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ABSTRACT Anastomotic leakage after intestinal resection is one of the most serious complications of surgical intervention for hollow viscus injury. Adequate vascular perfusion of the

anastomotic site is essential to prevent anastomotic leakage. Near-infrared imaging using indocyanine green (NIR-ICG) is useful for the objective assessment of vascular perfusion. The aim of

this study was to evaluate the association of NIR-ICG with intestinal and mesenteric injuries. This was a retrospective, single-center study of patients undergoing surgery for intestinal

and mesenteric injuries. NIR-ICG was used to evaluate vascular perfusion. Postoperative complications were assessed between NIR-ICG and non-NIR-ICG groups.The use of NIR-ICG was associated

with a lower incidence of Clavien-Dindo grade ≥ III complications with a statistical tendency (p = 0.076). When limited to patients that underwent intestinal resection, the use of NIR-ICG

was significantly associated with a lower risk of perioperative complications (p = 0.009). The use of NIR-ICG tended to associate with the lower incidence of postoperative complications

after intestinal and mesenteric trauma surgery. NIR-ICG was associated with a significantly lower risk of complications in patients undergoing intestinal resection. The NIR-ICG procedure is

simple and quick and is expected to be useful for intestinal and mesenteric trauma. SIMILAR CONTENT BEING VIEWED BY OTHERS ASSESSMENT OF GASTRIC POUCH BLOOD SUPPLY WITH INDOCYANINE GREEN

FLUORESCENCE IN CONVERSIONAL AND REVISIONAL BARIATRIC SURGERY: A PROSPECTIVE COMPARATIVE STUDY Article Open access 06 June 2023 ADDED VALUE OF POSITIVE INTRALUMINAL CONTRAST CT OVER

FLUOROSCOPIC EXAMINATION FOR DETECTING GASTROINTESTINAL LEAKAGE AFTER GASTROINTESTINAL SURGERY Article Open access 10 January 2024 INFLUENCE OF INTRAOPERATIVE VASOPRESSOR USE ON INDOCYANINE

GREEN FLUORESCENCE ANGIOGRAPHY: FIRST EVALUATION IN AN EXPERIMENTAL MODEL Article Open access 06 May 2021 INTRODUCTION Early surgical intervention is essential for the management of hollow

viscus injury (HVI). A delay in diagnosis and treatment results in peritonitis, hemodynamic instability, and increased mortality and morbidity rates1,2,3,4. However, because the incidence of

HVI after blunt abdominal trauma is low, surgeons have limited experience in managing these injuries5. Surgical interventions for HVI are associated with several complications. Anastomotic

leakage (AL) after intestinal resection, especially colocolic or colorectal anastomosis, is one of the most serious and potentially life-threatening post-operative complications which has

been reported to occur in 2.5%–6.6% of colonic injuries6,7. Adequate vascular perfusion to the anastomotic site is important to prevent AL8,9. One technique commonly used to assess regional

intestinal vascular perfusion is subjective clinical assessment by the surgeon performing the procedure, including evaluation of the color of the serosa and mucosa, bleeding at the bowel

edge, beating of the mesenteric vessels, and bowel peristalsis. However, the accuracy of this method is limited as it is strongly influenced by the surgeon's personal experience and

other external factors10. Further, subjective assessment of vascular perfusion may be difficult during acute mesenteric ischemia, and the accuracy of intestinal survival prediction using

only clinical criteria was as low as 57.7%11,12. In contrast, near-infrared (NIR) imaging using indocyanine green (ICG) (NIR-ICG) is useful for the objective assessment of vascular

perfusion13. The use of this tool could increase the accuracy of assessment of vascular perfusion status and reduce complications compared to clinical assessment. To our knowledge, however,

there have been no reports on the effectiveness of NIR-ICG to prevent complications associated with intestinal and mesenteric injuries. Thus, the aim of this study was to evaluate the

association of NIR-ICG with postoperative complications after surgery for intestinal and mesenteric injury. RESULTS Among the trauma patients transported to our hospital, 37 patients with

abdominal trauma who required surgery for intestinal or mesenteric injury were included in this study. The NIR-ICG group included 11 patients, and the non-NIR-ICG group included 26 patients.

The baseline characteristics of both groups are presented in Table 1. As the prevalence of male trauma cases was three times higher than that of females, NIR-ICG was only used in male

patients. There was no difference in the mechanism of injury or the type of trauma between the two groups, and the AAST grade was significantly higher in the NIR-ICG group (p < 0.01).

Regarding vital signs on admission, heart rate was higher in the non-NIR-ICG group, but there was no difference in indicators of circulatory failure including systolic blood pressure, base

excess, or lactate levels between the two groups. The sites of trauma were the colon (one patient), small bowel (2 patients), colon and mesenteric hematoma or injury (5 patients), small

bowel and mesenteric hematoma or injury (13 patients), mesenteric hematoma or injury (15 patients), and small bowel, colon and mesenteric injuries (one patient). Regarding AAST grading for

small and large bowel injury, there were 16, 4, and 2 cases of grade 2, grade 3, and grade 5 injuries, respectively. Table 2 summarizes the postoperative complications of the NIR-ICG group

and the non-NIR-ICG group. The overall rate of Clavien-Dindo (CD) grade ≥ III complications was 24.3% (9/37) and all cases were in the non-NIR-ICG group (p = 0.036). The complications

included surgical site infection (SSI) in 4 cases, paralytic ileus in 2 cases, AL in 1 case, adhesive obstruction and short bowel syndrome (SBS) in 1 case, and pancreatic fistula in 1 case.

Pancreatic fistula was caused by pancreatic injury and was excluded when examining the efficacy of NIR-ICG used to assess intestinal vascular perfusion. When limited to intestinal-related

complications, the incidence of CD grade ≥ III was 21.6% (8/37), and all the cases occurred in the non-NIR-ICG group (p = 0.076). When limited to intestinal complications, the rate of CD

grade ≥ II complications was 16.2% (6/37), and all cases occurred in the non-NIR-ICG group (p = 0.151). The complications included paralytic ileus in 4 cases, AL in 1 case, and adhesive

obstruction and SBS in 1 case. Seventeen patients required intestinal resection. All complications of CD grade ≥ III and intestinal complications of CD grade ≥ II only occurred in the

non-NIR-ICG group (CD grade ≥ III: 35.3% (6/17), p = 0.009; CD grade ≥ II: 23.5% (4/17), p = 0.08). In the NIR-ICG group, only one patient had CD grade I paralytic ileus, but no other

complications were observed (Table 3). There were no complications due to the use of ICG, and no patients in this group experienced a delay in oral intake or prolonged hospital stay.

DISCUSSION This study showed that the use of NIR-ICG tended to associate with the lower incidence of CD grade ≥ III complications (p = 0.076). No CD grade ≥ II intestinal complications were

observed in the NIR-ICG group. When limited to the group that underwent intestinal resection, the use of NIR-ICG significantly associated with the lower incidence of postoperative

complications (p = 0.009). Paralytic ileus was common in the non-NIR-ICG group. It is possible that a failure to identify poor vascular perfusion through subjective evaluation in this group

resulted in slowing of intestinal peristalsis and paralytic ileus. In the intestinal resection group, four cases of SSIs with CD grade ≥ II were observed. All patients were in the

non-NIR-ICG group. By evaluating vascular perfusion with NIR-ICG, it may be possible to avoid unnecessary intestinal resection and reduce the risk of SSI due to contamination. AL is one of

the most serious complications after intestinal resection for HVI, with a reported incidence of 2.5%–6.6% of all colonic injuries6,7. In addition, emergency resection is an independent risk

factor for AL (relative risk 4–6, 95% confidence interval 1.9–9.8). The presence of peritonitis is also a predictor of AL14. Since trauma patients who require emergency surgery are presumed

to be at high risk for AL, preventive measures should be implemented. Previous studies have reported that vascular perfusion is important for reducing AL8,9. Compared to the less reliable

subjective assessments12, objective confirmation of good vascular perfusion in the resected bowel stump by NIR-ICG may help prevent complications due to impaired vascular perfusion.

Considering the incidence of AL reported so far, further studies are needed to evaluate the efficacy of NIR-ICG for HVI. AL increases mortality, length of hospital stay, 30-day readmission,

and postoperative infection rates14,15,16,17. As a result, hospital costs increased by more than $25,000 in the United States17 and more than €50,000 in Europe18 when compared to low-cost

ICG. Complications, not limited to AL, doubled the length of hospital stay, increased the average total cost by $25,000, and decreases total balance and turns negative, resulting in a large

loss19. In addition, treatment of SBS requires long-term infusions, leading to an increased risk of infection and increased cost and mortality20. The same is true for SSI, which has

disadvantages such as prolonged hospital stay, increased costs, and prolonged use of antimicrobials21. We believe that the use of NIR-ICG will reduce the risk of these complications and

their associated consequences. A few studies have also investigated the use of NIR-ICG for brain injuries and burns. However, there are no reports of its use in torso trauma and to the best

of our knowledge, this is the first report using NIR-ICG for intestinal and mesenteric injury. The use of NIR-ICG has made it possible to objectively evaluate intestinal vascular perfusion,

which was previously evaluated using subjective evaluation of mucosal color, mesenteric vascular pulsation, and intestinal peristalsis8. An objective evaluation of intestinal vascular

perfusion can ensure sufficient perfusion at the intestinal anastomosis and avoid unnecessary intestinal resection, which may reduce the incidence of complications caused by intestinal and

mesenteric injuries, such as AL and SSI. In addition to improving patient outcomes, this could shorten hospital stays, reduce costs, and optimize the use of antimicrobials. NIR-ICG has

several advantages including the ability to perform rapid evaluation of vascular perfusion within 60 s in real-time using a simple technique, and the ability to record images allowing for

retrospective evaluation. Achieving hemostasis is the mainstay of treatment in hemodynamically unstable patients. NIR-ICG should be performed in patients with stable disease. The results of

this study demonstrate the feasibility of NIR-ICG in patients with intestinal and mesenteric injury with stable hemodynamics after emergency surgery. This study has several limitations worth

noting. First, this was a retrospective, single-center study; as this was not a randomized controlled trial, the selection bias could not be ruled out and we could not confirm the

effectiveness of NIR-ICG. Second, our selection of patients was based on the surgeon’s evaluation. Thus, we could not exclude the possibility of categorizing a patient that did not show any

impaired perfusion parameters and thereby, be considered a negative control in patients with normal bowel perfusion following mesenteric resection. Third, the number of included patients was

small and further studies with a large study population warranted to validate our results. In this study, the NIR-ICG group included only males, and so randomization for gender differences

is also needed. Fourth, factors other than vascular perfusion might be the cause of intestinal complications such as AL. Future studies should consider the association of other traumatic

sites, operator factors, and preoperative nutritional status on the risk of intestinal complications. Fifth, the factors affecting vascular perfusion should be considered. Although none of

the patients in the present study had undergone multiple abdominal surgeries in the past, the effect of multiple previous abdominal surgeries on the fluorescence intensity of ICG cannot be

denied. In addition, it might be necessary to examine whether the size of the resected mesentery affects vascular perfusion evaluation. Sixth, the delayed outflow type was not examined in

this study. Thus, we could not exclude the possibility of a bias, which could be attributed to a different type of perfusion mode. Seventh, a difference in the proportion of complications

among subgroups was significant but underpowered, due to a limited sample size. Finally, due to the diverse background of trauma, the protocol for using NIR-ICG has not been determined.

Therefore, multi-institutional randomized studies are needed to confirm whether NIR-ICG can reduce complications such as the AL rate in intestinal mesenteric injury. METHODS STUDY DESIGN

This was a retrospective, single-center study of patients undergoing surgery due to intestinal and mesenteric injuries from December 2006 to March 2021. This observational study protocol was

reviewed and approved by the Institutional Review Board, the Ethics Committee of the Yokosuka Kyosai Hospital (No. 18-14). The Ethics Committee of the Yokosuka Kyosai Hospital also approved

that; the requirement for written informed consent was waived; and the individual informed consent was opted out, due to a nature of retrospective study design, per the Personal Information

Protection Law and National Research Ethics Guideline in Japan. The study was conducted in accordance with the principles of the Declaration of Helsinki. The following patient data were

collected from clinical records: age, sex, vital signs, blood test results, characteristics and mechanism of injury, severity of intestinal injury, length of hospital stay, days until oral

intake and postoperative complications. The inclusion criteria were (1) cases of blunt or penetrating injuries and (2) cases diagnosed with intestinal injury or mesenteric injury before or

during surgery. NEAR-INFRARED IMAGING USING INDOCYANINE GREEN13 ICG is a water-soluble compound with a molecular weight of 774.96 Da and fluorescent properties. ICG binds to serum proteins

that are taken up by liver cells and excreted in bile; therefore, it is widely used clinically as a test drug for hepatic and circulatory functions. ICG contains iodine and is

contraindicated in patients with iodine hypersensitivity; however, it is a relatively safe reagent with low toxicity and a short biological half-life of 3–4 min in healthy adults. The rate

of allergic reaction was one per 333,000. The use of ICG for intraoperative perfusion angiography has been described previously22,23. ICG absorbs light in the NIR range of 790–805 nm, and

then reemits electromagnetic energy at 835 nm. This can be visualized by fluorescence due to the NIR irradiation13. The HyperEye Medical System (HEMS) provided by MIZUHO Medical (Tokyo,

Japan) was used at our institution. The HEMS super-sensitive optical sensor displays simultaneous fluorescence and color visible light images (Fig. 1). PROCEDURE Achieving hemostasis is the

main priority in hemodynamically unstable patients. NIR-ICG should be reserved for stable patients or during planned reoperation after emergency surgery. Intestinal resection was performed

in cases of grade ≥ 3 small bowel injury assessed using the American Association for the Surgery of Trauma (AAST) criteria. Colonic resection or stoma formation were performed in cases of

extensive colonic injury. After resection of the injured intestine, vascular perfusion at the stump was evaluated using NIR-ICG (Fig. 1a,b). Intestinal resection was performed for mesenteric

hematomas in cases of intestinal necrosis or vascular perfusion disorder. NIR-ICG was used to assess vascular perfusion where this was not clear, and in cases of intestinal strangulation by

the abdominal wall due to penetrating stab wounds. If there was a fluorescence delay, the intestine was resected (Fig. 1c,d). In the assessment of vascular perfusion, no resection was

performed for the normal flow type. In case of delayed inflow type, the area with impaired vascular perfusion compared to the surrounding bowel was resected. The delayed outflow type was not

measured in this study24. NIR-ICG was introduced into routine practice in 2013; prior to this date, the technique was used at the surgeon’s discretion. The dosage of ICG was 0.25 mg/kg. ICG

dye was injected and flushed through with 20 ml of saline, following which the ICG time was started and assessed using NIR fluorescence. Time to perfusion < 60 s was considered normal,

whereas a delay beyond 60 s or slower than the surrounding area suggested the presence of a vascular perfusion disorder requiring intestinal resection. STATISTICAL ANALYSIS All study

variables were compared between the NIR-ICG and non-NIR-ICG groups. Statistical analyses were performed using Mann–Whitney’s _U_ test for continuous variables or Fisher’s exact test for

categorical variables. A detailed analysis of cases with complications was performed, using Fisher’s exact test as well. Based on observed proportions in the study sub-group, 17 patients

guaranteed a power of 0.71 for 66% difference in a proportion of complications among two groups. All statistical analyses were performed using IBM SPSS Statistics for Windows, Version 25.0.

(Armonk, NY: IBM Corp.). Statistical significance was set at p < 0.05. CONCLUSIONS The use of NIR-ICG tended to associate with the lower postoperative complications of intestinal and

mesenteric trauma. In addition, the use of NIR-ICG was associated with lower complications with statistical significance after intestinal resection. The NIR-ICG procedure is simple and quick

and is expected to be useful in intestinal and mesenteric trauma. Further studies are needed to confirm whether NIR-ICG can reduce complications, such as the AL rate in intestinal and

mesenteric injury. ABBREVIATIONS * HVI: Hollow viscus injury * AL: Anastomotic leakage * NIR: Near-infrared imaging * ICG: Indocyanine green * NIR-ICG: Near-infrared imaging using

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Surg._ 221, e37–e42 (2015). Article  Google Scholar  Download references ACKNOWLEDGEMENTS We thank all participants for attending and working through the study protocol. We would like to

thank Editage (www.editage.com) for English language editing. FUNDING This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit

sectors. AUTHOR INFORMATION AUTHORS AND AFFILIATIONS * Department of Emergency Medicine, Yokohama City University Graduate School of Medicine, 4-57 Urafunecho, Minamiku, Yokohama, Japan

Keishi Yamaguchi, Takeru Abe, Kento Nakajima, Chikara Watanabe, Yusuke Kawamura, Tomoki Doi & Ichiro Takeuchi * Department of Surgery, Yokosuka Kyosai Hospital, 1-16 Yonegahama-dori,

Yokosuka, Japan Hirokazu Suwa, Yuta Minami, Kazunori Nojiri, Hidetaka Ono, Kenichi Yoshida & Hidenobu Masui Authors * Keishi Yamaguchi View author publications You can also search for

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inPubMed Google Scholar * Ichiro Takeuchi View author publications You can also search for this author inPubMed Google Scholar CONTRIBUTIONS K.Y., T.A., H.S., Y.M., K.N., H.O., K.Y., H.M.,

and T.D. were involved in study design, data collection and data interpretation. K.Y., T.A., K.N., C.W., Y.K. and I.T. were involved in the data analysis. All authors critically revised the

report, commented on drafts of the manuscript, and approved the final report. CORRESPONDING AUTHOR Correspondence to Keishi Yamaguchi. ETHICS DECLARATIONS COMPETING INTERESTS The authors

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CITE THIS ARTICLE Yamaguchi, K., Abe, T., Nakajima, K. _et al._ Use of near-infrared imaging using indocyanine green associates with the lower incidence of postoperative complications for

intestinal and mesenteric injury. _Sci Rep_ 11, 23880 (2021). https://doi.org/10.1038/s41598-021-03361-1 Download citation * Received: 04 September 2021 * Accepted: 01 December 2021 *

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