bowel thickening

11
AJR:174, January 2000 107 he potential value of transabdom- inal sonography in the diagnosis of bowel diseases is often not suf- ficiently appreciated and is even underesti- mated. Bowel gas artifacts and the somewhat confusing sonographic appearance of the gas- trointestinal tract may render orientation and interpretation of sonographic structures diffi- cult. Bowel wall thickening, the main sono- graphic correlate of bowel disorders, seems at first glance a very nonspecific sign, which may explain why inexperienced investigators do not feel confident in the sonographic eval- uation of the gastrointestinal tract. However, it has been shown that transabdominal sonog- raphy achieves good to excellent results as a directed tool for evaluating potential bowel disorders: appendicitis can be diagnosed with a sensitivity ranging from 80% to 93% and a specificity between 94% and 100% [1, 2]. Reported sensitivity rates for evaluating in- flammatory bowel disease range between 67% and 96%, with specificities of 79–97% [3, 4]. Equal diagnostic accuracy of 84% was found for CT and for sonography in the workup of diverticulitis, with sensitivities of 91% and 85%, respectively, and specificities of 84% and 77%, respectively [5]. Although the sonographic appearance of bowel wall thick- ening of different diseases sometimes over- laps, careful examination of the thickened bowel segment in context with the clinical in- formation often leads to a limited differential diagnosis or to the correct diagnosis. The differential diagnoses of small- bowel wall thickening and of colonic wall thickening are shown in Appendixes 1 and 2, respectively. This article provides a systematic overview of diseases that may cause bowel wall thick- ening. Typical sonographic features of these disorders are discussed and compared. A re- view of the literature further summarizes the reported diagnostic potential of sonography and its limitations. Technique Examination of the intestinal tract usually begins with a systematic standardized survey using a curvilinear 3.5–5-MHz transducer. In patients with localized abdominal pain, how- ever, it may be helpful and timesaving to let patients indicate the position of maximum pain with their fingers on the abdominal wall and begin the examination there. In case of diffuse abdominal pain, the frame of the co- lon is identified by its strong gas artifacts and is screened from the cecum to the sigmoid colon. The rest of the abdomen is examined in an individual standardized fashion to assure complete coverage of the entire gastrointestinal tract. If intestinal wall thick- ening is found, detailed evaluation of the dis- eased segment is performed with a linear or curved high-frequency (7.5–13 MHz) trans- ducer. When the affected bowel segment is far from the abdominal surface and when the patient is obese, a fair amount of pressure must be applied to the transducer to get ac- ceptable images. For optimal results, it may be necessary to change the patient’s position several times during the examination. Only careful methodic examination of the entire abdomen leads to acceptable results; the ac- curacy of the examination depends largely on the radiologist’s experience and patience [5]. Ideally, patients fast overnight before the examination, but at least 4–5 hr of fasting are needed to avoid excessive gas in the intesti- nal lumen. Normal Sonographic Bowel Wall Anatomy The typical sonographic appearance of the normal bowel wall consists of five concen- tric, alternately echogenic and hypoechoic layers that we describe from the lumen out- ward (Fig. 1). First, a small echogenic layer is seen that reflects the superficial mucosal interface. The deep mucosa, including the muscularis mucosa, is seen as a second hyper- Bowel Wall Thickening on Transabdominal Sonography Hans Peter Ledermann 1 , Norbert Börner 2 , Holger Strunk 3 , Georg Bongartz 1 , Christoph Zollikofer 4 , Gerd Stuckmann 4 Received January 27, 1999; accepted after revision June 7, 1999. 1 Department of Radiology, University Hospital of Basel, Petersgraben 4, CH-4031 Basel, Switzerland. Address correspondence to H. P. Ledermann. 2 Gastroenterologische Gemeinschaftspraxis, Parcusstr. 8, 55116 Mainz, Germany. 3 Department of Radiology, Friedrich-Wilhelms-Universität Bonn, Sigmund-Freud-str. 25, 53105 Bonn, Germany. 4 Department of Radiology, Kantonsspital Winterthur, Brauerstr. 15, 8400 Winterthur, Switzerland. AJR 2000;174:107–117 0361–803X/00/1741–107 © American Roentgen Ray Society T Review

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Page 1: Bowel Thickening

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107

he potential value of transabdom-inal sonography in the diagnosisof bowel diseases is often not suf-

ficiently appreciated and is even underesti-mated. Bowel gas artifacts and the somewhatconfusing sonographic appearance of the gas-trointestinal tract may render orientation andinterpretation of sonographic structures diffi-cult. Bowel wall thickening, the main sono-graphic correlate of bowel disorders, seems atfirst glance a very nonspecific sign, whichmay explain why inexperienced investigatorsdo not feel confident in the sonographic eval-uation of the gastrointestinal tract. However,it has been shown that transabdominal sonog-raphy achieves good to excellent results as adirected tool for evaluating potential boweldisorders: appendicitis can be diagnosed witha sensitivity ranging from 80% to 93% and aspecificity between 94% and 100% [1, 2].Reported sensitivity rates for evaluating in-flammatory bowel disease range between67% and 96%, with specificities of 79–97%[3, 4]. Equal diagnostic accuracy of 84% wasfound for CT and for sonography in theworkup of diverticulitis, with sensitivities of91% and 85%, respectively, and specificities of84% and 77%, respectively [5]. Although thesonographic appearance of bowel wall thick-ening of different diseases sometimes over-laps, careful examination of the thickened

bowel segment in context with the clinical in-formation often leads to a limited differentialdiagnosis or to the correct diagnosis.

The differential diagnoses of small-bowel wall thickening and of colonic wallthickening are shown in Appendixes 1 and2, respectively.

This article provides a systematic overviewof diseases that may cause bowel wall thick-ening. Typical sonographic features of thesedisorders are discussed and compared. A re-view of the literature further summarizes thereported diagnostic potential of sonographyand its limitations.

Technique

Examination of the intestinal tract usuallybegins with a systematic standardized surveyusing a curvilinear 3.5–5-MHz transducer. Inpatients with localized abdominal pain, how-ever, it may be helpful and timesaving to letpatients indicate the position of maximumpain with their fingers on the abdominal walland begin the examination there. In case ofdiffuse abdominal pain, the frame of the co-lon is identified by its strong gas artifacts andis screened from the cecum to the sigmoidcolon. The rest of the abdomen is examinedin an individual standardized fashion toassure complete coverage of the entire

gastrointestinal tract. If intestinal wall thick-ening is found, detailed evaluation of the dis-eased segment is performed with a linear orcurved high-frequency (7.5–13 MHz) trans-ducer. When the affected bowel segment isfar from the abdominal surface and when thepatient is obese, a fair amount of pressuremust be applied to the transducer to get ac-ceptable images. For optimal results, it maybe necessary to change the patient’s positionseveral times during the examination. Onlycareful methodic examination of the entireabdomen leads to acceptable results; the ac-curacy of the examination depends largelyon the radiologist’s experience and patience[5]. Ideally, patients fast overnight before theexamination, but at least 4–5 hr of fasting areneeded to avoid excessive gas in the intesti-nal lumen.

Normal Sonographic Bowel Wall Anatomy

The typical sonographic appearance of thenormal bowel wall consists of five concen-tric, alternately echogenic and hypoechoiclayers that we describe from the lumen out-ward (Fig. 1). First, a small echogenic layeris seen that reflects the superficial mucosalinterface. The deep mucosa, including themuscularis mucosa, is seen as a second hyper-

Bowel Wall Thickening on Transabdominal Sonography

Hans Peter Ledermann

1

, Norbert Börner

2

, Holger Strunk

3

, Georg Bongartz

1

, Christoph Zollikofer

4

, Gerd Stuckmann

4

Received January 27, 1999; accepted after revision June 7, 1999.

1

Department of Radiology, University Hospital of Basel, Petersgraben 4, CH-4031 Basel, Switzerland. Address correspondence to H. P. Ledermann.

2

Gastroenterologische Gemeinschaftspraxis, Parcusstr. 8, 55116 Mainz, Germany.

3

Department of Radiology, Friedrich-Wilhelms-Universität Bonn, Sigmund-Freud-str. 25, 53105 Bonn, Germany.

4

Department of Radiology, Kantonsspital Winterthur, Brauerstr. 15, 8400 Winterthur, Switzerland.

AJR

2000;174:107–117 0361–803X/00/1741–107 © American Roentgen Ray Society

T

Review

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echoic layer. A third hyperechoic layer isproduced by the submucosa and the muscu-laris propria interface. The muscularis pro-pria is seen as a fourth hypoechoic layer.Finally, the marginal interface to the serosa isseen as the fifth small hyperechoic layer. Theaverage thickness of the normal gut wall is2–4 mm [6].

Inflammatory Bowel Disease

The classic sonographic feature of Crohn’sdisease is the “target” sign (Fig. 2) on trans-verse images, which means a strong echogeniccenter surrounded by a relatively sonolucentrim of more than 5 mm. This transmural in-flammation or fibrosis can lead to completecircumferential loss of the typical gut wall lay-

ers, which results in a thick hypoechoic rim onaxial images. Strictures are shown as markedthickening of the gut wall with a fixed hyper-echoic narrowed lumen (Fig. 3A), dilatation,and hyperperistalsis of the proximal gut. Peri-intestinal inflammation leads to the “creepingfat” sign, which appears as a uniform hyper-echoic mass typically seen around the ileumand cecum. Mesenteric lymphadenopathy isseen as multiple oval hypoechoic masses, usu-ally in the right lower quadrant. In contrast toother forms of colitis, Crohn’s disease is sug-gested by skip areas and involvement of thedistal ileum [7]. Possible complications ofCrohn’s disease comprise fistulas, abscess for-mation, mechanical bowel obstruction, andperforation [8]. Abscesses are seen as poorlydefined, mostly hypoechoic focal masses thatcan contain hyperechoic gas (Fig. 3B). Fistulasare a hallmark of Crohn’s disease and are seenin as many as one third of patients with ad-vanced disease as hypoechoic tracts with gasinclusions connecting bowel loops or adjacent

Fig. 1.—4-year-old girl with gastroenteritis. Sagittalsonogram shows normal gut wall layering of rectum(RE) from lumen outward. Note small echogenic layerin lumen that reflects superficial mucosal interface(short thin arrow ). Deep mucosa, including muscu-laris mucosa, is seen as second hypoechoic layer(long thin arrow ). Third broad hyperechoic layer isproduced by submucosa and muscularis propria inter-face (open arrow ). Muscularis propria is seen asfourth hypoechoic layer (short thick arrow ). Marginalinterface to serosa is seen as small fifth hyperechoiclayer (curved arrow ). ASC = ascites in retrovesicalspace, B = bladder.

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Fig. 2.—25-year-old woman with Crohn’s disease who presented with new onset of crampy abdominal pain. A, Transverse sonogram shows concentric echolucent wall thickening producing typical “target” sign. B, Close-up longitudinal sonogram of same segment as A shows circular hypoechoic wall thickening and loss ofstratification that, together with clinical information, led to diagnosis of Crohn’s disease. C, Small-bowel contrast-enhanced enema shows segmental bowel wall edema (arrow ) with “thumbprinting” andnarrowing of jejunal lumen in left lower abdomen. Diagnosis of Crohn’s disease was later clinically confirmed.

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structures (bladder, abdominal wall, vagina,psoas muscle) (Fig. 3C). Detection of gas bub-bles in abnormal locations raises the possibil-ity of fistulous communication.

In expert hands, the distribution of franklesions of inflammatory bowel disease canbe determined with a sensitivity of 73–87%on sonography [3, 9, 10]. However, mild le-sions that produce less bowel wall thicken-ing are frequently not diagnosed, and thesensitivity for these lesions drops to 52%[3]. These results indicate that sonographycannot replace a contrast-enhanced exami-nation or endoscopy when highly accurate

assessment of the extent of the inflammatorylesion is requested [3].

Determination of disease activity by sonog-raphy is controversial. Whereas some investiga-tors showed correlation with disease activity [4,10, 11], others found only a loose correlationbetween bowel wall thickening and disease ac-tivity [9]. The ranges of reported sensitivitiesand specificities in the diagnosis of Crohn’s dis-ease are 67–96% and 79–97%, respectively [4,12–14]. The relatively wide range in the valuesof sensitivity and specificity may be explainedby the use of low-frequency transducers (3.5MHz) in older studies and the use of high-reso-

lution equipment using 5–10-MHz broadbandlinear transducers. In ulcerative colitis, sensitiv-ity reaches 89% and specificity reaches 100%[11]. Differentiation between Crohn’s diseaseand ulcerative colitis based on sonographic find-ings includes the location of the disease, thepresence of skip lesions, and the presence ofpericolic abscesses [14]. Bowel wall thickeningis usually less marked in ulcerative colitis withpreserved stratification [15] (Fig. 4). However,definite differential diagnosis is difficult ontransabdominal sonography [4, 16].

Non-Hodgkin’s Lymphoma of the Gastrointestinal Tract

The gut is the most commonly involved ex-tranodal site of lymphoma [17]. The mostcommon sites, in order of descending fre-quency, are stomach, small intestine, and co-lon, especially cecum [17]. Eighty percent ofgastrointestinal lymphomas are of B-cell ori-gin. In patients with underlying celiac disease,however, T-lymphocyte origin predominates.Sonography classically shows transmural cir-cumferential, profoundly hypoechoic wallthickening up to 4 cm in diameter [18], withloss of normal stratification (Fig. 5A). Thispattern, also known as the “pseudokidney”sign in longitudinal views, is observed in 70%of patients [19] (Fig. 5B). The pseudokidneysign is often seen in lymphoma because of ex-tensive hypoechoic bowel wall thickening, butit can be seen in any bowel disorder leading tomarked bowel wall thickening [20, 21]. Otherfindings include nodular or bulky tumor spread

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Fig. 3.—Complications of Crohn’s disease.A, Stricture with obstruction in 52-year-old man. Transverse sonogram of ileum (arrows) shows severe narrowing of small hyperechoic central lumen caused by exces-sively echolucent wall thickening and loss of stratification, indicating scarring of entire bowel wall. B, Hypoechoic ileal abscess (A) in highly hypertrophic and inflamed hyperechoic fat of mesentery of 25-year-old woman.C, Sonogram obtained at time of suspected relapse of 31-year-old woman shows hypoechoic fistula with small hyperechoic gas inclusion (arrow ).

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Fig. 4.—26-year-old man with ulcerative colitis and new onset of bloody diarrhea. A, Sagittal sonogram of descending colon reveals only subtle thickening of bowel wall (4.2-mm-thick submucosabetween crosses) with preserved stratification and normal echo texture of adjacent mesenteric fat. B, Large-bowel enema with fine granularity of mucosa reflecting hyperemia and edema confirms suspectedsonographic diagnosis of early changes in ulcerative colitis.

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caused by extraluminal involvement [18] (Fig.5C). Mesenteric tumor spread and bulky tumorgrowth need biopsy for definite diagnosis be-cause they cannot be reliably differentiatedfrom other diseases such as primary bowel tu-mors or metastases. Isolated mucosal in-volvement is rare and leads to hyperechoicthickening of the mucosa (Fig. 5D). Sono-graphic patterns favoring the diagnosis of anon-Hodgkin’s lymphoma over adenocarci-noma are transmural circumferential, pro-foundly hypoechoic wall thickening withpreserved peristalsis; lack of intestinal obstruc-tion, because narrowing of the lumen is un-common; involvement of a long stretch of thegut; and the presence of multiple prominentregional lymph nodes [22]. Typical complica-tions are mucosal ulceration leading in 10–50% of patients to bleeding, perforation of thesmall intestine, and intussusception of the

bowel [23]. The most commonly involvednodal groups in non-Hodgkin’s lymphoma ofthe gastrointestinal tract are the celiac, retro-crural, perirenal, perisplenic, perihepatic, andmesenteric nodes [22].

Acute Terminal Ileitis

The clinical symptoms of acute ileitis areright-sided lower abdominal pain, diarrhea,and nausea, with an accelerated erythrocytesedimentation rate, positive C-reactive protein,and leukocytosis. Only careful evaluation inthe preoperative workup for suspected appen-dicitis can prevent an unnecessary operation[24]. Acute ileitis is caused by

Yersinia

speciesbut

Campylobacter

and

Salmonella

speciesmay also be cultured. Reported sonographicfeatures include hypoechogenic mural thicken-ing of the terminal ileum and cecum between 6

and 10 mm with hypoechoic swollen ilealfolds in the edematous mucosa [24, 25]. Hypo-echoic enlarged mesenteric lymph nodes rang-ing from 7 to 21 mm in diameter were found inmost patients. Color Doppler sonography inpatients with infectious ileitis shows increasedflow centrally rather than peripherally (as inappendicitis) [26].

Tuberculous enteritis and Behçet’s syn-drome also predominantly affect the ileoce-cal region [27]. In a series of 45 patientssuffering from ileocecal tuberculosis, sonog-raphy showed segmental predominantly con-centric thickening of the terminal part of theileum and cecum in 43 patients [13], with en-largement of the regional mesenteric lymphnodes in 50% of these patients.

Appendicitis

The typical finding of acute appendicitis intransverse sonograms is the target sign with ahypoechoic center, an inner hyperechoic ring,and an external thicker hypoechoic ring (Fig.6A). In sagittal images, the inflamed appendixis seen as a blind-ending noncompressible tu-bular structure (Fig. 6B). Focal or circumferen-tial loss of the inner layer of echoes usuallyindicates gangrenous inflammation and ulcer-ation of the submucosa. Several studiesachieved sensitivities of 80–93% and specifici-ties of 94–100% in the sonographic workup ofacute appendicitis [1, 2]. On the other hand, CThas shown sensitivities of 90–100% with speci-ficities of 83–98% [28–30]. In one study with alow (76%) sensitivity for sonography, CT wasfound to be more accurate than sonography inthe diagnosis of acute appendicitis [28].Graded compression sonography gained wide-spread acceptance as a useful technique toexamine patients with atypical signs of appen-dicitis [31]. In a prospective study, the pro-posed treatment after clinical examinationchanged in 26% of all patients after sono-graphic examination [2]. The diagnosis can beestablished with confidence if the appendix isnoncompressible, shows no peristalsis, andmeasures more than 6 mm in diameter [32] onaxial images, and if compression leads to a lo-calized pain response. The surrounding mesen-tery is often inflamed, which can be seen as ahyperechoic diffuse halo sign around the ap-pendix (Fig. 6A). If an appendicolith is identi-fied in an appendix of any size, the findings ofthe examination are always considered positive[33] (Fig. 6C). A simple additional color Dop-pler examination may be helpful in the diagno-sis of early acute appendicitis [34]. The

Fig. 5.—Four typical sonographic variants of non-Hodgkin’s lymphoma.A, Most common circular involvement of entire wall with preserved peristalsis in 45-year-old man with unchar-acteristic abdominal pain. Transverse sonogram reveals profound hypoechoic wall thickening. B, “Pseudokidney” sign in ileocecal region: marked hypoechoic thickening of bowel wall resembling form of kid-ney in longitudinal sonogram of cecum. Patient is 57-year-old woman.C, Bulky disease in cecum in 63-year-old woman. Axial sonogram reveals large eccentric hypoechoic mass withcompression of hyperechoic lumen. D, Isolated mucosal involvement in 43-year-old man. Transverse sonogram of ileum with marked hyperechoic gy-ral thickening of mucosa and preserved layering of bowel wall.

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presence of visible hyperemia or increasedflow in the hypoechoic muscular layer of thebowel wall may be a marker of appendicitis,whereas increased flow in the mucosal layermost likely represents enteritis [26]. Increasedflow in the fat surrounding the appendix is in-dicative of transmural extension of the inflam-mation with mesenteric response. An inflamedappendix rarely measures more than 15 mm intransverse diameter [33], which usually allowsdifferentiation from ileitis. A markedly en-larged or perforating appendix or dilated fallo-pian tubes may lead to interpretive pitfalls [33].

Perforation occurs in 20–30% of young pa-tients with appendicitis (Fig. 6D). A statisti-cally significant association exists betweenperforation and two sonographic findings: loc-ulated pericecal fluid and loss of the echogenicsubmucosa [35]. Abscess formation is the ma-jor complication of perforating appendicitis.Abscesses may extend into the pelvis or intothe peritoneal spaces of the upper abdomen.They may be sonolucent or appear as a com-plex mass. Advantages of sonography are wideavailability, lack of radiation, and lack of con-trast administration. Limitations of sonogra-phy occur in obese and extremely meteoristicpatients and in patients with severe pain due toperitonitis. Retrocecal appendicitis may be dif-

ficult to diagnose on sonography. Because CThas been shown to be more accurate in stagingperiappendiceal inflammation and abscesses[5, 28, 36], CT may be preferred in patientswith suspected perforation or abscess; CT reli-ably differentiates phlegmon from abscess andserves as an accurate “road map” for potentialabscess drainage.

Small-Bowel Diseases

Mesenteric infarction in its late stagesleads to small-bowel wall thickening [37, 38].In the early stages, however, no bowel wallthickening may be seen. Doppler sonographycan aid in differentiating ischemic and in-flammatory bowel wall thickening. In ap-proximately 90% of cases, small-bowelinfarctions are due to arterial hypoperfusion;only 10% are caused by mesenteric vein oc-clusion. Acute intramural intestinal he-matoma leads typically to a homogeneoushypoechoic symmetric thickening of a longstretch of the affected bowel segment, withreduced or absent peristalsis and marked lu-minal narrowing [39] (Fig. 7). In the subacutestage, strong internal echoes caused bythrombi may mimic an abscess [40].

Amyloidosis is a rare condition; however,gastrointestinal involvement in patients with

amyloid is frequently seen [41]. Marked hypo-echoic thickening of the affected bowel seg-ments is found [42, 43].

Eosinophilic enteritis is a rare disease charac-terized by infiltration of the stomach or bowelwall with eosinophilic leukocytes. In three re-ported cases, hypoechoic thickening of multipleileal loops, narrowing of the lumen, and loss oflayer structure were described [44, 45].

Fig. 6.—Sonographic findings in acute appendicitis.A, “Target” sign (curved arrows) in acute appendicitisin 12-year-old girl. On transverse image, inflamed ap-pendix is seen with hypoechoic center, inner hyper-echoic ring, and outer hypoechoic ring. Notehyperechoic circular area (straight arrows) of in-flamed mesentery (“halo” sign). B, Longitudinal sonogram of inflamed appendix insame patient shows blind-ending tubular structure(arrow ) of at least 6 mm in diameter. C, Multiple appendicoliths in 6-year-old girl. Longitudi-nal section of inflamed appendix reveals five roundhyperechoic appendicoliths with acoustic shadows. D, Perforating appendicitis in 6-year-old girl. Longitu-dinal sonogram of inflamed appendix shows typicalblind-ending tubular structure and hypoechoic collec-tion around tip, indicative of perforation.

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Fig. 7.—72-year-old woman with intramural hematomadue to anticoagulant drug therapy. Patient was sent forsonography to rule out atypical appendicitis. Trans-verse sonogram of small-bowel segment discloses cir-cumferential hypoechoic thickening of bowel wall withloss of stratification and compression of lumen.

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The sonographic features of primary lym-phangiectasia have been described in four pa-tients [46, 47]. Diffuse hypoechoic small-bowelwall thickening, ascites, mesenteric edema, andthickened walls of the gallbladder and urinarybladder are found.

One case report describes the sonographicfindings of nontropical sprue (celiac disease)as diffuse hypoechoic thickening of the entiresmall-bowel wall that disappears completelyafter 3 months of a gluten-free diet [48].

Sonographic findings in a patient withWhipple’s disease (intestinal lipodystrophy)disclosed hyperechoic concentric thickeningof the small bowel with enlarged hyper-echoic lymph nodes [49]. The hyperechoicstructure of the intestinal wall and the en-larged lymph nodes are explained by fat ac-cumulation in these structures [50] (Fig. 8).

Markedly thickened hypoechoic bowel loops,preferentially in the distal ileum, were found inintestinal anisakiasis, a parasitic disease of thegastrointestinal tract caused by ingestion of

Anisakis

larvae in raw or undercooked fish [51]. Hypoechoic small-bowel wall thickening

reaching 11 mm and revealing a pseudokid-ney appearance was found in a patient suffer-ing from intestinal Behçet’s disease [21].Cytomegalovirus enteritis in AIDS patientsleads to wall thickening of the small andlarge bowels with preserved stratification.

Tumors of the Small Intestine Other Than Lymphomas

Peritoneal carcinomatosis is the most fre-quent malignant lesion of the small bowel and

may lead to irregular wall thickening with thetypical contraction of several bowel loops to aconglomerate. Most frequent primary tumorsoriginate from the ovary, stomach, colon, pan-creas, gallbladder, lung, and uterus. Primarysmall-bowel tumors constitute only 3–6% ofgastrointestinal neoplasms. Abdominal symp-toms are usually vague and poorly defined, andconventional radiography of the upper andlower intestinal tract often has normal results.These factors may lead to a delayed diagnosis.Carcinoid tumor is the most frequent small-bowel tumor [52] and occurs in 80% of cases in

the distal ileum (Fig. 9). All small-bowel carci-noids are considered malignant because theyeventually grow, invade, and metastasize. Me-tastases will occur in 10% of lesions smallerthan 1 cm and 95% of lesions larger than 2 cm[53]. Only 4% of patients present with the typi-cal carcinoid syndrome [54]. In a series of sixpatients, small bowel carcinoids presented ashypoechoic, homogeneous predominantlyintraluminal masses with smooth intralumi-nal contour [54]. The tumors were attached tothe wall by a broad base, with interruption ofthe submucosa and thickening of the muscularis

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Fig. 8.—50-year-old man with Whipple’s disease (intestinal lipodystrophy) presenting with steatorrhea. A, Longitudinal sonogram depicts marked hyperechoic jejunal fold thickening.B, Transverse sonogram shows jejunal thickening and hyperechoic lobulated lymph node (arrow ).C, CT scan shows prominent jejunal folds and enlarged mesenteric lymph nodes. (Courtesy of Disler M, Kantonsspital Liestal, Switzerland)

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Fig. 9.—57-year-old man with ileal carcinoid tumor presenting with mechanical small-bowel obstruction.A, Transverse sonogram of terminal ileum reveals hypoechoic, homogeneous intraluminal mass with smooth in-traluminal contour and broad-based hypoechoic infiltration of submucosa posteriorly. Note fluid-distendedsmall-bowel segments ventral to tumor, indicating mechanical obstruction.B, CT scan reveals strongly enhancing mass (arrow ) in terminal ileum, with infiltration of mesenteric fat dorsallyand mechanical obstruction of small bowel.

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propria in all cases. Carcinoid tumors of the ap-pendix were described in two cases [55] as hy-poechoic, well-delineated elongated masses inthe distal lumen and the tip of the appendix.

Lipomas are the second most common tumorsof the small intestine and occur with greatest fre-quency in the distal ileum and at the ileocecalvalve. The location of these tumors is submu-cosal, or, less frequently, is subserosal. In threefourths of cases, the tumors are clinically silent[56]. If the lipoma becomes larger than 4 cm,chronic hemorrhage caused by ulceration of themucosa or intestinal obstruction resulting from in-tussusception may cause symptoms [57, 58]. Typ-ical sonographic features are a well-circumscribedhyperechoic round or oval mass with deformationunder compression. Leiomyomas and schwanno-mas are seen as hypoechoic intramural roundstructures with smooth boundaries [52, 58, 59].Ulceration of the mucosa may cause gastrointesti-nal hemorrhage of varying severity. Leiomyosar-comas were described as large irregular masseswith a heterogeneous echo pattern [58]. Adeno-carcinoma is the second most common small in-testine malignancy and the peak incidence is inthe seventh decade of life [52]. A series of fourcases with duodenal adenocarcinomas showedmoderately large intraluminal masses with me-dium echogenicity [58]. The authors report im-proved sonographic detection of small-boweltumors by intermittent observation of the small-bowel lesions during the first hour after wateringestion. Transabdominal sonography reachedexcellent sensitivity in detecting small-boweltumors in unexplained gastrointestinal bleeding[59] and in small-bowel obstruction [60]. Inmost cases, the tumors were seen as round andsmoothly delineated hypoechoic masses.

Colitis

The sonographic features of pseudomembra-nous colitis have been described in a number ofreports [61, 62]. Striking thickening of the co-lonic wall with a wide inner circle of heteroge-neous medium echogenicity surrounded by anarrow hypoechoic muscularis propria is foundin all patients, reflecting the gross submucosaledema. The lumen of the colon is almost com-pletely effaced by the mural edema, and 64–77% of the patients have ascites [61, 62]. Thepresence of these sonographic features in a pa-tient with watery diarrhea and a history of anti-biotic therapy strongly suggests the diagnosisof pseudomembranous colitis. Pseudomembra-nous colitis shows typically a strong folding orgyral pattern of the swollen submucosa.

Ischemic colitis cannot be differentiatedsolely by sonography from inflammation or anyother form of colonic wall thickening. However,duplex and color Doppler sonography may behelpful in differentiating between ischemic andinflammatory bowel wall thickening [63]. Ab-sence of or barely visible color Doppler flowand absence of arterial signal suggest ischemia.On the other hand, readily visible color Dopplerflow and a stratified echo texture suggest in-flammation. Various case reports have describedcolonic wall thickening in different forms of in-fectious and noninfectious colitis [24, 64–67].

Diverticulitis

Sonographic features of diverticulitis in-clude visualization of diverticula (Fig. 10A),thickening of the bowel wall, inflammatorychanges in the pericolic fat (typically on themesenteric side of the colonic wall) (Fig.

10B), intramural or pericolic abscess (Fig.10C), and (usually) severe local tenderness in-duced by graded compression. Diverticula areround or oval echogenic foci seen in or rightnext to the gut wall, mostly with internalacoustic shadowing. Thickening of the bowelwall is usually considered present when thedistance from the echogenic lumen interface tothe hyperechogenic serosa and pericolic fat ex-ceeds 4 mm [5]. Inflammatory changes in thepericolic fat are seen as ill-defined echogenicareas surrounding the thickened colon seg-ment. Pericolic abscesses typically present ashypoechoic masses adjacent to the inflamedbowel. The major sonographic finding in pa-tients with uncomplicated acute diverticulitisof the right colon has been found to be a hypo-echoic round or oval focus protruding from thesegmentally thickened colonic wall and repre-senting small abscesses in the pericolic fat[68]. The sensitivity of sonography in the diag-nosis of acute colonic diverticulitis ranges inthe literature from 84% to 100% [5, 69–71]. Ina recent study comparing sonography and CTin the evaluation of acute colonic diverticulitis,both techniques reached a similar sensitivity(85% and 91%, respectively) and specificity(84% and 77%, respectively) [5]. False-nega-tive results may occur if inflammatory bowelwall thickening is only mild [3]. False-positiveresults are reported in adenocarcinoma, lym-phoma, Crohn’s disease, ischemic colitis, andextracolic inflammatory conditions adjacent tothe colonic wall [69, 71]. False-positive resultsmay be reduced with Doppler sonography[63]. Potential pitfalls in diagnosing pericolicabscesses are collections smaller than 2.5 cmin diameter [5], interloop abscesses, and ab-

C

Fig. 10.—Sonographic features of diverticulitis.A, Diverticulum of sigmoid colon in 63-year-old man is seen as focal hyperechoic intramural structure with acoustic shadow.B, Massive hyperechoic inflammatory infiltration in 76-year-old woman is seen on mesenteric side of sigmoid colon. C, Echolucent fistula in 67-year-old woman is seen in mesentery with small, hyperechoic, gas-containing abscess (arrow ).

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scesses with gas inclusions [69]. CT is moreaccurate than sonography in revealing ab-scesses [5, 28, 36] and is helpful in planningpercutaneous drainage by exactly delineatingthe bowel loops [5].

Colonic Carcinoma

Abdominal sonography may be the first im-aging method that patients with colonic cancerundergo when they present with nonspecificgastrointestinal symptoms. Careful sono-graphic evaluation of the bowel may disclose afocal mass or mural thickening. Sonographicdiagnosis of colonic carcinoma has been de-scribed by several authors [72–74]. Coloniccarcinomas have two typical sonographic ap-pearances [75]. The first type is seen as a local-ized hypoechoic mass up to 10 cm or morewith an irregular shape and a lobulated con-tour. The intraluminal gas, seen as a cluster ofhigh amplitude, is usually eccentrically locatedaround the mass (Fig. 11A). The second typeshows segmental eccentric or circumferentialthickening of the colonic wall. The muralthickening may be irregular but not as severeas in the first type (Fig. 11B). The central echoclusters are small because the diseased lumenis usually narrow. This type leads frequently to

colonic obstruction. Rectum carcinomas areseen only when the bladder is well-filled (Figs.11B and 11C). Sonography enables localiza-tion of large-bowel obstruction in 85% ofpatients and diagnosis of the cause of large-bowel obstruction in 81% of patients [76].Shirahama et al. [77] described four sono-graphic patterns that allowed correct diagnosisof colonic carcinoma in 90% of patients: local-ized irregular thickening of the colonic wallwith heterogeneous low echogenicity; irregu-lar contour; lack of movement or change inconfiguration on real-time scanning; and ab-sence of a layered appearance of the colonicwall. Other findings include lymphadenopathyin most patients and abscess formation in 10%of patients. In a recent publication, malignantconditions of the colon showed the followingcharacteristics: loss of stratification, absence ofperigut findings, and involvement of a shortbowel segment with significantly greater wallthickness than is present in benign processes[62]. However, negative findings on sono-graphic examinations do not rule out the diag-nosis of colonic carcinoma because smallmasses and overlying bowel gas can lead tofalse-negative results [72, 76]. Because ofthese limitations, mainly in sensitivity, abdom-

inal sonography is not an effective screeningtechnique in the diagnosis of colonic cancer.

Intussusception

Only 5–10% of all intussusceptions occur inadults [78, 79]. The clinical symptoms may sug-gest partial obstruction of the intestine, but diag-nosis may be difficult because symptoms areoften nonspecific [79]. The ileocecal region isthe most commonly affected area in children,whereas there is no clearly preferred anatomicsite in adults. Most intussusceptions in childrenare idiopathic and are presumed to be the resultof enlarged lymphoid follicles in the terminal il-eum. An organic cause can be shown in as manyas 90% of cases in adults [78, 79]. The leadingmass is nearly always a tumor of the intestinalwall, usually malignant in intussusceptions ofthe colon [80] and benign in intussusceptions ofthe small intestine [57, 78]. The sonographichallmark of intussusception has been describedas the target [81], “doughnut,” or “bull’s-eye”sign [82]. Typically, one finds two hypoechoicrings separated by a hyperechoic ring or crescenton axial images (Fig. 12). On longitudinal im-ages, a pseudokidney structure or layering of hy-poechoic lines with hyperechoic areas isobserved. The outer hypoechoic ring is formed

C

Fig. 11.—Sonographic features of colonic carcinoma.A, Eccentric type in 52-year-old man. Transverse sonogram shows typical irregular eccentric thickening of cecumwall and loss of stratification. Note eccentrically located intraluminal air (arrow ).B, Circumferential type in 66-year-old man. Longitudinal sonogram of sigmoid colon with irregular circumferentialthickening (arrows) of short colonic wall segment.C, Polypoid rectal carcinoma in 59-year-old man. Transvesical transverse sonogram of rectum shows endoluminalround polypoid tumor measuring 3 cm in diameter (between crosses). D, CT correlation of lesion in C.

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by the intussuscipiens and the everted returninglimb of the intussusceptum, with their mucosalsurfaces face to face [83]. The center of the intus-susception varies with the scan level. At theapex, the center is hypoechoic because of the en-tering limb of the intussusceptum. At the base,the entering bowel wall forms a hypoechoic cen-ter that is surrounded by the hyperechoic mesen-tery [83]. In a case of surgically proven triplejejunojejunocolonic intussusception [84], threehypoechoic rings separated by two hyperechoicrings were found on sonography.

Conclusion

Sonography of the gastrointestinal tractshould be included in abdominal sonographyof patients presenting with abdominal pain ofunknown origin to look for potential boweldisorders. Careful analysis of the sonographicchanges of a thickened bowel segment in con-text with the clinical information often leads toa limited differential diagnosis or even to thecorrect diagnosis. If a bowel disorder is de-tected, targeted use of barium enemas, CT, en-doscopy, or biopsy can be performed ifadditional workup is needed.

More large-scale studies are needed tocompare the use of sonography with othermethods for imaging the various diseases ofthe gastrointestinal tract.

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APPENDIX 1: Differential Diagnosis of Small-Bowel Wall Thickening

Common: • Inflammatory bowel disease (Crohn’s disease and backwash ileitis)• Acute ileitis (Yersinia, Campylobacter species)• Postoperative edema• Peritoneal carcinomatosis• Mesenteric infarction (arterial, venous)• Extraintestinal inflammatory conditions adjacent to bowel wall

Less common: • Intestinal hematoma• Cytomegalovirus enteritis in AIDS patients• Intussusception• Lymphoma• Carcinoid and other malignant tumors• Benign tumors (lipoma, adenoma, and schwannoma)

Rare: • Tuberculosis• Celiac disease• Whipple’s disease• Eosinophilic enteritis• Endometriosis• Amyloidosis• Anisakiasis• Behçet’s disease• Sarcomas

APPENDIX 2: Differential Diagnosis of Colonic Wall Thickening

Common: • Diverticulitis• Carcinoma• Inflammatory bowel disease (Crohn’s disease and ulcerative colitis)• Colitis• Appendicitis• Postoperative edema• Peritoneal carcinomatosis

Less common: • Extracolic inflammatory conditions adjacent to the colonic wall • Intussusception

Rare: • Lymphoma• Amyloidosis• Endometriosis