Ultrasound demonstration of bowel wall thickness in inflammatory bowel disease

ClinicalRadiology (1984) 35, 227-231 © 1984Royal College of Radiologists

0009-9260/84/258227502.0C

Ultrasound Demonstration of Bowel Wall Thickness in Inflammatory Bowel Disease P. A. DUBBINS

The Division of Diagnostic Radiology (Ultrasound), Plymouth General Hospital (Freedom Fields), Plymouth

The idiopathic inflammatory bowel diseases include ulcerative colitis and proctitis and Crohn's disease. Their aetiology and the relationship of the one to the other remain obscure. The incidence of the inflammatory bowel diseases, especially Crohn's disease, has increased throughout the world (Mendeloff, 1980). Diagnosis of the inflammatory bowel diseases depends upon history, radiological and endoscopic findings and the results of biopsy. Contrast radiology is predominantly used to assess the site and extent of bowel involvement and, subsequently, may be used at intervals to assess response to treatment and the development of complications. Grey-scale ultrasound is a simple, non-invasive technique which, until recently, was considered of limited value in the investigation of bowel-associated disease, largely because of the deleterious effects of luminal gas upon the ultrasound image. However, several factors, including technological advances in equipment and a greater appreciation of ultrasound appearances of normal and abnormal bowel, have allowed the recognition of many bowel pathologies (Fleischer et al., 1980). Indeed, ultrasound has been shown capable of demonstrating abnormality in Crohn's disease (Holt and Samuel, 1979; Sonnenberg et al., 1982). Specifically, areas of bowel with demonstrably thickened bowel wall and matted bowel loops were identified. This study assessed the value of ultrasound in the differential diagnosis of inflammatory bowel disease and its efficacy in the assessment of response to treatment.

amination. In three of these patients a histological diagnosis of non-specific or indeterminate colitis was made and these were excluded from the study. In 26 of the cases the inflammatory bowel disease was newly diagnosed and ultrasound was used as part of the diagnostic work-up. Two other patients had established diagnoses of Crohn's disease and ulcerative colitis, respectively, but presented with recrudescence or change in symptoms. In all patients the diagnosis was confirmed by histology. Although clinical details were known at the time of the examination, histology and radiographic findings were not available. Appropriate contrast radiology was performed within i month of the ultrasound examination in all but one case (Crohn's disease Case 9) where the most recent contrast radiological studies had been made 1 year previously. All patients were examined on commercially available static B-mode and real-time equipment. Transducer frequencies of 3-5MHz were used, usually selecting medium or short internal focus. Static scans were performed in both longitudinal and transverse planes over the entire abdomen at 1 cm intervals. Later cases were at first surveyed with real-time and, subsequently, areas of suspected abnormality were further evaluated with the static scanner. Measurements were made on screen using electronic callipers. Images were recorded on multiformat film or multiformat photographic paper. Bowel wall thickness was assessed on undistended bowel measuring the maximum thickness of the echo-poor halo of bowel exhibiting the 'mucous pattern', the so-called 'target' appearance (Fleischer et al., 1981). The measurement was repeated after compression was applied to the abdominal wall by pressure on the transducer in order to obviate confusion with fluid-filled loops of bowel. All of the examinations were performed and interpreted by the author. All patients were examined following a 6h fast but no other attempts were made to diminish bowel gas. Bowel contrast agents were not used for the ultrasound examination but in one patient who initially had a normal ultrasound examination the study was repeated with full-bladder technique. Twenty-two patients were examined at an interval of 2-4 months from the original ultrasound investigation after anti-inflammatory and/or immunosuppressive treatment. One patient was examined at both 2 and 4 months. This patient had initially responded clinically and ultrasonically to steroid therapy. However, symptoms recurred following steroid reduction and ultrasound was performed to assess change in bowel wall thickness.

PATIENTS AND METHODS

RESULTS

Thirty-one patients with known inflammatory bowel disease were referred for abdominal ultrasound ex-

The results are summarised in Table 1. There were 19 patients with Crohn's disease and nine patients with

Twenty-eight patients with inflammatory bowel disease were examined with ultrasound. When possible, maximum bowel wall thickness was measured and the site of any focal abnormality recorded. There were 19 patients with Crohn's disease and nine with ulcerative colitis. Bowel wall thickness ranged from 0 . 5 - 1 . 8 m m in the Crohn's group to 0 . 3 - 0 . 8 c m in the ulcerative colitis group. Following treatment, a measurable reduction in bowel wall thickness was demonstrated in 13 of the patients with Crohn's disease. No significant change in bowel wall thickness was detected in five of the patients with ulcerative colitis. The results echo the findings at double-contrast radiography and suggest a possible role for ultrasound in the assessment and follow-up of inflammatory bowel disease.

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Table 1 - Summary of results Case

Involved regions as assessed by ultrasound

Actual site at barium study

Max. wall Thickness at thickness (ram) follow-up (ram)

Crohn' s disease

1 2 3

4 5

6 7

8 9 10 11

12 13

14 15 16 17 18 19

Ascending colon, mid-abdomen Ascending colon Pelvis - ?sigmoid Right lower quadrant Descending colon and sigmoid Transverse and descending colon Pelvis Right lower quadrant Right iliac fossa (previous subtotal colectomy), Right iliac fossa ?terminal ileum/ascending colon Several loops - mid-abdomen Descending colon Multiple loops Sigmoid colon Right iliac fossa Descending colon Pelvis Ascending colon Transverse and descending colon

Ulcerative colitis" 1 2 Probable descending colon 3 4 5 Ascending and descending colon 6 7 8 9 -

Ascending colon, distal ileum Ascending colon Sigmoid Terminal ileum Descending colon and sigmoid Transverse and descending colon Sigmoid colon Terminal ileum Not performed

9

4

10

Lost to follow-up

12 11 16 18 11 9 5.~

6 7 8 6 (10)* 6 8?

Terminal ileum/ascending colon

11

4

Ileum Descending colon Jejunum and ileum Sigmoid colon Terminal ileum Descending colon Sigmoid colon Terminal ileum Transverse and descending colon

8 9 9 12 10 14 11 8 13

3 4 6 5§ 4 8 ** ** **

Transverse and left colon Left colon Left colon Total colitis with carcinoma of descending colon Total colitis Transverse and left colon Left colon Descending colon Total colitis

3 4 7 5 Difficult to measure bowel wall 4 (but with focal area of 18 mm) 8 3 3 5 4 4 3 4

* Increase in thickness noted after clinical relapse. clinical improvement. SAssociated right iliac fossa abscess drained surgically. §Abnormality detected only after full-bladder technique. ** Follow-up not yet available.

? No

ulcerative colitis. Bowel wall thickness in the patients with Crohn's disease ranged from 5 mm to 18 mm with a mean of 10.9 mm (Fig. 1). Bowel wall thickness in the patients with ulcerative colitis ranged from that in one patient in whom it was difficult to measure the bowel wall thickness (Fig. 2) to 8 mm. The mean thickness in those patients in whom bowel wall thickness could be measured was 4.75 mm. Statistical analysis utilising the Wilcoxon (Mann-Whitney) two-tailed test indicates that the differences between these two groups is highly significant (P<10-4). Other features suggesting intestinal pathology were not specifically evaluated but dilated loops of bowel were detected in three cases of Crohn's disease. One patient (Crohn's disease Case 9) had had a previous subtotal colectomy for Crohn's disease and presented with low-grade fever, a tender mass in the right iliac fossa and a leucocytosis. Ultrasound demonstrated a complex fluid collection in the right iliac fossa but without evidence of definite thickened bowel wall in the adjacent bowel (Fig. 3). Simple surgical drainage of a Crohn's-associated abscess was performed. One patient (ulcerative colitis Case 4) was known to have had extensive ulcerative colitis for 12 years but presented with worsening of symptoms and further loss of weight. There was no evidence of general thickening of the bowel wall but there was an abnormal gas shadow in the region of the descending colon with a short

segment of bowel wall thickening (Fig. 4). Doublecontrast barium enema examination demonstrated an irregular area of narrowing in the distal descending colon but without clear evidence of mucosal destruction. A total colectomy was performed and histology of the colectomy specimen confirmed a carcinoma. Following treatment with anti-inflammatory drugs and/or immunosuppressives, follow-up ultrasound examinations were performed in 22 patients after an interval of 2-4 months. In 13 of the 14 patients with Crohn's disease who were thus examined, a reduction in bowel wall thickness of between 4 mm and 12 mm was demonstrated (Fig. 5). This reflected an improvement in the clinical condition. In one patient (Case 8) there was no change and no clinical improvement. The mean reduction in bowel wall thickness was 6 ram. In five patients with ulcerative colitis who were similarly examined there was no significant change in the bowel wall thickness. DISCUSSION Ulcerative colitis and Crohn's disease are probably heterogeneous disorders which share similar clinical and pathological features. Epidemiological surveys in areas with stable populations have shown a generalised increase in inflammatory bowel disease over former

ULTRASOUND DEMONSTRATION OF BOWEL WALL THICKNESS

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the extent, particularly of ulcerative colitis, is underestimated by the contrast examination (Bartram and Walmsley, 1978). Radiological findings in ulcerative colitis include the demonstration of granular mucosa, ulceration and polypoid change; the radiological features of Crohn's disease are reported as much more variable, including discrete and fissure ulcers, strictures, proximal dilatation, thickening and distortion of mucosal folds and cobblestoning, as well as the complication of sinuses and fistulae (Nolan and Gourtsoyiannis, 1980). Recent reports in the literature have demonstrated that numerous intestinal pathologies can be demonstrated by ultrasound. The most commonly encountered

Fig. 1 - Longitudinal ultrasound scan of the pelvis in a patient with C r o h n ' s disease. A n atypical target lesion (arrowheads) is noted just cephalad to the bladder (B). This represents an area of bowel wall thickening. A further area of abnormal bowel is demonstrated by the curved arrow.

Fig. 3 - Transverse scan at the level of the mid-pole of the right kidney (K); a fluid collection (curved open arrow) is demonstrated in the right paracolic gutter lateral and posterior to the liver (L). This was found to •represent an abscess complicating C r o h n ' s disease at operation.

Fig. 2 - Longitudinal ultrasound scan in the left side of the a b d o m e n in a patient with ulcerative colitis. T h e small arrows demonstrate long axis views of collapsed bowel t h o u g h t to be colon. A d j a c e n t to these areas are areas of 'ringdown' and reverberation artefact due to bowel gas (curved arrows). These appearances are indistinguishable from normal.

years. However, more recent reports suggest that this continued rise may have stabilised (Kirsner and Shorter, 1982). The diagnosis of ulcerative colitis and Crohn's disease may be made from clinical, endoscopic and histological evidence. Contrast radiological studies have been used to assess the extent and severity of inflammatory bowel disease although, not infrequently,

Fig. 4 - Parasagittal scan in the region of the left paracolic gutter. A normal gas pattern of bowel with multiple reverberations is shown by the curved arrows. However, caudad to this is an area of abnormally thickened bowel (open arrowheads). This proved to be a carcinoma complicating ulcerative colitis. T h e patient was diagnosed as having h a d ulcerative colitis for 12 years previously.

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(a)

(b)

Fig. 5 - Parasaginal scans in the left upper quadrant. (a) An area of markedly thickened bowel (arrows) overlies the left kidney (K); the patient had extensive Crohn's disease involving the colon. (b) The bowel wall thickening (arrowheads) has markedly diminished in degree following a course of treatment. (K=left kidney).

appearance representing abnormal bowel is the atypical target lesion (Fleischer et al., 1980) (Fig. 1). This reflects infiltration and thickening of bowel wall. The sign is non-specific and has been reported in bowel tumours, inflammatory lesions, intussusception, intramural haematoma and hypertrophic pyloric stenosis (Fleischer et al., 1980; Blumhagen and Coombes, 1981). There have been several reports in both the English and the European literature which record the value of sonography in the detection of bowel abnormality in Crohn's disease (Holt and Samuel, 1979; Sonnenberg et al., 1982). Further, the diagnosis of complications of Crohn's disease by ultrasound has also been reported. Thus, fistulae as well as abscesses have been demonstrated (Jenss et al., 1980). Indeed, in the German literature ultrasound is suggested as the primary imaging mode for the assessment of Crohn's disease in the acute stage, relying entirely on the demonstration by ultrasound of infiltration of the bowel wall (Wellman et al., 1980). Ultrasound appearances in Crohn's disease are reported as variable. The target or pseudo-kidney sign is the commonest abnormality detected but other abnormal findings have included a solid abdominal mass, distended, fluid-filled loops of bowel, luminal narrowing, reduced peristalsis and 'stiffening' of bowel loops and mesentery. Pathological differences between ulcerative colitis and Crohn's disease are not limited to the mucosal surface but involve the effect of the diseases on the entire bowel wall. The inflammatory changes in ulcerative colitis are usually limited to the mucosa except in the fulminating state, whereas in Crohn's disease the changes are transmural (Morson and Dawson, 1972). This infiltration of the bowel wall in Crohn's disease explains the common finding of the abnormal target sign at ultrasound examination.

Differences in bowel wall thickness have been measured radiologically on plain film and contrast studies. Normal bowel wall thickness as demonstrated radiologically is 2mm. In 50% of cases with Crohn's colitis the bowel thickness is above 5 ram, whereas in ulcerative colitis bowel wall thickness is usually less than 5mm (Bartram and Herlinger, 1979). It is also possible to quantify bowel wall thickness with ultrasound. Normal bowel in the non-distended state measures less than 5 mm while in the distended state the mean thickness is 3mm (Fleischer et al., 1981). Similarly, quantitative analysis of bowel wall thickening has been made in a variety of pathological states with wall thicknesses varying from 5 mm to 30 mm. The results reported in this paper confirm the findings of other workers, that ultrasound can demonstrate regions of bowel wall thickening in patients with Crohn's disease. The typical finding of abnormal bowel was that of an atypical target lesion reflecting bowel wall infiltration. Further, however, it was possible to quantify the thickening by measurements of the bowel wall. These measurements would not necessarily be expected to correlate numerically with those recorded by orthodox radiology since, in the latter, measurements were made on areas of distended bowel (Bartram and Herlinger, 1979) whereas measurements in this study were made from non-distended bowel. However, although the numbers of patients examined are small, a similar trend can be observed. As might be expected from the pathological differences in the two diseases and from the radiological findings, significant bowel wall thickening was demonstrated in Crohn's disease in all but one case, while but a single patient with ulcerative colitis demonstrated similar changes. While there are many features which may suggest intestinal pathology, bowel wall thickening is the commonest and least subjective of these features.

ULTRASOUND DEMONSTRATION OF BOWEL WALL THICKNESS

Further, measurement of bowel wall thickening allows comparison with the findings at follow-up after treatment. Thus, in all but one of the patients in this series who were followed after steroids and/or immunosuppressive therapy there was a measurable reduction in bowel wall thickening. This correlated well with clinical response to treatment and the correlation was further confirmed in one patient who underwent relapse after reduction of steroid dosage and in whom increase in bowel wall thickness was demonstrated. It is suggested that ultrasound be used as part of the initial work-up of a patient with inflammatory bowel disease. Contrast radiology would still be used to assess extent of involvement of the disease and the diagnosis would still depend upon a combination of the history, sigmoidoscopic, radiological and histological findings. The demonstration of bowel wall thickening by ultrasound might find a place in a scoring system in the differential diagnosis of inflammatory bowel disease (Clamp et al., 1982) but it is not proposed as a specific diagnostic tool. However, once the diagnosis is established it should be possible to use ultrasound at intervals to assess the response of the patient to treatment, to assist the early diagnosis of complications and as a discriminant for the performance of follow-up contrast studies. Ultrasound is a quick, non-invasive method capable of detecting Crohn's disease, of measurement of bowel wall thickening and of assessment of response to treatment. It should be possible, with the use of ultrasound, to avoid repeated follow-up contrast radiological studies with their attendant discomfort and radiation exposure to the patient.

Acknowledgements. I thank Mrs Pippa Turner for secretarial assistance and Mr Mike Casebow for assistance with the statistical analysis.

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REFERENCES

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