When performing hemicolectomy for right-sided colon cancer, complete mesocolic excision and central vascular ligation are recommended as the standard procedures for radical lymph node dissection [1,2]. Surgical effort is usually made to ligate the vascular root of the feeding artery at the branching point of the superior mesenteric artery (SMA). When the ileocolic artery (ICA) root is retrieved while dissecting the anterior chamber of the superior mesenteric vein (SMV), the ICA is easily found on the right side of the SMV [3]. Rarely, the ileal branch of the SMA might travel across the behind of the SMV to the right colon and could be confused with the ICA. If the ileal branch of the SMA is mistaken for the ICA, unintentional ligation could cause long-segment ischemia in the ileum. We encountered a rare case of ileal ischemia which was caused by unintentional ligation of the ileal branch of the SMA during laparoscopic right hemicolectomy and confirmed by indocyanine green (ICG) angiography and hyperspectral imaging (HSI).

A 72-year-old woman was diagnosed with a hepatic flexure cancer. Preoperative computed tomography (CT) revealed an ulceroinfiltrating mass at the hepatic flexure of the right colon and enlarged pericolic lymph nodes (cT3N1M0). On the serial coronal reformatted CT images during portal venous phase, the ileal branch of the SMA (red arrows in Fig. 1) runs across the SMV forward to the cecum. And then, that ileal branch travels downward into the distal ileum (Fig. 1). One day before surgery, diluted ICG (Diagnogreen Inj. 25 mg; Daiichi Sankyo, Tokyo, Japan) solution (0.5 mg/mL) was injected into the submucosal layer for tumor localization and fluorescent lymph node mapping [4,5]. The patient underwent a laparoscopic right hemicolectomy on May 13, 2021. Tumor location was identified by fluorescence using a near-infrared (NIR) camera system (1588 AIM camera system; Stryker, Kalamazoo, MI, USA). Fluorescent lymph nodes which were directly connected to the primary tumor were observed around the middle colic artery (MCA). The mesentery was incised along the anterior surface of the SMV while pulling the transverse colon and cecum upward laterally. One mesenteric arterial branch passed across the behind of the SMV toward the cecum; therefore, this artery was considered the ICA. The artery directing to the ascending colon was assumed to be the right colic artery (RCA). However, these vascular diameters were larger than usual, leading to suspicion of an abnormal mesenteric vascular structure. Fluorescent lymph nodes were safely removed using MCA root ligation. After ligation of ICA and RCA following complete mobilization of the right colon, a pale color change in the ileal segment was identified as a warning of ileal ischemia under white light view of conventional laparoscopic camera. For real-time assessment of bowel perfusion status, we performed additional ICG angiography and HSI. On the planned transection line in the transverse colon, favorable perfusion status was identified through ICG angiography. However, the ileal segment had unfavorable perfusion without fluorescence enhancement on ICG angiography and poor oxygen saturation ranging from 20.0% to 22.9% through HSI (TIVITA Tissue System; Diaspective Vision GmbH, Am Salzhaff, Germany) (Fig. 2). With the second ICG angiography and HSI performed on the more proximal ileum, fluorescence enhancement was still slow, and tissue oxygen saturation remained at 33.0% to 35.9%. Adequate arterial flow could maintain tissue oxygen saturation at 85.4% in the proximal ileum 60 cm from the ileocolic valve. Therefore, the third point was determined to be the modified transection line for anastomosis (Supplementary Video 1).

The total operation time was 150 minutes with an estimated blood loss of 15 mL. The resected right colon was 30.5 cm in length, and the ileum was 63.5 cm. No metastatic lymph node was found, and the pathologic tumor stage was pT3N0M0. A liquid diet was started on the second postoperative day, and the patient was discharged on the fifth day. No postoperative complications occurred.

When performing a right hemicolectomy, preservation of the main trunk of the SMA is important to preserve blood flow to the small intestine. Since the mesenteric artery to the small intestine is also considered to have sufficient collateral circulation, the perfusion status of the ileum has not been a serious concern for surgeons during right hemicolectomy. Unusually, the ileal branch of the SMA might pass behind the SMV and travel to the cecum; therefore, it could be confused with the ICA. If the collateral circulation of the jejunal and ileal artery systems is not sufficiently formed in these cases, unintended ligation of the ileal branch of the SMA can lead to catastrophic long-segment ischemia of the ileum.

In this case, the ileal branch of the SMA ran to the right side across the SMV leading to the ileum, which could be traced on the portal venous phase of the preoperative CT. It is not easy to routinely evaluate arterial branching patterns of the SMA using conventional CT in all patients. In addition, when the mesentery is pulled in the operating field, the distorted orientation of the mesenteric vasculature could increase the risk of mistaking the variant ileal branch of the SMA for the colonic artery. Therefore, if the vascular diameter is larger than that of the usual colic artery, it is necessary to make a more careful decision on vascular ligation by suspecting a variant ileal branch of the SMA. If the bowel color is pale or hypoperfusion is suspected during surgery, objective perfusion status can be evaluated using ICG angiography and HSI [6,7]. ICG angiography can visualize the dynamic perfusion status in real time, and repetitive angiography with low-dose ICG (0.02 mg/kg) allows multiple sites to be explored in the case of hypoperfusion. However, repeated intravenous injections of ICG may accumulate in the intestine prior to washing out and be mistaken for fluorescence enhancement. To compensate for these shortcomings of repetitive ICG angiography, quantitative analysis based on the dynamic fluorescence intensity-time curve can be helpful in determining perfusion status [7,8]. Currently, real-time tissue oxygen saturation levels can be easily measured using HSI in the surgical field. A tissue oxygen saturation maintained at 80% to 90% or more can be interpreted as reflecting a safe perfusion state. The development of intraoperative image analysis is expected to reduce complications that may occur due to unintentional errors made by inexperienced surgeons. In our previous study with laparoscopic low anterior resection, there was no anastomotic leak in patients with favorable perfusion segments, but the anastomotic leak rates were 11.1% to 71.4% in patients using moderate to poor perfusion segments [9]. Changing the primary planned transection line was required on 18.6% after detecting a hypoperfusion segment by the quantitative perfusion analysis of ICG angiography [10]. The drug price of ICG is only $25, and the fluorescence image is installed as an essential function on the laparoscopic NIR camera system. So, ICG angiography is expected to become a promising method for real-time perfusion assessment method that can improve patient safety to prevent the hypoperfusion-related anastomotic complication. In this case, the variant ileal branch of the SMA was mistaken for the ICA and ligated unintentionally. However, long-segment ischemia was confirmed using ICG angiography and HSI in the ileum, and the bowel segment with good perfusion was anastomosed. The patient recovered safely without complications.

In conclusion, intraoperative real-time perfusion monitoring using ICG angiography and tissue oxygen saturation monitoring using HSI may be helpful in detecting segments of hypoperfusion to prevent anastomotic complications.

Ethical statements

This study was conducted after receiving the approval of the Institutional Review Board of the Pusan National University Yangsan Hospital (No. 05-2022-127). Written informed consent was obtained from a patient.

Authors’ contributions

Conceptualization: GMS

Writing–original draft: GMS

Writing–review & editing: All authors

All authors read and approved the final manuscript.

Conflict of interest

All authors have no conflicts of interest to declare.

Funding/support

This study was supported by a 2022 research grant from Pusan National University Yangsan Hospital.

Acknowledgments

The authors would like to thank Kyung Hee Kim, RN; Hyun Seok Jung, RN; and Sung Mi Yoon, RN for technical assistance with fluorescence image-guided surgery in the surgical field of Pusan National University Yangsan Hospital.