Laparoscopic surgery has gained wide clinical acceptance in surgical practice because of its many advantages, including smaller surgical incisions, less intraoperative blood loss, faster recovery of normal bowel function, and shorter hospital stays than in the case of conventional open surgery. Because laparoscopic cholecystectomy has become the gold standard for benign gallbladder diseases, laparoscopic surgery has been applied to advanced surgical fields including colorectal cancer. Recently in colorectal cancer surgery, randomized studies have shown less invasiveness in laparoscopic surgery without compromising the oncologic outcome [1, 2]. However, despite the advantages of this procedure, there remain several disadvantages: limited images of the entire operative field under laparoscopy and a lack of tactile sensation interfere with direct manipulation by the surgeon during the procedure. For this reason, it takes a long time to identify the proper vessels where there might be major variations in each patient. Moreover, vessels and organs could be injured during lymph nodes dissection and vessel ligation under laparoscopic guidance, which leads to major complications, such as massive bleeding and bowel ischemia. Therefore, it is quite important to perform a preoperative assessment of the vascular anatomy with adjacent organs using three-dimensional (3D) computed tomographic (CT) imaging before surgery, which should be very helpful to achieve the safe and rapid ligation of vessels and dissection of lymph nodes [3, 4].

We performed multiphase contrast-enhanced examinations using multidetector-row CT (MDCT) before laparoscopic colorectal surgery. Slice data at the individual phase were converted into a 3D imaging format by using a volume-rendering technique. We previously used the fused image of 3D images of arteries, veins, the colon, organs, and tumor for preoperative assessment before laparoscopic surgery and called the utilization of 3D imaging virtual CT colectomy. In this study, we examined the usefulness of virtual CT colectomy for laparoscopic colorectal surgery.

Indications of laparoscopic colorectal surgery and operative procedure

Laparoscopic colorectal surgery is indicated for patients with early (excluding cases indicated for endoscopic mucosal resection) and advanced colorectal cancer. Exclusion criteria are bulky tumors, cancer invading other organs, and an uncontrollable cancerous ileus. In cases of early cancer invading the submucosa, intermediate lymph nodes dissection is performed. In advanced cancer, en bloc lymph nodes dissection including the apical lymph nodes along the superior mesenteric artery (SMA) or at the root of the inferior mesenteric artery (IMA) is performed depending on the tumor location. In our institution, according to oncologic principles, we use the medial approach [5], which first dissects the proximal lymph nodes and ligates the vessels and then mobilizes the bowel to lessen the risk of tumor exfoliation into the peritoneal cavity and the portal vein upstream.

CT protocol (Fig. 1)

CT images were obtained with an Aquilion MULTI scanner composed of four or 16 detectors (Toshiba Corporation Medical Systems Company, Tokyo, Japan). After a colon fiberscopy, which was routinely performed for the marking of the mucosa around the colon cancer in an endoscopy room before laparoscopic surgery, a patient who had an air-filled colorectum was carried to the CT room. A 20-gauge intravenous catheter was inserted into the right medial cubital vein. The range of contrast-enhanced CT was set to cover the area from the dome of the liver to the pubis, with reference to the scout image. Imaging was performed under the following conditions: in cases using 4-MDCT, 120 kVp, 300 mA, 0.5-s gantry rotation speed, 5.5 helical pitch, 2-mm slice thickness, 11 mm/ rotation table speed, and reconstruction intervals of 1 mm; in cases using 16-MDCT, 120 kVp, 300 mA, 0.5-s gantry rotation speed, 15 helical pitch, 1-mm slice thickness, 15 mm/rotation table speed, and reconstruction intervals of 1 mm. In the contrast-enhanced CT examination, a nonionic contrast agent (Omnipaque; Daiichi Pharmaceutical, Tokyo, Japan; 300 mg of iodine per milliliter) was infused rapidly at 5 mL/s by using an automated injector (Autoenhance A-250; Nemotokyorindou, Tokyo, Japan) in a total volume of 100 mL for patients weighing less than 40 kg, in a total volume equivalent to body weight (kg) × 2.5 mL for patients weighing 40 to 60 kg, and in a total volume of 150 mL for patients weighing more than 60 kg

Figure 1
figure 1

Time table during contrast-enhanced CT examination for colorectal cancer. Arterial phase images were obtained by using computer-assisted bolus-tracking technology, and then venous phase images were obtained at 10 or 15 s after the arterial phase; excretory phase images were obtained 300 s after the start of contrast agent injection. Slice data at the individual phase were converted by 3D reconstruction by using the volume-rendering technique. A 3D CT arteriography. B 3D CT venography.C 3D CT urography.

Arterial phase images were obtained by using computer-assisted bolus-tracking technology, which sets a region of interest in the aorta at the level of the bifurcation of the celiac artery and is designed so that imaging begins when the CT number of the region of interest is 50 HU higher than that of precontrast imaging (scanning time is ∼20 s after the start of injection). The arterial phase scan started from the dome of the liver to the pubis. Venous phase images were obtained (scanning time is ∼50 s after the start of injection) in images 10 s after the arterial phase on 4-MDCT or 15 s after the arterial phase on 16-MDCT. The venous phase scan started from the pubis to the dome of the liver (go and return). On the venous phase images, metastases distant from the lymph nodes and liver were examined. In cases of sigmoid colon and rectal cancer, excretory phase images were obtained 300 s after the start of contrast agent injection.

3D reconstruction (Fig. 1)

Slice data obtained from triple phases were transferred to a work station (WS; M900QUADRA; Zio Software Co., Tokyo, Japan), where data at the individual phase were converted by 3D reconstruction using the volume-rendering technique. The 3D CT images of arteries, veins, and ureters were reconstructed by using all voxels higher than the selected minimum threshold of 200 HU, when vessels and bones were sufficiently segmented. Then the 3D CT images of the ribs, vertebrae, and tumor were manually removed. In addition, the attenuation was set at 100% for voxels with a CT number higher than 400 to 500 HU and at 0% for voxels with a CT number lower than 100 to 200 HU. We used a linearly decreasing curve from 100% to 0% for CT numbers between 400–500 and 100–200 HU. Then, in each case, we adjusted the upper and lower cutoff CT numbers that corresponded to 100% and 0% attenuations, respectively, so that the branches of the abdominal aorta, mesenteric veins, and ureters were the most visible on the 3D image. For reconstructing the 3D air image of the colorectum at the arterial phase, we used a trapezoid curve from 100% to 0% for CT numbers between −400 and −800 HU. Then we manually selected the image of the colorectum. A 3D CT image of the arteries at the arterial phase (3D CT arteriogram) and a 3D CT image of the air-filled colorectum at the arterial phase were individually prepared and fused together (Fig. 1A). A 3D CT image of the veins at the venous phase (3D CT venogram Fig. 1B) and a 3D CT image of the urologic system at the excretory phase (3D CT urogram Fig. 1C) were prepared. The 3D CT images at different phases were then fused together. We called the use of the 3D CT images a virtual CT colectomy.

Important technical considerations during laparoscopic colectomy and use of virtual CT colectomy

Laparoscopic surgery for ascending colon and right transverse colon cancer

During surgery for ascending colon cancer or right transverse colon cancer (right hemicolectomy), the proximal portion of the ileocolic artery (ICA) and the ileocolic vein (ICV) are ligated. Then the right branch of the middle colic artery (MCA) is ligated and the draining portion of the accessory right colic vein (ARCV), which commonly drains into the Henle's gastrocolic trunk (Henle's trunk) also ligated. The MCA commonly divides into right and left branches (Fig. 2), whereas the right and left branches may originate directly from the SMA (Fig. 3). The right colic artery (RCA) frequently branches directly from the SMA, in which case the proximal portion of the RCA must also be carefully isolated and ligated during the dissection along the SMA (Fig. 2B).

Figure 2
figure 2

Three-dimensional CT arteriogram demonstrates accurately the existence and location of the RCA directly branching from the SMA. A When the RCA does not directly branch from the SMA, we ligate the proximal portion of the ICA, dissect lymph nodes along the SMA, and identify the proximal portion of the MCA along the SMA. MCA-rt right branch of MCA, MCA-lt left branch of MCA. B When the RCA directly branches from the SMA, we carefully isolate and ligate the proximal portion of the RCA during dissection of lymph nodes along the SMA.

Figure 3
figure 3

Three-dimensional CT arteriogram shows the right and left branches originating directly from the SMA.

When the ICA runs ventrally to the SMV (type A), one must carefully isolate and ligate the proximal portion of the ICA without injuring the SMV or ICV (Figs. 4A, 5). When the ICA runs behind the SMV (type B), the isolation of the ICA requires the meticulous dissection of the dorsal portion of the SMV (Figs. 4B, 6).

Figure 4
figure 4

Diagram of approaches to ligation of the proximal portion of ICA. A In the case of an ICA running ventrally to the SMV, we must carefully isolate and ligate the proximal side of the ICA without injuring the SMV or ICV running dorsally to the ICA. B In the case of an ICA running dorsally to the SMV, isolation of the ICA requires the meticulous dissection of the intermediate lymph nodes (LNs) along the ICA dorsally to the SMV

Figure 5
figure 5

Fused image of 3D CT arteriographic and venographic images and intraoperative view. A The fused image shows clearly an ICA running ventrally to the SMV, the Henle's trunk draining into the SMV, and the ARCV draining into the Henle trunk. B An intraoperative view demonstrates the ICA running ventrally to the SMV, which is similar in finding to the fused image finding. C An intraoperative view demonstrates the Henle trunk running parallel to the right branch of MCA (MCA-rt) and draining into the SMV, which is similar in finding to the fused image finding.

Figure 6
figure 6

Fused image of 3D CT arteriographic and venographic images. The fused image shows clearly the ICA running dorsally to the SMV.

Three-dimensional CT arteriogram demonstrates the precise vascular anatomy of the MCA, with the RCA directly branching from the SMA. Three-dimensional CT venogram demonstrates the accurate vasculature of the ICV, Henle's trunk, and ARCV draining into the SMV. The fused image of 3D-CT arteriographic and venographic images simultaneously shows these arteries and veins.

Laparoscopic surgery for cancer of the left transverse colon and descending colon

During surgery for the left transverse colon and descending colon cancer (left hemicolectomy), the left branch of the MCA is commonly isolated and ligated. The accessory left colic artery (ALCA), also known as the Riolan artery, frequently originates from the SMA and runs toward the splenic flexure along the lower border of the pancreatic body [6]. In case the left transverse colon is fed by the ALCA, on only has to isolate and ligate the ALCA and preserve the MCA (Fig. 7). During left hemicolectomy, the proximal portion of the left colic artery (LCA) is isolated and ligated. In case the sigmoid artery (SA) branches from the LCA, the LCA should be ligated just distal to the junction with the SA (Fig. 8).

Figure 7
figure 7

Three-dimensional CT arteriogram shows that the left transverse colon tumor is fed by the ALCA, known as the artery of Riolan, which originates from the SMA and running below the pancreas. On the basis of 3D CT arteriogram, we can isolate the proximal portion of the ALCA as the feeding artery (dotted line) and preserve the MCA. P pancreas.

Figure 8
figure 8

Three-dimensional CT arteriogram shows that the left transverse colon tumor is fed by the ALCA and the LCA originating from the IMA. Moreover, it shows SAs branching from the LCA. On the basis of 3D CT arteriography, we can isolate the proximal portion of ALCA (upper dotted line) and the LCA (lower dotted line) distal to the branching portion and preserve the SAs.

Three-dimensional CT arteriogram demonstrates accurately these vascular anatomies including the ALCA, LCA, and SA.

Laparoscopic surgery for sigmoid colon and rectal cancer

During sigmoidectomy, in case the SA feeds the tumor-bearing segment, the SA is selectively isolated and ligated, and the LCA and superior rectal artery (SRA) can be preserved. In contrast, during surgery for rectal cancer, we usually dissect the proximal lymph nodes and preserve the LCA (Fig. 9). The SA branches from the LCA or SRA. The left ureter and left gonadal vein run close to the proximal portion of SA; the SA must be carefully isolated and ligated without injuring the ureter and gonadal vein during sigmoidectomy (Figs. 10, 11). Moreover, the inferior mesenteric vein (IMV) may run near the LCA. The LCA is usually preserved during the resection of sigmoid colon and rectal cancer; therefore, the IMV must be carefully ligated without injury to the LCA (Fig. 12).

Figure 9
figure 9

Three-dimensional CT arteriogram and intraoperative view. A A 3D CT arteriogram demonstrates the sigmoid colon tumor fed by the SA branching from the LCA. B In reference to the 3D CT arteriographic finding, we accurately isolate and ligate the proximal portion of the SA and preserve the LCA and SRA.

Figure 10
figure 10

Fused image of 3D CT arteriographic and urographic images. A Image shows the sigmoid tumor fed by the SAs. B Image demonstrates the left ureter running near the proximal portion of the SA. From this finding, we carefully isolate and ligate the proximal portion of SAs without injuring the ureter.

Figure 11
figure 11

Fused image of 3D CT arteriographic and venographic images. Image demonstrates the gonadal vein running near the SA. From this finding, we carefully isolate and ligate the origin of SA without injuring the gonadal vein.

Figure 12
figure 12

Fused image of 3D CT arteriographic and venographic images. The image demonstrates the IMV running near the LCA. From this finding, we carefully ligate the IMV without injuring the LCA.

Three-dimensional CT arteriogram demonstrates the precise vascular anatomy of the SA and the feeding artery. Moreover, the fused image of 3D-CT arteriographic and venographic or urographic images shows simultaneously the branches of the IMA, ureter, gonadal vein, and IMV and are useful for the demonstration of their anatomical relations.

Simulated and navigated surgery for virtual CT colectomy

On the basis of virtual CT colectomy, we can isolate and ligate vessels and resect the colon and rectum with the tumor on a WS as simulated surgery (Fig. 13). This technique is quite useful for deciding and confirming the operative procedure, particularly among the surgical staff. Moreover, it is very useful to explain the individual surgical approach to the patient and family.

Figure 13
figure 13

Three-dimensional CT image at arterial phase and the resected macroscopic specimen. A, B On the WS, we ligate the proximal portions of the ICA (red dotted line) and MCA-rt (blue dotted line) and resect the ascending colon and tumor in simulated surgery. The macroscopic specimen (D) removed by laparoscopic surgery is consistent with the 3D image (C) of the resection performed in simulated surgery.

In our institution, surgeons previously performed laparoscopy by referring to hard copies of 3D CT images at limited angles. However, they were often required to observe the 3D CT images at optimal angles depending on the operative field during laparoscopy. Therefore, we reconstructed 3D CT images on a WS with a grid computing system. In the operating room, by using a grid computing system, surgeons could easily observe, tilt, and rotate the 3D CT image depending on the operative field in the personal computer connected to the WS through a LAN cable far from the WS, which can support a safe and rapid performance of lymph nodes dissection and vessel ligation under laparoscopy (Fig. 14).

Figure 14
figure 14

Intraoperative navigation. Surgeons can easily observe, tilt, and rotate the 3D CT image in real time by using a grid computing system, depending on the operative view in the personal computer connected to the WS through a LAN cable in the operation room far from the WS.