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Patients with ischemia isolated to the right side of the colon (IRCI) frequently have poor outcomes. IRCI and acute mesenteric ischemia (AMI) are caused by reductions in blood supply from the superior mesenteric artery and its branches. We investigated a group of patients with IRCI associated with AMI that developed initially or shortly thereafter, and compared outcomes of patients with IRCI and AMI vs those with only IRCI.
We performed a retrospective study of data collected from 313 consecutive patients with colonic ischemia who were hospitalized at Montefiore Medical Center in New York from 1998 through 2009. Based on colonoscopy, biopsy analyses, and surgery reports, we identified patients with IRCI with concurrent or proximately developing AMI (IRCI+AMI) and those with only IRCI. Demographics, evaluation, disease distribution, and outcome data were compared between groups.
Of 313 patients with colonic ischemia, 20.8% had IRCI; of these, 84.6% had only IRCI and 15.4% had IRCI+AMI. Chronic obstructive pulmonary disease was found more frequently in patients with IRCI+AMI (40.0%) than in patients with IRCI alone (12.7%; P < .05). At the time of IRCI diagnosis, mean levels of blood urea nitrogen were significantly higher in patients with IRCI+AMI than with IRCI alone (37.9 ± 14.4 mEq/L vs 26.4 ± 18.8 mEq/L; P < .05), as were mean white blood cell counts (20.3 ± 12.1 vs 12.7 ± 6.8 × 103/μL; P < .01). A higher proportion of patients with IRCI+AMI underwent surgery than patients with only IRCI (100.0% vs 43.1%; P = .001), and 30-day mortality was higher among patients with IRCI+AMI (70.0% vs 14.5% for patients with only IRCI; P < .001).
Based on an analysis of 313 patients with colonic ischemia, patients with IRCI+AMI have even more severe disease than those with IRCI alone. Chronic obstructive pulmonary disease was observed more frequently in patients with IRCI+AMI. Patients with IRCI+AMI had increased levels of blood urea nitrogen and/or white blood cell counts. Patients with IRCI should undergo vascular imaging analyses immediately to detect AMI; patients without AMI should be monitored closely for its subsequent development.
Abdominal pain, rectal bleeding, and diarrhea are its most common presenting symptoms, although the classic disease presentation sequence of abdominal pain, urgent desire to defecate, and bloody diarrhea occur in only approximately 50% of patients.
It is believed that the unique colonic vascular supply contributes to the differences in presentation and outcome of IRCI. Branches of the superior mesenteric artery (SMA), in addition to perfusing the entire small intestine, supply blood to the cecum, ascending colon, hepatic flexure, and a portion of the transverse colon.
If untreated, mortality from AMI approaches 100%. We postulated that a subset of IRCI is associated with or at risk for temporally proximate AMI because of the following: (1) IRCI has a worse outcome than CI affecting other anatomic segments of the colon; (2) both IRCI and AMI share a common vascular (SMA) blood supply; and (3) we have had some patients with IRCI who soon after CI developed AMI with intestinal gangrene and died shortly after surgery. This is a subgroup that needs to be identified promptly if we hope to reduce the mortality rate of this occurrence. This study was designed to test the hypothesis that the subset of patients with IRCI who concurrently have AMI or subsequently develop this disease (IRCI+AMI) have worse outcomes than patients with IRCI without AMI (IRCI alone). Our secondary goals were to identify characteristics, if any, that could be used to differentiate this potentially higher-risk cohort from patients who likely will have a better, although still precarious, course.
After institutional review board approval, we performed a retrospective chart review of consecutive patients with CI hospitalized at the Montefiore Medical Center from 1998 to 2009. By using Clinical Looking Glass software (Emerging Health, Yonkers, NY), patients were identified by International Classification of Diseases, 9th revision codes (557.0, 557.1, and 557.9) for mesenteric ischemia or infarction, bowel ischemia or infarction, or CI. Each chart then was reviewed for pathologically proven disease, which included the following: (1) colonoscopic or surgical evaluation of the entire colon; (2) a colonoscopy or surgical report that described signs of ischemia, including subepithelial hemorrhage, edema ulceration, and/or gangrene; and (3) a pathology report that concluded the findings were pathognomonic or consistent with the diagnosis of CI.
Based on the colonoscopy and/or surgical reports, patterns of colonic distribution for ischemia were tabulated; only patients with IRCI were included in our study. IRCI included isolated cecal, ascending colon, and hepatic flexure ischemia. When the distal transverse colon was affected in continuity with one of the other segments of the right colon, it was considered part of IRCI, given the vascular distribution of the SMA. Data from each patient with IRCI were analyzed at the time of diagnosis with CI and each patient’s course was followed up for a minimum of 5 years to assess for subsequent development of AMI. AMI was confirmed by imaging and surgical evaluation showing evidence of ischemic injury to the small intestine. Patients who had IRCI and AMI either at the time of initial diagnosis or subsequently comprised the IRCI+AMI group, whereas those who had IRCI without simultaneous or subsequent AMI (IRCI alone group) were the comparators.
For each patient, age, sex, ethnicity, specific causes of ischemia, and patient comorbidities were recorded. If the patient had a computed tomography (CT) or CT angiography within 5 days of their diagnosis, the results of that imaging study were recorded. Serology from the day of colonoscopy or surgical intervention initially diagnosing IRCI was obtained, including blood urea nitrogen (BUN), creatinine, sodium, white blood cell count (WBC), hemoglobin (Hgb), serum lactate dehydrogenase and serum lactate levels. Surgical treatment was any related surgical exploration or intervention within 120 days of diagnosis with IRCI. Mortality within 120 days of diagnosis was noted. Poor outcome was defined by a combination of surgical intervention and/or mortality within 120 days of IRCI diagnosis.
Data were collated in a Microsoft Excel database (Microsoft, Seattle, WA) and then imported into SPSS for Windows (23.0, IBM SPSS, Armonk, NY). Continuous baseline descriptive variables were expressed as means with standard deviations and were compared using the Student t test. Categoric variables were expressed as absolute numbers and proportions. The χ2 statistic was used to compare most categoric variables, and the Fisher exact test was used for small numbers. The Bonferroni method was used to correct for multiple comparisons. A univariate analysis initially was performed to assess for independent predictors of 120-day mortality in both the IRCI+AMI and IRCI-alone populations. Variables considered in this analysis included demographics, medical comorbidities, CT findings, disease distribution, and serologic results. Significant independent predictors of mortality then were added to a multivariate analysis using a Cox proportional hazards model. Only multivariate hazard ratios are presented in the text. A 2-sided P value of less than .05 was considered statistically significant.
A total of 957 patients with CI originally were identified by International Classification of Diseases, 9th revision codes during our study period; 554 were excluded from the study because of insufficient evidence to support the diagnosis and 90 were excluded because of incomplete evaluation of the colon. Of the 313 patients with confirmed CI, 65 (20.8%) had IRCI, with 10 (15.4%) developing AMI either acutely or subsequent to the initial presentation. Pathologic evidence of ischemic injury was obtained in 33 patients via colonoscopy, and in the remainder during surgical evaluation (Figure 1).
There were no significant differences in age, sex, or ethnicity between the 2 cohorts. A nonsignificant trend was observed toward IRCI patients who had or developed AMI being older (77.8 ± 11.7 and 70.4 ± 13.0, respectively; P = .09) and more likely Hispanic (60.0% and 34.5%, respectively; P = .13) compared with patients who had IRCI alone. IRCI+AMI patients also were more likely to have suffered from chronic obstructive pulmonary disease (COPD) (40.0% and 12.7%, respectively; P = .03), with a nonsignificant trend toward higher Charlson comorbidity scores than patients with IRCI alone (2.9 ± 2.4 and 2.2 ± 2.0, respectively; P = .09). There were no other significant differences in medical comorbidities between the groups. Subsegmental involvement of disease (eg, cecum, ascending, or transverse colon) within the right colon did not differ significantly between the 2 cohorts but there was a nonsignificant trend toward higher rates of ascending colon involvement in patients who developed AMI (87.5% and 51.7%, respectively; P = .07) (Table 1).
CT of the abdomen and pelvis was performed on all patients with IRCI+AMI and on 68.6% of those with IRCI alone (P = .04). CT angiography was performed infrequently in both cohorts. Pneumatosis linearis (50.0% and 17.2%, respectively; P < .05) and colon or small-bowel dilatation (50.0% and 13.8%, respectively; P < .05) were seen more commonly in IRCI+AMI, whereas pericolonic fat stranding (0.0% and 37.9%, respectively; P < .05) was seen more frequently in IRCI alone (Table 2).
Table 2CT: Frequency and Findings
Conventional CT performed
Colon or small-bowel dilatation
Pericolonic fat stranding
Portal venous gas
NOTE. Bolded values reflect statistically significant differences between groups.
Comparison of serologic values at the time of IRCI diagnosis showed that the IRCI+AMI cohort had significantly higher mean BUN level (37.9 ± 14.4 and 26.4 ± 18.8 mEq/L, respectively; P < .05) and mean WBC (20.3 ± 12.1 and 12.7 ± 6.8 × 103/μL, respectively; P < .01). There were no other significant serologic differences between the 2 cohorts (Table 3). Patients with IRCI+AMI had a greater need for surgery (100.0% and 43.1%, respectively; P < .001) and a higher 30-day mortality rate (70.0% and 14.5%, respectively; P < .001) than did patients with IRCI alone. The mortality rate within 120 days was 90% for patients with IRCI+AMI (Figure 2).
Table 3Serologic Comparison of IRCI+AMI and IRCI Alone
IRCI + AMI
37.9 ± 14.4
26.4 ± 18.8
Creatinine level, mg/dL
2.54 ± 1.90
2.7 ± 3.0
Hemoglobin level, mg/dL
9.9 ± 1.7
10.8 ± 1.8
Lactate dehydrogenase level, U/L
271.2 ± 194.9
727.6 ± 1328.8
Lactate level, mg/dL
5.9 ± 4.8
4.0 ± 6.1
Sodium level, mEq/L
138.3 ± 3.9
139.9 ± 5.8
20.3 ± 12.1
12.7 ± 6.8
NOTE. Bolded values reflect statistically significant differences between groups.
There were no univariate predictors of mortality in the IRCI+AMI cohort. In the IRCI alone cohort, COPD (hazard rate [HR], 5.9 ± 0.9; P < .05), atrial fibrillation (HR, 13.3 ± 0.86; P < .01), and mean WBC (HR, 1.15 ± 0.06; P < .05) were associated with 120-day mortality through univariate and multivariate Cox regression analysis.
Within the IRCI+AMI group, 20% of patients had occlusion of the celiac artery and 50% had SMA obstruction. Nine of the 10 patients with IRCI+AMI were diagnosed at the time of initial assessment of the ischemic episode; the 1 patient who was not diagnosed simultaneously re-presented 15 days subsequently with AMI.
IRCI is a known risk factor for poor outcome in patients with CI.
Our study of 65 patients with IRCI showed a subset of patients comprising 15% of the IRCI cohort who simultaneously had ischemic small-bowel involvement (IRCI+AMI) with even worsened outcome (90% mortality) than the patients who had IRCI alone. Patients with IRCI+AMI suffered from COPD more frequently, had higher BUN and creatinine levels at the time of diagnosis, and imaging studies that commonly showed small-bowel dilatation or pneumatosis linearis. It is critical that all patients with IRCI have appropriate vascular imaging studies to diagnose concurrent AMI or a vascular predisposition to develop AMI.
COPD has been shown in our series as well as in a long-term epidemiologic analysis to be associated with poor outcome in patients with CI.
In AMI, COPD is associated with postoperative morbidity, possibly because of chronic hypoxia and a susceptibility to other ischemic triggers. It also is possible that COPD is a surrogate marker for tobacco use. In our analysis, we found COPD to be associated more commonly with small-bowel involvement than with IRCI alone. It seems likely that the previous observations of COPD as a risk factor for poor outcome in CI might be explained partly by this subgroup of patients with concurrent or subsequent AMI.
Patients with IRCI+AMI presented with a greater WBC and BUN level at diagnosis compared with patients with IRCI alone. In the setting of ischemic disease, the WBC is believed to increase as a result of inflammatory responses to the ischemic episode. Mosele et al
detailed mild WBC increases (12.2 ± 5.6 × 103/μL) in 46 patients with biopsy-proven CI. In another study of 364 patients with definite or probable CI, a WBC greater than 15.0 × 103/μL was more frequent in patients with more severe disease.
Our study was consistent with these reported differences because patients with IRCI+AMI had a WBC of 20.3 ± 12.1 × 103/μL, which is higher than the previously reported 15.0 × 103/μL level that defined patients with either severe CI or AMI
(12.2 ± 5.6 × 103/μL) of patients with CI in general. Therefore, WBC can be used to differentiate patients with IRCI+AMI from those without AMI.
Ischemic disease of the digestive tract is believed to increase the BUN level as a result of catabolic processes. As with a WBC increase, severity of ischemia also is associated with the magnitude of BUN increase. Mosele et al
compared the BUN in patients with biopsy-proven CI and in controls and showed the BUN was significantly higher in patients with CI (10.2 ± 7.3 mEq/L), and even higher in patients with severe CI compared with mild CI (14.5 ± 8.9 mEq/L and 8.2 ± 5.3 mEq/L, respectively; P < .05). In a study of 124 patients with surgically and pathologically proven AMI, BUN was significantly higher in patients who died (53.8 ± 42.0 mEq/L) than in patients who survived (33.5 ± 35.3 mEq/L; P < .01), and predicted mortality (OR, 7.2; CI, 1.2–44.7; P < .05).
Our study showed that patients with IRCI alone had mean BUN levels of 26.4 ± 18.8 mEq/L, which is intermediate between the reported levels in CI (10.2 ± 7.3 mEq/L) and AMI (33.5 ± 35.3 to 53.8 ± 42.0 mEq/L).
in patients who were diagnosed with AMI and survived (33.5 ± 35.3 mEq/L). IRCI+AMI has a continuum of disease severity that is reflected by the BUN level. Patients with IRCI alone appear to be at the lowest risk of mortality and have lower BUN levels than patients who have concurrent AMI or AMI alone. Higher BUN levels are seen in patients with IRCI+AMI whose worsened outcomes and BUN measurements are similar to patients who survived AMI without colonic involvement. Patients with AMI who died had the highest BUN levels.
In our study, serum lactate dehydrogenase and lactate values, which are increased only in the presence of irreversible ischemic injury with intracellular acidosis, were unable to differentiate IRCI+AMI from IRCI alone.
The most recent guideline for the diagnosis and management of CI recommends CT with oral and intravenous contrast as the imaging modality of choice to assess the distribution, phase of colitis, and severity of disease for patients admitted with CI.
In our study, 100% of patients with IRCI+AMI and 68.6% of those with IRCI alone had CT performed. These differences in CT performance frequencies are likely a result of disease severity at the time of presentation and clinicians’ concerns to exclude AMI. Because of the poor outcome for patients with IRCI alone, it is important to obtain a CT scan for these patients as well because their management should be more aggressive than that of non-IRCI patients.
CT findings can be used to differentiate IRCI alone from IRCI+AMI. In CI, common findings include a thickened colonic wall, loss of colonic haustra with varying degrees of pericolonic stranding, concentric and symmetric mild mural thickening with homogenous attenuation of the colon wall and minimal pericolic stranding, pericolonic ascites, and the ominous findings of pneumatosis coli linearis and portal venous gas, which are associated with necrosis.
In AMI, colon dilatation, bowel wall thickening, abnormal bowel wall enhancement, lack of enhancement of arterial vasculature with timed intravenous contrast injections, arterial occlusion, venous thrombosis, engorgement of mesenteric veins, intramural gas, and mesenteric or portal venous gas are seen commonly.
In our study, pericolonic fat stranding appeared more frequently in patients with IRCI alone and in none of the patients with IRCI+AMI, its presence arguing against AMI. Pneumatosis linearis and colon or small-bowel dilatation, however, were seen more commonly in IRCI+AMI than in those without AMI and, in the setting of IRCI, consistently identify a population of patients with CI who require more urgent and aggressive management including surgical intervention.
Existing literature on patients with combined small- and large-bowel ischemia is limited. Aliosmanoglu et al
assessed 95 consecutive patients undergoing emergency surgery for AMI and showed that 27.4% of these patients had co-existing small- and large-bowel involvement; 68.4% of those with colonic involvement died whereas 25.6% died when there was no colonic involvement. In the study by Aliosmanoglu et al,
the cohort with both small-bowel and colonic involvement was older, and those with only small-bowel involvement had more comorbidities, a higher serum lactate level at diagnosis, and a higher frequency of surgery within 24 hours, but lower mortality rates (25.6% and 68.4%, respectively; P < .001) than the cohort with combined small- and large-bowel involvement.
In another study of 132 patients who underwent surgery for AMI, 43.2% had combined small- and large-bowel involvement and, in this group, cardiac illness, BUN levels, and small- and large-bowel distribution were the only significant predictors of perioperative mortality; 82.5% of those with both small- and large-bowel involvement died while hospitalized after surgical intervention compared with a 64.5% mortality rate for those patients who had only small-bowel involvement.
Studies analyzing AMI that include cases of CI and AMI commonly include only patients who underwent surgical resection for disease identification and treatment, whereas studies of CI use only pathologic diagnoses established by colonoscopic evaluation. This distinction leads to a selection bias with the surgically selected patients who have combined small- and large-bowel involvement being sicker than those with CI alone. The surgical literature shows that patients with combined small- and large-bowel involvement have higher mortality rates (68.4%–82.5%) than those with isolated small-bowel involvement (25.6%–64.5%),
found that of 8% of 445 patients with definite or probable CI had small-bowel involvement; this distribution was associated independently with increased mortality through multivariate analysis (HR, 3.2; CI, 2.0–5.2; P < .001). Our study focused on a specific cohort of patients with CI, namely IRCI, who are considered at higher risk of poor outcome within the CI population. A subcohort of those with IRCI (ie, those patients with IRCI+AMI), had an even worse outcome of disease, especially when associated with higher WBC and BUN levels and more ominous findings on CT (eg, pneumatosis linearis, portal venous gas, and small- and large-bowel dilatation). We believe this small but important group of patients, in whom small-bowel involvement might not have been diagnosed, explains some of the differences in poor outcome observed for patients with IRCI. IRCI alone is associated with poor outcome (43.1% surgery, 14.5% mortality), and those with IRCI+AMI are at even higher risk for poor outcome (100% surgery, 90% mortality).
There were some potential weaknesses of our study. First, it was retrospective, with all the weaknesses inherent in such studies. As such, we were unable to identify the exact causes of death for those who died. Review of the records showed that patients with IRCI+AMI most frequently died of immediate complications of AMI whereas those with IRCI alone died from a variety of other causes including sepsis most frequently. Second, the size of our cohorts were small. Our stringent criteria for the diagnosis of CI was a strength of our study, but limited the number of patients we could include. One trend that might achieve statistical significance with a larger cohort was the patients with IRCI+AMI being older and with higher Charlson comorbidity scores. We believe the differences in outcome were so striking between IRCI+AMI compared with IRCI alone, however, that these potential differences would not alter the observed outcome variation between groups significantly.
In summary, this study presents a cohort of patients with CI at higher risk for poor outcome: patients with IRCI who also have small-bowel ischemia. Every time a patient presents with findings of IRCI, concurrent ischemia of the small bowel should be sought by appropriate imaging studies. In approximately 15% of cases, IRCI may be accompanied by AMI, and in some cases the index episode of IRCI is the heralding presentation of disease involving the SMA, which may present days to weeks later with AMI. All patients with IRCI, but especially those who present with IRCI and also have COPD, a markedly increased BUN level and/or WBC, should have vascular imaging to assess for SMA occlusive or nonocclusive disease. If AMI is not present, this cohort nevertheless should be monitored closely for its subsequent development.
Feuerstadt et al1 confirmed that isolated right-side colon ischemia (IRCI) is typically severe, and they found a much worse outcome when there is concurrent acute mesenteric ischemia (AMI). Comorbidity, laboratory, and computed tomography (CT) features differentiated IRCI alone from IRCI plus AMI. They advised immediate vascular imaging for patients with IRCI to detect AMI and vascular disease that could indicate a high risk of subsequent AMI. The accompanying editorial praised the study for supporting prompt identification of potentially treatable vascular disease.