9
AJR:201, August 2013 W283 establishing the correct diagnosis more chal- lenging for the radiologist. CT is the modality of choice and is the best radiologic tool currently available for reveal- ing both perforation and the underlying condi- tion when the diagnosis is unexpected. Unlike CT, sonography does not typically play a role in investigation of suspected small bowel per- foration or other acute abdominal conditions associated with overt peritonitis, pneumoperi- toneum, and bowel obstruction. However, so- nography may be the initial test chosen in pa- tients with localized abdominal symptoms when gastrointestinal perforation is not a ma- jor clinical consideration. This patient group typically includes referrals for acute appendi- citis, cholecystitis, pyelonephritis, colonic di- verticulitis, and pelvic inflammatory disease. Therefore, we believe that an understanding of the appearances of small bowel perforation seen during general abdominal sonography will aid the radiologist in identifying the true cause of abdominal pain when this condition presents with nonspecific symptoms. Further- more, there is a growing interest in recogniz- ing the role of sonography in imaging of the bowel [8], which, combined with the rising utilization of this noninvasive radiation-free modality in both the emergency department and outpatient settings [9], makes this area of abdominal imaging particularly pertinent to the radiologist. In a recent article [10], investigators high- lighted the potential role of sonography in the diagnosis of perforated pyloroduodenal Sonography of Small Bowel Perforation Siarhei Kuzmich 1,2 Christopher J. Burke 3 Chris J. Harvey 1 Tatsiana Kuzmich 4 Daniel T. M. Fascia 1 Kuzmich S, Burke CJ, Harvey CJ, Kuzmich T, Fas- cia DTM 1 Department of Imaging, Hammersmith Hospital, London, United Kingdom. 2 Present address: Department of Radiology, Newham University Hospital, Glen Rd, London E13 8SL, United Kingdom. Address correspondence to S. Kuzmich ([email protected]). 3 Department of Radiology, Guy’s and St. Thomas’ Hospitals, London, United Kingdom. 4 Department of Radiology, North Middlesex University Hospital, London, United Kingdom. Gastrointestinal Imaging • Clinical Perspective WEB This is a web exclusive article. AJR 2013; 201:W283–W291 0361–803X/13/2012–W283 © American Roentgen Ray Society erforation of the mesenteric small bowel, although uncommon in North America and Western Eu- rope, remains a potentially life- threatening condition associated with high morbidity and mortality and poorer outcomes when the diagnosis is delayed [1–3]. The ra- diologist is usually the first to suggest a pre- operative diagnosis because the clinical pre- sentation of small bowel perforation may be variable and is related to a multitude of fac- tors, including the source of the perforation and its mechanism, the site and extent of the perforation, time since perforation, the degree of contamination of the peritoneal cavity, and the patient’s age and comorbidity burden. Causes of small bowel perforation are man- ifold and include trauma and iatrogenic inju- ry, inflammatory conditions, infection, isch- emic change, diverticula, foreign bodies, and malignancy. Although some contribut- ing conditions such as traumatic or iatrogenic injury and Crohn disease are often anticipat- ed, other rare culprits such as an ingested for- eign body are commonly unexpected. Anoth- er unusual but important cause—perforated intestinal tuberculosis—is likely to continue to present a diagnostic challenge to the radi- ologist; this old disease is a growing concern, particularly in urban areas, because of com- bined effects of immigration, HIV infection, drug resistance, and rising poverty [4–7]. Whatever the cause, the rarity of small bow- el perforation combined with its propensity for nonspecific clinical presentation makes Keywords: CT, small bowel perforation, sonography DOI:10.2214/AJR.12.9882 Received August 28, 2012; accepted after revision October 28, 2012. P OBJECTIVE. This article aims to illustrate the spectrum of sonographic findings in per- foration of the small bowel due to a variety of causes and discusses the potential role of so- nography in the diagnosis. CONCLUSION. Although sonography is not the first-line investigation of choice in sus- pected small intestinal perforation, an understanding of the characteristic appearances seen during general abdominal sonography may aid the radiologist in the early diagnosis. Recog- nition of small bowel perforation on general abdominal sonography will shorten the time to diagnosis and ultimate surgical management. Kuzmich et al. Sonography of Small bowel Perforation Gastrointestinal Imaging Clinical Perspective Downloaded from www.ajronline.org by 180.246.46.25 on 08/17/14 from IP address 180.246.46.25. Copyright ARRS. For personal use only; all rights reserved

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Page 1: Sonography of Small Bowel Perforation 2013

AJR:201, August 2013 W283

establishing the correct diagnosis more chal-lenging for the radiologist.

CT is the modality of choice and is the best radiologic tool currently available for reveal-ing both perforation and the underlying condi-tion when the diagnosis is unexpected. Unlike CT, sonography does not typically play a role in investigation of suspected small bowel per-foration or other acute abdominal conditions associated with overt peritonitis, pneumoperi-toneum, and bowel obstruction. However, so-nography may be the initial test chosen in pa-tients with localized abdominal symptoms when gastrointestinal perforation is not a ma-jor clinical consideration. This patient group typically includes referrals for acute appendi-citis, cholecystitis, pyelonephritis, colonic di-verticulitis, and pelvic inflammatory disease. Therefore, we believe that an understanding of the appearances of small bowel perforation seen during general abdominal sonography will aid the radiologist in identifying the true cause of abdominal pain when this condition presents with nonspecific symptoms. Further-more, there is a growing interest in recogniz-ing the role of sonography in imaging of the bowel [8], which, combined with the rising utilization of this noninvasive radiation-free modality in both the emergency department and outpatient settings [9], makes this area of abdominal imaging particularly pertinent to the radiologist.

In a recent article [10], investigators high-lighted the potential role of sonography in the diagnosis of perforated pyloroduodenal

Sonography of Small Bowel Perforation

Siarhei Kuzmich1,2

Christopher J. Burke3

Chris J. Harvey1

Tatsiana Kuzmich4

Daniel T. M. Fascia1

Kuzmich S, Burke CJ, Harvey CJ, Kuzmich T, Fas-cia DTM

1Department of Imaging, Hammersmith Hospital, London, United Kingdom.

2 Present address: Department of Radiology, Newham University Hospital, Glen Rd, London E13 8SL, United Kingdom. Address correspondence to S. Kuzmich ([email protected]).

3 Department of Radiology, Guy’s and St. Thomas’ Hospitals, London, United Kingdom.

4Department of Radiology, North Middlesex University Hospital, London, United Kingdom.

Gastrointest ina l Imaging • Cl in ica l Perspect ive

WEB This is a web exclusive article.

AJR 2013; 201:W283–W291

0361–803X/13/2012–W283

© American Roentgen Ray Society

erforation of the mesenteric small bowel, although uncommon in North America and Western Eu-rope, remains a potentially life-

threatening condition associated with high morbidity and mortality and poorer outcomes when the diagnosis is delayed [1–3]. The ra-diologist is usually the first to suggest a pre-operative diagnosis because the clinical pre-sentation of small bowel perforation may be variable and is related to a multitude of fac-tors, including the source of the perforation and its mechanism, the site and extent of the perforation, time since perforation, the degree of contamination of the peritoneal cavity, and the patient’s age and comorbidity burden.

Causes of small bowel perforation are man-ifold and include trauma and iatrogenic inju-ry, inflammatory conditions, infection, isch-emic change, diverticula, foreign bodies, and malignancy. Although some contribut-ing conditions such as traumatic or iatrogenic injury and Crohn disease are often anticipat-ed, other rare culprits such as an ingested for-eign body are commonly unexpected. Anoth-er unusual but important cause—perforated intestinal tuberculosis—is likely to continue to present a diagnostic challenge to the radi-ologist; this old disease is a growing concern, particularly in urban areas, because of com-bined effects of immigration, HIV infection, drug resistance, and rising poverty [4–7]. Whatever the cause, the rarity of small bow-el perforation combined with its propensity for nonspecific clinical presentation makes

Keywords: CT, small bowel perforation, sonography

DOI:10.2214/AJR.12.9882

Received August 28, 2012; accepted after revision October 28, 2012.

P

OBJECTIVE. This article aims to illustrate the spectrum of sonographic findings in per-foration of the small bowel due to a variety of causes and discusses the potential role of so-nography in the diagnosis.

CONCLUSION. Although sonography is not the first-line investigation of choice in sus-pected small intestinal perforation, an understanding of the characteristic appearances seen during general abdominal sonography may aid the radiologist in the early diagnosis. Recog-nition of small bowel perforation on general abdominal sonography will shorten the time to diagnosis and ultimate surgical management.

Kuzmich et al.Sonography of Small bowel Perforation

Gastrointestinal ImagingClinical Perspective

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peptic ulcer. By contrast, this article stems from our wish to share our experiences in so-nographic diagnosis of common and unusual perforations of the jejunum and ileum encoun-tered during general abdominal sonography. Correlation with CT is given when possible, and examples of surgically and histologically proven cases are discussed.

Sonographic ConsiderationsTechnique and Normal Appearances

The primary general abdominal survey is followed by focused assessment of the symp-tomatic area using 2-6–MHz curvilinear and 6-12–MHz linear multifrequency transduc-ers, depending on the achievable distance to the area of interest. Any area of potential bow-el-related disease or injury is analyzed as de-scribed later in this article. Probe compression is used judiciously to facilitate visualization by bringing the area of interest into focus and displacing loops of bowel. We did not use hy-drosonography for any of the cases presented here. This technique can potentially improve bowel conspicuity and aid evaluation but may be of limited use in practice because small bowel perforation is usually encountered when it is not expected and the patient may be in pain and experiencing nausea, making admin-istration of water unwanted. Furthermore, the finding of perforation would precipitate a nil-by-mouth status as a prerequisite to a possible operative procedure.

In most patients, much of the small bow-el, from the duodenum to the terminal ileum, can be imaged with conventional sonography

without any special preparation [11]. The small intestine usually lies in a regular manner in the abdomen with the jejunum positioned higher and more to the left and the ileum lower and more to the right, although loops can alter their position. The caliber of the normal small bowel does not usually exceed 3 cm. The nor-mal wall thickness is less than 3 mm. Small bowel loops are usually mobile; are compress-ible; and show peristalsis, which may be lively or sluggish depending on the physiologic state (Fig. 1). The circular folds are more prominent in the jejunum, diminishing toward the termi-nal ileum, which may be foldless.

Like elsewhere in the gastrointestinal tract, the bowel wall can be visualized as a five-lay-ered structure under optimal scanning con-ditions, but basic identification of thin dark muscularis and more echogenic mucosa will usually suffice in practice [12].

Abnormal Small BowelWhen diseased, the bowel wall often thick-

ens and becomes rigid with reduced or absent peristalsis. Sonographic identification of the site of abnormality therefore relies on detec-tion of tangible bowel wall thickening, which varies in extent depending on the underlying condition. Similar to a pattern approach used in CT evaluation, observing the degree of wall thickening, the length of abnormal bow-el, and associated perienteric changes on so-nography can be used to narrow the differen-tial diagnosis [13].

Sonographic Signs of PerforationLike with gastrointestinal perforation from

locations other than the small bowel, pneumo-peritoneum may be present but is often mini-mal or absent outside the setting of traumatic and iatrogenic bowel injuries. Walled-off or localized perforation is common. Free sponta-neous perforation usually results in a dramatic clinical presentation with generalized peritoni-tis and thus is optimally imaged with CT.

On sonography, small amounts of free gas are seen as strongly echogenic foci or lines on the liver surface producing ring-down or comet-tail artifacts (Fig. 2A). Free air can also be detected beneath the anterior abdom-

Fig. 1—Sonographic appearance of normal small bowel in healthy 25-year-old man. Oblique color Doppler image, paraumbilical view, obtained using 10-MHz transducer depicts cross sections of mid small bowel (asterisks), captured during peristaltic wave, and mesentery with vessels (m).

AFig. 2—Sonographic appearances of free intraperitoneal gas.A, 39-year-old man with perforated ileal tuberculosis. Right intercostal view obtained with 6-MHz transducer shows bright echogenic line of free air (arrows) overlying liver (L) surface with posterior comet-tail artifact (arrowheads). Inset shows corresponding axial CT image.B, 35-year-old woman with Crohn’s disease who presented with perforated ileum. Transverse right flank view obtained with 6-MHz transducer depicts pocket of dependent free gas (arrows) with “dirty shadowing” (arrowheads) in fluid collection (asterisks) beneath abdominal wall (aw). Inset shows corresponding axial CT image.

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inal wall where it accumulates with the pa-tient supine [10] (Fig. 2B). With judicious use, careful sonography can detect a minimal amount of free gas, equating to a single bub-ble, because of its exclusive ability to pro-duce distinctive bright echoes and artifacts [14, 15]. Nevertheless, it is worth remember-ing that although sonography has a number of strengths including its unique real-time value and excellent spatial resolution, the di-agnostic quality of a sonographic study can be compromised by obesity, extensive fecal loading in the colon, bowel obstruction, and pain. Other potential weaknesses of this mo-dality may be related to the skill of the opera-tor; the equipment used; and availability of ex-pertise for this type of evaluation, which will depend on the local radiology practice model.

Sonographic findings that suggest a per-foration site typically include unusual fluid collections related to a thickened segment of bowel associated with echogenic change in adjacent perienteric fat due to inflammation. Similar to CT, the presence of extraluminal gas on sonography provides a useful clue to the diagnosis [16, 17].

Perforated DiverticulumJejunal Diverticulum

Jejunal diverticula are usually multiple ac-quired pseudodiverticula along the mesen-teric border seen in middle-aged and elderly

patients. Most patients are asymptomatic. Je-junal diverticula can be recognized on sonog-raphy as fluid-filled pouchlike structures ad-jacent to the normal bowel [18].

Diverticulitis and perforation do occur and are thought to be caused by infection, blunt trauma, and foreign-body impaction [19–21]. Localized perforation with abscess formation is common. Sonography often shows a col-lection of fluid related to a segment of mildly thickened jejunum, echogenic perienteric fat caused by inflammatory change, and pockets of extraluminal gas [22] (Fig. 3A).

Ileal DiverticulumIleal diverticulum is usually caused by a

congenital Meckel diverticulum but can also be acquired [23–25]. The “rule of twos” is frequently quoted—that is, Meckel divertic-ulum occurs in 2% of the population 2 feet from the ileocecal valve and is usually 2 inches long. However, the size and site vary. Right lower quadrant and mid abdominal loca-tions with a tendency of the diverticulum to lie toward the midline are frequently reported [26].

Uncomplicated Meckel diverticulum is usually too subtle and is rarely seen. When diverticulitis occurs, the area of abnormality may become conspicuous and is recognized owing to the presence of echogenic inflam-matory change in the fat surrounding the di-verticulum next to a mildly thickened ileal

segment. The inflamed diverticulum is visu-alized as a blind-ending thick-walled pouch or tubular fluid-filled structure surrounded by echogenic fat. This structure is usually con-stant in position and inflexible. Visualization of a communication of the structure with the ileum provides a helpful clue to the diagno-sis (Fig. 3B). Similar to our experience, sono-graphic manifestation of an inflamed Meckel diverticulum has been consistently described, both in children and adults [27–29].

When perforation occurs, sonography shows a fluid collection next to a thickened segment of small bowel and often the pres-ence of extraluminal gas in the fluid [30] (Fig. 3C). In our experience, a perforated diverticulum may or may not be evident de-pending on its size, the degree of its col-lapse resulting from perforation, and the quality of the sonographic study, which may be restricted by guarding.

Potential pitfalls may arise, most commonly from perforated appendicitis and colonic diver-ticulitis, that can result in fluid collections and extraluminal gas lying near the small bowel. A periappendiceal abscess, for instance, can mimic perforated Meckel diverticulum when it involves the ileum. Visualization of an ab-normal appendix in such cases will confirm the correct diagnosis (Fig. 4A). Care should be taken not to confuse colonic diverticulum for a pocket of extraluminal gas when it lies close

AFig. 3—Perforated versus nonperforated small bowel diverticulitis.A, 61-year-old man who presented with 5-day localized left abdominal pain and fever thought to be caused by pyelonephritis. Sonogram of left flank obtained with 6-MHz transducer shows oblique section of mildly thickened jejunum (j) and two small fluid collections (asterisks) of similar shape surrounded by echogenic fat. Small bright free gas bubbles (arrows) are difficult to see on this still image but were obvious during real-time scanning. Surgical resection revealed perforated jejunal diverticulitis and mesenteric abscess. Inset shows corresponding axial CT image.B, 32-year-old woman who presented with 3-day history of right upper quadrant pain and low-grade fever thought to be result of cholecystitis. Inset shows position of transducer (bar). Sonogram obtained with 3.5-MHz transducer depicts hypoechoic blind-ending structure (d) with thick irregular wall (arrowheads) arising from mildly thickened ileum (i). No extraluminal gas was identified. Pathology confirmed nonperforated inflamed Meckel diverticulum, which measured 3 × 2 cm.C, 72-year-old man with perforated ileal diverticulitis. Oblique pelvic view obtained using 3.5-MHz transducer shows segment of mildly thickened ileum (i) and adjacent fluid collection (asterisks) with surrounding echogenic fat. Note extraluminal gas pocket (arrows) seen as bright dependent line with “dirty shadowing” (arrowheads) in collection on left. Inset shows corresponding axial CT image.

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to the small bowel (Fig. 4B). In perforated co-lonic diverticulitis, the diverticular abscess may also lie close to the small bowel. In this case, sonography can suggest the true cause by showing involvement of the mildly thick-ened colon with evidence of diverticulosis. Although sonographic differentiation may be problematic, CT will usually help (Fig. 4C). Finally, when extensive bowel thickening, a mass, or significant lymphadenopathy is pres-

ent, other causes including perforated malig-nancy should be considered.

Crohn DiseaseBecause sonography readily displays thick-

ened small bowel, this noninvasive radiation-free modality is increasingly being chosen as both the initial test and follow-up technique in Crohn disease, particularly in the younger population [31]. Sonographic manifestations

of active Crohn disease are often characteris-tic. The hallmark of the disease is circumfer-ential encasement of a thickened bowel loop with echogenic fat, which reflects transmural inflammation and is sometimes referred to as the “creeping fat” sign [32] (Fig. 5A). The mesentery is often thickened and echogenic. A predilection of this disease for the terminal ileum is well known.

Abscess formation is common and can re-sult from transmural inflammation and a deep ulcer penetrating into perienteric tissues or may be caused by localized perforation [32, 33]. A Crohn abscess is usually walled off because of preexisting fibrotic and adhesive perienteric changes and may be mesenteric, interloop, abdominal wall, or retroperitone-al in location. Sinuses and fistulas are fre-quent. Free spontaneous perforation and in-traperitoneal rupture of a Crohn abscess also occur, although much less frequently [34]. Free perforation will typically present with overt peritonitis unless the patient is receiv-ing high-dose corticosteroid therapy.

Sonography can be the first modality to de-tect an extraluminal Crohn abscess, which is usually visualized as a fluid collection with or without free gas near the diseased bowel (Fig. 5B). Focal perforation may be seen as a track of bright echogenic gas bubbles extend-ing through the irregularly thickened bowel wall beyond its outline [32]. Detection of free intraperitoneal gas will suggest free perfora-tion (Fig. 2B).

AFig. 4—Potential mimics of perforated small bowel diverticula.A, 30-year-old woman with perforated appendicitis. Inset shows position of transducer (bar). Sonogram obtained with 2.5-MHz probe shows mildly thickened ileum (i) next to small fluid collection (asterisk) that contains pocket of dependent gas (arrowhead) with shadow. Because there is also enlarged appendix (arrow) involved in collection, small periappendiceal abscess was suggested, which was confirmed at surgery.B, 69-year-old man with colonic diverticulitis. Inset shows position of transducer (bar). Sonogram obtained using 10-MHz transducer shows jejunum (j) lying close to descending colon (c) and colonic diverticulum seen as bright shadowing pocket (arrowhead) between cross sections of jejunum and colon. This finding should not be confused with pocket of extraluminal gas seen in perforation.C, 66-year-old man with sigmoid diverticulitis complicated by pericolonic abscess. Sonogram of left iliac fossa obtained with 3.5-MHz probe depicts abscess (asterisks) lying close to bowel loop that was identified to be sigmoid colon (s) with diverticulosis on careful survey. Inset shows corresponding axial CT image.

CB

A B

Fig. 5—Nonperforated versus perforated small bowel in patients with Crohn’s disease.A, 50-year-old woman with Crohn’s disease involving distal ileum. Inset shows position of transducer (bar). Color Doppler sonogram obtained with 3.5-MHz probe shows thick-walled hyperemic ileum in cross section (i) next to bladder (ub). Note thickened echogenic mesentery (m) and layer of echogenic fat (arrowheads) encasing whole bowel circumference including antimesenteric border.B, 25-year-old woman with Crohn’s disease involving terminal ileum complicated by mesenteric abscess. Inset shows position of transducer (bar). Sonogram obtained with 3.5-MHz probe shows thickened terminal ileum (i) and adjacent abscess (asterisk).

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The major differential diagnosis of Crohn disease is tuberculosis, which should be con-sidered in a high-risk population.

Intestinal TuberculosisThe clinical manifestations of intestinal tu-

berculosis are often nonspecific. Patients may present with diarrhea, weight loss, and abdom-inal pain [35, 36]. The ileocecal region is the most common intestinal site. Ulcerative, hy-pertrophic, and combined forms are usually described [37, 38].

The most frequent finding in cases of intes-tinal tuberculosis on sonography is moderate hypoechoic thickening of the terminal ileum and cecum, which may be quite irregular de-pending on the disease stage (Fig. 6A). When

the distal ileum becomes tightly narrowed in advanced disease, dilatation of the proximal bowel will be seen. Mesenteric lymphadenop-athy is often evident, which may show central necrosis but can be nonspecific.

A CB

Fig. 6—Nonperforated versus perforated small bowel in patients with ileal tuberculosis.A, 29-year-old man with ileocecal tuberculosis. Inset shows position of transducer (bar). Sonogram obtained using 3.5-MHz probe shows thickened terminal ileum (ti) and cecum (c). Note gas pocket (arrowhead) retained within terminal ileum wall; this finding suggests presence of ulceration.B, 34-year-old man with perforated distal ileum from tuberculosis. Inset shows position of transducer (bar). Sonogram obtained using 3.5-MHz probe shows cross section of thickened terminal ileum (ti) and large pockets of dependent extraluminal gas (arrow) in adjacent fluid collection (asterisk), which is obscured by gas shadow and thus is poorly seen.C, Same patient as in B. Coronal reformatted CT image depicts cecum (c), distal ileum (i), pockets of gas (arrow), and fluid collection (asterisk). These findings were difficult to assess with sonography. Site of perforation is not evident on CT, but subsequent surgery revealed ileal perforation was 4 cm proximal to ileocecal junction.

A B

C D

Fig. 7—Peritoneal involvement in tuberculosis versus mesothelioma and carcinomatosis.A, 52-year-old man with peritoneal tuberculosis. Transverse sonogram of right flank obtained using 6-MHz transducer shows omental cake (o) adherent to mildly thickened hypoechoic parietal peritoneum (asterisk) in ascites. Corresponding axial CT image (inset) shows findings indicating close correlation between two modalities.B, Same patient as in A. Transverse sonogram of left flank (inset) shows jejunal loops (b) clumped together and small pool of ascitic fluid, which allows visualization of small adhesion (arrow), nodule (arrowhead), and minimally thickened parietal peritoneum (asterisk). Minimal peritoneal thickening is also evident on corresponding axial CT image, but adhesion and nodule are not visible.C, 62-year-old man with malignant abdominal mesothelioma. Inset shows position of transducer (bar). Sonogram of left flank obtained using 9-MHz transducer shows small bowel (b) encased by extensively thickened visceral peritoneum (asterisk) outlined with ascites. D, 59-year-old man with peritoneal carcinomatosis from colorectal carcinoma. Inset shows position of transducer (bar). Transverse sonogram of right flank shows ascites (A) and peritoneal metastatic deposits (arrows).

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Diseased bowel can perforate spontaneous-ly during and after antituberculous treatment. Perforation is frequently solitary and walled off but can also be multifocal and free, resulting in generalized peritonitis [3, 39]. Sonography may uncover the usual features of perforation such

Fig. 8—40-year-old man with abdominal pain and known polyarteritis nodosa. Inset shows position of transducer (bar). Paraumbilical view obtained using 6-MHz transducer shows concentrically thickened ileal loops (i) and small amount of ascites (asterisk). Moderate dilatation of proximal small bowel was also present (not shown).

Fig. 9—Perforations caused by foreign bodies.A, 62-year-old man with acute left abdominal colicky pain suspected of having renal colic. Sonographic view (inset) of left flank obtained using 10-MHz transducer shows linear foreign body (arrows) embedded in thickened wall of jejunum (j) and trace of fluid (asterisks), which correlates with subsequent CT. No free gas is present. Fish bone perforating jejunum was found at surgery.B, 64-year-old man suspected of having colonic diverticulitis. Sonogram of left lower flank obtained using 6-MHz transducer shows fluid collection (asterisks) next to thickened small bowel (j) and echogenic curvilinear structure piercing bowel wall with its end (arrow) in fluid collection. A few small bubbles of gas were present in collection. Correlation of these sonographic findings is shown with unenhanced axial CT image (inset). Chicken bone fragment perforating mid small bowel was revealed at surgery.C, 40-year-old man with paraumbilical pain of 5 days’ duration with fever. Paraumbilical sonogram shows echogenic linear structure (arrows) related to fluid collection (asterisks). Patient consented to CT 2 days later after his symptoms had worsened. Multiplanar reformatted CT image (inset) shows corresponding foreign body, which is now lying deeper than on sonography 2 days earlier, surrounded by larger collection. No free gas is present. Surgery revealed toothpick in perienteric collection and perforated ileum.D, 30-year-old woman who presented with 2-month history of nonspecific pelvic pain and low-grade fever. Infraumbilical sonogram reveals bright linear structure (cursors) embedded in abdominal wall at one end and projecting toward abdomen with another end (arrows). Sonogram (inset) obtained using 10-MHz transducer shows morphology suggestive of intrauterine contraceptive device (IUCD). IUCD embedded in ileum with interloop abscess was found at surgery.

as a fluid collection, pneumoperitoneum, and extraluminal gas pockets near thickened bow-el. Sonographic evaluation, however, may be complicated by pockets of extraluminal gas obscuring views and by guarding in the area of interest (Fig. 6B). CT in these cases is more likely to be diagnostic (Fig. 6C).

Other helpful sonographic findings are re-lated to peritoneal involvement, which is of-ten associated with intestinal tuberculosis. These findings are ascites, mesenteric thick-ening, omental caking, peritoneal thickening, adhesions, and peritoneal tuberculous nod-ules [40–43]. Ascites may be diffuse or locu-lated, with fluid ranging from simple to com-plex containing movable strands and strings. The mesentery is often thickened and echo-genic with mesenteric leaves clamped togeth-er. Bowel loops are frequently fixed, which is recognized by their lack of movement and lack of separation in ascites. The great-er omentum is often thickened, echogenic, and heterogeneous. Omental cakes are recognized as bulks of thickened omentum seen beneath the abdominal wall anterior to the bowel loops. Omental caking is most easily seen in

ascites (Fig. 7A). Omental cakes may be free floating or may be adherent to the abdominal wall or visceral peritoneum. Mild hypoechoic thickening of the parietal and visceral perito-neum may be evident.

The presence of ascites greatly enhances the sonographic ability to detect subtle perito-neal changes that are otherwise occult such as minimally thickened peritoneum, adhesions, and small tuberculous nodules (Fig. 7B). De-tecting these signs on sonography, which are often too subtle to be seen on CT, will provide valuable additional clues to the diagnosis.

The appearances of peritoneal tuberculosis largely overlap with those of malignant con-ditions involving the peritoneum such as me-sothelioma and carcinomatosis. Care should be taken not to confuse thickened peritoneum and nodules caused by malignant mesotheli-oma with peritoneal tuberculosis. Unlike tu-berculosis, peritoneal thickening and nodules in mesothelioma tend to be much more ex-tensive (Fig. 7C). Peritoneal implants in car-cinomatosis are much larger, are discrete, or are congregated soft-tissue nodules of vary-ing sizes, whereas tuberculous nodules are

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typically small [35, 44] (Fig. 7D). Nontuber-culous peritonitis should also be considered.

In the correct clinical context, combined sonographic and CT findings may be highly suggestive but often are nonspecific. Tubercu-losis, unfortunately, remains a great mimicker.

VasculitisVasculitis is a rare cause of perforation, but

sonography may be the initial investigation in patients with vasculitis of various causes pre-senting with abdominal symptoms. The main finding is usually diffuse small bowel thicken-ing, which is thought to be caused by a combi-nation of edema and hemorrhage in the bowel wall (Fig. 8). Sonography will also show edem-atous mesentery; bowel dilatation; ascites; and, in the case of perforation, free gas. Similar to the CT appearances of vasculitis, the sonographic appearances are nonspecific and overlap con-siderably with findings of other conditions such as infection, ischemia, radiation enteritis, an-gioedema, and hemorrhage [45–47].

Polyarteritis NodosaPolyarteritis nodosa is a fibrinoid necro-

tizing vasculitis that mainly involves small and medium-sized arteries of the muscles. When it occurs in the small bowel, the con-dition causes acute abdominal pain. Perfora-tion occurs in an estimated 5% of cases [48].

Wegener GranulomatosisWegener granulomatosis is an uncommon

multisystemic disorder characterized histopath-ologically by necrotizing granulomatous vascu-litis that can affect the small bowel, although it most commonly involves the respiratory tract and kidneys. Bowel ulcerations resulting in perfora-tions have been reported [49–51].

Henoch-Schönlein PurpuraHenoch-Schönlein purpura is frequently as-

sociated with bowel involvement, but perfora-tion is very rare [52, 53].

Foreign BodiesPerforation is uncommon because ingested

foreign bodies that have passed below the di-aphragm will usually pass in the stool. When perforation occurs, localized abdominal symp-toms usually imitate various inflammatory conditions depending on the site of the per-foration and the patient’s medical history and age [54–56]. Most patients will have no recol-lection of ingesting a foreign body. Both sharp and blunt foreign bodies can cause bowel per-foration, which is thought to result from slow pressure necrosis.

A B

Fig. 10—Nonperforated versus perforated small bowel in patients with lymphoma.A, 62-year-old woman with proven non-Hodgkin B-cell lymphoma involving mid ileum. Inset shows position of transducer (bar). Paraumbilical sonogram obtained with 5-MHz probe shows abnormal segment of ileum with concentrically thickened hypoechoic wall (w) and dilated lumen (L). This sonographic finding was unexpected in this patient who was clinically suspected of having cholelithiasis.B, 56-year-old woman with follicular lymphoma involving mid small bowel loop who presented with increasing abdominal pain and rising inflammatory markers. Coronal CT image shows large mesenteric mass (M) infiltrating and causing perforation of jejunal loop (j) with adjacent pockets of free gas (arrows) and free fluid (asterisk) extending into pelvis.

In very recent or early perforation, there may be no fluid collection or extraluminal gas, but sonography may uncover the cause of abdomi-nal pain by showing a foreign body embedded in the thickened bowel wall (Fig. 9A). How-ever, more commonly, sonography will reveal a fluid collection adjacent to a short segment of mildly thickened bowel and inflammatory change in the perienteric fat [57–60]. Extralumi-nal gas next to the bowel is a helpful finding, but free gas is not always present in our experience.

Examples of ingested foreign bodies in-clude fish and chicken bones and toothpicks, which are seen as bright linear or curvilin-ear objects of peculiar geometry piercing the bowel wall or lying in a fluid collection adja-cent to the bowel [61–63] (Figs. 9B and 9C). Ingested wire bristle from a grill cleaning brush is another example of a potential per-forating foreign body that radiologists should be aware of, as Grand and colleagues [64] re-ported in a recent study. Perforating ingested plastic bread-bag clips have also been report-ed, although rarely [65, 66].

A variety of other rare perforating foreign bodies have been reported in the literature. On the very odd occasion, even an intrauterine contraceptive device may perforate the uterus and invade the small bowel [67, 68] (Fig. 9D).

MalignancyA variety of intraabdominal malignancies,

both primary and secondary, may cause small bowel perforation. Even benign desmoid tu-

mors leading to perforation have been reported [69, 70]. Nevertheless, of all small bowel ma-lignant perforations, lymphoma is the most fre-quent cause [71].

Intestinal lymphomas may be primary le-sions or part of disseminated disease and are usually non-Hodgkin type. Typical sono-graphic findings include concentric asymmet-ric or symmetric homogeneous hypoechoic bowel thickening with loss of the layered pat-tern. Wall thickening is usually more than 2 cm. The affected segment is frequently in the ileum and may be single or multiple with nar-rowing or enlargement of the lumen. Aneu-rysmal dilatation of the lumen, although not always present, is characteristic (Fig. 10A). Single or multiple ill-defined extraluminal masses and mesenteric and retroperitoneal lymphadenopathy may be evident.

Perforation can occur spontaneously and during treatment [72, 73]. Sonography may detect both an intestinal lesion and typical signs of perforation as discussed earlier, but the role of this modality is limited and CT is invariably preferred (Fig. 10B).

Other CausesSonography is of very limited use and is typ-

ically not chosen for evaluation of traumatic and iatrogenic perforations, which are usually a major clinical consideration.

Advanced segmental or focal bowel ischem-ia of various causes such as thromboembolic occlusion of the mesenteric vessels, strangu-

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Kuzmich et al.

lated hernias, adhesive bands, volvulus, and vasculitis can result in transmural necrosis and perforation. At our institutions, sonography is not chosen when ischemic bowel is a consid-eration. Although a variety of suggestive fea-tures such as bowel thickening and dilatation, free fluid, portal vein gas, and mesenteric and portal vein thrombosis may be identified, so-nographic assessment is often disappointing when such patients are, on occasion, referred for sonography instead of CT.

Radiotherapy for cervical carcinoma and other intraabdominal malignancies may be as-sociated with late complications including bowel perforation [74]. AIDS-related infec-tions such as Mycobacterium avium–intracel-lulare and cytomegalovirus infections may involve the small bowel and may cause perfora-tion in severely immunocompromised patients [75, 76]. Long-standing use of nonsteroidal an-tiinflammatory drugs may lead to small bow-el ulceration and perforation, although this is rare. Various small bowel infections and infes-tations, particularly typhoid, can cause small bowel perforation, but these entities are excep-tionally rare in the western population [77].

ConclusionSmall bowel perforation is uncommon but

often produces subtle yet diagnostic sonograph-ic abnormalities of which the radiologist should be aware. Detection of localized extralumi-nal gas, a fluid collection, and inflammatory change adjacent to a thickened bowel segment should alert the radiologist to suspect a per-foration. A targeted CT study may be instigated when required depending on the initial sono-graphic study.

Familiarity with the characteristic sono-graphic appearances combined with a careful sonographic technique should allow a timely diagnosis during general abdominal sonogra-phy. Prompt diagnosis will facilitate correct management planning and a prompt opera-tive procedure.

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