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.
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.
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).
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).
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.
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 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).
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 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).
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).
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.
Supplementary material is available at the Korean Journal of Gastroenterology website (https://www.kjg.or.kr/).
Notes
REFERENCES
1. Greenwald DA, Brandt LJ. 1998; Colonic ischemia. J Clin Gastroenterol. 27:122–128. DOI: 10.1097/00004836-199809000-00004. PMID: 9754772.
2. Rizwan R, Feuerstadt P. 2022; Bad blood: ischemic conditions of the large bowel. Curr Opin Gastroenterol. 38:72–79. DOI: 10.1097/MOG.0000000000000797. PMID: 34871196.
3. Clair DG, Beach JM. 2016; Mesenteric Ischemia. N Engl J Med. 374:959–968. DOI: 10.1056/NEJMra1503884. PMID: 26962730.
4. Ahmed M. 2021; Ischemic bowel disease in 2021. World J Gastroenterol. 27:4746–4762. DOI: 10.3748/wjg.v27.i29.4746. PMID: 34447224. PMCID: PMC8371501.
5. Brandt LJ, Feuerstadt P, Longstreth GF, Boley SJ. American College of Gastroenterology. 2015; ACG clinical guideline: epidemiology, risk factors, patterns of presentation, diagnosis, and management of colon ischemia (CI). Am J Gastroenterol. 110:18–44. quiz 45DOI: 10.1038/ajg.2014.395. PMID: 25559486.
6. Hreinsson JP, Gumundsson S, Kalaitzakis E, Björnsson ES. 2013; Lower gastrointestinal bleeding: incidence, etiology, and outcomes in a population-based setting. Eur J Gastroenterol Hepatol. 25:37–43. DOI: 10.1097/MEG.0b013e32835948e3. PMID: 23013623.
7. Xu Y, Xiong L, Li Y, Jiang X, Xiong Z. 2021; Diagnostic methods and drug therapies in patients with ischemic colitis. Int J Colorectal Dis. 36:47–56. DOI: 10.1007/s00384-020-03739-z. PMID: 32936393. PMCID: PMC7493065.
8. Maimone A, De Ceglie A, Siersema PD, Baron TH, Conio M. 2021; Colon ischemia: A comprehensive review. Clin Res Hepatol Gastroenterol. 45:101592. DOI: 10.1016/j.clinre.2020.101592. PMID: 33662779.
9. Misiakos EP, Tsapralis D, Karatzas T, et al. 2017; Advents in the diagnosis and management of ischemic colitis. Front Surg. 4:47. DOI: 10.3389/fsurg.2017.00047. PMID: 28929100. PMCID: PMC5591371.
10. Trotter JM, Hunt L, Peter MB. 2016; Ischaemic colitis. BMJ. 355:i6600. DOI: 10.1136/bmj.i6600. PMID: 28007701.
11. Theodoropoulou A, Koutroubakis IE. 2008; Ischemic colitis: clinical practice in diagnosis and treatment. World J Gastroenterol. 14:7302–7308. DOI: 10.3748/wjg.14.7302. PMID: 19109863. PMCID: PMC2778113.
12. Gilshtein H, Hallon K, Kluger Y. 2018; Ischemic colitis caused increased early and delayed mortality. World J Emerg Surg. 13:31. DOI: 10.1186/s13017-018-0193-2. PMID: 30008799. PMCID: PMC6042445.
13. Hung A, Calderbank T, Samaan MA, Plumb AA, Webster G. 2019; Ischaemic colitis: practical challenges and evidence-based recommendations for management. Frontline Gastroenterol. 12:44–52. DOI: 10.1136/flgastro-2019-101204. PMID: 33489068. PMCID: PMC7802492.
14. Horvath B, Kloesel B, Todd MM, Cole DJ, Prielipp RC. 2021; The evolution, current value, and future of the American Society of Anesthesiologists Physical Status Classification System. Anesthesiology. 135:904–919. DOI: 10.1097/ALN.0000000000003947. PMID: 34491303.
15. Knuf KM, Maani CV, Cummings AK. 2018; Clinical agreement in the American Society of Anesthesiologists physical status classification. Perioper Med (Lond). 7:14. DOI: 10.1186/s13741-018-0094-7. PMID: 29946447. PMCID: PMC6008948.
16. Knuf KM, Manohar CM, Cummings AK. 2020; Addressing inter-rater variability in the ASA-PS classification system. Mil Med. 185:e545–e549. DOI: 10.1093/milmed/usz433. PMID: 31875897.
17. Nikolic AL, Keck JO. 2018; Ischaemic colitis: uncertainty in diagnosis, pathophysiology and management. ANZ J Surg. 88:278–283. DOI: 10.1111/ans.14237. PMID: 29124893.
18. MacDonald PH. 2002; Ischaemic colitis. Best Pract Res Clin Gastroenterol. 16:51–61. DOI: 10.1053/bega.2001.0265. PMID: 11977930.
19. O'Neill S, Yalamarthi S. 2012; Systematic review of the management of ischaemic colitis. Colorectal Dis. 14:e751–e763. DOI: 10.1111/j.1463-1318.2012.03171.x. PMID: 22776101.
20. Khrucharoen U, Jensen DM. 2022; Ischemic colitis as a cause of severe hematochezia: A mini review. J Clin Exp Gastroenterol. 1:22–26. DOI: 10.46439/gastro.1.005. PMID: 36092274. PMCID: PMC9464092.
21. Moghadamyeghaneh Z, Sgroi MD, Chen SL, Kabutey NK, Stamos MJ, Fujitani RM. 2016; Risk factors and outcomes of postoperative ischemic colitis in contemporary open and endovascular abdominal aortic aneurysm repair. J Vasc Surg. 63:866–872. DOI: 10.1016/j.jvs.2015.10.064. PMID: 26747680.
22. O'Neill S, Elder K, Harrison SJ, Yalamarthi S. 2012; Predictors of severity in ischaemic colitis. Int J Colorectal Dis. 27:187–191. DOI: 10.1007/s00384-011-1301-x. PMID: 21842142.
23. Qian W, Bruinsma J, Mac Curtain B, Ibraheem M, Temperley HC, Ng ZQ. 2024; Surgical prevalence and outcomes in ischemic colitis: A systematic review and meta-analysis. World J Surg. 48:943–953. DOI: 10.1002/wjs.12123. PMID: 38441288.
24. Sotiriadis J, Brandt LJ, Behin DS, Southern WN. 2007; Ischemic colitis has a worse prognosis when isolated to the right side of the colon. Am J Gastroenterol. 102:2247–2252. DOI: 10.1111/j.1572-0241.2007.01341.x. PMID: 17561968. PMCID: PMC2805903.
25. Vigorita V, García-Señoráns MP, Pellino G, et al. 2022; Ischemic colitis. Does right colon location mean worst prognosis? Cir Esp (Engl Ed). 100:74–80. DOI: 10.1016/j.cireng.2022.01.004. PMID: 35120849.
26. Medina C, Vilaseca J, Videla S, Fabra R, Armengol-Miro JR, Malagelada JR. 2004; Outcome of patients with ischemic colitis: review of fifty-three cases. Dis Colon Rectum. 47:180–184. DOI: 10.1007/s10350-003-0033-6. PMID: 15043287.
27. Brandt LJ, Feuerstadt P, Blaszka MC. 2010; Anatomic patterns, patient characteristics, and clinical outcomes in ischemic colitis: a study of 313 cases supported by histology. Am J Gastroenterol. 105:224522–52. quiz 2253DOI: 10.1038/ajg.2010.217. PMID: 20531399.
28. Oglat A, Quigley EM. 2017; Colonic ischemia: usual and unusual presentations and their management. Curr Opin Gastroenterol. 33:34–40. DOI: 10.1097/MOG.0000000000000325. PMID: 27798439.
29. Añón R, Boscá MM, Sanchiz V, et al. 2006; Factors predicting poor prognosis in ischemic colitis. World J Gastroenterol. 12:4875–4878. DOI: 10.3748/wjg.v12.i30.4875. PMID: 16937472. PMCID: PMC4087624.
30. Chung JW, Cheon JH, Park JJ, Jung ES, Choi EH, Kim H. 2010; Development and validation of a novel prognostic scoring model for ischemic colitis. Dis Colon Rectum. 53:1287–1294. DOI: 10.1007/DCR.0b013e3181e74171. PMID: 20706072.
31. Demetriou G, Nassar A, Subramonia S. 2020; The pathophysiology, presentation and management of ischaemic colitis: A systematic review. World J Surg. 44:927–938. DOI: 10.1007/s00268-019-05248-9. PMID: 31646369.