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1 Department of Radiology, Hospital Universitario Dr. Peset, 90 Gaspar Aguilar
Ave., Valencia 46017, Spain.
2 Department of Gastroenterology, Hospital Universitario Dr. Peset, Valencia
46017, Spain.
Received May 4, 2004;
accepted after revision July 21, 2004.
Address correspondence to T. Ripollés
(ripolles_tom{at}gva.es).
Abstract
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MATERIALS AND METHODS. We reviewed the histories of patients diagnosed with ischemic colitis over a period of 5.5 years. Sixty-two patients had undergone sonographic examinations. The spectrum of sonographic findings in ischemic colitis was based on the original imaging report, with an analysis of the presence of colonic abnormalities and their associated alterations. In the second part of the study, we divided the patients into two groups according to the presence or absence of transmural necrosis, and the sonographic findings of each group were compared. Ten patients had sonographic follow-up studies during their hospital stay.
RESULTS. The prospective sensitivity of sonography for the characterization of colonic abnormalities was 93.5% (58/62 patients). Segmental involvement was detected in 57 of the 58 patients, with left-sided colitis in 47 (81%). The mean length of bowel involved was 19 cm, with a mean wall thickness of 7.6 mm. Colon wall stratification was preserved in 38 patients (66%). Altered pericolic fat was observed in 16 patients (28%). Absence of or barely visible color Doppler flow in the thickened bowel wall was recorded in 80% of patients. Altered pericolic fat was the only sonographic variable significantly associated with the presence of transmural necrosis (p = 0.004). Improvement as assessed on sonography was observed in all patients with a good clinical course. In patients with transmural necrosis, sonography did not show improvement.
CONCLUSION. Sonography is a valuable technique for the detection of colonic abnormalities resulting from ischemic colitis. In this study, altered pericolic fat or the absence of improvement in sonographic follow-up studies were factors associated with transmural necrosis.
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Barium enema and CT findings of ischemic colitis have extensively been described in the radiology literature [7–12]. However, few publications have addressed the sonographic findings of this disorder. At present, sonography is the first diagnostic imaging technique used in many hospitals in patients with abdominal disorders. As a result, the sonographic features of ischemic colitis should be known to radiologists in order to avoid delays in diagnosis and treatment. Previous studies have shown gray-scale and color Doppler sonography to be useful in the differentiation between inflammatory and ischemic bowel wall thickening [13, 14]. A study has also shown the absence of arterial flow in the wall of the ischemic colon to be a good predictor of an unfavorable outcome of ischemic colitis [15]. However, in these series, sonographic evaluation was limited to a small number of cases and mainly to severe forms of intestinal infarction. On the other hand, diagnostic protocols have not yet defined the role of sonography in application to ischemic colitis [16].
The aim of this study was to describe the sonographic findings of ischemic colitis in an extensive series of patients and to evaluate whether any findings carry a prognostic value in relation to the presence or absence of transmural necrosis.
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Sonography was performed by residents on duty or by experienced sonographers, depending on the time of the request. Sonography was performed using a Sonolayer SSH-140A or a PowerVision 5000 scanner (Toshiba) and convex 3- to 6-MHz, linear 5- to 10-MHz, and transvaginal 8- to 4-MHz transducers. Transabdominal scanning was performed in all cases, transvaginal scanning was used in 10 patients, and endorectal scanning in none. Sonographic findings of ischemic colitis were obtained from the original sonography reports. In only a few cases, the hard-copy images were reviewed to complete some sonographic characteristic (i.e., length of affectation or stratification of the wall). In these cases, the sonographic findings were assessed in consensus by two radiologists who were blinded to results.
The following findings were assessed: the location and approximate length of the involved colonic segment, colon wall thickness, symmetric versus asymmetric thickening, bowel wall stratification or nonstratification, abnormal echogenicity of the pericolic fat, and the presence of peritoneal fluid. A wall thickness of greater than 3 mm was considered abnormal. Symmetric involvement was considered when the same degree of thickening was present throughout the circumference of the abnormal segment. The colon wall was considered to be stratified when the mucosa, submucosa, and muscularis propria were visible as separate layers, and was considered nonstratified when all layers were indistinct (Figs. 1A, 1B, and 2). When a patient presented two different thickened bowel segments, the finding was considered to be nonstratified. Doppler parameters analyzed were presence of parietal vascular flow and calculation of resistive index. Color Doppler flow parameters were optimized for maximal sensitivity using a special presetting (filter at low setting [50 Hz] and lowest velocity scale [2 cm/sec]) designed for the detection of low-velocity flow in the bowel wall. Color Doppler flow was considered present when color pixels persisted throughout the observation period. Color Doppler flow was always confirmed by obtaining an arterial or venous signal at the location of the color pixel (Figs. 3A, 3B, and 3C). Color Doppler flow was subjectively graded as absent, barely visible, or readily visible. The color wall resistive index ([peak systolic velocity – end diastolic velocity]/peak systolic velocity) was calculated from the arterial waveforms.
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The sonographic findings were then correlated with the clinical and pathologic data to determine whether any findings were associated with transmural versus partial necrosis. Patients were classified as having transmural ischemia when it was shown at surgery (macroscopic appearance during laparotomy) or in a histologic study of the surgical specimen. Conversely, patients were classified as having transient ischemia if they recovered with conservative treatment or if they did not have transmural necrosis at surgery or in the histologic analysis. During hospitalization, 10 of 58 patients underwent sonographic control examinations between 3 and 5 days after the first sonogram.
Basic descriptive statistics, including the mean and SD for continuous variables, and the absolute frequency and percentage for discrete variables, were used to characterize the study patients. Later, patients were divided into two groups on the basis of the presence of infarction, and the variables observed in each group were compared. Before parametric tests were performed, the normal distribution of the continuous variables was ascertained by means of the Kolmogorov-Smirnov test. For univariate analysis, the Mann-Whitney U test was applied for comparing continuous variables and Fisher's exact test for contrasting categoric variables. A p value of less than 0.05 was considered to indicate a statistically significant difference. Finally, a multivariate nonconditional logistic regression model was developed, the dependent variable being the development or nondevelopment of transmural ischemia. The association measure was the odds ratio, with calculation of the corresponding 95% confidence interval (CI). The SPSS (Statistical Package for the Social Sciences) version 9.0 statistical package was used throughout.
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Segmental involvement of the colon was detected in 57 of 58 patients with ischemic colitis; the entire colon (pancolitis) was affected in only one patient. Ischemic colitis was identified on the right side in eight patients (14%) (Figs. 4A and 4B); in the hepatic flexure, ascending colon, and cecum in seven patients; and in the cecum in only one. Colitis was detected in the left side in 47 patients (81%); in the splenic flexure, descending colon, and sigmoid colon in 29 patients (six of them with rectal involvement); as isolated sigmoid colitis in six patients; in the descending colon in nine patients; and in the splenic flexure in three cases. Only two patients (3%) had isolated ischemic colitis of the transverse colon. There were no cases of discontinuous involvement or isolated rectal ischemia.
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The prospective sensitivity of sonography for colonic abnormalities was 93.5% (abnormal sonographic findings in 58/62 patients). The length of involvement varied from 6 to 80 cm (mean length, 19 cm). Six patients (10%) showed focal involvement (length, < 10 cm). Segmental involvement (10–30 cm) was identified in 46 cases (80%). Symmetric thickening was present in all patients. The thickness of the colon wall in the affected segments ranged from 3.5 to 15 mm (mean, 7.6 mm). Colon wall stratification was preserved in 38 patients (66%). Altered pericolic fat was seen in 16 patients (28%) (Fig. 2) and free fluid in 11 (19%). Intramural air (pneumatosis coli) was detected in only one patient and was associated with air in the portal vein (Figs. 4A and 4B). Color Doppler flow was observed in the wall of the affected colon segment in 40 (87%) of the 46 patients in whom it was evaluated, whereas flow was absent in the other six patients (13%). Color Doppler flow was considered to be barely visible in 31 patients (67%) and readily visible in nine patients (20%) (Figs. 2, 3A, 3B, 3C, 5A, and 5B). The resistive index could be calculated in 32 patients, with a range of 0.50–1 (mean, 0.73). In 90% of patients, the index was greater than 0.60.
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One case was seen to be the result of inferior mesenteric vein thrombosis, with diffusely echogenic pericolic fat that contained numerous blood vessels (vascular engorgement), a situation not seen in the rest of cases (Fig. 2). Two cases resulted from colon neoplasm having lengths of 9 and 23 cm, with no sonographic distinction between the ischemic segment and the tumor.
Four sonographic examinations were regarded as false-negative studies because of nonvisualization of colon wall thickening. Two of these patients presented free fluid. The histologic report of the surgical specimen in one of these cases described a paper-thin colon wall.
Laparotomy was performed in 13 patients (22%), and colonic resection was performed in 11. Two patients had surgically proven extensive necrosis, but resection was not considered in these cases and death occurred during follow-up. In six patients, the pathologic study of the partial colectomy specimen showed transmural necrosis. In three cases, partial colonic resection was performed but transmural necrosis was not shown by the histologic analysis. In two cases, segmental resection was performed for colon carcinoma associated with ischemic colitis. The patients were divided into two groups on the basis of the presence of infarction. The first group included eight patients (14%) with transmural ischemia that was histologically or surgically proven. The second group comprised 50 patients (86%) with transient ischemia. The time elapsed between sonography and surgery ranged from 1 to 5 days (mean, 2 days). Five deaths were considered to be related to ischemic colitis (mortality rate, 9%).
Tables 1 and 2 show the comparative clinical, biologic, and sonographic findings of the patients with nontransmural (n = 50) and transmural (n = 8) ischemic colitis. Of the hypothetic factors predicting outcome or the existence of transmural necrosis, only abnormal pericolic fat was seen to be significantly more frequent in the patients with transmural necrosis (p = 0.004), exhibiting a sensitivity of 75% and a specificity of 80% in relation to the diagnosis of transmural necrosis. No significant differences were observed for the other factors between the two patient groups. All patients (n = 4) with an affected colon length of more than 40 cm had transmural necrosis; however, no significant difference was seen in the length of the affected bowel segment between the two groups.
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The multivariate logistic regression model showed altered pericolic fat to be the only variable significantly associated with the presence of transmural necrosis (odds ratio, 19.269; 95% CI, 1.54–240; p = 0.0215). The rest of the sonographic, clinical, and biologic variables were not significant.
Of the 10 patients who underwent sonographic follow-up examinations, a clear reduction was observed in the length, thickness, and flow detected in the affected colon in all patients in whom the clinical outcome proved favorable (n = 7) (Figs. 6A and 6B). Absence of sonographic change was seen in the patients in whom transmural necrosis was identified on the histologic study after surgery (n = 3).
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During the study period there were 14 (18%) of 80 patients with transmural necrosis: eight with abnormal sonographic findings, two with false-negative sonographic findings (group of patients included in the study), and four with no sonographic examination (patients not included). No significant differences were observed in relation to transmural necrosis (p = 0.506) between the inclusion or exclusion patient groups.
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Colonic ischemia has been reported to be the most common vascular disorder of the digestive tract in patients older than 65 years [1, 20, 21], and its incidence continues to increase as the overall population ages. Despite this, the incidence of ischemic colitis may be underestimated in daily clinical practice [4, 16, 22]. A number of reasons can explain this underestimation, including its varied presentations (with sometimes unspecific manifestations), the fact that most patients with mild or transient disease do not seek medical help or are not hospitalized, its similarity to inflammatory bowel disease, and the absence of an obvious precipitating cause in most cases. Therefore, the initial step in the diagnosis of ischemic colitis is suspicion of the presence of ischemic disease. Colonic ischemia is clinically suspected when the patient manifests the classic presentation of abrupt onset of lower abdominal pain and rectal bleeding. However, if the clinical presentation is nonspecific or misleading, many of these patients are characteristically evaluated on an emergency basis with imaging techniques such as CT or sonography, which allow identification of bowel wall alterations. It is in these situations that the radiologist can suggest an ischemic cause, making possible an early diagnostic workup and immediate therapy, which is essential for a successful outcome [23]. The diagnosis as often as possible must be confirmed by colonoscopy and biopsy.
The colon is easily accessible to sonography, and information can be obtained regarding not only the intestinal wall but also the possible changes in pericolic tissues. The prospective detection in our study of colon wall thickening in 93% of cases shows sonography to be highly sensitive in showing the wall thickening that characterizes ischemic colitis. An important limitation of sonography is the lack of specificity (similar to CT) of bowel wall thickening, because that can be observed in a number of disorders (infection, inflammation, ischemia, or neoplasm). Despite this limitation, earlier studies indicate that an ischemic cause should be suspected in elderly patients presenting with wall thickening of a long colon segment (> 10 cm), particularly on the left side, with barely visible or no color Doppler signal intensity [11, 13]. Our results coincide with the results of these studies, because our affected patients were 75 years old on average, with a mean affected colon length of 19 cm, left-sided segmental involvement in 81%, and absent or barely visible color Doppler flow in 80% of patients.
The ischemic process exhibited a segmental distribution in 98% of our patients. Although the left side was the most frequent location, our results show that any segment or combination of segments of the colon can be involved. The rectum was affected in 10% of the patients, associated in all cases with leftsided colitis. We probably underestimated the incidence of rectal involvement because this area may be difficult to explore with transabdominal scanning. Endorectal or transvaginal sonography could increase the sensitivity of sonography when this area is affected. Isolated ischemic proctosigmoiditis was the only localization not seen in our series, but the proctosigmoid region seems to be an infrequent location [24]. Wall thickening was symmetric in all cases and exceeded 10 cm in 52 (90%) of the 58 patients, a fact that allows differentiation in most cases from neoplasia [25, 26]. Most primary neoplasms of the gastrointestinal tract present as short (< 10 cm) asymmetric lesions of bowel wall thickening with abrupt margins [25, 26]. However, when ischemic colitis is the result of colonic carcinoma, it may prove difficult to distinguish between the neoplastic and the ischemic segments on the basis of sonographic findings, as occurred in two of our patients. The mean bowel wall thickness in our series (7.6 mm) was similar to the 8 mm reported by Danse et al. [15], and slightly less than the 11 mm published in another series [13, 27]. Our results are also similar to those of a previous series with CT evaluation [11]: mean of thickening and length of involvement values of 8 mm and 19 cm, respectively, and segmental distribution in 89% of patients.
Color Doppler flow was evaluated in only 46 of our 58 patients. In 80% of patients, absent (n = 6) or barely visible (n = 31) color Doppler flow was observed in the thickened bowel wall of patients with ischemic colitis. According to Teefey et al. [13], these color Doppler findings should prompt a strong consideration for ischemia. In their series, 86% of the cases of ischemic flow were barely visible or not shown with color Doppler flow, compared with 90% of the patients with acute inflammatory disease who showed abundant color Doppler flow at the wall level [13]. That same study showed an absence of flow in 50% of the cases of ischemia, a percentage far greater than the 13% recorded in our series. In any case, the authors of that study admit the existence of patient selection bias because they examined seriously ill patients, which may have skewed their results.
In 20% (n = 9) of the 46 patients in whom bowel wall flow was evaluated, hyperemia of the thickened wall was noted, with readily visible color Doppler flow, all corresponding to patients with transient ischemia. Ischemic segment hyperemia is a finding that has already been reported on angiography in some cases of reversible ischemic colitis [28]. Possibly increased vascularization was shown in such patients because sonography was performed in the reperfusion phase as a result of resolution of ischemia. In routine clinical practice, these patients would be indistinguishable from patients with active inflammatory disease. With regard to the resistive index, 90% of the cases had a value of more than 0.60, coinciding with previous series that reported increased resistive indexes in all cases of ischemia in which an intramural waveform could be recorded [13, 14].
Once the condition has been diagnosed, it is important to identify those patients who will develop complicated forms of the disease. Knowledge of these severity factors can help define adequate treatment and may improve the prognosis of the disorder [6, 19, 29]. Classically, a number of clinical factors have been associated with ischemic colitis outcome, including patient age, affected bowel length, hypovolemic shock, concomitant cardiovascular disease, and the time elapsed to treatment application [30, 31]. Nevertheless, the usefulness of these parameters in predicting the course or outcome of the ischemic process remains controversial [5, 6, 16, 31].
Along this same line, the second objective of our study was to determine whether some sonographic feature can predict the presence or development of transmural necrosis. Tables 1 and 2 show the frequencies of the clinical, biologic, and sonographic findings in patients with reversible ischemia versus those with transmural infarction. Only altered pericolic fat was significantly more frequent in patients with transmural necrosis (p = 0.004) than in patients without infarction. Moreover, the multivariate analysis of logistic regression showed fat involvement to be the only predictive factor for the development of transmural necrosis, the probability of the latter being almost 20-fold greater in the presence of fat alterations. Altered pericolic fat has been described mainly in inflammatory processes such as diverticulitis, acute appendicitis, or Crohn's disease, indicating extramural spread of the disease. Pericolic fat changes have not been reported in earlier clinical series, although as early as 1963, Boley and Schwartz [20], in an experimental study in dogs, observed pericolic fat changes that were more severe when obstruction affected the terminal vascular branches. The exact cause or mechanism underlying this sign in ischemic phenomena is not clear. Balthazar et al. [11], in a CT study, described two CT appearances of the colon wall: wet and dry. In this context, a wet or shaggy appearance with varying degrees of pericolic streakiness could be similar to the fatty tissue alterations seen in our series. However, no correlation was established between the gross CT appearance and the development of transmural necrosis in that series.
In our series, absence of flow in the ischemic colon wall was not significantly more frequent in patients with transmural ischemia than in patients with transient ischemia (17% vs 13%, respectively) (Table 1). Previous experimental and clinical studies have shown the value of absent flow in predicting the viability of the ischemic intestine. Danse et al. [15] detected flow in only 18% of patients with severe ischemia versus 92% of patients with transient ischemia. This contrasts with our series, in which most patients (83%) with transmural necrosis showed flow in the ischemic segment wall. This difference could not be attributed to error, because color Doppler flow was always confirmed by the detection of an arterial or venous signal, thus excluding that these signals were originated by flash or motion artifacts. The discrepancy between earlier results and our findings may be due to the fact that the previous studies were clinical surveys related to outcome, whereas our study was a clinical survey with histology as the gold standard. Some patients can undergo surgery in the absence of transmural necrosis (five patients in our series). It is also possible that flow detection in cases of severe ischemia in our series was related to technical improvements in the sonographic systems that allowed the detection of slow flow. However, our results must be analyzed with caution, because in some patients the time elapsed from sonographic examination to surgery was too long (range, 1–5 days), thereby preventing us from ruling out the possibility that the sonograms may have been obtained while the disease process was still in the transient ischemic phase and before the appearance of transmural necrosis. Partial ischemia can rupture the intestinal mucosal barrier and cause systemic damage, and some toxins released during reperfusion of the ischemic segment can contribute to the pathogenesis of severe intestinal necrosis [32].
Nevertheless, we agree with Teefey et al. [13] that the absence of color Doppler flow does not prove that an intestine is nonviable. The absence of flow may be due both to technical factors (the flow rate being too low to allow detection with currently available sonographic equipment) and to patient-related variables, including body habitus and breathing motion artifacts in uncooperative individuals or seriously ill patients. Moreover, in our series we observed the disappearance of parietal flow in the sonographic follow-up of some patients, coinciding with clinical improvement in relation to resolution of the ischemic process. In our experience, parietal flow detectable on color Doppler sonography is variable, depending on the phase in which the study is made (ischemia, reperfusion, or resolution).
Pneumatosis intestinalis or portomesenteric venous gas in patients with ischemia is considered an ominous radiographic finding, usually indicating transmural necrosis. Nevertheless, recent articles have suggested that portomesenteric venous gas is not intrinsically a predictor of mortality [33, 34], as we saw in the only such case in our series, which evolved favorably with conservative treatment.
Most of the patients in our study showed a good clinical outcome: in 45 patients ischemic process resolved with conservative management; eight patients underwent surgery with good outcome; and five patients died after surgery for transmural necrosis of the colon (9%). Balthazar et al. [11], in 1999, recorded a global mortality rate of 11%. This figure is similar to our own and is in marked contrast to the 36% mortality rate reported by Wittenberg et al. [7] in 1975. These differences may be explained in part by the improvements made during the past 25 years in both surgical techniques and postoperative care and in part by an earlier detection capability and the identification of milder cases of ischemia.
Fulminant cases of ischemic colitis with peritonitis are rare, indicate gangrene or perforation, and are a clear mandate for immediate surgery; in most such situations imaging is not required. However, most cases of ischemic colitis resolve spontaneously (78% in our series). Colonoscopy in these cases of transient ischemia should be performed at an early stage, because in the absence of transmural necrosis the endoscopic lesions show rapid improvement (48 hr–1 week) [19, 29, 35]. This has been our experience with sonographic follow-up examinations as well. In our series, sonographic follow-ups in patients without transmural necrosis (n = 7) showed a marked decrease in the length of the involved bowel segment, wall thickness, and color Doppler signal intensity. Therefore, the rapid evolutive endoscopic changes can be observed and monitored on sonography. In contrast, in our series, the patients with transmural necrosis (n = 3) showed no improvement at serial sonographic examinations. According to Greenwald and Brandt [29], prompt recognition of persistent disease, together with early diagnosis and close follow-up, are the keys to successful management of ischemic colitis. An active observation period of patients with continuing symptoms is necessary for early recognition of persistent disease (which is an indication of segmental colectomy) [16]. Serial sonographic examinations could be an effective method to monitor the course of the ischemic process. These initial results will require larger patient series to be conducted before consideration for possible application in clinical practice.
Our series was performed in a common clinical setting, a general community teaching hospital, with many of the studies made by residents on duty who had limited experience in sonography. Consequently, our results may be extrapolated to any other similar hospital. The high sensitivity (93%) shown in our study is far greater than previously published values (26–36%) with CT evaluation [36, 37]. We expect that MDCT will be even more sensitive in depicting the alterations of ischemic colitis, although its sensitivity is not known because of a lack of prospective studies. During our study period, 18 patients with ischemic colitis did not undergo sonographic examination. Even if sonography were found to be negative in these 18 patients (a situation we consider unlikely), the sensitivity would still be great (73%). False-negative sonographic studies can be explained by a number of circumstances. In patients with early ischemia, imaging findings can be normal [30]. On the other hand, there are no doubts that ischemic colitis with wall thinning (as in one of our patients) can be missed on sonography, although this circumstance is more frequent in acute mesenteric ischemia. Also, the sonographic evaluation of the splenic flexure, behind the ribs, and especially of the rectum on transabdominal sonography, may be limited and therefore may be the cause of a false-negative examination. Finally, some false-negative results are inherent to the technique because sonography is operator-dependent.
Limitations of our study include the small number of cases with transmural necrosis, which reduces the significance of our results in relation to the prognostic value of pericolic fat changes, parietal vascularization, and the sonographic follow-up. Our low prevalence (14%) of cases with transmural necrosis is similar to the only published report that included all patients hospitalized with ischemic colitis [31]; we therefore believe that this experience accurately reflects real-world clinical practice. The limited number of patients with transmural ischemia was possibly the cause for our not seeing significant differences in the length of the affected segment. Previous studies have also shown that the severity of the disease is related to the length of affected colon [3, 33].
Another limitation is that this was a retrospective study, as a result of which no analysis of specificity has been possible. Moreover, the fact that a retrospective design was adopted, with the collection of data over a period of years and involving sonographic studies performed by different radiologists, could imply the existence of variability in the evaluation of the sonographic findings, particularly with respect to parietal vascularization determined by color Doppler flow.
The consensus at present is that CT is the technique of choice in the evaluation of abdominal ischemia. This affirmation is uncontestable when small-bowel involvement is suspected. However, in disorders at the colon level, our results suggest that sonography may be a valuable technique, with results comparable to CT for showing colon wall changes. Only in detecting air in the intestinal wall is CT clearly superior, but this finding is infrequent in ischemic colitis (three cases [5%] in the series of Balthazar et al. [11]). Further prospective studies contrasting sonography with CT are needed to confirm these opinions.
In conclusion, on the basis of our results, sonography may play an important role in both the diagnosis and follow-up of ischemic colon disease. On one hand, sonography is a sensitive technique for the early detection of changes in the colon wall resulting from ischemia, and it can suggest this cause in the appropriate clinical setting. Absent or barely visible color Doppler flow is highly suggestive of ischemic thickening of the bowel wall. On the other hand, although the number of patients with transmural necrosis in our series is too small to allow definitive conclusions, our experience suggests that sonography may provide data for identifying patients with an increased probability of developing necrosis, either by detecting cases with altered pericolic fat or through sonographic follow-up studies to identify patients who fail to improve, both of which, according to our results, are associated with the existence of transmural necrosis. Further studies will be necessary to confirm these preliminary results.
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