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Korean J Gastroenterol 2024; 84(4): 160-167  https://doi.org/10.4166/kjg.2024.055
Risk Factors Associated with Progression to Surgery in Patients with Ischemic Colitis
Je-Seong Kim, Ho-Jin Choi, Chan-Mook Im, Ga-Ram You, Young-Eun Seo, Chae-June Lim, Jae-Woong Lim, Hyung-Hoon Oh, Young-Eun Joo
Department of Internal Medicine, Chonnam National University Medical School, Gwangju, Korea
Correspondence to: Young-Eun Joo, Department of Internal Medicine, Chonnam National University Medical School, 264 Seoyang-ro, Hwasun-eup, Hwasun 58128, Korea. Tel: +82-61-379-7602, Fax: +82-61-379-7628, E-mail: yejoo@chonnam.ac.kr, ORCID: https://orcid.org/0000-0003-0422-2439

*These authors contributed equally to this study.
Received: June 10, 2024; Revised: September 19, 2024; Accepted: September 23, 2024; Published online: October 25, 2024.
© The Korean Journal of Gastroenterology. All rights reserved.

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.
Abstract
Background/Aims: Ischemic colitis (IC), the most common ischemic syndrome affecting the gastrointestinal tract, results from a decreased blood supply to the colon. Persistent symptoms can lead to complications, necessitating surgery. This study assessed the clinical characteristics and risk factors for poor outcomes in IC.
Methods: This retrospective observational study examined the medical records of 141 patients diagnosed pathologically with IC via surgery or colonoscopy at Chonnam National University Hwasun Hospital between April 2004 and August 2023.
Results: Eighteen (12.8%) and 123 (87.2%) patients were diagnosed by surgical biopsy and biopsy with colonoscopy, respectively. Multivariate analysis identified right-sided colon involvement, fever, and the absence of hematochezia as risk factors for the progression to surgery (odds ratio [OR]=5.924, 95% confidence interval [CI] 1.009–34.767, p=0.049; OR=24.139, 95% CI 5.209–111.851, p<0.001; and OR=0.076, 95% CI 0.013–0.446, p=0.004, respectively). The in-hospital mortality was 5.7% (8/141), and the patients who died exhibited higher rates of shock. The median (interquartile range) hospital stay was 11 (1–219) days. Patients who had longer hospital stays (≥14 days) had a significantly higher rate of fever but a lower rate of hematochezia.
Conclusions: A multidisciplinary approach is crucial for determining the need for surgery in patients with right-sided colon involvement, fever, or the absence of hematochezia.
Keywords: Ischemia; Colon; Risk; Surgery
INTRODUCTION

Ischemic colitis (IC) is the most common ischemic syndrome occurring in the gastrointestinal tract.1,2 The disease is caused by various disorders that decrease the blood supply to the bowel.3 The most common cause is transient nonocclusive hypoperfusion of a colonic segment, often without an apparent cause.4,5 IC is diagnosed in approximately 16–24% of patients who present to the hospital with low gastrointestinal bleeding, and its incidence was estimated to be 16.3 cases per 100,000 person-years in the general population.2,6,7

IC is more common in females over 65 years of age, highlighting old age and female sex as important risk factors.7 The other significant risk factors associated with IC include hypertension, hyperlipidemia, diabetes mellitus, coronary artery disease, and arrhythmia.8

Most patients with IC present acutely with colicky lower abdominal pain, fecal urgency, diarrhea, and hematochezia.9 A physical examination typically reveals a soft abdomen with tenderness over the affected portion of the colon and abdominal distention.10 These observations may be confused with acute mesenteric ischemia, inflammatory bowel disease, infectious colitis, pseudomembranous colitis, diverticulosis, or colorectal cancer.11 As with acute mesenteric ischemia, the presence of perforation, peritonitis, and severe hemorrhaging mandates prompt surgical consultation.8

No single test can diagnose IC conclusively, but the diagnosis can be established with the judicious use of diagnostic modalities, including computed tomography scans with angiography and colonoscopy in the appropriate clinical context.3 IC is usually transient, and symptoms generally resolve with supportive care. On the other hand, patients with persistent symptoms have a higher incidence of complications, including gangrene, perforation, segmental ulcerating colitis, and stricture.4,12

The presentation of the injury, management, and outcomes vary according to several factors: acuity, the splanchnic vessels affected, the presence or absence of collateral circulation, the segment and length of the bowel involved, and whether the arterial or venous circulation is compromised.13 Recognition and appropriate management are crucial to improving patient outcomes. Therefore, this study examined the clinical characteristics and risk factors for poor outcomes in IC.

SUBJECTS AND METHODS

1. Study design and population

This retrospective study assessed consecutive patients diagnosed pathologically with IC using a colonoscopic or surgical biopsy at Chonnam National University Hwasun Hospital between April 2004 and August 2023. One hundred and forty- one patients with IC were analyzed retrospectively for various clinicopathological characteristics by reviewing the medical records of enrolled patients. This study was performed in accordance with the ethical principles of the Declaration of Helsinki and was approved by the Institutional Review Board of Chonnam National University Hwasun Hospital (IRB No.: CNUHH-2024-083).

2. Data collection

The data from enrolled patients were included prospectively in an institutional study register database. The records were analyzed retrospectively for demographic data such as age, sex, alcohol consumption, smoking history, American Society of Anesthesiology (ASA) classification,14-16 previous colorectal surgery history, co-morbidities (hypertension, diabetes mellitus, dyslipidemia, congestive heart failure, cardiovascular disease, chronic kidney disease, and liver cirrhosis), medications (antiplatelet agents, anticoagulants, nonsteroidal anti-inflammatory drugs [NSAIDs], and diuretics), and extent of colon involvement (the cecum, ascending colon, and transverse colon were regarded as the right-sided colon, and the descending colon, including the span from the splenic flexure to the rectosigmoid colon, was regarded as the left-sided colon).

3. Statistical analysis

The clinical characteristics, risk factors, and outcomes of the groups were compared using a chi-square test, Student’s t-test, or analysis of variance, where appropriate. Descriptive analyses included proportions for categorical data and median (range) for continuous data. All statistical analyses were conducted with the Statistical Packages for the Social Sciences (SPSS, version 22.0; SPSS Inc., Chicago, IL, USA). A difference with p<0.05 was considered significant.

RESULTS

1. Baseline characteristics of enrolled patients

Table 1 lists the baseline characteristics of the 141 patients with IC. The median age of enrolled patients was 72 years old (range 23–90 years). The study group included 74 men (52.5%) and 67 women (47.5%). Thirty-three (23.4%) patients received outpatient treatment, and 108 (76.6) patients received inpatient treatment. Eighteen (12.8%) and 123 (87.2%) patients were diagnosed using a surgical biopsy and a colonoscopic biopsy, respectively. A history of heavy alcohol consumption and smoking was observed in 4 (2.8%) and 28 (19.9%) patients, respectively. According to the ASA classification, the number of subjects (percentage) in ASA classes 1, 2, 3, and 4 were 21 (14.9%), 60 (42.6%), 50 (35.5%), and 10 (7.1%), respectively. Hypertension, diabetes mellitus, dyslipidemia, congestive heart failure, cardiovascular disease, chronic kidney disease, and liver cirrhosis were observed in 70 (49.6%), 29 (20.6%), 6 (4.3%), 7 (5.0%), 23 (16.3%), 11 (7.8%), and 3 (2.1%) patients, respectively. Of the patients, 60 (42.6%) patients received medications including antiplatelet agents (27, 19.1%), anticoagulants (7, 5.0%), NSAIDs (10, 7.1%), and diuretics (16, 11.3%). The median number of hospital days was 11 days (range, 1–219 days). Right colon involvement was observed in 28 (19.9%) patients. Previous colorectal surgery history was observed in 31 (22.0%) patients. Recurrence occurred in four (2.8%) patients. Shock, fever, abdominal pain, tenderness, rebound tenderness, and hematochezia were noted in 12 (8.5%), 31 (22.0%), 57 (40.4%), 34 (24.1%), 4 (2.8%), and 69 (48.9%) patients, respectively.

Table 1 . Baseline Characteristics of Ischemic Colitis Patients with and without Surgical Progression

VariablesWith surgical progression (n=18)Without surgical progression (n=123)Total (n=141)p-value
Age (years)67.28±12.2769.67±12.0169.36±12.02
Median 72 (range, 23–90)
0.783
Sex0.821
Female9 (50.0)58 (47.2)67 (47.5)
Male9 (50.0)65 (52.8)74 (52.5)
Smoking0.788
None14 (77.8)99 (80.5)113 (80.1)
Current smoker or Ex-smoker4 (22.2)24 (19.5)28 (19.9)
Alcohol0.457
None or Social17 (94.4)120 (97.6)122 (86.5)
Heavy1 (5.6)3 (2.4)19 (13.5)
ASA class0.736
1–211 (61.1)70 (56.9)81 (57.4)
3–47 (38.9)53 (43.1)60 (42.6)
Hypertension7 (38.9)63 (51.2)70 (49.6)0.328
Diabetes mellitus3 (16.7)26 (21.1)29 (20.6)0.661
Dyslipidemia1 (5.6)5 (4.1)6 (4.3)0.770
Congestive heart failure1 (5.6)6 (4.9)7 (5.0)0.902
Cardiovascular disease2 (11.1)21 (17.1)23 (16.3)0.523
Chronic kidney disease2 (11.1)9 (7.3)11 (7.8)0.575
Liver cirrhosis0 (0.0)3 (2.4)3 (2.1)0.503
Antiplatelet agents1 (5.6)26 (21.1)27 (19.1)0.117
Anticoagulants1 (5.6)6 (4.9)7 (5.0)0.902
NSAIDs1 (5.6)9 (7.3)10 (7.1)0.786
Diuretics1 (5.6)15 (12.2)16 (11.3)0.407
Hospital period (days)25.83±15.3216.62±28.4018.16±26.83
Median 11
(range, 1–219)
0.617
Right-sided colon involvement7 (38.9)21 (17.1)28 (19.9)0.030
Previous colorectal surgery history5 (27.8)15 (12.2)31 (22.0)0.077
Shock4 (22.2)8 (6.5)12 (8.5)0.026
Fever13 (72.2)18 (14.6)31 (22.0)<0.001
Abdominal pain11 (61.1)46 (37.4)57 (40.4)0.056
Tenderness7 (38.9)27 (22.0)34 (24.1)0.117
Rebound tenderness1 (5.6)3 (2.4)4 (2.8)0.457
Hematochezia2 (11.1)67 (54.5)69 (48.9)<0.001

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

ASA, American Society of Anesthesiology; NSAID, Nonsteroidal anti-inflammatory drug.



2. Factors associated with surgical progression in IC patients

Table 1 lists the baseline characteristics of the IC patients with or without surgical progression. Concerning patient-related factors, no significant differences were observed in age, sex, smoking, alcohol, ASA class, hypertension, diabetes mellitus, dyslipidemia, congestive heart failure, cardiovascular disease, chronic kidney disease, liver cirrhosis, medication history of antiplatelet agents or anticoagulants, NSAIDs, diuretics, previous colorectal surgery history, abdominal pain, and tenderness or rebound tenderness. The patients who underwent surgery had a higher incidence of right-sided colon involvement (p=0.030). Patients who required surgery also showed a higher rate of shock and fever at diagnosis (p=0.026 and p≤0.001, respectively) but a lower rate of hematochezia (p<0.001).

Table 2 lists the results of univariate and multivariate logistic analyses of the risk factors for progression to surgery. Univariate analysis revealed right-sided colon involvement, presence of shock, fever, and the absence of hematochezia to be risk factors for progression to surgery (odds ratio [OR]=3.091, 95% confidence interval [CI] 1.073–8.900, p=0.037; OR=4.107, 95% CI 1.095–15.409, p=0.036; OR=15.167, 95% CI 4.821–47.718, p<0.001; OR=0.104, 95% CI 0.023–0.474, p=0.003, respectively). Multivariate analysis revealed right-sided colon involvement, fever, and the absence of hematochezia to be risk factors for the progression to surgery (OR=5.924, 95% CI 1.009– 34.767, p=0.049; OR=24.139, 95% CI 5.209–111.851, p<0.001; and OR=0.076, 95% CI 0.013–0.446, p=0.004, respectively).

Table 2 . Risk Factors Associated with Surgical Progression in Ischemic Colitis Patients

VariablesUnivariateMultivariate
OR (95% CI)p-valueOR (95% CI)p-value
Right-sided colon involvement
NoRefRef
Yes3.091 (1.073–8.900)0.0375.924 (1.009–34.767)0.049
Previous colorectal surgery history
NoRefRef
Yes2.769 (0.864–8.871)0.0861.538 (0.261–9.080)0.635
Shock
NoRefRef
Yes4.107 (1.095–15.409)0.0361.558 (0.190–12.757)0.679
Fever
NoRefRef
Yes15.167 (4.821–47.718)<0.00124.139 (5.209–111.851)<0.001
Abdominal pain
NoRefRef
Yes2.630 (0.953–7.263)0.0622.753 (0.676–11.207)0.157
Hematochezia
NoRefRef
Yes0.104 (0.023–0.474)0.0030.076 (0.013–0.446)0.004

OR, odds ratio; CI, confidence interval; ASA, American Society of Anesthesiology; NSAID, Nonsteroidal anti-inflammatory drug.



3. Factors associated with prolonged hospital stay in IC patients

The comparison of baseline characteristics of IC patients with or without prolonged hospital stay is Table 3 compares the baseline characteristics of IC patients with or without prolonged hospital stay. Concerning patient-related factors, no significant differences were observed in age, sex, smoking, alcohol, ASA class, hypertension, diabetes mellitus, dyslipidemia, congestive heart failure, cardiovascular disease, chronic kidney disease, liver cirrhosis, medication history of antiplatelet agents or anticoagulants, NSAIDs, diuretics, right-sided colon involvement, previous colorectal surgery history, shock, abdominal pain, and tenderness or rebound tenderness. Patients with lengthy stays in the hospital had a higher incidence of fever at diagnosis (p<0.001) but a lower rate of hematochezia (p=0.005).

Table 3 . Baseline Characteristics of Ischemic Colitis Patients with and without Prolonged Hospital Stay

VariablesWith longer hospital stay (≥14 days) (n=42)With shorter hospital stay (≤13 days) (n=66)p-value
Age (years)68.40±11.9771.33±11.690.781
Sex0.930
Female22 (52.4)34 (51.5)
Male20 (47.6)32 (48.5)
Smoking0.102
None31 (73.8)57 (86.4)
Current smoker or Ex-smoker11 (26.2)9 (13.6)
Alcohol0.208
None or Social41 (97.6)66 (100.0)
Heavy1 (2.4)0 (0.0)
ASA class0.154
1–217 (40.5)36 (54.5)
3–425 (59.5)30 (45.5)
Hypertension20 (47.6)34 (51.5)0.693
Diabetes mellitus9 (21.4)15 (22.7)0.874
Dyslipidemia2 (4.8)2 (3.0)0.642
Congestive heart failure2 (4.8)4 (6.1)0.774
Cardiovascular disease6 (14.3)14 (21.2)0.366
Chronic kidney disease4 (9.5)7 (10.6)0.856
Liver cirrhosis1 (2.4)1 (1.5)0.745
Antiplatelet agents7 (16.7)16 (24.2)0.349
Anticoagulants2 (4.8)4 (6.1)0.774
NSAIDs6 (14.3)3 (4.5)0.074
Diuretics7 (16.7)7 (10.6)0.361
Right-sided colon involvement9 (21.4)12 (18.2)0.678
Previous colorectal surgery history6 (14.3)6 (9.1)0.402
Shock6 (14.3)6 (9.1)0.402
Fever21 (50.0)10 (15.2)<0.001
Abdominal pain21 (50.0)35 (53.0)0.759
Tenderness16 (38.1)18 (27.3)0.238
Rebound tenderness2 (4.8)2 (3.0)0.642
Hematochezia17 (40.5)45 (68.2)0.005

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

ASA, American Society of Anesthesiology; NSAID, Nonsteroidal anti-inflammatory drug.



Table 4 lists the results of univariate and multivariate logistic analyses of the risk factors for prolonged hospital stay. Univariate analysis revealed fever and the absence of hematochezia to be risk factors for a prolonged hospital stay (OR=5.600, 95% CI 2.266–13.840, p<0.001; and OR=0.317, 95% CI 0.142–0.710, p=0.005, respectively). Multivariate analysis revealed fever and the absence of hematochezia to be risk factors for prolonged hospital stay (OR=4.947, 95% CI 1.955–12.523, p<0.001; and OR=0.376, 95% CI 0.159– 0.886, p=0.025, respectively).

Table 4 . Risk Factors Associated with Prolonged Hospital Stay in Ischemic Colitis Patients

VariablesUnivariateMultivariate
OR (95% CI)p-valueOR (95% CI)p-value
Fever
NoRefRef
Yes5.600 (2.266–13.840)<0.0014.947 (1.955–12.523)<0.001
Hematochezia
NoRefRef
Yes0.317 (0.142–0.710)0.0050.376 (0.159–0.886)0.025

OR, odds ratio; CI, confidence interval.



4. Factors associated with in-hospital mortality in IC patients

Supplementary Table 1 compares the baseline characteristics of the ischemic colitis patients who survived and those who died. The in-hospital mortality was 5.7% (8/141). Regarding patient-related factors, no significant differences were observed in sex, smoking, alcohol, ASA class, hypertension, diabetes mellitus, dyslipidemia, congestive heart failure, cardiovascular disease, chronic kidney disease, liver cirrhosis, medication history of antiplatelet agents or anticoagulants, NSAIDs, diuretics, right-sided colon involvement, previous colorectal surgery history, abdominal pain, tenderness or rebound tenderness, and hematochezia. Patients who died in hospital were likelier to be older and had a higher frequency of NSAID use (p=0.031 and p=0.042). Patients who died also showed a higher rate of shock and fever at diagnosis (p<0.001 and p=0.049, respectively).

Supplementary Table 2 lists the results of univariate and multivariate logistic analyses of the risk factors for in-hospital mortality. Univariate analysis revealed shock to be a risk factor for in-hospital mortality (OR=15.625, 95% CI 3.285–74.310, p<0.001). Multivariate analysis revealed shock to be a risk factor for in-hospital mortality (OR=10.768, 95% CI 1.871–61.980, p=0.008).

DISCUSSION

IC is the most common form of ischemic bowel disease, with an increasing incidence.4 In most cases, IC is regarded as a benign and self-limiting condition.8 The disease results from an acute, transient compromise in mesenteric blood flow. Patients typically respond to conservative management such as volume replacement, bowel rest, and broad-spectrum antibiotics.10 Nevertheless, early surgical intervention may be necessary in severe cases with signs and symptoms of transmural infarction, gangrene, perforation, or massive bleeding.17-20 One hundred and forty-one 141 patients diagnosed pathologically with IC by a biopsy with colonoscopy or surgery were enrolled, and the clinical characteristics, risk factors, and long-term outcome of IC were evaluated.

The significant risk factors associated with IC are old age, female sex, hypertension, dyslipidemia, cardiovascular disease, nephropathy, diabetes mellitus, atrial fibrillation, smoking, and a history of previous surgery, including gastrointestinal surgery, abdominal aortic aneurysm surgery, or major cardiovascular surgery.2,7,9,21 In the present study, the mean age of enrolled patients was 69.36 years, and the male-to-female ratio was 5.25 to 4.75. The frequency of comorbid conditions, hypertension, diabetes mellitus, smoking history, cardiovascular disease, alcohol consumption, chronic kidney disease, congestive heart failure, dyslipidemia, and liver cirrhosis were 49.6%, 20.6%, 19.9%, 16.3%, 13.5%, 7.8%, 5.0%, 4.3%, and 2.1% of enrolled IC patients, respectively. A previous colorectal surgery history was observed in 22.0% of patients.

The ASA physical status classification system was developed to offer perioperative clinicians a simple categorization of a patient's physiological status that can help predict the operative risk. The classification has been revised over time and is a simple and rapid assessment of a patient’s physical status.14-16 In this study, ASA classes 1, 2, 3, and 4 were 14.9%, 42.6%, 35.5%, and 7.1%, respectively.

First, the baseline characteristics of IC patients with and without surgical progression were compared, and univariate and multivariate analyses were performed. In the present study, right-sided colon involvement was a risk factor for progression to surgery. This conclusion is consistent with other studies that reported right-sided IC as a predictor of severity and mortality.10,20,22-25 The right colon is generally less susceptible to ischemic injury than other parts of the colon, so right-sided involvement indicates more severe disease.26 The right colon disease indicates that a compromised blood supply from the superior mesenteric artery has occurred, which is a high-risk condition. Right-sided involvement was also related to other chronic diseases, such as coronary artery disease and end-stage renal failure.4,27 Therefore, the early identification of right-sided colon involvement should prompt immediate vigorous treatment, including surgery if needed.

Fever and the absence of hematochezia were risk factors for both surgical progression and prolonged hospital stay. The absence of hematochezia is considered a significant predictor of a poor prognosis.8,10,13,22,28 Hematochezia is believed to prompt earlier hospital visits and diagnosis, leading to an improved prognosis. Fever indicates a severe condition, and patients who undergo surgery exhibit a significantly higher rate of fever.

In addition, the baseline characteristics of IC patients who died were compared with those who survived and identified the risk factors for in-hospital mortality. Shock was identified as a risk factor, which is consistent with previously reported results.23,29,30 The in-hospital mortality rate among the patients was 5.7%, which is lower than that (15.7%) reported in a recent systematic review.31

The present study had some limitations. First, the study design was retrospective and nonrandomized, so several biases were unavoidable. Second, only a few databases in a single center were retrieved, which, to some extent, affected the completeness of the information obtained. Therefore, a large prospective, multicenter, randomized control trial is required to provide more definitive evidence regarding the clinical characteristics, risk factors, and long-term outcomes of IC.

In conclusion, right-sided colon involvement, fever, and the absence of hematochezia were risk factors for the progression to surgery. Fever and the absence of hematochezia were also risk factors for prolonged hospital stay. Shock was a risk factor for in-hospital mortality. Therefore, a multidisciplinary approach regarding the need for surgery is necessary in IC patients with right-sided colon involvement, fever, and the absence of hematochezia.

AUTHOR CONTRIBUTIONS

Conceptualization: JSK, HJC and YEJ Investigation: HHO, CMI, GRY, YES, CJL and JWL Resources: JSK and HJC Supervision: YEJ Writing-original draft: JSK, HJC and YEJ Writing-review & editing: HHO and YEJ.

SUPPLEMENTARY MATERIAL

Supplementary material is available at the Korean Journal of Gastroenterology website (https://www.kjg.or.kr/).

Financial support

None.

Conflict of interest

None.

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  • DOAJ
  • ORCID