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Original Article
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 Enhancing anastomosis safety with intraoperative perfusion assessment: a visual grading system for tailoring resection and ostomy formation in sigmoid colon and rectal cancer surgery
Soo Young Oh1orcid, Seok-Byung Lim1orcid, Eu-Tteum Choi2orcid, Min Hyun Kim1orcid, Young Il Kim1orcid, Jong Lyul Lee1orcid, Yong Sik Yoon1orcid, Chan Wook Kim1orcid, In Ja Park1orcid, Chang Sik Yu1orcid
Annals of Coloproctology 2026;42(3):303-314.
DOI: https://doi.org/10.3393/ac.2025.01081.0154
Published online: June 26, 2026

1Division of Colon and Rectal Surgery, Department of Surgery, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea

2Division of Nursing, Asan Medical Center, Seoul, Korea

Correspondence to: Seok-Byung Lim, MD, PhD Division of Colon and Rectal Surgery, Department of Surgery, Asan Medical Center, University of Ulsan College of Medicine, 88 Olympic-ro 43-gil, Songpa-gu, Seoul 05505, Korea Email: sblim@amc.seoul.kr
• Received: September 8, 2025   • Revised: December 17, 2025   • Accepted: December 28, 2025

© 2026 The Korean Society of Coloproctology

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

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  • Purpose
    Anastomotic leakage remains challenging in left-sided colorectal surgery. We previously proposed a 5-grade visual grading system based on marginal vessel bleeding, indicating that good (grades A/B) to moderate (grade C) perfusion generally ensures safe anastomosis. However, borderline perfusion (grade C) carried additional risk, particularly among older patients or those with comorbidities. We refined this system to determine whether selective resection of grade C bowel could improve perfusion and guide ostomy diversion decisions.
  • Methods
    Eighty patients with left-sided colorectal cancer underwent curative-intent surgery. Intraoperatively, both marginal vessel and mucosal bleeding were assessed. Initial perfusion grade-guided decision-making: grades A/B proceeded to anastomosis, whereas for grade C, additional resection was performed to upgrade perfusion. Ostomy diversion was performed for persistent grade C or prophylactically in high-risk patients.
  • Results
    Among 80 patients, 67 (83.8%) had grades A/B and 13 (16.3%) were initial grade C. Additional resection (mean, 4.5 cm) upgraded perfusion to final grade B in 9 patients (69.2%), enabling primary anastomosis. Overall, 12 patients (15.0%) received ostomy: 4 for persistent grade C and 8 for high-risk indications despite adequate final perfusion. All 76 patients with final grade A/B achieved 0% anastomotic leakage and ischemic colitis. Grade C patients had longer operative times (108.8 minutes vs. 86.6 minutes, P=0.003) with additional procedures. Patients requiring diversion were older with more comorbidities.
  • Conclusion
    By actively applying the intraoperative visual grading system to upgrade borderline perfusion, we achieved low postoperative complication rates. This approach provides a simple and practical strategy to support intraoperative clinical judgment and optimize anastomotic safety.
  • Keywords: Colorectal neoplasms; Anastomotic leak; Perfusion; Surgical stomas
With improvements in preoperative preparation, antibiotic prophylaxis, surgical technique, and postoperative management, the safety of colorectal surgery improved dramatically over the last 50 years [1, 2]. Nevertheless, complications related to colorectal anastomosis continue to occur, and efforts to overcome such detrimental results have been ongoing. The incidence of anastomotic leakage (AL) is reported to range from 2% to 21%, and even when performed by experienced surgeons, the overall incidence of anastomotic dehiscence and subsequent leak is still 3% to 6% [1, 3, 4]. AL is associated with significant risk of both short- and long-term morbidity and mortality. Not only compromising postoperative hospital courses with devastating complications, AL decreases overall survival, cancer-specific survival, and disease-free survival [5–10]. Moreover, increased systemic and local recurrence rates have been reported in some series [11, 12].
Known unmodifiable risk factors are mostly patient-related, such as diabetes mellitus, male sex, use of tobacco, high body mass index, immunosuppressed state, malnutrition, and inflammatory bowel disease [13–15]. Additional risk factors include advanced tumor stage, more distal anastomosis and neoadjuvant pelvic radiation therapy [14, 16]. Despite multifactorial etiology of AL, tension-free anastomosis and sufficient blood supply to the terminal ends of bowel for anastomosis are 2 most well-noted factors for stable anastomosis intraoperatively [13–15, 17, 18]. These factors stem from decisions made during the operation and can be modified with greater care and precision. Although numerous advanced technical methods have been introduced to more accurately predict the perfusion of the anastomosis, particularly for the proximal colon, these new techniques are not readily applicable in most hospitals and may not be available in emergency situations. Therefore, the surgeon's decision during the operation remains the most critical factor.
We previously reported the clinical feasibility and usefulness of the 5-grade visual grading system in left-sided colorectal cancer surgery for safe anastomosis (Table 1, Fig. 1) [19]. In the study, 50 colorectal cancer patients underwent anastomosis when marginal vessels showed good (grades A/B; n=30, 60%) or moderate (grade C; n=20, 40%) perfusion state. The previous study demonstrated that patients with good perfusion (grades A/B) generally underwent anastomosis safely, whereas those with borderline perfusion (grade C) showed a potential risk of inadequate blood supply, as evidenced by one case of ischemic colitis requiring reoperation. Based on this study, we began to explore whether we could potentially upgrade the perfusion in patients with grade C, thereby minimizing the risk of anastomotic failure. Moreover, recent microcirculatory studies have demonstrated that mucosal perfusion characteristics are distinct from serosal findings, supporting the value of intraluminal assessment during colorectal anastomosis [20, 21]. Based on this rationale, we additionally assessed mucosal bleeding at the proximal colonic end to aid evaluation of mucosal perfusion, which is critical for anastomotic healing.
The purpose of this study was to evaluate the clinical feasibility and refine the application of our previously proposed visual grading system by investigating whether selective additional resection of grade C bowel could improve perfusion, while also incorporating an evaluation of mucosal bleeding at the proximal colonic end. Furthermore, we explored the characteristics of patients with poor perfusion in detail to identify suitable candidates for ostomy diversion rather than further resection, aiming to prevent complications associated with AL and potentially minimize unnecessary ostomy creation.
Ethics statement
The study protocol, including study objectives and data collection procedures, was reviewed and approved by the Institutional Review Board of Asan Medical Center (No. 2022-0618). Informed consent was obtained from all participants in accordance with institutional guidelines.
Study population
This study was a prospective observational study designed to evaluate the feasibility of the intraoperative visual perfusion grading system. To ensure uniform data collection and consistent application of the grading system, all surgeries during the 1-year study period (July 2021 to March 2022) were performed by a single experienced colorectal surgeon (SBL), who has been practicing for more than 30 years as a board-certified specialist in colorectal surgery and performs over 300 colorectal operations annually. Considering the average annual case volume of the operating surgeon, the study was initially planned to include approximately 100 consecutive eligible patients; 80 patients were enrolled and included in the final analysis. Patients were eligible if they were aged 30 years or older and had histologically confirmed sigmoid colon to rectal cancer. Patients were excluded if they underwent emergency surgery, had prior malignancy or metastatic disease at diagnosis, had a history of inflammatory bowel disease, hereditary colorectal cancer syndromes, or synchronous colorectal cancers.
The predefined primary outcome was the feasibility of the refined intraoperative visual perfusion grading system, assessed by its ability to guide additional resection or ostomy diversion decisions to optimize anastomotic perfusion. Secondary outcomes included immediate postoperative complications (such as AL, ischemic colitis, and ileus), rates of ostomy diversion, and intraoperative and postoperative characteristics including operative time, additional resection length, and hospital stay.
Tumors were classified into 3 groups based on location: sigmoid colon, rectal cancer above the peritoneal reflection, and rectal cancer below the peritoneal reflection. Prospectively collected data included clinicopathological characteristics, operative findings, intraoperative perfusion grading, short-term postoperative complications, and morbidities. All intraoperative and postoperative variables were recorded using a standardized case report form.
Operative procedure and intraoperative perfusion assessment
Conventional laparoscopic approach was preferred but some patients with history of open abdominal surgery had laparotomy. High ligation of inferior mesenteric artery was done, and inferior mesenteric vein was ligated around the inferior border of the pancreas in all cases. Systolic blood pressure of the patients was targeted between 90 to 120 mmHg by the anesthesiologists during the procedure, but permissively regulated according to the patient’s basal blood pressure. The “cutting blood pressure” was defined as the systolic and diastolic blood pressures recorded by the anesthesiologist immediately before bowel transection, at the time of marginal vessel perfusion assessment. Following transection of the distal bowel, the supplying mesenteric vessels were sequentially ligated, leaving only the marginal vessel intact. To prevent any thermal artifact that could affect the bleeding assessment, the marginal vessel was sharply divided with Metzenbaum scissors rather than by electrocautery. The perfusion of the marginal vessel was then assessed at the planned anastomosis site immediately before the transection of proximal bowel using the 5-grade visual grading system (Table 1, Fig. 1). Additionally, for proximal colonic ends, mucosal bleeding was evaluated and classified as “multiple” if bleeding was observed at 3 or more points (Fig. 2).
While the majority of patients with grade A or B perfusion underwent immediate anastomosis without ostomy diversion, additional resection was performed for grade C or D perfusion to achieve grade B or higher. Ostomy diversion was performed based on the following indications: (1) perfusion-based indication, defined as persistent grade C perfusion despite additional resection; or (2) high-risk indication, defined as prophylactic diversion in patients with adequate final perfusion (grade A or B) who had undergone preoperative chemoradiotherapy (PCRT) and/or had a low-lying rectal tumor (≤5 cm from the anal verge). The decision for prophylactic diversion was made at the surgeon's discretion based on the combination of risk factors present, including significant comorbidities. Splenic flexure mobilization was performed as needed to reduce anastomotic tension. All anastomoses were double-stapled with reinforcement sutures, and an air-leak test was routinely conducted. A closed suction drain was placed at the anastomosis site, and low-molecular-weight heparin was administered postoperatively to mitigate coagulation-related complications.
Definition of postoperative morbidities
All patients were prospectively followed for 30 days after surgery to monitor for postoperative complications, including AL. Postoperative evaluation was performed daily during hospitalization and at scheduled outpatient visits after discharge. No patient was lost to follow-up during this period. AL was defined as a clinically apparent defect in the intestinal wall integrity at the anastomosis site, confirmed by radiologic or operative findings, and accompanied by symptoms such as fever, abdominal pain, or purulent drainage. Asymptomatic radiologic findings without clinical evidence of leakage were not classified as AL. Postoperative ileus was defined by at least 2 of the following criteria: nausea or vomiting, inability to tolerate a solid diet, abdominal distension, absence of flatus for 24 hours, or radiological evidence of ileus [22]. A delayed diet was recorded when planned dietary progression was delayed by more than 3 mealtimes.
Statistical analysis
The normality of continuous variables was assessed using the Shapiro-Wilk test. Normally distributed variables are presented as mean±standard deviation and were compared using the Student t-test, whereas non-normally distributed variables are presented as median (interquartile range) and were compared using the Mann-Whitney U-test. Categorical variables were analyzed using the Fisher exact test. To identify independent predictors of postoperative complications, univariate logistic regression analysis was performed for each candidate variable. Variables with P<0.1 in univariate analysis were included in a multivariable logistic regression model to control for potential confounders. A sensitivity analysis was performed to compare outcomes between patients with initial grade A/B perfusion and those upgraded from grade C to B. All statistical analyses were performed using IBM SPSS ver. 22.0 (IBM Corp) and Python ver. 3.10 (Python Software Foundation), with a statistical significance set at P<0.05.
A total of 80 patients were included in the study. The clinicopathological characteristics of the patients are summarized in Table 2. The mean age of the cohort was 60.4±9.9 years, and 54 patients (67.5%) were male. Initially, 67 patients (83.8%) were graded as having good perfusion (grades A or B), while 13 patients (16.3%) were graded as having moderate perfusion (grade C). Patients with initial grade C were significantly older than those with initial grades A/B (65.9±7.8 years vs. 59.4±9.9 years, P=0.028). Among the 13 patients initially graded as C, 9 (69.2%) achieved grade B perfusion after additional resection and underwent anastomosis, while 4 (30.8%) remained at grade C and received ostomy diversion.
Operative characteristics according to initial perfusion grade are summarized in Table 3. Patients with initial grade C had significantly longer operative times compared with those with initial grades A/B (108.8±31.9 minutes vs. 86.6±21.9 minutes, P=0.003). There were no significant differences in procedure type (P=0.358), surgical approach (P=0.238), or cutting blood pressure between groups (both P>0.05). Mucosal bleeding patterns differed significantly, with fewer grade C patients showing multiple bleeding points (23.1% vs. 62.7%, P=0.008). Splenic flexure mobilization was performed more frequently in grade C patients, although this difference was not statistically significant (23.1% vs. 11.9%, P=0.286). Ostomy diversion was significantly more common in the initial grade C group (38.5% vs. 10.4%, P=0.010).
Among the 12 patients (15.0%) who received ostomy diversion, 4 (33.3%) had perfusion-based indications due to persistent grade C perfusion despite additional resection, and 8 (66.7%) had high-risk indications requiring prophylactic diversion despite adequate final perfusion. Of the 8 patients who received prophylactic diversion, 7 had initial grade A/B and 1 had initial grade C that was successfully upgraded to grade B. High-risk indications included PCRT with low-lying tumor (≤5 cm from anal verge) in 4 patients, PCRT alone in 1 patient, low-lying tumor alone in 2 patients, and significant comorbidities in 1 patient. The detailed characteristics of all patients who received ostomy diversion, including specific indications for each case, are presented in Supplementary Table 1. Despite the high-risk features in patients who received diversion, postoperative complication rates were comparable between the stoma and non-stoma groups (8.3% vs. 8.8%, P>0.999).
To address anastomotic safety outcomes, we distinguished between initial perfusion grade (which guided intraoperative decision-making) and final perfusion grade (which reflects the perfusion status at the time of anastomosis). The following postoperative outcome analysis was therefore performed according to final perfusion grade (Table 4). Among all 80 patients, 76 (95%) achieved final grade A/B perfusion (including 67 patients with initial grade A/B and 9 patients successfully upgraded from grade C), while 4 patients (5%) remained at grade C and underwent ostomy diversion. When comparing these 2 groups, there were no significant differences in postoperative hospital stay (5 days [IQR, 5–6] vs. 6 days [IQR, 6–7.5], P=0.059), delayed diet (0 days [IQR, 0–0] vs. 0 days [IQR, 0–1.0], P=0.439), or overall complication rates (7.9% vs. 25.0%, P=0.312), and no AL or ischemic colitis occurred in either group. To further evaluate anastomotic safety in patients who underwent primary anastomosis, a sensitivity analysis compared initial grade A/B patients (n=67) with patients whose grade upgraded from C to B (n=9) (Supplementary Table 2), and no significant differences were observed between the groups.
To identify independent predictors of postoperative complications after controlling for potential confounders, multivariable logistic regression analysis was performed according to initial grade (Table 5). In the multivariable analysis, 3 variables remained significant: age (odds ratio [OR], 0.85; 95% confidence interval [CI], 0.75–0.97; P=0.016), low anterior resection (LAR) procedure (OR, 13.01; 95% CI, 1.20–141.00; P=0.035), and initial grade C perfusion (OR, 24.86; 95% CI, 1.75–353.63; P=0.018), indicating that initial grade C classification was an independent predictor of postoperative complications. A sensitivity analysis was further performed using multivariable logistic regression in patients who underwent anastomosis (n=76, excluding the 4 patients with persistent grade C who received ostomy) to evaluate whether successfully upgraded patients had comparable risk to those with initially good perfusion (Supplementary Table 3). In this analysis, although age and LAR procedure remained independent risk factors, upgraded status (C to B) was not a significant predictor of postoperative complications compared with initial grade A/B (OR, 4.50; 95% CI, 0.69–29.15; P=0.115), suggesting that successful perfusion upgrade may mitigate the increased risk associated with initial grade C classification.
All 13 patients initially graded as C underwent additional resection of the proximal bowel to improve perfusion. The detailed characteristics of these patients are summarized in Supplementary Table 4. Patients initially graded as C were older (mean age, 65.9 years) than those with grades A/B, and those who failed to achieve grade B after additional resection were even older (mean age, 69.8 years) and had more comorbidities, such as cardiac problems and cerebrovascular diseases. The mean additional resection length was 4.5 cm, with patients achieving grade B requiring a longer mean resection (5.1 cm) compared to those who remained at grade C (3.3 cm). Splenic flexure mobilization was performed in 3 patients (23.1%), enabling further resection of up to 9 cm and resulting in successful tension-free anastomosis. Moreover, patients with multiple mucosal bleeding sites (≥3) were more likely to achieve grade B, while those with fewer sites often remained at grade C (33.3% vs. 0%). A higher proportion of patients with persistent grade C had a history of smoking (75% vs. 44%), had undergone PCRT (50% vs. 11%), and presented with advanced-stage cancer.
This study demonstrated the clinical feasibility of applying the visual grading system during colorectal anastomosis, with all 80 patients achieving uneventful postoperative recovery without anastomotic complications. The previously proposed 5-grade visual grading system was further refined by incorporating selective additional resection for “borderline” perfusion (grade C), mucosal bleeding assessment of the proximal colonic end, and individualized ostomy diversion decisions for patients with persistent poor perfusion despite further resection. Compared with our prior study, which concluded that grades A, B, and C generally allow safe anastomosis but noted an increased risk among grade C patients (including a single case of ischemic colitis), our new protocol offers a more proactive approach to upgrading colonic perfusion. In this study, we distinguished between initial and final perfusion grades for outcome analysis. Initial perfusion grade was used to guide intraoperative decision-making, including the need for additional resection or ostomy diversion. Final perfusion grade, determined after any additional resection, was used to evaluate anastomotic safety outcomes. Consequently, no AL or ischemic complications occurred in this series, highlighting the potential utility of additional resection for borderline perfusion areas.
A key differentiator from the previous pilot study is the addition of mucosal bleeding evaluation. In our earlier work, the focus was on marginal vessel bleeding alone, which does not directly assess the intraluminal mucosal microcirculation. In contrast, the current study prospectively evaluated mucosal bleeding assessment simultaneously, and the presence of multiple-point mucosal bleeding (≥3 bleeding spots) correlated with better perfusion, supporting its utility as an additional simple and practical intraoperative indicator of adequate microvascular flow. Another novel step was the implementation of selective additional resection of 3 to 5 cm of bowel to “upgrade” perfusion, readily done during the surgery. Even a short ischemic segment near the anastomosis may precipitate leakage, and a study using Doppler flowmetry showed reduced perfusion within 2 cm proximal and distal to the mesenteric division [23]. Given that the additionally resected bowel was 4.5 cm in our study, it is reasonable to conclude that removing borderline segments improves anastomotic perfusion. Moreover, the visual grading system allows for a more individualized approach to ostomy diversion in patients who remain at grade C despite resection, alongside considering clinical risk factors such as advanced age, multiple comorbidities, or a history of neoadjuvant chemoradiotherapy. Either upgrading perfusion or diverting in selected high-risk patients according to the perfusion grade resulted in zero clinically evident anastomotic leaks.
Our institution previously reported a 5.6% leakage rate for rectal cancer and a 2% anastomotic complication rate when the visual grading system was used intraoperatively [19, 24]. Although no leak was observed in the current cohort, only 10% of these patients had PCRT, and individuals at the highest risk (very low-lying anastomosis, severe comorbidities) often proceeded directly to ostomy without formal grading, potentially weakening statistical power to evaluate the effect of PCRT on perfusion [25]. This selection might attenuate direct comparisons to other studies with higher proportions of high-risk patients. Moreover, while 40% (20 out of 50 patients) were initially graded as C in the previous study, 13 patients among the 80 colorectal cancer patients (16.3%) were classified as grade C in the present study. This may be attributed to the younger average age of patients in the current study, which was 60.4 years, compared to 63.3 years in the previous study. Nonetheless, the analysis showed that age was significantly associated with perfusion grading (P=0.028), consistent with our prior finding that older age is linked to lower perfusion.
To address concerns that differences in outcomes may be confounded by patient characteristics rather than perfusion status itself, we performed multivariable logistic regression analysis. Initial grade C classification remained an independent predictor of postoperative complications (OR, 24.86; P=0.018) after adjusting for age and procedure type. However, our sensitivity analysis demonstrated that upgraded status (C to B) was not a significant predictor compared with initial grade A/B (OR, 4.50; P=0.115), and both groups achieved 0% rates of AL. These findings suggest that while initial grade C identifies higher-risk patients, additional resection to achieve grade B can effectively mitigate this risk, enabling comparable anastomotic safety despite the initial poor perfusion status. Notably, younger age was paradoxically associated with higher complication risk in this analysis (OR, 0.85; P=0.016). Although older age has traditionally been considered a risk factor for AL [26], some large database studies have reported conflicting results. Parthasarathy et al. [27], with 17,518 patients, found that younger age was an independent risk factor for AL, and Zaimi et al. [28], with 45,488 patients, similarly reported a protective effect of older age on AL (OR, 0.965 per 5 years; P<0.001), although older patients had significantly higher mortality when leakage occurred. These counterintuitive findings have been attributed to selection bias, as surgeons may preferentially perform ostomy diversion rather than primary anastomosis in older patients with significant comorbidities. In our study, older patients with initial grade C perfusion and multiple comorbidities (e.g., cardiac disease, cerebrovascular disease) were indeed more likely to receive ostomy diversion, which may explain the observed association. However, given our relatively small sample size (n=80) and low complication rate (8.8%), this finding should be interpreted with caution and warrants validation in larger multicenter studies.
For additional safety of the anastomosis, tension-free construction has long been emphasized, typically involving splenic flexure mobilization and division of the inferior mesenteric vein at the lower border of the pancreas [29]. In the present study, patients with initial grade C perfusion underwent proactive interventions to optimize anastomotic conditions, including additional bowel resection and splenic flexure mobilization when needed. The longer operative time observed in grade C patients (86.6 minutes vs. 108.8 minutes, P=0.003) may be attributable to these additional procedures performed to achieve better perfusion. Following these interventions, 69.2% of grade C patients (9 of 13) achieved grade B perfusion and were able to undergo primary anastomosis. Despite this, the overall operation duration remained shorter than reported by some other centers, and this additional effort is likely justified by the improved patient safety, particularly since many institutions routinely perform splenic flexure mobilization to minimize tension [30, 31]. Furthermore, it should be noted that perfusion assessment alone does not encompass all risk factors for anastomotic complications. In the present study, 8 of 12 patients (66.7%) who received ostomy diversion had adequate final perfusion (grade A or B) but underwent prophylactic diversion due to the presence of other established risk factors, including PCRT, low-lying tumor location, or significant comorbidities. This underscores that the visual perfusion grading system should be used as a complementary tool alongside conventional risk assessment rather than as a standalone criterion.
Another consideration is the potential use of advanced technologies, such as Doppler ultrasound, flowmetry, oxygen spectroscopy, and particularly near-infrared fluorescence imaging with indocyanine green (ICG) [32–38]. While some multicenter trials, such as the PILLAR II trial, suggest that ICG fluorescence may reduce anastomotic leaks by guiding resection margins, these benefits have not been consistently demonstrated, and the cost and equipment requirements may limit its widespread adoption [35, 39, 40]. In the PILLAR II trial, decisions regarding proximal resection were altered in 7.9% of cases [35], whereas our clinical assessment tool led to changes in 16.2% of patients (13 of 80). Kream et al. [41] reported that clinical assessment alone could achieve outcomes comparable to fluorescence angiography, with a low anastomotic leak rate (1.6%) comparable to that observed in the PILLAR II trial. Although ICG fluorescence angiography provides quantitative perfusion data, it requires specialized equipment, additional operative time, and higher cost. In contrast, the visual grading system offers an immediate, equipment-free evaluation that can be universally applied to support real-time intraoperative decision-making.
This study has certain limitations. It was conducted at a single center with a relatively small sample size (n=80), although this number was sufficient to evaluate the feasibility of the visual grading system. Anastomotic outcomes are influenced by multiple confounding factors, including anastomotic tension, infection, and patient comorbidities; therefore, the absence of complications in this cohort should be interpreted as preliminary rather than causal evidence of the system’s clinical benefit. Prophylactic stoma creation is often performed in these high-risk patients to prevent severe complications [42]. Nevertheless, by applying the visual grading system, there is potential to identify improved perfusion intraoperatively, thereby allowing more patients to safely avoid a stoma and maintain a better postoperative quality of life [43]. Furthermore, although our findings provide valuable insight into the practical feasibility and clinical applicability of this system, a formal validation of the visual grading system using an objective modality such as ICG fluorescence angiography could not be performed, as ICG imaging was not uniformly available during the study period. Subjective assessments, including perfusion grading and the newly incorporated mucosal bleeding evaluation, require correlation with objective perfusion measurements such as ICG fluorescence intensity scores to validate their reproducibility. This limitation restricted our ability to directly compare the visual grading results with quantitative perfusion data. Future multicenter studies are warranted to correlate these subjective assessments with objective perfusion measurements, thereby establishing standardized criteria and validating their clinical utility across different operators and institutions. Finally, because all assessments were performed by a single surgeon, inter-observer agreement data (e.g., κ statistics) could not be obtained. Although this single-operator design ensured consistency, future multicenter studies including multiple surgeons are warranted to evaluate the reproducibility of the grading system. Ultimately, all efforts to reduce anastomotic complications are crucial for both postoperative and oncological outcomes, demonstrating that such improvements do not always require the latest technology.
In this prospective study of 80 patients with sigmoid colon and rectal cancer, we applied the previously established 5-grade visual grading system and added mucosal bleeding assessment of the proximal colonic end to enhance intraoperative perfusion evaluation and aid surgical decision-making. Using this approach, surgeons can intraoperatively assess perfusion adequacy more objectively and make timely adjustments, such as additional bowel resection or selective diversion, thereby supporting safer anastomosis and potentially reducing unnecessary stoma formation. Future research should aim to validate these findings in larger, multicenter studies and explore the integration of visual grading with other perfusion assessment techniques to further refine surgical decision-making and improve patient outcomes.

Conflict of interest

In Ja Park is the editor-in-chief and Young Il Kim is an editorial board member of this journal, but were not involved in the peer reviewer selection, evaluation, or decision process of this article. No other potential conflict of interest relevant to this article was reported.

Funding

None.

Author contributions

Conceptualization: SYO, SBL; Data curation: SYO; Formal analysis: SYO; Investigation: SYO, SBL; Methodology: ETC, SBL; Supervision: SBL; Validation: ETC, MHK, YIK, JYL, CWK, YSY, IJP, CSY; Writing–original draft: SYO; Writing–review & editing: all authors. All authors read and approved the final manuscript.

Supplementary Table 1.

Detailed characteristics of patients who received ostomy diversion (n=12)
ac-2025-01081-0154-Supplementary-Table-1.pdf

Supplementary Table 2.

Sensitivity analysis of postoperative outcomes in patients who underwent primary anastomosis: initial grade A/B patients versus patients with upgraded status (C to B)
ac-2025-01081-0154-Supplementary-Table-2.pdf

Supplementary Table 3.

Sensitivity analysis using multivariable logistic regression analysis for postoperative complications in patients who underwent primary anastomosis (n=76)
ac-2025-01081-0154-Supplementary-Table-3.pdf

Supplementary Table 4.

Detailed characteristics of patients with initial grade C perfusion (n=13)
ac-2025-01081-0154-Supplementary-Table-4.pdf
Supplementary materials are available from https://doi.org/10.3393/ac.2025.01081.0154.
Fig. 1.
Schematic illustration of the 5-grade visual perfusion grading system. Intraoperative assessment of marginal vessel perfusion was classified into 5 grades according to the degree and color of bleeding from the divided marginal vessel.
ac-2025-01081-0154f1.jpg
Fig. 2.
Intraoperative process for assessment of marginal vessel perfusion. (A) Sequential ligation of mesenteric vessels. (B) Sharp division of the marginal vessel using Metzenbaum scissors. (C) Assessment of bleeding at the planned anastomotic site using the visual grading system. (D) Final ligation of the marginal vessel after perfusion assessment. (E) Optional intraoperative perfusion evaluation using indocyanine green fluorescence, if available. (F) Evaluation of mucosal bleeding at the proximal colonic end.
ac-2025-01081-0154f2.jpg
ac-2025-01081-0154f3.jpg
Table 1.
Visual grading system of marginal vessel perfusion assessment
Grade Definition Degree of perfusion
A Brisk, bright red, ≥1 cm projectile bleeding Good
B Bright red, pulsatile, but not projectile bleeding Good
C Two color bleeding with bright red arterial and the dark red venous blood, not pulsatile Moderate
D Only dark red venous blood is observed Poor
E No bleeding None
Table 2.
Clinicopathological characteristics of the patients according to initial grade
Characteristic Overall (n=80) Grade A/B (n=67) Grade C (n=13) P-value
Age (yr) 60.4±9.9 59.4±9.9 65.9±7.8 0.028
Male sex 54 (67.5) 43 (64.2) 11 (84.6) 0.150
Body mass index (kg/m2) 24.3±3.3 24.4±3.4 24.1±2.2 0.809
Smoking 39 (48.8) 32 (47.8) 7 (53.8) 0.688
Comorbidity
 Diabetes mellitus 9 (11.3) 9 (13.4) 0 (0) 0.161
 Hypertension 30 (37.5) 23 (34.3) 7 (53.8) 0.183
 Cerebrovascular disease 4 (5.0) 3 (4.5) 1 (7.7) 0.626
 Ischemic heart disease 5 (6.2) 3 (4.5) 2 (15.4) 0.137
 COPD 4 (5.0) 3 (4.5) 1 (7.7) 0.626
Serum cholesterol (mg/dL) 179.9±38.2 178.1±39.3 189.5±31.4 0.327
ASA physical status 0.615
 I 9 (11.2) 8 (11.9) 1 (7.7)
 II 64 (80.0) 54 (80.6) 10 (76.9)
 III 7 (8.8) 5 (7.5) 2 (15.4)
Tumor location 0.526
 Sigmoid colon 36 (45.0) 32 (47.8) 4 (30.8)
 Above peritoneal reflection 30 (37.5) 24 (35.8) 6 (46.2)
 Below peritoneal reflection 14 (17.5) 11 (16.4) 3 (23.1)
Preoperative chemoradiotherapy 8 (10.0) 5 (7.5) 3 (23.1) 0.086
T category 0.902
 Tis, T1, T2 32 (40.0) 27 (40.3) 5 (38.5)
 T3, T4 48 (60.0) 40 (59.7) 8 (61.5)
N category 0.484
 N0 44 (55.0) 38 (56.7) 6 (46.2)
 N1, N2 36 (45.0) 29 (43.3) 7 (53.8)
Preoperative CEA (ng/mL) 1.95 (1.00–3.50) 1.90 (1.20–3.60) 2.20 (0.83–2.90) 0.518

Values are presented as mean±standard deviation, number (%), or median (interquartile range).

COPD, chronic obstructive pulmonary disease; ASA, American Society of Anesthesiologists; CEA, carcinoembryonic antigen.

Table 3.
Operative characteristics according to initial perfusion grade
Characteristic Overall (n=80) Grade A/B (n=67) Grade C (n=13) P-value
Operative time (min) 90.3±24.9 86.6±21.9 108.8±31.9 0.003
Procedure 0.358
 Anterior resection 37 (46.2) 33 (49.3) 4 (30.8)
 Low anterior resection 28 (35.0) 23 (34.3) 5 (38.5)
 Ultralow anterior resection 15 (18.8) 11 (16.4) 4 (30.8)
Surgical approach 0.238
 Laparoscopic 74 (92.5) 63 (94.0) 11 (84.6)
 Open 6 (7.5) 4 (6.0) 2 (15.4)
Cutting SBP (mmHg) 115.5±41.9 117.7±45.0 104.2±16.5 0.293
Cutting DBP (mmHg) 62.8±10.9 63.6±10.7 59.0±11.6 0.171
Mucosal bleeding 0.008
 <3 35 (43.8) 25 (37.3) 10 (76.9)
 ≥3a 45 (56.2) 42 (62.7) 3 (23.1)
Splenic flexure mobilization 11 (13.8) 8 (11.9) 3 (23.1) 0.286
Ostomy diversion 12 (15.0) 7 (10.4) 5 (38.5) 0.010

Values are presented as mean±standard deviation or number (%).

SBP, systolic blood pressure; DBP, diastolic blood pressure.

aClassified as “multiple.”

Table 4.
Postoperative outcomes according to final perfusion grade
Outcome Overall (n=80) Grade A/B (n=76) Grade C (n=4) P-value
Postoperative hospital stay (day) 5 (5–6) 5 (5–6) 6 (6–7.5) 0.059
Delayed diet (day) 0 (0–0) 0 (0–0) 0 (0–1) 0.439
Complication 7 (8.8) 6 (7.9) 1 (25.0) 0.312
 Cystitis 1 (1.2) 1 (1.3) 0 (0) >0.999
 Postoperative ileus 6 (7.5) 5 (6.6) 1 (25.0) 0.272
 Anastomotic leakage 0 (0) 0 (0) 0 (0) -
 Ischemic colitis 0 (0) 0 (0) 0 (0) -

Values are presented as median (interquartile range) or number (%).

Table 5.
Multivariable logistic regression analysis for postoperative complications (n=80)
Variable Univariable analysis Multivariable analysis
OR (95% CI) P-value OR (95% CI) P-value
Age (yr) 0.90 (0.83–0.98) 0.019 0.85 (0.75–0.97) 0.016
Sex
 Female 1 (Reference)
 Male 1.22 (0.22–6.78) 0.817
Body mass index (kg/m2) 1.04 (0.82–1.32) 0.745
Smoking
 No 1 (Reference)
 Yes 1.45 (0.30–6.93) 0.643
Hypertension
 No 1 (Reference)
 Yes 0.25 (0.03–2.21) 0.214
Diabetes mellitus
 No 1 (Reference)
 Yes NA NA
Cerebrovascular disease
 No 1 (Reference)
 Yes NA NA
Ischemic heart disease
 No 1 (Reference)
 Yes 2.88 (0.28–29.99) 0.377
COPD
 No 1 (Reference)
 Yes 5.92 (0.47–75.09) 0.170
ASA physical status 2.53 (0.45–14.29) 0.295
Serum cholesterol (mg/dL) 1.00 (0.98–1.02) 0.699
Preoperative CEA (ng/mL) 1.03 (0.98–1.08) 0.247
Tumor location
 Sigmoid colon 1 (Reference)
 Above peritoneal reflection 2.41 (0.50–11.61) 0.273
 Below peritoneal reflection 0.77 (0.09–6.94) 0.815
Preoperative chemoradiotherapy
 No 1 (Reference)
 Yes NA NA
Operative time (min) 1.01 (0.98–1.04) 0.550
Procedure
 Anterior resection 1 (Reference)
 Low anterior resection 13.91 (1.58–122.46) 0.018 13.01 (1.20–141.00) 0.035
 Ultralow anterior resection 0.70 (0.08–6.31) 0.752
Surgical approach
 Laparoscopic 1 (Reference)
 Open NA NA
Initial perfusion grade
 Grade A/B 1 (Reference)
 Grade C 4.72 (0.92–24.33) 0.063 24.86 (1.75–353.63) 0.018
Mucosal bleeding
 <3 1 (Reference)
 ≥3a 1.04 (0.22–4.99) 0.960
Splenic flexure mobilization
 No 1 (Reference)
 Yes 1.05 (0.11–9.66) 0.966
Ostomy diversion
 No 1 (Reference)
 Yes 0.94 (0.10–8.58) 0.956

ORs for continuous variables represent the change in odds per 1-unit increase: age (per year), body mass index (per kg/m2), serum cholesterol (per mg/dL), preoperative CEA (per ng/mL), and operative time (per minute).

OR, odds ratio; CI, confidence interval; NA, not applicable (complete separation in logistic regression); COPD, chronic obstructive pulmonary disease; ASA, American Society of Anesthesiologists; CEA, carcinoembryonic antigen.

aClassified as “multiple.”

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        Enhancing anastomosis safety with intraoperative perfusion assessment: a visual grading system for tailoring resection and ostomy formation in sigmoid colon and rectal cancer surgery
        Ann Coloproctol. 2026;42(3):303-314.   Published online June 26, 2026
        DOI: https://doi.org/10.3393/ac.2025.01081.0154
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      Enhancing anastomosis safety with intraoperative perfusion assessment: a visual grading system for tailoring resection and ostomy formation in sigmoid colon and rectal cancer surgery
      Image Image Image
      Fig. 1. Schematic illustration of the 5-grade visual perfusion grading system. Intraoperative assessment of marginal vessel perfusion was classified into 5 grades according to the degree and color of bleeding from the divided marginal vessel.
      Fig. 2. Intraoperative process for assessment of marginal vessel perfusion. (A) Sequential ligation of mesenteric vessels. (B) Sharp division of the marginal vessel using Metzenbaum scissors. (C) Assessment of bleeding at the planned anastomotic site using the visual grading system. (D) Final ligation of the marginal vessel after perfusion assessment. (E) Optional intraoperative perfusion evaluation using indocyanine green fluorescence, if available. (F) Evaluation of mucosal bleeding at the proximal colonic end.
      Graphical abstract

      Fig. 1.

      Fig. 2.

      Graphical abstract

      Enhancing anastomosis safety with intraoperative perfusion assessment: a visual grading system for tailoring resection and ostomy formation in sigmoid colon and rectal cancer surgery
      Grade Definition Degree of perfusion
      A Brisk, bright red, ≥1 cm projectile bleeding Good
      B Bright red, pulsatile, but not projectile bleeding Good
      C Two color bleeding with bright red arterial and the dark red venous blood, not pulsatile Moderate
      D Only dark red venous blood is observed Poor
      E No bleeding None
      Characteristic Overall (n=80) Grade A/B (n=67) Grade C (n=13) P-value
      Age (yr) 60.4±9.9 59.4±9.9 65.9±7.8 0.028
      Male sex 54 (67.5) 43 (64.2) 11 (84.6) 0.150
      Body mass index (kg/m2) 24.3±3.3 24.4±3.4 24.1±2.2 0.809
      Smoking 39 (48.8) 32 (47.8) 7 (53.8) 0.688
      Comorbidity
       Diabetes mellitus 9 (11.3) 9 (13.4) 0 (0) 0.161
       Hypertension 30 (37.5) 23 (34.3) 7 (53.8) 0.183
       Cerebrovascular disease 4 (5.0) 3 (4.5) 1 (7.7) 0.626
       Ischemic heart disease 5 (6.2) 3 (4.5) 2 (15.4) 0.137
       COPD 4 (5.0) 3 (4.5) 1 (7.7) 0.626
      Serum cholesterol (mg/dL) 179.9±38.2 178.1±39.3 189.5±31.4 0.327
      ASA physical status 0.615
       I 9 (11.2) 8 (11.9) 1 (7.7)
       II 64 (80.0) 54 (80.6) 10 (76.9)
       III 7 (8.8) 5 (7.5) 2 (15.4)
      Tumor location 0.526
       Sigmoid colon 36 (45.0) 32 (47.8) 4 (30.8)
       Above peritoneal reflection 30 (37.5) 24 (35.8) 6 (46.2)
       Below peritoneal reflection 14 (17.5) 11 (16.4) 3 (23.1)
      Preoperative chemoradiotherapy 8 (10.0) 5 (7.5) 3 (23.1) 0.086
      T category 0.902
       Tis, T1, T2 32 (40.0) 27 (40.3) 5 (38.5)
       T3, T4 48 (60.0) 40 (59.7) 8 (61.5)
      N category 0.484
       N0 44 (55.0) 38 (56.7) 6 (46.2)
       N1, N2 36 (45.0) 29 (43.3) 7 (53.8)
      Preoperative CEA (ng/mL) 1.95 (1.00–3.50) 1.90 (1.20–3.60) 2.20 (0.83–2.90) 0.518
      Characteristic Overall (n=80) Grade A/B (n=67) Grade C (n=13) P-value
      Operative time (min) 90.3±24.9 86.6±21.9 108.8±31.9 0.003
      Procedure 0.358
       Anterior resection 37 (46.2) 33 (49.3) 4 (30.8)
       Low anterior resection 28 (35.0) 23 (34.3) 5 (38.5)
       Ultralow anterior resection 15 (18.8) 11 (16.4) 4 (30.8)
      Surgical approach 0.238
       Laparoscopic 74 (92.5) 63 (94.0) 11 (84.6)
       Open 6 (7.5) 4 (6.0) 2 (15.4)
      Cutting SBP (mmHg) 115.5±41.9 117.7±45.0 104.2±16.5 0.293
      Cutting DBP (mmHg) 62.8±10.9 63.6±10.7 59.0±11.6 0.171
      Mucosal bleeding 0.008
       <3 35 (43.8) 25 (37.3) 10 (76.9)
       ≥3a 45 (56.2) 42 (62.7) 3 (23.1)
      Splenic flexure mobilization 11 (13.8) 8 (11.9) 3 (23.1) 0.286
      Ostomy diversion 12 (15.0) 7 (10.4) 5 (38.5) 0.010
      Outcome Overall (n=80) Grade A/B (n=76) Grade C (n=4) P-value
      Postoperative hospital stay (day) 5 (5–6) 5 (5–6) 6 (6–7.5) 0.059
      Delayed diet (day) 0 (0–0) 0 (0–0) 0 (0–1) 0.439
      Complication 7 (8.8) 6 (7.9) 1 (25.0) 0.312
       Cystitis 1 (1.2) 1 (1.3) 0 (0) >0.999
       Postoperative ileus 6 (7.5) 5 (6.6) 1 (25.0) 0.272
       Anastomotic leakage 0 (0) 0 (0) 0 (0) -
       Ischemic colitis 0 (0) 0 (0) 0 (0) -
      Variable Univariable analysis Multivariable analysis
      OR (95% CI) P-value OR (95% CI) P-value
      Age (yr) 0.90 (0.83–0.98) 0.019 0.85 (0.75–0.97) 0.016
      Sex
       Female 1 (Reference)
       Male 1.22 (0.22–6.78) 0.817
      Body mass index (kg/m2) 1.04 (0.82–1.32) 0.745
      Smoking
       No 1 (Reference)
       Yes 1.45 (0.30–6.93) 0.643
      Hypertension
       No 1 (Reference)
       Yes 0.25 (0.03–2.21) 0.214
      Diabetes mellitus
       No 1 (Reference)
       Yes NA NA
      Cerebrovascular disease
       No 1 (Reference)
       Yes NA NA
      Ischemic heart disease
       No 1 (Reference)
       Yes 2.88 (0.28–29.99) 0.377
      COPD
       No 1 (Reference)
       Yes 5.92 (0.47–75.09) 0.170
      ASA physical status 2.53 (0.45–14.29) 0.295
      Serum cholesterol (mg/dL) 1.00 (0.98–1.02) 0.699
      Preoperative CEA (ng/mL) 1.03 (0.98–1.08) 0.247
      Tumor location
       Sigmoid colon 1 (Reference)
       Above peritoneal reflection 2.41 (0.50–11.61) 0.273
       Below peritoneal reflection 0.77 (0.09–6.94) 0.815
      Preoperative chemoradiotherapy
       No 1 (Reference)
       Yes NA NA
      Operative time (min) 1.01 (0.98–1.04) 0.550
      Procedure
       Anterior resection 1 (Reference)
       Low anterior resection 13.91 (1.58–122.46) 0.018 13.01 (1.20–141.00) 0.035
       Ultralow anterior resection 0.70 (0.08–6.31) 0.752
      Surgical approach
       Laparoscopic 1 (Reference)
       Open NA NA
      Initial perfusion grade
       Grade A/B 1 (Reference)
       Grade C 4.72 (0.92–24.33) 0.063 24.86 (1.75–353.63) 0.018
      Mucosal bleeding
       <3 1 (Reference)
       ≥3a 1.04 (0.22–4.99) 0.960
      Splenic flexure mobilization
       No 1 (Reference)
       Yes 1.05 (0.11–9.66) 0.966
      Ostomy diversion
       No 1 (Reference)
       Yes 0.94 (0.10–8.58) 0.956
      Table 1. Visual grading system of marginal vessel perfusion assessment

      Table 2. Clinicopathological characteristics of the patients according to initial grade

      Values are presented as mean±standard deviation, number (%), or median (interquartile range).

      COPD, chronic obstructive pulmonary disease; ASA, American Society of Anesthesiologists; CEA, carcinoembryonic antigen.

      Table 3. Operative characteristics according to initial perfusion grade

      Values are presented as mean±standard deviation or number (%).

      SBP, systolic blood pressure; DBP, diastolic blood pressure.

      aClassified as “multiple.”

      Table 4. Postoperative outcomes according to final perfusion grade

      Values are presented as median (interquartile range) or number (%).

      Table 5. Multivariable logistic regression analysis for postoperative complications (n=80)

      ORs for continuous variables represent the change in odds per 1-unit increase: age (per year), body mass index (per kg/m2), serum cholesterol (per mg/dL), preoperative CEA (per ng/mL), and operative time (per minute).

      OR, odds ratio; CI, confidence interval; NA, not applicable (complete separation in logistic regression); COPD, chronic obstructive pulmonary disease; ASA, American Society of Anesthesiologists; CEA, carcinoembryonic antigen.

      aClassified as “multiple.”

      Table 1.

      Table 2.

      Table 3.

      Table 4.

      Table 5.

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