Clinical Radiology (1993) 47, 46-48
The Small Bowel Enema: A Ten Year Review P. M. D I X O N , M. E. R O U L S T O N and D. J. N O L A N
Department of Radiology, John Radcliffe Hospital, Oxford In a retrospective study the radiological reports of small bowel enema (enteroclysis) examinations of 1465 patients were reviewed and compared with the subsequent clinical outcome, and where possible with findings at laparotomy. A sensitivity of 93.1% and a specificity of 96.9% was found, based on whether the small intestine was reported as normal or an abnormality was diagnosed to account for the patient's clinical presentation. The correct specific diagnosis was made in 67.5% of the examinations that were considered abnormal. We believe that these figures support the use of small bowel enema as the routine barium examination for suspected disorders of the small intestine. Dixon, P.M., Roulston, M.E. & Nolan, D.J. (1993). Clinical Radiology 47, 46-48. The Small Bowel Enema: A Ten Year Review
Accepted for Publication 17 August 1992
Barium studies continue to be the principal imaging technique for the diagnosis and management of disorders of the small intestine. Endoscopy is widely used for examining the upper gastrointestinal tract and colon but it has not yet proved practical for investigating the jejunum and ileum. There is an increasing number of centres using the small bowel enema (enteroclysis) as the barium technique of choice while others continue to use the barium small bowel follow-through series (SBFT). Disagreement persists as to which is the best barium technique for examining the small intestine [1,2]. It has been suggested that a controlled trial should be carried out to compare the barium follow-through with enteroclysis [3] but such a study would be difficult to perform and would require a large number of cases to provide a definite result. McNeil and colleagues state that the best estimate of the reliability of a diagnostic test in clinical decision making is its sensitivity and specificity [4,5]. The small bowel enema became our routine method for examining the small intestine in October 1976. We have reviewed all the examinations performed at this institution since then in an effort to establish the sensitivity and specificity of the technique. Previous reports from our department on the role of enteroclysis in the diagnosis and management of certain disorders of the small intestine [6-20] included examinations that are evaluated as part of this study.
When laparotomy was not performed the eventual clinical diagnosis and the outcome at clinical follow-up were compared with the radiological findings. In patients who underwent surgery, the diagnosis was made at laparotomy and in some cases on pathological examination of the resected intestine. These surgically confirmed diagnoses have also been analysed separately. The diagnosis was considered to be a true positive if an abnormality shown on the barium examination accounted for the patients presenting symptoms and outcome. It was a false positive diagnosis if an abnormality was diagnosed radiologically and the subsequent evidence indicated that the small intestine was normal. A diagnosis was considered a true negative if no abnormality was seen on the small bowel enema and follow-up indicated that this was correct. The diagnosis was considered false negative if an abnormality was subsequently shown to be present that had not been detected on the radiological examination. The examination technique we use is based on the Sellink [21] method and has previously been described in detail [22-24]. A large volume of dilute barium suspension, about 1000 ml, is infused under gravity throug h a nasoduodenal tube into the small intestine and the radiographs are exposed at high kilovoltage. RESULTS
PATIENTS AND METHODS All patients examined with the small bowel enema in Oxford between October 1976 and 1985 are included. Before June 1979 the examinations were performed at the Radcliffe Infirmary; after that date gastroenterology and the acute services moved to the new John Radcliffe Hospital. Some patients had more than one examination and in such cases the results of the first examination were chosen for this study. The radiological diagnosis was based on the written report issued at the time of the examination. The case notes were reviewed to establish the diagnosis. Correspondence to: Dr D. J. Nolan, Department of Radiology, John Radcliffe Hospital, Headington, Oxford OX3 9DU.
A total of 1726 small bowel enema examinations were performed on 1639 patients in the period 1976-1985. The case notes were incomplete or not available in 174, leaving 1465 patients for analysis. Surgical confirmation of the radiological findings was available in 371 cases. The mean period of follow-up was 5.1 years, with a minimum of 2 years. The results are classified according to the main indications for the examination in Table 1. Classification is according to the main indication for the examination. 'Pain only' indicates patients in whom abdominal pain was the dominant symptom, although there were often other features to suggest small intestinal pathology. A positive diagnosis, in keeping with the patient's symptoms and eventual clinical outcome, was made in 434 of the 466 cases with disease, giving a sensitivity of
SMALL BOWEL ENEMA Table 1 - Results according to main indications for the investigation
Indication
True positive
False negative
True negative
False positive
Diarrhoea Pain only Bleeding/anaemia Malabsorption Obstruction Other
206 44 19 1 150 14
16 2 6 0 3 5
495 210 119 42 62 4l
17 5 4 0 3 1
To.lal
434
32
969
30
47
98% and a positive predictive value of 92%, and the approximate level was demonstrated in many cases, which was helpful in the patients' management. The specificity in the patients with surgical correlation was 90.0%. The negative predictive value was 90.4%. Patients with a normal small bowel enema underwent surgery for a variety of conditions including colitis, peptic ulcer and gall-bladder disease. Those with colitis were investigated to exclude disease o f the small intestine while in others the presenting symptoms initially suggested a disorder of the small intestine.
DISCUSSION Table 2 - Final diagnosis in patients who underwent surgery
True positive
False negative
Crohn's Disease Obstruction Neoplasm Radiation enteritis Other diagnosis
116 55 23 5 22
5 1 3 ! 3
Total
221
13
True negative
False positive 4 5 1 0 4
123
14
93.1%. The positive predictive value was 93.5%. O f the 1001 patients who had no subsequent evidence of small bowel disease, the examination was reported as normal in 969, a specificity of 96.9%. The negative predictive value was 96.8%. Twenty-five patients in the series had coeliac disease, only 10 of whom showed evidence of the disorder on the small bowel enema, usually a reduction in the size and number ofmucosal folds in the jejunum and 'jejunization' of the ileum. Thus the sensitivity in this condition was 40%. An abnormality was demonstrated on small bowel enema to account for the patient's presenting symptoms in 221 of the 234 patients who were shown to have disease in the small intestine at laparotomy, a sensitivity of 94.4%. The correct specific diagnosis was made on the barium study in 162 (67.5%). In the remainder of the positive examinations, a non-specific abnormality such as obstruction or mucosal-fold thickening was present. The actual diagnosis was included in the differential diagnosis on the report in some, while in others no specific diagnosis was suggested. The results according to diagnostic group, are shown in Table 2. Neoplasms include primary and secondary neoplasia although in most cases the histological type was suggested. Other diagnoses include the identification of Meckel's diverticulum (n--6), jejunal diverticulosis (n = 3), adhesions without obstruction (n = 3) and appendicitis (n=2). There were a number o f patients where it was not possible to make a specific diagnosis, although a definite abnormality was shown. It was not possible to make a specific diagnosis in most cases of small bowel obstruction although the site of obstruction was clearly identified in the majority. In other patients the barium column either did not reach the site of obstruction or failed to show the obstructing lesion. HOWever, obstruction was confirmed with a sensitivity o f
Our study has shown that enteroclysis is a reliable technique with a sensitivity of 93.1% and a specificity of 96.9%. The purpose in carrying out the barium examination of the small intestine is to detect and assess the extent of any disorder that may be present and whenever possible to make a specific diagnosis. If the examination is normal it should be sufficiently reliable to exclude the presence of an abnormality. Because the sensitivity for the detection of coeliac disease is so poor, we recommend that jejunal biopsy alone should be used for the diagnosis of this disease, and that enteroelysis be reserved for the investigation of suspected complications such as the development of lymphoma. This is routine practice in Oxford and as a result patients with suspected coeliac disease at presentation do not have a barium examination. Most of our patients subsequently found to have coeliac disease presented with atypical symptoms and this probably also contributed to the low sensitivity. Our findings are in broad agreement with those of Kumer and Bartram [25], who found that only 54% of patients with coeliac disease show characteristic radiological changes in the small intestine on SBFT. Previous studies comparing enteroclysis and the SBFT give conflicting results. Gurian et al. [26] reported the results of 88 patients examined with enteroclysis, 52 of whom were also examined with SBFT. In their series there was an overall accuracy of 96% for enteroclysis compared to 72% for SBFT. However, the diagnosis was confirmed by surgery or endoscopy in only 27 cases. In a study of 370 small bowel examinations Diner et al. [27] found no significant difference in accuracy between a number o f SBFT techniques and enteroclysis. Ott et al. [28], in a study of 442 patients who had SBFT and 106 who had enteroclysis, showed a sensitivity for the B M F T of 92% and a specificity of 94% compared to enteroclysis where the sensitivity was 94% and the specificity 89%. Sanders and Ho [29] showed that the additional study added useful information in 13 of the 26 patients who underwent SBFT followed by enteroclysis. A recent study showed a sensitivity of 95% in the detection o f malignant neoplasms o f the small bowel by enteroclysis [30]. However, in these studies the patients were not randomized and the number of patients having enteroclysis was small. In a study of 46 patients the SBFT was found to have a 90% sensitivity compared to ileoscopy and biopsy [31]. However, several relatively small series have shown the SBFT to have a low sensitivity [26,29,32]. This makes the technique inappropriate as an initial investigation. Our experience has shown that small bowel enema can be used
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CLINICAL RADIOLOGY
r o u t i n e l y . Its h i g h sensitivity a n d specificity m e a n that, a p a r t f r o m m a l a b s o r p t i o n states s u c h as c o e l i a c disease, the t e c h n i q u e c a n be relied u p o n as t h e m a i n c o n t r a s t i n v e s t i g a t i o n o f the s m a l l intestine. The radiological appearances of disorders causing m o r p h o l o g i c a l c h a n g e s in t h e s m a l l i n t e s t i n e a r e m o r e clearly demonstrated by enteroclysis than SBFT because the s m a l l i n t e s t i n e is d i s t e n d e d b y t h e c o n t r a s t m e d i u m . T h i s m a k e s it easier to i d e n t i f y the r a d i o l o g i c a l signs t h a t are p r e s e n t . A s we i n c r e a s e o u r k n o w l e d g e o f t h e c h a r a c t e r i s t i c r a d i o l o g i c a l a p p e a r a n c e s o f d i f f e r e n t diso r d e r s it s h o u l d be p o s s i b l e to m a k e a m o r e a c c u r a t e specific d i a g n o s i s w i t h e n t e r o c l y s i s . T h e r e will a l w a y s be cases w h e r e o n l y a d i f f e r e n t i a l d i a g n o s i s c a n be s u g g e s t e d , H o w e v e r , the reliability o f a n y p a r t i c u l a r b a r i u m techn i q u e s h o u l d c o n t i n u e to be j u d g e d o n its a b i l i t y to d e t e c t a symptomatic abnormality or confidently establish that the s m a l l i n t e s t i n e is n o r m a l [4].
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