abd utz in infectious enteritis

8/6/2019 Abd Utz in Infectious Enteritis

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57 T O U C H B R I E F I N G S 2 0 0 8

Gastrointestinal Imaging

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.1,2 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 abdominalsyndromes. 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.3 Furthermore, since US is a repeatable

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.7 In these infections, abdominal

US examination can show ileal and/or colonic involment.46,816 US

findings include:

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. coliinfections, 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:

marked wall thickening of the terminal ileum and the caecum

(see Figures 3a and3b), 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 (adeno-

mesenteritis);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 incidenceof 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 withbloody diarrhoea usually involving the colon and a diffuse wall thickening

Abdominal Ultrasound in Infectious Enteritis

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: [email protected]


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with distinct layer stratification in the descending and sigmoid colonhas been described.21

Gastroenteritis infection from enterotropic viruses (rotavirus,

adenovirus, Epstein-Barr virus) is frequently encountered in children.7

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 intra-

abdominal 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

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

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 theterminal 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

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 ofmalignancy.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 above-

described 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

Figure 1: Schematic Drawing of Ultrasound Scan of Bowel

LM

M1S

S

M

L

M1

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 aPatient with Salmonella Group D Enteritis

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.

Figure 3: Lower Right Abdominal Quadrant Ultrasound Scans in aPatient with Thyphoid Fever

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).

A B

A B

C D

A B

C D


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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 andsometimes 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 metronidazoleand 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 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 andstool 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.

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 beaffected.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 thick-

walled 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

Figure 5: Pseudomembranous Colitis in a Patient with AIDS

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.

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

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).

A B C

A B


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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 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 ofamoebic aetiology.

Gastrointestinal Infections in the Immunodepressed Host

In acquired immunodeficiency syndrome (AIDS), when T4 cell depletion is

marked (CD4 30mm; median 15mm), with target

appearance. In later stages, granulomatosis and deep ulcers caused by

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 seriousinfections with ulcers of the oral cavity, oesophagus, colon and,

moreover, ano-rectum.92

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 thejejunum 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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