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1
Department of Radiology, Université Catholique
de Louvain, St-Luc University Hospital, Avenue Hippocrate 10, B-1200 Brussels,
Belgium.
2
Center for Biostatistics and Medical Documentation, Mont-Godinne University
Hospital, Avenue Therasse I, B-5530 Yvoir, Belgium.
3
Department of Internal Medicine, St-Luc University Hospital, B-1200 Brussels,
Belgium.
4
Department of Intensive Care and Emergency, St-Luc University Hospital, B-1200
Brussels, Belgium.
5
Department of Surgery, St-Luc University Hospital, B-1200 Brussels,
Belgium.
Received January 20, 2000;
accepted after revision March 17, 2000.
Address correspondence to E. M. Danse.
Abstract
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SUBJECTS AND METHODS. We reviewed the early clinical, laboratory, and color Doppler sonographic data of 24 patients with ischemic colitis. The patients were divided into two groups on the basis of their outcome. The first group comprised the patients with transient ischemia who recovered uneventfully, and the second group included the patients who needed surgery because of symptomatic transmural colic gangrene or colic stricture. Clinical data and laboratory values were compared with color Doppler sonographic findings including colic wall thickness, presence of stratification, and arterial flow in the bowel wall.
RESULTS. At univariate analysis, increased age (p = 0.007), leukocyte count (p = 0.030), lactate dehydrogenase level (p = 0.030), blood lactate level (p = 0.041), and absence of vascular flow in the colic wall (p < 0.001) were significantly related to complicated ischemic colitis. At multivariate analysis, absence of arterial flow was the only significant predictor of complicated ischemic colitis (p = 0.002), with a sensitivity of 82%, a specificity of 92%, a positive predictive value of 90%, and a negative predictive value of 86%.
CONCLUSION. Absence of arterial flow in the wall of the ischemic colon on initial color Doppler sonography is suggestive of an unfavorable outcome and is more closely associated with outcome than early clinical and laboratory findings.
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Sonography and Doppler sonography have been reported to be useful for assessing the severity of ischemia on exposed tissues in animals and humans [8,9,10,11,12]. Noninvasive transabdominal Doppler sonography may show bowel changes caused by ischemia [13,14,15]. It remains to be proven whether this imaging method is helpful to assess the stage of ischemia. Therefore, the aim of our study was to compare the value of Doppler sonography with early clinical and laboratory findings in determining the prognosis of ischemic colitis.
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The leukocyte count and lactate dehydrogenase (LDH) level obtained at presentation were recorded. The blood lactate level was also noted when it was available. Sonography was performed with 2.5- to 5-MHz convex and 5- to 10-MHz linear transducers (model 128 XP 10, Acuson, Mountain View, CA; model 140 HG, Toshiba Europe, Zoetermeer, The Netherlands). The colic wall was considered to be thickened when the diameter from the outer hyperechoic layer (the serosa) to the inner hyperechoic layer (the mucosal surface) was greater than 4 mm. The wall was considered to be stratified when the mucosa, submucosa, and muscularis propria were visualized as separate layers. The vascularization of the colic wall was studied with color Doppler flow parameters optimized for maximal sensitivity. Specific parameters included a filter for low-volume flow (Filter 1, Acuson; 50 Hz, Toshiba Europe), lowest velocity scale (from 2.5 to 9 cm/sec), large gate width, and maximal gain adjusted until all color artifacts were eliminated [13, 14]. Doppler flow was considered to be present in the colic wall when colored pixels were identified throughout the observation period. Duplex Doppler samples oriented on the main colored pixels were used to confirm the arterial nature of the color signal identified in the colic wall.
Data analysis was done with statistical software (Statistical Package for the Social Sciences, Chicago, IL). Numeric variables were expressed as median and interquartile range. The numeric variables observed in transient and complicated ischemia were compared with the Wilcoxon's rank sum test. The Fisher's exact test was used to compare categoric variables. To identify the best parameters to differentiate transient and complicated ischemic colitis on the basis of the initial sonographic, biologic, and clinical data, we performed a logistic regression analysis with forward selection of variables, using the Wald test [16]. Sensitivity, specificity, and positive and negative predictive values of the absence of arterial flow as a sign of complicated ischemia were given with exact 95% confidence intervals.
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Logistic regression including age, duration of symptoms, leukocyte count, LDH level, and arterial flow in the colic wall as explanatory variables revealed the absence of arterial flow as the only significant predictor of complicated ischemic colitis (p = 0.002). Blood lactate level was not included in the regression analysis because of the small amount of available data (12/24 patients). When absence of arterial flow in the colic wall was considered as a prognostic factor of complicated ischemic colitis, it had a sensitivity of 82% (9/11) with a confidence interval of 95% (48-98%), a specificity of 92% (12/13) with a confidence interval of 95% (64-100%), a positive predictive value of 90% (9/10) with a confidence interval of 95% (55-100%), and a negative predictive value of 86% (12/14) with a confidence interval of 95% (57-98%).
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Regarding biologic data, increased blood lactate is related to the severity of acute mesenteric ischemia [17,18,19]. This relation has not, to our knowledge, been reported in ischemic colitis. In our series, lactate levels were obtained at the early stage of the disease in only 12 of the 24 patients. Lactate level was significantly higher in the complicated group with a median value of 1.8 mmol/L but, because of the small amount of available data, its prognostic value must be confirmed in a larger series of patients. The serum enzyme levels including LDH are not considered useful for predicting the outcome of ischemic colitis [1, 2, 20]. We observed that LDH levels and leukocyte count were significantly higher in patients with complicated ischemia, but these variables were not significant predictors of complicated ischemic colitis in the multivariate analysis.
From a morphologic point of view, animal and human studies have shown that the severity of the disease is related to the depth of the lesions in the bowel wall, the length of the affected colon, and the integrity of the residual microvascular bed [4, 6, 21,22,23]. Several methods have been used in an attempt to show these prognostic factors. Colonoscopy is frequently used for the diagnosis of ischemic colitis. However, its value is limited because endoscopy of the entire colon is dangerous in severe colitis. Furthermore, endoscopic biopsy often cannot reveal the extension of the ischemic injury into the colic wall because the biopsied fragments are limited to the mucosa and part of the submucosa. Some colic wall changes including wall thickening, mural heterogeneity, and pneumatosis may be shown on CT [7, 24, 25]. However, the prognostic value of CT in ischemic colitis has not been shown [2]. Sonography may be used to assess the morphologic changes of the colic wall [13,14,15, 26,27,28]. In our series, the wall thickness and stratification were not significantly different in the two groups of ischemic colitis. In contrast, Cheung et al. [8] observed that the progressive disappearance of the stratification of the bowel wall was related to the duration of the splanchnic blood-flow reduction and to the severity of the ischemic injury. The discrepancy between the results of Cheung et al. and our findings may be related to the different study design. The study of Cheung et al. was an experimental study performed on exposed tissue with histology as the gold standard. Our study was a clinical study related to outcome.
Vascular signals can be observed, although not constantly, in the normal colic wall when Doppler sonographic parameters are optimized to detect low-velocity flow [13]. We think that in the diseased colon, mural flow might be more easily detected for two reasons. First, the colic wall is thickened. Second, the vascularity is often increased. Both are particularly true not only in inflammatory bowel disease, including Crohn's disease [13, 26, 27], but also in transient ischemia in which increased vascularity can be observed during reperfusion [29]. In contrast, absence of flow is a sign of severe ischemia as observed in our study. Absence of flow is not unexpected because the value of Doppler sonography for predicting the viability of the ischemic intestine has been previously shown on exposed tissue in animals and humans [9,10,11,12]. According to O'Donnel and Hobson [12], the use of Doppler sonography allowed prediction of intestinal viability with a sensitivity ranging from 83% to 86%. The results of our noninvasive transabdominal approach correlate with the findings of O'Donnel and Hobson. Indeed, the sensitivity and the specificity of the absence of arterial flow to predict an unfavorable outcome were, respectively, 82% and 92% in our series.
Three types of ischemic colitis have been described by Marston et al. [3], namely the gangrenous, stricturing, and transient forms. More recently, ischemic colitis has been classified as transient or severe [2, 30]. We categorized our four patients with ischemic strictures as severe because these patients had severe persistent symptoms requiring surgery.
Our study has some limitations. First, the duration of symptoms before hospitalization could not be specified in all patients. This lack of information is a frequent limitation in clinical studies and weakens the assessment of the duration of symptom as a prognostic indicator. Second, the number of patients was limited. Therefore, these initial results must be confirmed in larger study groups before being used in clinical practice. Third, it should be remembered that the evaluation of flow on Doppler sonography is related to technical factors, such as gain settings, angulation of flow to the transducer, and transducer sensitivity. High-frequency probes cannot be used appropriately in obese patients or when the colon is deeply located. In future studies, the use of contrast agents might help to detect colic ischemia and to quantitate flow. In conclusion, in agreement with previous experimental studies, absence of blood flow in the ischemic colon on Doppler sonography is a better predictor of an unfavorable outcome than early clinical and laboratory findings.
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