Ultrasound of selected pathologies of the small intestine.

UNLABELLED: Intestines, especially the small bowel, are rarely subject to US assessment due to the presence of gases and chyme. The aim of this paper was to analyze ultrasound images in selected pathologies of the small intestine in adults, including the aspects of differential diagnosis.
MATERIAL AND METHODS: In 2001-2012, abdominal ultrasound examinations were conducted in 176 patients with the following small bowel diseases: Crohn's disease (n=35), small bowel obstruction (n=35), yersiniosis (n=28), infectious diarrhea (n=26), bacterial overgrowth syndrome (n=25), coeliac disease (n=15) and small bowel ischemia (n=12). During examinations patients were fasting and no other particular preparations were needed. Convex transducers of 3.5-6 MHz and linear ones of 7-12 MHz were used. The assessment of the small intestine in four abdominal quadrants constituted an integral element of the examination. The following features of the small bowel ultrasound presentation were subject to analysis: thickness and perfusion of the walls, presence of thickened folds in the jejunum, reduction of their number, presence of fluid and gas contents in the intestine, its peristaltic activity, jejunization of the ileum and enteroenteric intussusception. Furthermore, the size of the mesenteric lymph nodes and the width of the superior mesenteric artery were determined and the peritoneal cavity was evaluated in terms of the presence of free fluid.
RESULTS: Statistically significant differences were obtained between the thickness of the small intestine in Crohn's disease or in ischemic conditions and the thickness in the remaining analyzed pathological entities. Small bowel obstruction was manifested by the presence of distended loops due to gas and fluid as well as by severe peristaltic contractions occurring periodically. In the course of ischemic disease, the intestinal walls were thickened without the signs of increased perfusion and in the majority of cases intestinal stenosis was observed. Fluid in the intestine was detected in all patients with coeliac disease, gas in 86.7% of patients, thickening of the folds in the jejunum in 86.7%, their reduction in 80%, increased (enhanced) peristalsis in 93.3% and jejunization in 40%. In 80% of coeliac disease cases, the intestine showed the features of hyperemia on color Doppler examination and in 53.3% of patients the dilated lumen of the superior mesenteric artery was detected. Enlarged mesenteric lymph nodes were visualized in 73.3% of the subjects, enteroenteric intussusception in 33.3% and free fluid in the peritoneal cavity in 60%.
CONCLUSIONS: Small bowel obstruction is manifested by the presence of evidently dilated intestinal loops filled with gas and fluid and periodical severe deepened peristalsis.Ischemic changes and Crohn's disease are characterized by the presence of fragmentarily thickened intestinal walls and intestinal stenosis. Moreover, in Crohn's disease, increased wall perfusion and mesenteric adenomegaly is encountered.Coeliac disease is manifested by: increased amount of fluid mainly in the jejunum, thickened and hyperemic jejunal walls, increased peristalsis;hypertrophied mucosal folds - often their number is reduced, jejunization and transient enteroenteric intussusception;ultrasound changes that require the differentiation with small intestinal bacterial overgrowth syndrome and, to a lesser degree, with infectious diarrhea.

The small intestine is the most difficult part of the gastrointestinal tract to diagnose. Thanks to considerable technological progress of endoscopic apparatus, computed tomography (CT) and magnetic resonance imaging (MRI), we may diagnose most of the inflammatory and neoplastic diseases as well as ischemic conditions of the intestine and we may determine the causes of bleeding from various parts of the gastrointestinal tract. Currently, the greatest diagnostic successes are brought about by endoscopic capsule, double-balloon enteroscopy, CT and MRI enterography/enteroclysis(. Ultrasound examination (US) of the intestine is performed rarely since its contents inhibit interpretation of US images. However, information from literature and the author's own experience show that transabdominal US examination allows for the visualization of a range of changes in the small bowel such as: intussusceptions, intestinal obstruction, inflammatory lesions and neoplasms provided that they are of adequate size(.

In the case of coeliac disease, the visualization of characteristic changes in the small bowel on US examination may accelerate the diagnostic process, especially in adults. In this age group, coeliac disease is rarely included in differential diagnosis although statistical data from the developed countries indicate that it occurs in 1/130–350 persons(. The diagnosis is complicated due to diversified clinical picture of coeliac disease. Particularly in adults, it does not have a typical course and does not manifest itself overtly. It is believed that atypical forms are prevalent(.

The aim of this paper was to analyze ultrasound features of selected pathologies of the small intestine in adults, including the aspects of differential diagnosis.

Material and methods

In 2001–2012, US examinations of the abdominal cavity were performed in 2850 patients with clinical suspicion of bowel diseases. Intestinal pathologies were confirmed in 223 out of 2850 patients who underwent colonoscopy with pathomorphological analysis of the taken tissue sample, CT enteroclysis, various serological tests, immunoenzymatic tests, stool culture, parasitological and mycological stool examinations as well as tests for food allergy. Seventeen patients underwent surgeries (9 due to enteritis ischaemica and 8 with Crohn's disease). Forty-seven patients were excluded from the analysis (37 due to small intestinal neoplasms and 10 with allergic enteropathy, cryptococcal infection or amyloidosis of the small intestine). The material comprised a group of 176 patients suffering from: Crohn's disease (n=35), small bowel obstruction (n=35), yersiniosis (n=28), infectious diarrhea (n=26), small intestinal bacterial overgrowth syndrome (n=25), coeliac disease (n=15) and small bowel ischemic disease (n=12). All patients underwent abdominal US examination whose integral element was the assessment of the intestine in accordance with the criteria proposed by Rettenbacher et al.( and supplemented with the reduction of the folds in the jejunum, presence of thickened mucosal folds of in the ileum, i.e. so called jejunization( and transient enteroenteric intussusception(. US examinations were performed in fasting patients. Moreover, prior to the examination, the patients did not smoke, chew gum or take any medications, including gas-reducing agents or laxatives. The examinations were performed with the use of convex transducers of 3.5–6 MHz and linear ones of 7–12 MHz. The small intestine was assessed in four abdominal quadrants with particular attention paid to: 1) thickness of the intestinal walls and mucosal folds, 2) their distribution and hypertrophy in particular fragments of the bowel, 3) presence of fluid and gas in the intestine, 4) peristalsis, 5) perfusion of the analyzed intestinal walls, 6) width of the superior mesenteric artery, 7) size of the mesenteric lymph nodes, 8) presence of the free fluid in the peritoneal cavity, 9) presence of transient enteroenteric intussusception. The thickening of the small intestinal wall and mucosal folds was observed if their thickness exceeded 3 and 2 mm respectively(. The mucosal folds occupying a half of the lumen were termed “tongue-like elongations” and the folds with side branching were called “shrub-like hypertrophy.” Furthermore, the reduction of the number of folds in the jejunum was also assessed. The presence of thickened and numerous mucosal folds in the ileum was considered as a sign of jejunization. The amount of fluid in the intestine was understood as raised when it increased the diameter of the bowel to 10–20 mm and as substantial when it increased the intestine to over 20 mm. Slight amount of gas in the intestinal lumen was considered normal. When, however, its amount hindered imaging of certain fragments of the bowel (up to 5 cm), it was interpreted as slightly elevated and when gas filled intestinal loops on their entire length, its amount was considered to be elevated substantially. Intestinal stenosis was diagnosed when the thickened fragment of the bowel was occluded during the entire examination especially when it was accompanied by the dilatation of the prestenotic loop that showed increased peristaltic activity. Peristalsis was considered normal when it was slow and occurred periodically, not more frequently than 3 peristaltic waves a minute(. Increased peristalsis, on the other hand, occurred when the intestine contracted more frequently than 3 waves a minute and when, sometimes, antiperistaltic waves occurred, but with no evident tension of the walls (flaccidity). In the fragments preceding the intestinal stenosis, periodical, deep and ineffective peristaltic contractions were observed with evident tension of the walls. The failure to visualize peristalsis in a pathologically altered fragment of the small intestine in subsequent stages of the examination was considered as a motility disorder. What is more, the mesenteric lymph nodes were interpreted as enlarged when their longitudinal size exceeded 10 mm and their transverse dimension – 5 mm. Intestinal wall hyperemia was diagnosed when in an area of 1 cm2 at least 3 vessels were detected(. The superior mesenteric artery was stated to be dilated when its width was greater than 8 mm as measured 2–3 cm from the branching of the aorta(. The presence of fluid in the peritoneal cavity was observed when in female patients in reproductive age it occupied the space between intestinal loops and in other patients – when it was present at any site of the peritoneal cavity. The presentation of the small intestine that resembled a target in transverse section and hay-fork in longitudinal section was interpreted as transient enteroenteric intussusception. It usually did not include the mesentery, did not exceed 35 mm and frequently disappeared during the examination or within subsequent 30 minutes following the examination. In certain cases of intussusception, a slight peristalsis and perfusion in color Doppler examination were observed(. The results connected with the thickness of the intestinal wall for individual pairs in the pathologies listed above were analyzed statistically with the help of the Student's t-test with 0.05 as a cut-off value.

Results

Tab. 1 includes the list of analyzed ultrasound features of the intestine in seven pathological entities. Statistically significant differences were observed between the altered fragments of the intestine in Crohn's disease and small intestinal obstruction, yersiniosis, small intestinal bacterial overgrowth syndrome, coeliac disease and infectious diarrhea (p<0.01–0.001). In 23 patients with complete obstruction (65.7%), the intestinal wall was thin – range: 1.5–2.5 mm and in the remaining patients the thickening was slight – from 3.2 to 5.2 mm. From the statistical point of view, significant differences (p=0.01–0.002) were also obtained between the thickness of the ischemic intestinal wall and the aforementioned pathological entities (figs. 1–3). No statistical difference, however, was observed between the thickening of the intestinal wall in Crohn's disease and the intestine altered in the course of ischemia (p<0.1) as well as between the remaining pathologies: intestinal obstruction, yersiniosis, bacterial overgrowth syndrome, coeliac disease and infectious diarrhea (p<0.1–0.2). In relation to other pathologies, the thickening of the folds in the jejunum was substantially larger in patients with bacterial overgrowth syndrome and particularly in coeliac disease (fig. 4). The hypertrophy of the folds was shrub-like only in coeliac disease (n=5, 33.3%) (fig. 5). Moreover, in coeliac disease and bacterial overgrowth syndrome, a various degree of the fold number reduction in the jejunum was observed (figs. 6, 7). Jejunization occurred mainly in the course of coeliac disease (6/15, 40%) (fig. 8) and in single cases of bacterial overgrowth syndrome (2/25, 8%). Furthermore, a large amount of fluid and gas accompanied small intestinal obstruction. These two signs were also present in patients with bacterial overgrowth syndrome, coeliac disease, infectious diarrhea (figs. 6, 7) and in ischemic bowel disease, but in a smaller amount and in various proportions. Intestinal stenosis, on the other hand, was detected mainly in patients with Crohn's disease and ischemic intestine (figs. 9, 10). The contracted bowel was more rarely noticed in yersiniosis (fig. 11). The periodically deep and ineffective peristaltic contractions accompanied only complete bowel obstruction. However, increased peristalsis but without tense walls was a permanent sign in bacterial overgrowth syndrome, coeliac disease, partial small bowel obstruction and infectious diarrhea (figs. 12, 13). On the other hand, in Crohn's disease and in ischemic changes, no peristalsis was observed in the inflamed fragments of the small bowel.

Tab. 1

Analyzed ultrasound features in seven disease entities

No.	Feature	Crohn's disease	Small intestinal obstruction	Yersiniosis	Bacterial overgrowth syndrome	Coeliac disease	Infectious diarrhea	Ischemic small bowel
1	Wall thickness in mm	5–12 (7,3)	1,5–5,2 (3,8)	3,3–5,5 (4,3)	3,8–6 (5,4)	3,5–6 (5)	3,8–6 (5,1)	5–9,5 (6,9)
2	Fold thickening in:Reduction of the number of folds in the jejunum	jejunum – 14.2%	jejunum – 11.4%	ileum – 14.2%	jejunum – 92%48%	jejunum – 86.7%80%	jejunum – 15.4%	small intestine – 40%
3	Jejunization				8%	40%
4	Increased amount of fluid in the intestine	14,3%	100%, substantial	10,7%	96%	100%	100%	25%
5	Increased amount of gas in the intestine	11,4%	100%	7%	88%	86,7%	92,3%	41,6%
6	Intestinal stenosis	94,2%	0%	50%	0%	0%	0%	91,6%
7	Increased motility of the intestine		97,1%		84%	93,3%	100%
8	Slow motility of the intestine	97,1%		53,6%				91,6%
9	Mesenteric adenomegaly	94,2%		100%	53%	73,3%	15,4%
10	Intestinal wall hyperemiaNo vessels	80%	17,1%	85,7%	76%	80%	23%	91,6%
11	Dilatation of the mesenteric artery	60%			20%	53,3%
12	Fluid in the peritoneal cavity	37%	48,6%	46,4%	52%	60%	50%	25%
13	Enteroenteric intussusception	11,4%		14,3%		33,3%

Fig. 1

Walls of the ileum, 8 mm thick in a 22-year-old male patient with Crohn's disease presented in two sections

Fig. 3

22-year-old female with coeliac disease – thickened wall of the jejunum to 4 mm

Fig. 4

Bacterial overgrowth syndrome – arrows indicate thickened mucosal folds

Fig. 5

Shrub-like hypertrophy of the mucosal folds (arrows) typical of coeliac disease and evident fold reduction in other fragments of the intestine

Fig. 6

46-year-old female with coeliac disease – slight dilatation of the small intestinal loops containing mainly fluid, no visible mucosal folds

Fig. 7

Bacterial overgrowth syndrome in a 62-year-old female with the history of gastrectomy; jejunum contains mainly fluid with slight amount of gas (arrows), reduction of the number of mucosal folds

Fig. 8

Jejunization in the course of coeliac disease: thickened mucosal folds in the ileum (arrows)

Fig. 9

Stenosed ileum in Crohn's disease. Color Doppler examination shows hyperemia of the wall

Fig. 10

Ischemic changes in the ileum in a 72-year-old female, slit-like narrowing of the lumen (arrows)

Fig. 11

Edema of the walls and folds of the ileum in yersiniosis with complete lumen occlusion

Fig. 12

Increased motility of the jejunum in coeliac disease

Fig. 13

Increased motility of the jejunum in bacterial overgrowth syndrome

Two fragments of the small bowel with thickened walls to 5 and 9 mm secondary to ischemic changes

In yersiniosis, however, the disorder of peristalsis was not permanent. Moreover, the enlarged mesenteric lymph nodes accompanied the majority of the analyzed disease entities except for the ischemic ones where the nodes were not detected (fig. 14). However, in the cases of infectious diarrhea and intestinal obstruction, they were rarely observed. What is more, no signs of flow were found in the intestinal walls in the course of ischemia (fig. 15). Due to lively peristalsis, the assessment of the wall perfusion was difficult in some patients with infectious diarrhea and intestinal obstruction. The dilated superior mesenteric artery was a frequent sign of the Crohn's disease, bacterial overgrowth syndrome and coeliac disease (fig. 16). The collection of free fluid in the peritoneal cavity was often observed in patients with coeliac disease and bacterial overgrowth syndrome (fig. 17) and in slight amounts also in the remaining disease entities. Last but not least, transient enteroenteric intussusception was encountered in patients with Crohn's disease, yersiniosis and coeliac disease (fig. 18). From among 15 patients with coeliac disease, US images were not “characteristic” in two cases i.e. neither fold reduction, nor increased peristalsis were observed.

Fig. 14

27-year-old male with coeliac disease – enlarged mesenteric lymph nodes

Fig. 15

Thickened wall of the small intestine without signs of perfusion as a consequence of ischemia

Fig. 16

Enlarged superior mesenteric vessels in coeliac disease. SMV – vein, SMA – artery

Fig. 17

46-year-old female with coeliac disease – free fluid in the peritoneum (F)

Fig. 18

36-year-old female with coeliac disease – transient enteroenteric intussusception shown in two sections

Discussion

The image of dynamic and morphological changes in 176 patients with small bowel diseases, as presented in this paper, confirmed the information reported by other authors( concerning the role of sonography in diagnosing small bowel pathologies. In the presented material, the most similar morphological and motor US features were observed in coeliac disease and bacterial overgrowth syndrome, which until now has not been emphasized in literature. The US differences between these two entities were slight and constituted the thickening of the mucosal folds and the reduction of their number in the jejunum in coeliac disease. In the majority of patients (20/25) with bacterial overgrowth syndrome, a partial or total gastrectomy was performed, in three patients Whipple procedure was conducted and in two – right hemicolectomy. These data practically determined the differentiation between these two disease entities. Similarly, sonography does not allow for the differentiation between two types of coeliac disease complications, i.e. ulcerative jejunoileitis and lymphoma. The results of the histopathological tests of the tissue collected by means of enteroscopy are decisive(. An interesting element that in this study distinguished coeliac disease was a type of mucosal fold thickening in the intestine. The fold hypertrophy of shrub-like type was observed solely in coeliac disease (in approximately ⅓ of patients). According to the authors’ knowledge, this type of hypertrophy has not been mentioned in the literature so far. In the five remaining disease entities, the thickened mucosal folds were flat and accompanied the thickening of the wall. Furthermore, jejunization, a characteristic feature of coeliac disease, was detected in 40% of patients with this disease and only in single cases (8%) in persons with bacterial overgrowth syndrome. The reduction of the mucosal folds in the jejunum was present in 80% of patients with coeliac disease and in merely 48% of patients with bacterial overgrowth syndrome. The occurrence of similar image features of the intestine in both these entities is justified despite their different proportions. Both diseases will finally lead to absorption disorders to the degree dependent on the duration of the disease. Therefore, clinical context is essential for differential diagnosis. Another pathology that requires the differentiation with coeliac disease is infectious diarrhea. The changes in its course also encompass the stomach and large intestine – the small bowel shows slight thickening of the walls and folds(. In three pathologies mentioned above (coeliac disease, bacterial overgrowth syndrome and infectious diarrhea) the intestinal lumen is slightly or poorly dilated but to a lesser degree than in the case of complete obstruction. Generally, fluid is dominant in the intestinal lumen and gas prevails in obstruction (tab. 1). One of the fundamental signs of numerous small bowel pathologies is increased amount of gas and fluid as well as increased peristalsis in a fasting patient(. Thus, a proper preparation for the examination is of crucial importance. If patients are not examined due to an emergency, they should be fasting and should not take any laxatives or gas-reducing agents prior to the examination. A failure to meet these requirements will entail false positive and false negative results. Furthermore, in Crohn's disease and nonocclusive ischemic disease, intestinal wall thickening is visibly greater and the lumen shows substantial stenosis in relation to other analyzed bowel diseases. Apart from the patients’ age, the difference between these two pathologies is reflected by hyperemia of the wall of the affected bowel, mesenteric adenomegaly and the presence of fistulae and/or abscesses in the course of Crohn's disease, which is not observed in ischemic segments and their surroundings. In the authors’ own research (tab. 1), it was demonstrated that hyperemia occurred in 80% of the patients with Crohn's diseases and in none of the patients with small intestinal ischemia. However, hyperemia of the wall of the intestine altered this way may be visualized in the period of reperfusion(. Currently, the most effective method to assess the perfusion in the intestinal walls is the administration of ultrasound contrast agents(. In coeliac disease, the examination may be difficult to interpret due to frequently occurring increased peristalsis(. What is more, numerous publications emphasize the usefulness of pulsed Doppler flow indicators measured in the superior mesenteric artery in evaluating the degree of activity of coeliac disease and in controlling the efficacy of treatment with gluten-free diet(. When examining a group of 50 patients with diagnosed coeliac disease, Castiglione et al.( demonstrated the diagnostic value of three factors assessed in US examination: fluid in the dilated loops, fold thickening and increased peristalsis of the small intestine. They obtained the following values: sensitivity – 66%, specificity – 96%, positive predictive value – 94% and negative predictive value – 74%. What is more, the aforementioned ultrasound signs were observed in 82% of the patients with coeliac disease which was confirmed on endoscopy, in 87.5% of patients with symptomatic course and in 61% of patients who did not manifest symptoms. The sensitivity of the US examination in the material of Soresi et al.( reached 83% and negative predictive value – 95%. In their analysis, the authors included only two features (small bowel dilatation and intestinal wall thickening). They emphasized the significance of US examination in seronegative coeliac disease. Some papers( suggest that a better visualization of the walls and mucosal folds in the patients with coeliac disease may be obtained after enteral administration of a contrast agent – so-called sonoenteroclysis.

Apart from the pathologies analyzed herein, the differential diagnosis should also encompass a range of other lesions localized in the small intestine such as: allergic enteropathy, systemic vasculitis, Whipple's disease, intramural bleeding and neoplasms, mainly carcinoma and lymphoma, which may appear particularly in patients with coeliac disease(. Two cases of lymphomas in the examined patients with coeliac disease were excluded from the presented clinical analysis.

Conclusions

Transabdominal US examination of the intestine allows for the diagnosis of numerous morphological and dynamic changes that indicate pathologies with various etiologies.

Small bowel obstruction is manifested by the presence of evidently dilated intestinal loops filled with gas and fluid and periodical deep peristaltic waves.

In ischemic conditions and Crohn's disease, a fragmentary thickening of the intestinal wall is observed in connection with intestinal stenosis; in the course of Crohn's disease, the lesions are accompanied by hyperemia of the walls and enlarged mesenteric lymph nodes.

In coeliac disease, the most often observed signs include: increased amount of fluid particularly in the jejunum, slightly thickened and hyperemic intestinal walls and increased peristalsis.

In the jejunum, characteristic signs of coeliac disease encompass: evident hypertrophy of the mucosal folds and often the reduction of their number, jejunization and transient enteroenteric intussusception.

In the presented material, coeliac disease required the differentiation from small intestinal bacterial overgrowth syndrome and, to a lesser degree, with infectious diarrhea.