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1 Department of Radiology, Asan Medical Center, University of Ulsan College of
Medicine, 388-1 Poongnap-dong, Songpa-gu, Seoul, 138-736, Korea.
2 Department of Gastroenterology, Asan Medical Center, University of Ulsan
College of Medicine, Songpa-gu, Seoul, 138-736, Korea.
Received November 6, 2001;
accepted after revision March 28, 2002.
Presented at the annual meeting of the American Roentgen Ray Society,
Seattle, April—May 2001.
Abstract
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MATERIALS AND METHODS. We retrospectively analyzed 33 patients with Crohn's disease who had undergone both barium enema study and abdominal CT. CT scans were evaluated for the presence and location of prominent vasculature. On the basis of the Crohn's disease activity index, the patients were assigned to one of three categories—active, intermediate, or quiescent disease groups—and the frequency of prominent vasculature was compared among them. Thereafter, erythrocyte sedimentation rates, C-reactive protein levels, treatment methods, and radiographic findings were compared in groups with and without prominent vasculature.
RESULTS. Prominent vasculature was more frequently found in patients with active disease (81%) than in those with intermediate (33%) and quiescent disease (0%) (p < 0.001). The erythrocyte sedimentation rates and C-reactive protein levels were higher in patients with prominent vasculature (but not at a statistically significant rate). Patients with prominent vasculature were more frequently admitted to the hospital (p = 0.024) and received more aggressive treatment (p = 0.049) than patients without prominent vasculature. The main differences of radiographic findings between the group with prominent vasculature and the group without prominent vasculature included the common occurrence of longitudinal and perpendicular ulceration (p = 0.017 for small bowel; p = 0.041 for colon) and the extensive length of organ involvement (p = 0.004 for small bowel; p = 0.036 for colon).
CONCLUSION. Prominent pericolic or perienteric vasculature seen on CT in patients with Crohn's disease suggests that the disease is clinically active, advanced, and extensive and that these patients require more aggressive treatment than patients without this CT finding.
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Although several types of CT findings have been described in patients with Crohn's disease, most reports have not focused on the vascular alteration surrounding the diseased bowel segments. In 1995, Meyers and McGuire [6] described mesenteric hypervascularity using single-detector helical CT with IV contrast enhancement. The researchers reported that tortuosity and dilatation with a prominent comb-like arrangement of the vasa recta in the small-bowel mesentery, the so-called comb sign, is a feature of active Crohn's disease. However, only two patients with active Crohn's disease were included in their study, and to our knowledge, no further work on this sign has been published.
The purpose of our study was to correlate the CT finding of prominent pericolic or perienteric vasculature with clinical disease activity, treatment methods, and barium enema study findings in 33 patients with Crohn's disease.
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The diagnosis of Crohn's disease was based on pathologic findings in 21 patients (surgery in 10 patients and endoscopic biopsy in 11). Surgical procedures included segmental small-bowel resection (n = 6), segmental resection of the colon (n = 2), and ileocecectomy (n = 2). Histologic tissue examinations of resected bowel and endoscopic biopsy specimens revealed chronic and active inflammation with formation of noncaseating granulomas and negative results for acid-fast staining in all 21 patients. In the remaining 12 patients, the diagnosis of Crohn's disease was based on the characteristic radiographic findings (such as a linear ulcer along the mesenteric border), negative results for acid-fast staining, and clinical response to the treatment for Crohn's disease, although histologic examinations of the biopsy specimens obtained at endoscopic biopsy showed only chronic or active inflammation with no evidence of granulomatous inflammation.
In 28 of the 33 patients, single-detector helical CT was performed using a Somatom Plus S scanner (Siemens, Erlangen, Germany). The entire abdomen and pelvis were scanned using 7-mm collimation and a pitch of 1.2-1.4. Conventional scanning was performed in the remaining five patients (9800 Quick system; General Electric Medical Systems, Milwaukee, WI). Scans of 8- or 10-mm slice thickness were obtained at intervals of 8 or 10 mm from the diaphragm to the symphysis pubis. Patients routinely received both oral and IV contrast material. Approximately 450 mL (E-Z-CAT [barium sulfate suspension concentrate]; E-Z-EM, Westbury, NY) was given orally 30 min to 2 hr before scanning. IV contrast medium (Iopamiro 300 [iopamidol]; Bracco, Milano, Italy) was given as a 100-125mL bolus (rate, 2.5-3.0 mL/sec) using an automated injector. In eight patients, follow-up CT was performed 3-48 months (mean, 20 months) after the initial CT. All follow-up CT was performed using a helical technique. The protocol for follow-up CT was the same as that for the initial CT. Barium enema studies were performed in all 33 patients: double-contrast barium enema in 15 patients, small-bowel follow-through in 32, and both in 13. The mean time interval between CT and barium enema studies was 5 days (range, 3-8 days).
In reviewing the medical records of each of the 33 patients, we collected the medical history, results of the physical examinations performed by physicians, and the laboratory data obtained within 1 week before or after each CT examination. To determine the clinical disease activity, we calculated the Crohn's disease activity index on the basis of the following data: the number of liquid or very soft stools per week, ratings of abdominal pain and general well-being, hematocrit level, height and body weight, presence of a palpable mass, and presence of complications [7]. We then classified the patients into three groups according to Crohn's disease activity index. Quiescent disease was defined as an index of less than 150, intermediate disease as an index equal to or more than 150 and less than 220, and active disease as an index equal to or more than 220. We also assessed laboratory data such as the erythrocyte sedimentation rate, the C-reactive protein level, and the length of time the patients had experienced symptoms before the initial CT was performed. To assess the clinician's overall assessment of a patient's status, we also evaluated the treatment methods and whether the patients were admitted to the hospital or treated as outpatients during the week after CT was performed. The treatment methods for Crohn's disease were divided into three groups: conservative management, sulfasalazine or corticosteroid therapy, and surgery.
The frequency of prominent pericolic or perienteric vasculature visible on CT was compared among the groups with quiescent, intermediate, and active disease activity. Thereafter, the erythrocyte sedimentation rates, C-reactive protein levels, treatment methods, and radiographic findings were compared for the groups with and without prominent pericolic or perienteric vasculature visible on CT.
Both CT and barium enema studies were analyzed independently by two experienced radiologists; discrepancies were resolved by consensus. Without knowledge of either the radiographic findings or the level of clinical disease activity, the reviewers retrospectively evaluated CT scans for the location of abnormal bowel segments as well as for the presence and the site of prominent pericolic or perienteric vasculature. A CT finding of prominent vasculature was considered to be present if the vasculature surrounding the diseased bowel segments was markedly tortuous and prominent [6] or if the number of the mesenteric vessels was considerably greater than the number of mesenteric vessels in the normal bowel and mesentery. A bowel was considered to be abnormal if it was more than 3 mm thick with the lumen well distended [8].
Two weeks after interpreting the CT scans, the same reviewers interpreted the barium enema studies without knowledge of the CT findings or the level of clinical disease activity. The reviewers evaluated the studies for the location of the disease (the small bowel, the colon, or both the small bowel and colon); the extent of the disease; and the presence or absence of an aphthoid lesion or nonaphthoid ulceration, a pattern of longitudinal and perpendicular ulceration (cobblestone mucosa), fold thickening, a stricture, or a fistula.
After evaluating the barium enema studies, the reviewers examined the CT scans and barium enema studies side by side. A segment-by-segment correlation was attempted between findings on the CT scans and barium enema studies, and each diseased segment visible on the barium enema studies was assigned to one of four groups according to the location of the diseased segments (small bowel or colon) and the presence or absence of prominent pericolic or perienteric vasculature on CT.
In eight patients who had follow-up CT, we noted whether a significant change in prominent pericolic or perienteric vasculature had occurred between the initial CT and the follow-up scannings.
The frequency of prominent pericolic or perienteric vasculature in the three different disease activity level groups (quiescent, intermediate, and active) was compared using the chi-square test. For statistical analysis of the findings of prominent vasculature and other clinical parameters of disease activity (erythrocyte sedimentation rate and C-reactive protein level), the Student's t test was used. The chi-square test was used to test the relationship between the treatment method selected and the presence of prominent vasculature. We used the chi-square test and Fisher's exact test to compare the frequency of each of the barium enema findings for the patient group with prominent vasculature with the frequency of the findings for the group without prominent vasculature.
The term "advanced disease" was applied to those cases in which radiographic findings—such as deep linear ulcer or fissure—indicated that the involvement of the transmural portion of the bowel extended to the serosa and beyond and in which the Crohn's disease activity index level indicated that the disease in that patient was clinically active. The term "extensive disease" was used for cases in which an extensive length of bowel was involved.
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CT failed to show one of the 27 diseased small-bowel segments and four of the 21 diseased colonic segments. Therefore, CT revealed 43 diseased bowel segments in 33 patients, only small-bowel disease in 12 of the 33 patients, only colonic disease in three, both small-bowel and colonic disease in 14, and no disease in four. CT revealed prominent pericolic or perienteric vasculature in 16 patients and depicted no prominent vasculature in 17.
Among 33 patients, 16 had an active level of the disease, nine had an intermediate level, and eight had a quiescent level. A CT finding of prominent pericolic or perienteric vasculature was more frequently found in patients with active disease (81%, 13/16 patients) than in patients with quiescent disease (none of eight patients) or intermediate disease activity (33%, 3/9 patients) (p < 0.001). Although erythrocyte sedimentation rates and C-reactive protein levels were higher in patients with prominent vasculature, no statistically significant difference was present between the group with prominent vasculature and the group without prominent vasculature. The mean erythrocyte sedimentation rate was 30.4 ± 18.9 mm/hr for the prominent vasculature group and 23.2 ± 15.7 mm/hr for the normal vasculature group (p = 0.212). The mean C-reactive protein level was 4.8 ± 5.7 for the prominent vasculature group and 3.0 ± 4.4 for the normal vasculature group (p = 0.273).
Comparison of the treatment methods and whether the patients were admitted to the hospital or treated as outpatients for the groups with and without prominent vasculature on CT is summarized in Table 1. These differences between the two groups were statistically significant (p = 0.049) for being admitted to the hospital during the week after initial CT and for receiving oral or IV corticosteroid. Surgical treatment was performed in two patients (13%) with CT finding of prominent vasculature and in two (12%) without the finding. The surgical procedures included a segmental resection of the jejunum for jejunal obstruction (n = 1), ileocecectomy with an impression of lymphoma (n = 1), segmental resection of colon for colovesical fistula (n = 1), and open drainage of an abdominal wall abscess (n = 1). The duration of symptoms before the patients underwent CT was not significantly different for the two groups (31.9 ± 29.9 months for prominent vasculature group vs 37.1 ± 39.3 months for normal vasculature group, p = 0.689).
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A side-by-side comparison of the CT scans and barium studies was possible for 41 (25 small bowel and 16 colon) of the 43 diseased bowel segments. Such comparison was not possible for two bowel segments (one small-bowel segment and one colon segment) of the two patients whose CT scans showed both small-bowel and colonic diseases. These patients had undergone only a small-bowel follow-through or colonic study. For the segments we were able to compare, we found that nine of the 25 diseased small-bowel segments and eight of the 16 diseased colonic segments exhibited prominent pericolic or perienteric vasculature on CT. The results of comparing the radiographic findings of the diseased small-bowel segments for the groups with and without this CT finding are summarized in Table 2 (Figs. 1A,1B,1C,2A,2B,3A,3B), and the results of comparing the radiographic findings of the diseased colonic segments for the two groups are summarized in Table 3 (Figs. 4A,4B,4C,5A,5B,6A,6B).
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In the eight patients who had follow-up CT, five exhibited prominent pericolic or perienteric vasculature on the initial CT scan. No significant interval change in prominent vasculature was seen on follow-up CT scans obtained between 3 and 48 months (mean, 20 months) after the initial CT (Fig. 1A,1B,1C). These patients had active Crohn's disease with a mean Crohn's disease activity index of 306 (range, 206-375) at the time of the initial CT; they still had active Crohn's disease at the time of the follow-up CT with a activity index of 279 (range, 183-342). In the other three patients, the initial CT scan did not show prominent vasculature, and this finding was also absent on the follow-up CT scan obtained between 14 and 48 months (mean, 30 months) later. These patients had mildly active Crohn's disease with a mean activity index of 203 (range, 174-230) at the time of the initial CT and a mean activity index of 215 (range, 205-223) at the time of the follow-up CT.
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Recently, Doppler sonography has shown that the activity of Crohn's disease causes a substantial increase in the arterial flow volume and a decrease in the resistive index [10,11,12]. In addition, Giovagnorio et al. [12] measured postprandial resistive change, showing the difference between the fasting resistive index and the restive index 15 min after a meal. These researchers found smaller postprandial resistive changes in patients with active Crohn's disease than in healthy volunteers or in patients with inactive Crohn's disease. In both the volunteers and patients with inactive Crohn's disease, the postprandial resistive index decreased more markedly than the fasting resistive index. Therefore, Giovagnorio et al. concluded that inflammatory hyperemia may cause an increase in blood flow and a decrease in resistance in patients with active Crohn's disease and that maximally dilated mesenteric vessels fail to dilate in response to eating. Recently, Spalinger et al. [13] reported that vessel density in diseased bowel loops was significantly higher on Doppler sonography in patients with active Crohn's disease than in patients with Crohn's disease that is in remission. These studies suggest that active Crohn's disease is related to increased mesenteric blood flow.
Various factors have been proposed as the cause of hypervascularity in patients with Crohn's disease. In examining resected bowel specimens from patients with ileocolonic Crohn's disease, Wakefield et al. [14] found a granulomatous vasculitis in the muscularis propria of the involved bowel and suggested that a multifocal gastrointestinal infarction resulting from the vasculitis may be involved in the pathogenesis of Crohn's disease. In addition, they identified areas of vascular proliferation and neovascularization attempting to bypass the areas of ischemia. In 1997, Bousvaros et al. [15] found a strong correlation between the serum level of the basic fibroblast growth factor and disease activity in patients with Crohn's disease. Basic fibroblast growth factor stimulates angiogenesis and promotes healing of wounds in tissue. Therefore, it may have a partial role in the neovascularization in active Crohn's disease. Several other factors, such as somatostatin and arachidonic acid [16, 17], have also been proposed as the possible causes of hypervascularity in patients with active Crohn's disease. Whether hypervascularity in patients with Crohn's disease is the result of neovascularization in the injured bowel wall or merely of inflammatory hyperemia is still not known.
Our study showed that CT findings of prominent pericolic or perienteric vasculature (i.e. hypervascularity) correlated well with higher Crohn's disease activity indexes. Although the Crohn's disease activity index has been criticized because of its subjectivity and interobserver variability, it is considered to be the most useful method of assessing overall disease activity in the Crohn's disease [18, 19]. Therefore, many studies have used Crohn's disease activity index as the gold standard for assessing disease activity [12, 13, 15, 20]. We also found that patients with prominent vasculature visible on CT received more aggressive treatment (such as corticosteroids) and that they were more frequently admitted to the hospital than the patients without this CT finding. Therefore, prominent vasculature on CT may have a therapeutic implication in the clinical setting. Erythrocyte sedimentation rate and C-reactive protein level are known to be potentially useful methods for assessing inflammatory activity in patients with Crohn's disease [21]. Erythrocyte sedimentation rates and C-reactive protein levels were also higher in patients with prominent vasculature on CT, although not to a statistically significant degree. Thus, we were able to confirm that the presence of this CT finding suggests clinically active Crohn's disease.
The radiographic findings of Crohn's disease vary from the earliest changes of lymphoid hyperplasia, aphthoid lesion, and fold thickening to the more advanced changes of deep linear and transverse ulcerations that create the classic cobblestoning pattern in the mucosa and finally to the development of strictures and fistulas [22,23,24]. In our side-by-side analysis of the CT scans and barium enema studies, we found that the main differences in the radiographic findings for the small bowel and colon between the group with prominent pericolic or perienteric vasculature and the group without this type of vasculature were the common occurrence of longitudinal and perpendicular ulceration (cobblestone mucosa) and the extensive length of involvement of the small bowel or colon in patients with the CT finding of prominent vasculature. In other words, the patients with prominent vasculature had clinically active, advanced, and extensive disease. Similar studies have been attempted by other researchers without using CT. Yao et al. [20] concluded that the cobblestone pattern correlated with disease activity in Crohn's disease; patients with cobblestoning had significantly higher Crohn's disease activity indexes, erythrocyte sedimentation rates, and C-reactive protein levels than did patients with longitudinal ulcers. Unlike Meyers and McGuire [6], who suggested hypervascularity is a feature of the early stage of Crohn's disease, our results indicate that prominent vasculature (hypervascularity) on CT correlates with the radiographic findings of advanced Crohn's disease, such as a pattern of longitudinal and perpendicular ulceration and an extensive length of involvement in the small bowel or colon.
We have also shown that the length of time that patients experienced symptoms before undergoing initial CT was the same for the groups with and without prominent pericolic or perienteric vasculature. Moreover, among the eight patients who had follow-up CT, the five who had prominent vasculature on their initial CT scans also showed the same CT finding on their follow-up CT scans. The Crohn's disease activity index in those patients at the time of the initial CT was similar to the disease activity index at the time of the follow-up CT. This result may suggest that prominent vasculature seen on CT may be irreversible in patients with high Crohn's disease activity indexes. However, further longterm follow-up investigation appears to be necessary to determine whether prominence of the vasculature on CT is reduced or appears normal when the disease activity index in such patients is converted to inactive levels.
Prominent pericolic or perienteric vasculature on CT is not a specific finding for diagnosing Crohn's disease. The same or similar CT findings have been reported for many other gastrointestinal tract diseases, including vasculitis (such as systemic lupus erythematosus and polyarteritis nodosa), mesenteric thromboembolism, strangulated bowel obstruction, colonic diverticulitis, ischemic colitis, and perforated colon cancer [25,26,27,28]. In addition, the presence of prominent vasculature on CT may help differentiate Crohn's disease from intestinal tuberculosis for those cases in which findings of colonoscopy or a barium enema study are equivocal, confounding attempts to establish the diagnosis [29].
The limitation of our study is that there may be a selection bias: 60% (33/55) of the patients who received a diagnosis of Crohn's disease had imaging studies available for review. We did not include the severity of patients' symptoms as one of the evaluation parameters, but possibly some patients with minor symptoms did not require an imaging study. Exclusion of these patients may have had a slight influence on our results.
In conclusion, the presence of prominent pericolic or perienteric vasculature on CT in patients with Crohn's disease suggests that the disease is clinically active, advanced, and extensive. Patients with this CT finding require more aggressive treatment than the patients without the finding.
Acknowledgments
We thank In Suk Lee, Department of Statistics, College of Natural Science,
Kyungpook National University, Taegu, Korea, for his advice on the statistical
analysis of the data and Bonnie Hami, Department of Radiology, University
Hospitals of Cleveland, OH, for her editorial assistance.
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