Gastrointestinal Imaging

Abdominal Ultrasound in Infectious Enteritis

a report by

Luciano Tarantino
Director of Hepatology and Interventional Ultrasound Unit, Department of Medicine, San Giovani di Dio Hospital

The diagnosis of infectious enteritis is usually based on clinical history, symptoms and serological and cultural tests.
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marked wall thickening of the terminal ileum and the caecum (see Figures 3a and 3b), mainly involving the middle hyperechoic layer (submucosa);4,5,916 enlargement of lymph nodes in ileocaecal region, sometimes arranged in a rosary-like shape (see Figure 3c) along the mesenterium.11 Sometimes, the lymph node imflammation can extend to mesentery that appears hyperechoic, thickened and irregular (adenomesenteritis);11 perivisceral soft-tissue hyperechogenicity due to oedema and inflammation;4,5,11 and ascites or fluid collections.10,11,16 Because of the wide variability of clinical signs, prevalence and incidence of bacterial ileocaecitis, as well as the sensitivity of US, the diagnosis of ileocaecitis is not well described. In a prospective study in a large series of adult patients affected by typhoid fever, wall thickening of ileum and/or ascending colon was reported in 36% and mesenteric lymph node enlargement in 56%.11 It has been widely shown that US may reveal a high incidence of infectious ileocaecitis in patients with acute right lower quadrant pain suspected for appendicitis.46,8,9 Sonography is useful in the differential diagnosis between infectious ileocolitis, Crohns disease and appendicitis. The appendix, when detectable, is normal (see Figure 3d). Crohns disease is characterised by transmural inflammation, abscesses or fistulae and pre-stenotic dilatation.12,20 However, all of these signs are found in the advanced phases of Crohns disease, while early phases can show an aspecific inflammatory US pattern very similar to infectious ileocaecitis.20 The patients history, clinical and US follow-up and bacteriological tests will allow differential diagnosis in these cases.12 In patients with shigellosis, an acute bacterial infection presenting with bloody diarrhoea usually involving the colon and a diffuse wall thickening

However, in many cases

symptoms can mimic other intestinal diseases (e.g. appendicitis, inflammatory bowel diseases) or can be indistinguishable from disease involving other abdominal organs.16 Ultrasonography (US) is a fast, effective, non-invasive and well-tolerated diagnostic tool that has proved to be effective in the diagnosis of many acute and chronic diseases of the gastrointestinal tract as well as in other abdominal syndromes. US can be usefully employed for fast detection of enteritis in order to exclude unnecessary laparotomies or, in contrast, to avoid delaying prompt surgical therapy. Furthermore, since US is a repeatable
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and well-tolerated examination without any significant side effects, it can be used for frequent follow-up of patients with doubtful diagnosis or severe enteritis.3,4 Infectious Enteritis and Colitis The most frequent causes of bacterial enteritis and colitis in Italy are Escherichia coli and Salmonella spp. In these infections, abdominal
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US examination can show ileal and/or colonic involment. findings include:

46,816

US

Diffuse ileal and/or colonic wall thickening in 3681% of cases.9,10 In the transverse and axial US scans, the gastrointestinal tract shows a target-like appearance and a multiple parallel bands appearance, respectively (see Figures 1a and 1b). The inner hypoechoic layer (mucosa) and middle hyperechoic layer (submucosa)
18

are generally

diffusely thickened (see Figures 2a and 2b) while the muscular layer is normal;817 since the mucosal walls are effaced, the absence of intraluminal gas results in excellent visualisation of the intestinal aspect. Enlargement of mesenteric lymph nodes (see Figure 2c).915 Perivisceral (mainly peri-ileal) soft tissue hyperechogenicity because of oedema and inflammation.915 Ascites and fluid collections.10,11,16 The severity and persistence of US findings depend upon the infectious agent involved; in the case of the common minor agents (i.e. non-typhoid Salmonella, E. coli infections, etc.) the syndrome is generally self-limiting, while the symptoms and the US pattern can be rapidly worsening in cases of more specific infections (S. typhy, Shigella spp., mycobacteria, Chlostridium spp., etc.).36,816 Transient episodes of intussusception easily detectable with US (see Figure 2d) can suddenly modify the clinical presentation.19 In most cases, the occlusion is self-limiting since the invagination reduces spontaneously.19 Bacterial ileocaecitis from S. typhy, group B salmonella, Yersinia enterocolitica, Campylobacter jejunii, etc.46,817 can mimic a number of different abdominal diseases above all appendicitis.4,5,8,9,11 For these reasons, knowledge of characteristic US findings of ileocaecitis is crucial:

Luciano Tarantino is Director of Hepatology and the Interventional Ultrasound Unit at San Giovanni di Dio Hospital in Frattamaggiore, Naples, a Professor of Interventional Procedures at the School for Specialisation in General Surgery at the University of Naples and Director of the School for Postgraduate Training in Interventional Ultrasound of the Italian Society for Ultrasound in Medicine and Biology (SIUMB). He has been an invited speaker at numerous international congresses and is the author of 43 articles in international journals indexed in Medline, as well as several book chapters in the field of diagnostic and interventional ultrasound. He graduated in 1981 and specialised in infectious diseases in 1985. From 1985 to 2003 he ran research protocols in the diagnosis and therapy of hepatocellular carcinoma on cirrhosis, ultrasound of the gastrointestinal tract, ultrasound-guided abscess drainage and ultrasound-guided ablation of liver and thyroid tumours. E: luciano.tarantino@fastwebnet.it

TOUCH BRIEFINGS 2008

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Gastrointestinal Imaging

Figure 1: Schematic Drawing of Ultrasound Scan of Bowel A B

Figure 3: Lower Right Abdominal Quadrant Ultrasound Scans in a Patient with Thyphoid Fever A B

M1 M1 S M L S M L

C
In the transverse ultrasound (US) scan, the gastrointestinal tract shows a target-like appearance (A), while in the axial US scan it shows a multiple parallel bands appearance (B). The lumen (L) is hyperechoic; the inner hypoechoic layer (M) corresponds to the mucosa; the middle hyperechoic layer (S) corresponds to submucosa; and the outer hypoechoic layer (M1) corresponds to the muscularis.

Figure 2: Lower Right Abdominal Quadrant Ultrasound Scans in a Patient with Salmonella Group D Enteritis A B
A, B: Axial and transverse ultrasound (US) scans of the last ileal loop. Marked mural thickening of the bowel wall mainly involving the mucosa (M) and the submucosa (S). The muscular layer is normal. The peri-ileal tissue is hyperechoic because of oedema and inflammation. C: Mesenteric lymph nodes (L) in the ileocaecal region are enlarged, arranged in a rosary-like shape along the mesenterium. (IA = iliac artery.) D: US differential diagnosis: the hyperechoic aspect of perivisceral fat helps the detection of a normal appendix (A) beside a thickened ileal loop (I).

Tuberculous Enteritis and Colitis Tuberculous enteritis is generally described in young adults. In 90% of cases it involves the ileocaecal tract2426 and presents with a palpable C D mass in the right lower quadrant and/or complications of obstruction, perforation or malabsorption. Symptoms are rarely specific.26 Rx barium studies may show strictures, dilatation of bowel loops, narrowing of the terminal ileum, and distortion of caecum and ascending colon,27,28 but cannot detect mural lesions of ileum and colon and peritoneal involvement. US is very useful for imaging intestinal and peritoneal tuberculosis.2933 Bowel wall thickening is best appreciated in the ileocaecal region. In the early phases, ileocaecal phlogosis may show only
A, B: Axial and transverse ultrasound scans of the last ileal loop. The mucosa layer (M) and the submucosa (S) are moderately diffusely thickened, while the muscular layer is normal. The mucosal walls are effaced so that the absence of intraluminal gas results in excellent visualisation of the intestinal aspect. C: Enlargement of mesenteric lymph nodes (L). (I = ileum loops; IA = iliac artery.) D: Target inside target pattern of ileoileal invagination in enteritis. In this case the symptoms and the invagination showed spontaneous resolution after 20 minutes from the diagnosis.

regular thickening of muscosa and submucosa, a pattern that can mimic an aspecific ileocaecitis from common bacteria.30,32 Subsequently, because of granulomas and caseosis, the bowel wall appears heterogeneous and hypoechoic (see Figure 4a) with loss of normal stratification.31 Thickening (thickness up to 15mm) is uniform and concentric as opposed to the eccentric thickening at the mesenteric border found in Crohns disease or the marked irregular appearance of malignancy.33 Lymphadenopathy may be discrete or conglomerated (matted). The hypoechoic echotexture and the rounded shape (see Figure 4b) can mimic abdominal lymphoma.32,33 In tuberculosis the mesenteric, caeliac, porta hepatis and peri-pancreatic nodes are characteristically involved, reflecting the lymphatic drainage of the small bowel. The retroperitoneal nodes (i.e., the periaortic and pericaval) are relatively spared, and are almost never seen in isolation, unlike lymphoma. Ascites is present in 40% of the cases and may be free or loculated (honeycomb-like appearance) (see Figure 4c). Fluid collections in the pelvis may have thick septa and can mimic ovarian cyst.31,33 Abdominal computed tomography (CT) clearly shows all the abovedescribed US findings and accurately detects, by contrast enhancement, some specific signs, such as caseosis in the central portion of the lymph nodes as well as mesenteric and omental phlogosis.28,34 Howewer, even

with distinct layer stratification in the descending and sigmoid colon has been described.21 Gastroenteritis infection from enterotropic viruses (rotavirus, adenovirus, Epstein-Barr virus) is frequently encountered in children.
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In these cases, the main US sign is a significant enlargement of mesenteric and abdominal lymph nodes.16,22 The bowel wall thickness is rarely increased.16,22 Sonographic detection of ascites or intraabdominal fluid in children with infectious enteritis can distinguish S. enteritis from colitis due to rotavirus. In fact, despite the mural thickening, ascites is usually absent in rotavirus colitis.
16,23

In some viral

infections (e.g. Epstein-Barr virus), the severity of mesenteric lymph node involvement (see Figure 3) can suggest lynphoma; the fast and progressive decrease of lymph node hypertrophy at US follow-up helps in excluding lymphoma or other infectious conditions (such as abdominal tuberculosis).22

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Abdominal Ultrasound in Infectious Enteritis

Figure 4: Ultrasound Abdominal Scans in a Patient with Tuberculous Enteritis A B C

A: Marked heterogeneous, hypoechoic, tumour-like thickening of bowel wall (arrows), with loss of normal stratification. B: Mesenteric lymph nodes (LN) are markedly enlarged, rounded shape with heterogeneous and hypoechoic echotexture. In some cases the differential diagnosis with abdominal lymphoma is difficult. C: Pseudomembranous organisation of exudate in tuberculous ascites often shows a multiloculated aspect (honeycomb-like appearance).

with CT, differential diagnosis can be very difficult, as lymphoma or Crohns disease cannot be easily ruled out. Paracentesis and/or lymph node fine needle biopsy under US guidance shows phlogosis and sometimes granulomatus inflammation and, above all, detects mycobacteria by Zeel-Nielsen staining of the specimens.35,36 Antibiotic-associated Diarrhoea and Pseudomembranous Colitis Antibiotic-associated diarrhoea (AAD) occurs in about 530% of patients either early during antibiotic therapy or up to two months after the end of the treatment.37 Clinical presentations of AAD range from mild diarrhoea to fulminant pseudomembranous colitis.38 The latter is characterised by a watery diarrhoea, fever (in 80% of cases), leukocytosis (80%) and the presence of pseudomembranes on pathological gross specimens and endoscopic examination.39 Treatment with metronidazole and vancomycin is usually effective.38 If not treated promptly, severe complications including toxic megacolon, perforation and shock can occur, resulting in significant morbidity and mortality.4042 In moderate to severe cases, a diffuse or segmental thickening of the colonic wall is present at US.
4248

Figure 5: Pseudomembranous Colitis in a Patient with AIDS A B

A: Longitudinal ultrasound scan of ascending colon. Colonic wall is markedly thickened, heterogenous and hypoechoic. The presence of sligthly hyperechoic multiple deep ulcers (arrows) originating from the lumen gives an accordion sign appearance to the colonic segment. B: Transverse scan of the caecum. The colonic wall shows heterogeneous and hypoechoic texture with complete absence of the normal layer stratification because of the diffuse, deep inflammation and necrosis of the bowel wall.

Necrotising Colitis, Typhlitis (Neutropenic Colitis) and Pneumatosis Intestinalis Neutropenic colitis (also known as typhlitis) and acute necrotising enteritis occur in severely immunocompromised patients, characterised by thrombosis of intestinal wall vessels and necrosis that leads to oedema, thickening, mucosal ulcerations and eventual perforation.5255 Intestinal wall necrosis may result in intraluminal bacterial gas entering the bowel wall (pneumatosis intestinalis) due to increased mucosal permeability caused by defects in the bowel wall.56,57 The ileum and caecum are most commonly involved in typhlitis and necrotising enterocolitis, but the remaining colon and distal ileum may also be affected.58,59 Neutropenic typhlitis has a mortality rate of 50100%.53,54,60 The finding of pneumatosis intestinalis in this clinical context must be considered a poor prognostic sign.61 Sonography is a rapid, non-invasive means for the detection of a thickwalled caecum and ascending colon in these patients. The colonic wall echotexture is usually hypoechoic and heterogeneous, with loss of the common distinct layers.6268 It has been demonstrated that the degree of thickening is a valuable prognostic factor that adversely affects the outcome.62,66 The sonographic detection of increased colonic wall thickening (>4mm) twofour days after the end of intensive chemotherapy in neutropenic (neutrophils below 0.5x109/l) patients with a clinical syndrome characterised by fever, diarrhoea and abdominal pain, confirms the clinical diagnosis of infectious neutropenic enterocolitis. In particular, it has been proposed that those patients with thicker bowel

The wall of the affected colon is

markedly thickened, hypoechoic and heterogeneous, causing narrowing of the lumen (see Figures 5a and 5b). Ascites are present in 5080% of cases.43,47,48 The degree of colonic wall thickening is more marked in pseudomembranous colitis than with most other causes of colitis.47 Because other entities including ischaemic and infectious colitis may produce similar imaging findings, the clinical setting and stool cultures are helpful in establishing the correct diagnosis. Detection of Clostridium difficile toxins in the faeces is considered the gold standard for diagnosis. Howewer, the toxin can be found in many asymptomatic adult subjects taking antibiotics and in up to 50% of healthy neonates.49 Barium X-ray studies usually show aspecific signs since the thumb printing sign and nodular pattern of the mucosal surface are present only in late phases.42,50 Colonoscopy can show a specific mucosal pattern of pseudomembranes; howewer, it can be poorly tolerated by many with acute colitis.42 CT and US, by showing marked bowel wall thickening, mucosal nodular pattern and sometimes the more specific pattern of the accordion sign
51

in

patients with suggestive clinical history, can offer a reliable diagnosis of antibiotic-associated colitis and justify a prompt start to metronidazole and vancomycin therapy. US is also a valuable tool for follow-up of these severely ill patients.

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wall (>10mm) should receive intensive supportive treatment.62 Sonography is also an important tool in monitoring these patients in the intensive care setting.68 Pneumatosis intestinalis has been described at US as the presence of echogenic foci in the thickened intestinal wall, better detected with high-frequency probes.
6970

vasculitis and ischaemic phenomena produce an irregular, hypoechogenic, heterogeneous pattern of colonic wall.91 Thickening and hyperechogenicity of pericolic and mesenteric fat are always associated, whereas abdominal lymph node enlargement is infrequent. Ascites is present in 4050%. Early aetiologic diagnosis of CMV colitis is very important since effective (7080% of cases) antiviral therapies (ganciclovir) are available. X-ray, US and CT and even endoscopy may not allow differential diagnosis in comparison with other infectious enterocolitis, also frequent in AIDS patients. In focal forms, the signs of pericolic phlogosis allow a differential diagnosis between CMV pseudotumour, Kaposis sarcoma and non-Hodgkin lymphoma.89,90,91 Serological tests can have anamnestic value. Early and certain diagnosis must be obtained by means of histologic endoscopic examination, which shows the typical phlogistic pattern with giant cells and intranuclear inclusions by CMV.85,91 In AIDS patients, herpes simplex virus (HSV) can cause very serious infections with ulcers of the oral cavity, oesophagus, colon and, moreover, ano-rectum.92

This finding must be

differentiated from artefacts mimicking pneumatosis.70 In doubtful cases a more specific tool, such as CT, must be used to confirm the diagnosis.71 Amoebic Colitis Colonic infestation from Entamoeba hystolitica can result in asymptomatic to mild or moderate colitis to fulminant colitis.80 At US, marked thickening of the bowel wall with, specifically, thickening of the submucosal layer have been described. A mild to moderate colonic wall thickening can be observed also in asymptomatic patients with positive stool for amoebic cysts and trophozoites.81 Metronidazole treatment is rapidly and lastingly effective.80 Since an unsuitable corticosteroid therapy may precipitate a life-threatening manifestation of intestinal amoebiasis as fulminant colitis, an ex adjuvantibus attempt with metronidazole therapy is indicated when the patients history suggests the possibility of amoebic aetiology. Gastrointestinal Infections in the Immunodepressed Host In acquired immunodeficiency syndrome (AIDS), when T4 cell depletion is marked (CD4 <400/mm3), gastrointestinal infections by opportunistic agents, which only rarely cause infections in immunocompetent hosts, can occur.82,83 Cytomegalovirus (CMV) infection represents 13% of the gastrointestinal tract infections in AIDS patients. It often causes death and frequently represents the first clinical sign of HIV disease (in up to 25%).8486 In AIDS patients the colon is the main target of CMV. In CMV colitis the extent of the disease is very variable; most frequently the recto-sigmoidal and caecum-ascending colon tracts are involved, often associated with involvement of the terminal ileum (typhlitis or ileocolitis pattern).87 Lesions located in short tracts of colon (especially rectus, sigma and right colon) may mimic tumour-like patterns (CMV pseudotumour).88 However, pancolitis patterns, mimicking pseudomembranous colitis, are also reported.89 Also, skip areas have been described in 20% of cases.90 The US findings of intestinal affected segments include a marked and concentric mural thickening (even >30mm; median 15mm), with target appearance. In later stages, granulomatosis and deep ulcers caused by

At US, herpetic proctosigmoiditis shows thickening and a hypoechoic pattern of both the rectum and terminal tract of sigmoid walls.8 Surrounding soft tissues are strongly hyperechoic, because of perivisceral phlogosis. Transvescical abdominal US with a 5MHz probe or transperineal US can describe the extension of inflammation towards superior tracts of colon. The most frequent cause of opportunistic bacterial infections in AIDS patients is mycobacterium avium complex (MAC).93,94 The segments most frequently interested are jejunum and ileum.95 US can demonstrate thickening and increased reflectivity of the jejunum plicae and ileum submucosa,96,97 swelling and hypoechogenicity of mesenteric and retroperitoneal lymph nodes,9699 thickening and hyperechogenicity of mesentery, and also hepatosplenomegaly with multiple small parenchymal abscesses, usually very numerous in the spleen.99,100 The abscess size can be below 3.5MHz probe resolution, so that only with high-frequency probes is it possible to have a reliable estimate of the number and extension of the abscesses.101 Definitive diagnosis must be obtained by US-guided fine needle aspiration biopsy, either of a lymph node or a liver/splenic abscess, which always shows numerous acid-alcohol resistant bacilli.99,101103

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