Clinical Radiology (1991) 43, 171 175

Ultrasonic Patterns in Inflammatory Bowel Disease K. T. KHAW, L. J. YEOMAN, S. H. S A V E R Y M U T T U * , M. G. C O O K t and A. E. A. JOSEPH

Departments of Radiology, *Medicine and "~Histopathology, St George's Hospital, London Ultrasound examination was performed in 90 patients with varying bowel pathology. Ultrasound reliably demonstrated thickening of the bowel. In addition, the pattern of abnormality seen in Crohn's disease and ulcerative colitis was different, and corresponded to the pathological changes seen in these disease processes. The pattern of bowel abnormality seen in other bowel diseases with an inflammatory aetiology generally corresponded to either the Crohn's or ulcerative colitic pattern. The appearances are described, together with findings in other non-neoplastic diseases of the bowel. Khaw, K.T., Yeoman, L.J., Saverymuttu, S.H., Cook, M.G. & Joseph, A.E.A. (1991). Clinical Radiology 43, 171 175. Ultrasonic Patterns in Inflammatory Bowel Disease

It is recognized that despite the limiting factor of intraluminal gas, ultrasound can detect abnormalities in a wide range of bowel pathology, although the appearances may be non-specific (Lutz and Petzoldt, 1976; Fleischer et al., 1980; Limberg, 1987). Ultrasound has reliably demonstrated bowel abnormality in Crohn's disease and ulcerative colitis (Holt and Samuel, 1979; Sonnenberg et al., 1982; Dubbins, 1984; Kaftori, 1984; Dinkel et al., 1986). In this study we report our experience with ultrasound scanning in the diagnosis and assessment of non-neoplastic bowel disease.

RESULTS The numbers of patients and the diagnoses obtained are summarized in Table 1. The abnormality most commonly recognized was thickening of the bowel, which was often relatively aperistaltic. In addition, two main patterns of abnormality were noted. In the majority of patients with Crohn's disease, on transverse scans, an appearance corresponding to a target lesion was seen, with a central hyperechoic area surrounded by a welldefined wide hypoechoic region (Fig. 1a). On longitudinal

PATIENTS AND M E T H O D S A total of 118 ultrasound scans were performed on 90 patients with suspected bowel pathology. Fourteen patients had two scans and seven patients had three scans. In all 90 patients the diagnosis was proven by histology, radiology or other laboratory investigations. A single operator performed all ultrasound scans using a Technicare Autosector with a 5 MHz frequency transducer. Any abnormality present was recorded. Particular note was made of bowel thickening, its extent and the nature of the thickening. The findings were later correlated with clinical findings and the results of other diagnostic studies. (a) Table I

Diagnosis

No. of patients

Crohn's disease Ulcerative colitis Salmonella colitis Cytornegalovirus colitis Pseudomembranous colitis Tuberculous enteritis Amoebiasis Diverticular disease Ischaemic colitis Infarction Henoch-Schoenlein purpura

46 11 6 2 3 4 2 9 3 2 2

Correspondence to: Dr A. E. A. Joseph, Department of Radiology, St George's Hospital, London SWI7 0QT. ?Present address: Department of Histopathology, Royal Surrey County Hospital, Guildford, Surrey.

(b) Fig. 1 - Crohn's pattern. (a) Transverse section through bowel in Crohn's disease showing well-defined echo-poor outer rim and bright inner region. (b) Longitudinal section in Crohn's disease.

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CLINICAL RADIOLOGY

Fig_ 2 - Ulcerative colitic p a t t e r n w i t h p o o r l y defined, i n h o m o g e n o u s wall and lumen.

Table 2 - Correlation of diagnosis with appearance on ultrasound

Diagnosis

C r o h n ' s disease Ulcerative colitis I s c h a e m i c colitis Salmonella Cytomegalovirus Pseudomembranous Tuberculosis Amoebiasis Henoch-Schoenlein

Appearance Crohn 's-type

Colitic-type

Indeterminate

36 0 3 1

5 9

5 2

4 2 3

1

3 1

1 1 2

scanning the same two regions were identified (Fig. 1b). In the majority of patients with ulcerative colitis, the differentiation into two distinct regions was not seen. The pattern was that of thickened bowel with multiple echogenic foci centrally, although in a few patients, a thin outer hypoechoic zone was observed (Fig. 2). The number of patients with various other conditions was small but in general the appearances found usually corresponded to one of the two previously described patterns. The correlation of the ultrasonic pattern with the diagnosis is summarized in Table 2.

DISCUSSION Normal large bowel containing formed or semi-solid faecal material is usually seen as a column of echoes representing air and faeces in the lumen, with regularly interspersed echo-poor indentations which represent haustrae 3 5 cm apart (Fleischer et al., 1980). The most common ultrasonic finding described in bowel pathology is the 'target lesion', where an echogenic centre is surrounded by an echo-poor rim. The echogenic centre is thought to represent luminal residue and air. The echopoor region is likely to represent thickening of the submucous and muscular areas. This appearance is described in a wide range of pathological conditions including tumours, intussusception and inflammatory bowel disease (Bluth et al., 1979; Morgan et al., 1980).

Fleischer et al. (1981) performed measurements of bowel wall thickness and confirmed wall thickening in patients with abnormaI bowel. Thickening may be more localized or eccentric in mass lesions or turnouts compared to a more diffuse thickening in inflammatory bowel disease, but the appearances have been considered non-specific and it has proved difficult to differentiate the underlying pathology on ultrasound appearances alone. In this study, we noted a difference between the appearance of bowel in Crohn's disease and ulcerative colitis. The bowel in Crohn's disease usually resembled the typical 'target lesion'. In contrast the outer echo-poor region was poorly defined and thinner in ulcerative colitis. The ultrasound patterns seen in the two conditions probably reflects the macroscopic changes seen in the bowel and may be explained by the underlying pathology. In Crohn's disease, there is mural thickening with transmural inflammation, oedema and fibrosis affecting the submucosa and to a variable degree the muscularis propria. The mucosa itself may be sometimes relatively normal apart from linear fissures. The changes can be confined largely to the deeper layers, resulting in wall thickening. The previously described appearance corresponding to a well-defined hypo-echoic halo and bright central region we have termed the 'Crohn's pattern'. In contrast, there is florid mucosal hyperaemia and inflammation in ulcerative colitis. The submucosa and muscularis propria are much less frequently affected unless there is a severe exacerbation or megacolon. The extensive superficial ulceration results in a ragged mucosa with inflammatory polyps and inflammatory exudate and mucus in the lumen. Air is trapped between the mucosal folds and ulcers. These changes may be reflected in the ultrasound images as thickened bowel with multiple echogenic foci without a clearly defined outer hypoechoic region_ This was termed the 'ulcerative colitic pattern'. Dubbins (1984) measured bowel wall thickness using ultrasound in patients with inflammatory bowel disease. He noted significant bowel wall thickening in patients with Crohn's disease, whereas this was seen in only one patient with ulcerative colitis. We did not find bowel wall measurement possible in all our patients. Firstly, in the patients with an ulcerative colitic-type pattern, the wall often could not be delineated clearly from the lumen. Secondly, in some other patients, the bowel was collapsed and although the wall clearly appeared thickened, the mural thickening was not uniform throughout and again the lumen could not always be clearly differentiated. We did, however, observe a difference in the degree of mural thickening in Crohn's disease and ulcerative colitis, which supports his findings. The 'ulcerative colitic pattern' was also observed in patients with other inflammatory colitides such as those due to salmonella (Fig. 3) and cytomegalovirus (Fig. 4a,b). In these infective colitides, there is typically acute superficial inflammation and ulceration of the mucosa which may form a 'slough'. This pattern was also seen in pseudomembranous colitis (Fig. 5), where a 'membrane' formed of fibrinous exudate and mucus may cover an area of inflamed mucosa. The 'Crohn's pattern' with a well-demarcated outer region was seen in three of four patients with tuberculous enteritis, although in all cases the lumen appeared less well-defined than in Crohn's disease (Fig. 6). In tuberculous enteritis there is involvement of lymphoid tissue in the ileal wall with ulceration, necrosis, fibrosis and often

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ULTRASONIC PATTERNS IN INFLAMMATORY BOWEL DISEASE

Fig. 3 - Salmonella colitis. Fig. 5 - Pseudomembranous colitis.

Fig. 6 Tuberculous enteritis.

(a)

Fig. 7

(b) Fig. 4 - Cytomegalovirus colitis in an immunosuppressed patient. (a) Barium enema showing numerous mucosal ulcers. (b) Ultrasound scan: bright flecks correspond to air trapped in the ulcers.

Amoebiasis.

extensive g r a n u l o m a t o u s infiltrate with thickening. The ' C r o h n ' s p a t t e r n ' was also seen in one patient with amoebiasis of the ileo-caecal region (Fig. 7). This does n o t correlate with the pathological changes usually seen in acute amoebic dysentery, in which the ulcers are usually superficial a n d do n o t penetrate the muscle coat of the colon. I n l o n g - s t a n d i n g cases, however, g r a n u l o m a t o u s

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CLINICALRADIOLOGY

Fig. 8

Henoch-Schoenlein purpura.

changes may occur in the deeper layers of the wall resulting in bowel wall thickening. Our patient had a chronic history of bowel disturbance. The other patient with amoebiasis showed a colitic-type pattern. Both patients with Henoch-Schoenlein purpura showed the Crohn's-type pattern (Fig. 8). In this condition, an immunologically mediated vasculitis of arterioles and small blood vessels causes acute extravasation of blood into the bowel wall. The three patients with a diagnosis of ischaemic colitis also showed the 'Crohn's pattern'. In ischaemic colitis there is ulceration and mucosal oedema, but this is followed by fibrous thickening of the submucosa which contains m a n y haemosiderin laden macrophages. In two of these an appearance resembling 'thumb-printing' or mucosal oedema, as seen on plain films or barium studies, was evident (Fig. 9a,b). In two patients with caecal infarction, an additional finding, which we term the 'stepladder' pattern of alternating bands of increased and reduced echoes, was seen (Fig. 10a). Infarction was confirmed at surgery in one patient and by angiography in the other. A possible explanation of the ultrasonic appearance is that in infarction there is severe oedema of

(a)

(a)

ed and infolded bowel wall

Gas and faeces in / bowel lumen \

\

.-...

~----~?..~ /~'~i~,

,t ~,;

~.,,,, ~

f; b ~l',--" '. L. " , ~~ ~"

;,,~. "'-,,~,! "'";

,.;...,

~!2! ?~

(6)

(b)

Fig. 9 - (a) Ischaemic colitis showing 'thumb-printing' (arrowed). (b) Barium enema in the same patient.

Fig. I0 - (a) "Step-ladder' pattern in infarcted colon. (b) Illustration of wall infolding causing %tep-ladder' pattern.

ULTRASONIC PATTERNS IN INFLAMMATORY BOWEL DISEASE

(a)

175

the thickened bowel wall. These findings were confirmed on examination of the macroscopic specimen following surgery. The bowel wall infolding gives rise to wide bands of increased echoes corresponding to the air and faeces in the bowel lumen interspersed by bands of decreased echoes corresponding to the thickened infolded bowel (Fig. 10b). Other forms of bowel inflammation do not usually give rise to such extensive oedema and infolding of bowel. In some patients with diverticular disease we observed ultrasonic appearances similar to those seen on barium studies. A banded 'concertina' pattern could be seen which probably corresponds to the thickened circular muscle folds causing clefts between the diverticular (Fig. 1 la,b). In others, thickening of the bowel with a 'Crohn's pattern' may be seen. Our experience shows that ultrasound can reliably detect bowel abnormality. Recognition of different ultrasonic patterns may provide a useful clue to the diagnosis. Although it cannot replace contrast radiology and endoscopy in the assessment of bowel disease, ultrasound may be of use in reducing the number of diagnostic studies in these patients. Further studies with larger numbers of patients are required to substantiate these preliminary observations relating sonographic patterns to various types of inflammatory bowel disease. REFERENCES

(b) Fig. 11 - (a) 'Concertina pattern' ultrasound appearance of diverticular disease. (b) Barium enema in same patient.

relatively acute onset and submucosal haemorrhage resulting in thickening of the bowel wall. The teniae coli which run longitudinally restrict elongation along the length of the bowel which results in marked infolding of

Bluth, EI, Merritt, RB & Sullivan, MA (1979). Ultrasonic evaluation of the stomach, small bowel and colon. Radiology, 133, 677 680. Dinkel, E, Dittrich, M, Peters, H & Baumann, W (1986) Real-time ultrasound in Crohn's disease: characteristic features and implications. Paediatric Radiology, 16, 8-12. Dubbins, PA (1984). Ultrasound demonstration of bowel wall thickness in inflammatory bowel disease Clinical Radiology, 35, 227-231. Fleischer, AC, Muhletaler, CA & Everette James, A (1980) Sonographic patterns arising from normal and abnormal bowel. Radiologlc Clinics of North America, 18, 145 159. Holt, S & Samuel, E (1979). Grey scale ultrasound in Crohn's disease. Gut, 20, 590 595. Kaftori, JK, Pery, M & Kleinhaus, U (1984). Ultrasonography in Crohn's disease. Gastrointestinal Radiology, 9, 137 142. Lutz, HT & Petzoldt, R (1976). Ultrasonic patterns of space-occupying lesions of the stomach and intestine. Ultrasound in Medicine and Biology, 2, 129-132. Limberg, B (1987). Diagnosis of inflammatory and neoplastic colonic disease by sonography. Journal of Clinical Gastroenterology, 9, 607 611_ Morgan, CL, Trought, WS, Oddson, TA, Clark, WM & Rice, RP (1980). Ultrasound patterns of disorders affecting the gastrointestinal tract. Radiology, 135, 129 135 Sonnenberg, A, Erckenbrecht, J, Peter, P & Niederau, C (1982). Detection of Crohn's disease by ultrasound. Gastroenterology, 83, 430-434.

Ultrasonic patterns in inflammatory bowel disease.

Ultrasound examination was performed in 90 patients with varying bowel pathology. Ultrasound reliably demonstrated thickening of the bowel. In additio...
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