colic vessels. This initial dissection makes complete enucleation of an involved mesocolon under a standard ventral view much easier and safer because the combination of two approaches allows the surgeon to obtain a better orientation. In theory, colectomy is not needed when colic vessels are not damaged after enucleation of the mesocolon; therefore, using a dorsal approach may decrease the risk of unintended injury of colic vessels. In uncertain cases, we perform indocyanine green fluorescence angiography, and this procedure may also reduce the risk of postoperative colonic ischemia.

Anterior resection of the mesocolon is an important procedure for tumors invading the mesocolon. Traditionally, the standard operation for AGC included bursectomy, which comprises total omentectomy and resection of the anterior layer of the mesocolon. The clinical relevance of bursectomy for cT3‐T4a gastric cancer was not proven in the JCOG1001 large‐scale randomized controlled trial, ¹⁰ and partial omentectomy without resection of the anterior layer of the mesocolon is becoming more common in minimally invasive gastrectomy. However, we routinely dissect the right side of the anterior layer to expose the gastrocolic trunk and SMV in distal AGC because this procedure is needed to allow dissection of the #14v lymph node station (SMV lymph nodes). Gastric cancer in the lower third of the stomach often metastasizes to the #14v lymph nodes and some studies have shown improved survival by dissection of these lymph nodes. ¹¹ , ¹² Also, broader dissection of the anterior layer to expose the middle colic vessels and pancreas is helpful for creating the right orientation to dissect a tumor invading the mesocolon near the pancreas and/or middle colic vessels.

We applied more robotic approaches in recent advanced cases, because of its better dexterity and potential better outcomes. ¹³ , ¹⁴ We successfully applied a dorsal approach in five robotic cases by changing the table position from the 15‐degree reverse Trendelenburg's to the flat position. However, it may be difficult with the standard port setup and require additional caudal ports in some cases.

Large gastric cancer on the posterior wall can invade the mesocolon and the pancreas. In such cases, we have performed successful curative resection by laparoscopic total gastrectomy plus enucleation of the mesocolon and pancreato‐splenectomy. As we previously showed, laparoscopic combined resection is technically feasible if the surgeon can obtain a good surgical view and evaluate the extent of invasion. ⁶ , ⁷ A dorsal approach facilitates safe resection in these cases because partial division of the mesocolon using this approach improves the orientation under a better view. However, open conversion is recommended in a case in which a large tumor still blocks the view and prevents understanding of the anatomy, even after the dorsal procedure (tumor diameters in two conversion cases were 91 and 174 mm, while median diameter of the other cases was 62 mm). Finally, oncological feasibility of a dorsal approach needs to be confirmed in a longer follow‐up, although there is no local recurrence observed so far during a median follow‐up of 14.4 months.

In conclusion, a dorsal approach is useful for evaluation of the extent of invasion and facilitation of margin‐free resection of gastric cancer invading the transverse mesocolon using a minimally invasive approach.

FUNDING INFORMATION

The authors received no financial support for performance of the work and for publication of this article.

CONFLICT OF INTEREST

The authors declare no competing interests.

ETHICS STATEMENT

Approval of the research protocol: The protocol for this study was approved by the Ethics Committee of New Tokyo Hospital. All procedures were performed in accordance with the Helsinki Declaration and its later versions.

Registry and the Registration No. of the study/trial: N/A.

Animal Studies: N/A.

Supporting information

Video S1

Okabe H, Aoyama H, Miyahara Y, Sunagawa H. Dorsal approach for advanced gastric cancer invading the transverse mesocolon. Ann Gastroenterol Surg. 2023;7:678–683. 10.1002/ags3.12654