Sonography of the pediatric gastrointestinal system.

PICTORIAL ESSAY

Sonography of the Pediatric Gastrointestinal System Bo Arys, MD, Simone Mandelstam, MD, Padma Rao, MD, Sara Kernick, and Surekha Kumbla, MD Abstract: Sonography is a commonly used modality for the investigation of abdominal symptoms in the pediatric population. It is a highly sensitive, readily available imaging modality that does not require ionizing radiation, iodinated contrast material, or anesthesia and can be performed at the bedside if necessary. Abdominal ultrasound is therefore often the first examination performed. This article presents an overview of the ultrasound characteristics of some of the most frequently encountered pathologies as well as some more rarely encountered entities. Our aim was to present a series of characteristic images of a wide gamut of pediatric abdominal conditions. The goal was to familiarize the reader with key sonographic features of both congenital and acquired gastrointestinal pathologies in children, making them more easily recognizable. Key Words: ultrasonography, pediatrics, gastrointestinal tract, digestive system abnormalities (Ultrasound Quarterly 2014;30:101Y117)

CONGENITAL PATHOLOGIC FINDINGS Infantile Hypertrophic Pyloric Stenosis Infantile hypertrophic pyloric stenosis (IHPS) is characterized by failure of relaxation of the pyloric antrum of the stomach. It is the most common surgical cause of vomiting in infants. The disease usually presents between the second and sixth week of life and most commonly affects first-born white males.1 A high-frequency linear transducer, generally in the 12-5 MHz range, should be used to visualize the pylorus with the patient in supine position. For better evaluation of gastric outlet, patients can be placed in the anterior oblique position, and if needed, fluids can be administered to provide a better acoustic window. After feeding the baby water, it can be helpful to place the patient in the right lateral decubitus position to facilitate the passage of water through the pyloric channel. The typical sonographic findings are thickening and elongation of the pyloric canal bridging the duodenal bulb and a hyperperistaltic distended stomach. The length of the hypertrophied canal is variable and has a lower limit of as little as 12 mm, although using 15 mm as pathologic limit Received for publication March 19, 2013; accepted July 2, 2013. Department of Medical Imaging, The Royal Children’s Hospital, Victoria, Australia. The authors declare no conflict of interest. Reprints: Bo Arys, MD, The Royal Children’s Hospital, 50 Flemington Road, Parkville, Victoria, 3052 Australia (e-mail: [email protected]). Copyright * 2014 by Lippincott Williams & Wilkins

Ultrasound Quarterly

& Volume 30, Number 2, June 2014

provides a higher accuracy.2 The muscle of the pyloric canal is hypertrophied with a minimal thickness of 3 mm.1,3 This thickening of the antropyloric canal can be a transient phenomenon caused by peristaltic activity or pylorospasm, but in patients without IHPS, this thickening typically does not exceed 3 mm at any given point in time.3 A double internal layer of crowded and redundant mucosa can be seen, thickened and protruding into the distended portion of the antrum (known as the ‘‘nipple sign’’) (Fig. 1). During dynamic imaging, gastric peristaltic activity fails to distend the antropyloric region at all times. This dynamic evaluation is vital because a wide open pylorus with normal passage of gastric contents excludes IHPS.1 The differential diagnosis for IHPS is pyloric foveolar hyperplasia (PFH). The normal gastric epithelium consists of gastric foveolar. These are straight or slightly tortuous pits into which the gastric glands empty. In gastric foveolar cell hyperplasia, these pits become widened, tortuous, and polypoid. These lesions usually measure up to 5 mm and are often multiple, and when they affect the pyloric inlet, they can cause gastric outlet obstruction. The exact etiology in young children remains unclear but has been linked to prostaglandin therapy, severe upper airway obstruction, or Helicobacter pylori infection.4 On its own, PFH is a rare condition, but a recent study showed that PFH is relatively common in children with IHPS and can be the cause for postoperative vomiting.5 Sonography demonstrates mucosal folds with polypoid thickening that extend into the antrum lumen causing obstruction (Fig. 2).6 In PFH, the pyloric muscle is not thickened as seen in IHPS.4 Differentiation from pylorospasm can be made with dynamic imaging because again normal passage of gastric contents is absent. Other conditions causing gastric outlet obstruction are much rarer in children. Nevertheless, a wide range of entities should be considered when imaging findings are not straightforward for IHPS including but not limited to chronic granulomatous disease, Crohn disease (CD), eosinophilic gastritis, peptic ulcer disease, neoplasms, or polyps.7

Malrotation Malrotation represents an incomplete rotation of the intestine during fetal development. There is abnormal fixation of the small bowel mesentery, which results in an abnormally short mesenteric root. This allows the small bowel to twist around its mesentery. The most common complications are obstruction or volvulus. The classic clinical presentation is a neonate with bilious vomiting. Conventionally, the diagnosis is made with an upper gastrointestinal contrast series showing www.ultrasound-quarterly.com

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FIGURE 1. Infantile hypertrophic pyloric stenosis. A and B, Sonogram of the pylorus of a 2-week-old boy with history of vomiting. Longitudinal (A) and transverse (B) images demonstrate a normal pylorus. A thin pyloric muscle is seen (slender arrow) and a thin layer of mucosa (wider arrow). The pyloric canal (C) is open with hypoechoic fluid passing through. A = gastric antrum. C, Sonogram of the pylorus of a 3-week-old boy with history of vomiting. Longitudinal sonogram of the normal pylorus demonstrates the passage of hyperechoic air through the pyloric canal. D and E, Sonogram of the pylorus of a 5-week-old boy (D) and 3-week-old boy (E), both with history of explosive vomiting. Longitudinal sonogram demonstrates signs of IHPS in both patients. The pyloric canal is closed, with crowded and redundant mucosa filling the channel and protruding into the fluid-filled antrum (A). There is lengthening of the pyloric canal and thickening of the pyloric muscle in both patients, with measurements given in patient (E). D = duodenal cap.

an abnormal position of the duodenojejunal junction, usually to the right of the midline. The most important sonographic feature is the inversion of the position of the superior mesenteric artery (SMA) and the superior mesenteric vein (SMV). The SMV is then located to the left of the artery, which is the opposite of its usual orientation. Associated features are duodenal dilatation with distal tapering, duodenal wall

thickened over 2 mm, fixed midline bowel, ascites, the whirlpool sign (when the SMV and its tributaries swirl around the SMA in clockwise direction) (Figs. 3 and 4),8 and dilatation of the distal SMV.9 The distal SMV (measured below the umbilical level) is considered dilated if its diameter is greater than that of the proximal SMV (measured above the umbilical level).

FIGURE 2. Foveolar hyperplasia. Longitudinal sonogram of the pylorus is a 5-month-old girl on prostaglandin therapy. A, Thickened gastric mucosal and submucosal folds are seen filling the entire pyloric canal (between fat arrows) causing obstruction of gastric outflow. A = Antrum. B, More magnified view of the thickened mucosa demonstrates the polypoid thickening (skinny arrows).

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Sonography of Pediatric Gastrointestinal System

FIGURE 3. Malrotation. A, Transverse color Doppler image of the mesenteric vessels in a 3-week-old boy presenting with vomiting. A normal position of the SMV is seen to the right of the SMA. C and D, Transverse gray-scale (B) and color Doppler (C and D) images of the mesenteric vessels in a 3-week-old boy presenting with bilious vomiting. On the gray-scale image, the SMV is no longer seen in its normal position to the right of the SMA but is anterior to it, even crossing over to the left. On the color Doppler images, the ‘‘whirlpool sign’’ is demonstrated with the SMV swirling around the SMA, indicative for malrotation complicated by volvulus.

Water instillation into the bowel can be a helpful trick to better evaluate the duodenal configuration and in particular to look for the beak sign of acute volvulus.

Cystic FibrosisYRelated Bowel Disease

FIGURE 4. Malrotation. A 28-day-old boy presenting with bilious vomiting. Lateral fluoroscopy image of the upper abdomen after oral administration of barium. The corkscrew sign (spiral configuration of fourth portion of the duodenum and proximal jejunum) (arrows) is present, compatible with midgut volvulus. * 2014 Lippincott Williams & Wilkins

Cystic fibrosis (CF) is mainly characterized by exocrine pancreatic insufficiency and progressive pulmonary disease. Increased viscosity of intestinal mucus is responsible for a range of intestinal obstruction syndromes including meconium ileus at birth and distal intestinal obstruction syndrome (DIOS) and constipation during childhood and adulthood. Meconium ileus is the result of intraluminal obstruction of the colon and distal small bowel due to impaction of sticky inspissated meconium and can represent the earliest clinical manifestation of CF. It occurs at birth in 13% to 17% of all CF patients.10 When meconium fails to pass into the colon, microcolon occurs. Diagnosis is usually suspected when a neonate does not pass meconium on day 1 of life and is confirmed with contrast enema (Fig. 5A). Sonography usually does not play a role in diagnosis in the neonate, although increased echogenicity of the bowel on prenatal sonography can be suggestive of the diagnosis.11 In DIOS, occurring in approximately 15% of CF patients, affected children present with recurrent abdominal pain, rightlower-quadrant mass, and varying severity of bowel obstruction.12 Ultrasound imaging shows dilated, fluid-filled intestinal bowel loops containing echogenic material (calcified www.ultrasound-quarterly.com


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FIGURE 5. Meconium ileusVDIOS. A, A 1-day-old boy with CF and meconium ileus, not passing meconium in the first 24 hours of life. Fluoroscopy image during contrast enema shows a colon filled with long segments of thick, inspissated meconium. B and C, A 5-month-old boy with CF presenting with signs of obstruction. Sonography of the abdomen (B) demonstrates multiple dilated small bowel loops filled with echogenic material (arrows) representing impacted fecal matter. Fluoroscopy image (C) of the contrast enema performed in the same patient. Contrast has refluxed into the terminal ileum, which contains plugs of impacted fecal matter (arrows). These plugs correspond to the echogenic intraluminal content on ultrasound. E and F, A 4-year-old girl with CF presenting with signs of obstruction suspected to have DIOS. Abdominal x-ray (D) demonstrates multiple dilated small bowel loops. Abdominal ultrasound demonstrates multiple fluid-filled small bowel loops containing echogenic material. Some free fluid is also seen. Subsequent contrast enema (F) proved that there was no colonic cause for the obstruction in this patient.

meconium or impacted fecal matter) in the terminal ileum and cecum (Fig. 5). Meconium peritonitis is a chemical peritonitis resulting from intrauterine bowel perforation. The extruded bowel contents provoke an intense peritoneal inflammatory reaction leading to the formation of dense fibrotic tissue that often calcifies. On ultrasound, meconium peritonitis is typically either generalized or cystic (Fig. 6).13

Meckel Diverticulum When evaluating the bowel wall with sonography, a typical stratification pattern can be seen, called the ‘‘gut

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signature.’’ This consists of 3 distinct layers. The layer next to the lumen is hypoechoic and represents a combination of mucosa, lamina propria, and muscularis mucosae. The middle layer is the most echogenic layer and corresponds to the submucosa. The third, most outer layer is again hypoechoic and corresponds to the muscularis propria. The total thickness of the wall of normal small bowel in children is 1.5 mm or less and of normal colon 2 mm or less.14 Meckel diverticulum is the most common congenital anomaly of the gastrointestinal tract, occurring in 2% to 3% of the population. It is the result of incomplete atrophy of the omphalomesenteric duct and occurs along the antimesenteric border of the distal ileum. * 2014 Lippincott Williams & Wilkins





FIGURE 6. Meconium peritonitis. A and B, A 1-day-old boy with prenatal diagnosis of meconium peritonitis. Color Doppler image (A) and abdominal x-ray (B) show heavily calcified cysts (arrows) with twinkling artifact demonstrated on ultrasound. The twinkling artifact is caused by the reflections from the surfaces of the calcifications. C and D, Sonogram (C) of the left upper quadrant in a 2-month-old girl with CF who had an intrauterine diagnosis of meconium peritonitis. A large meconium cyst with calcified rim (arrows) can be identified adjacent to the spleen. The cyst (arrows) has decreased in size compared with the barium study (D) performed on the second day of life.

It is a true diverticulum consisting of all 3 layers of the bowel wall and is usually found within 100 cm of the ileocecal valve.15 On sonography, the Meckel diverticulum may present as a cystlike or cul-de-sac shaped mass

with ‘‘gut signature sign’’ (Fig. 7A). Symptoms usually arise from complications such as hemorrhage, diverticulitis, or small bowel obstruction. Because they often contain heterotopic gastric or pancreatic mucosa, diagnosis can be

FIGURE 7. Meckel diverticulum. A 9-month-old girl presenting with fever and tender abdomen. A, Transverse sonogram demonstrates a thick-walled, cystic-appearing structure between a small bowel loop (SB) and the bladder (Bl). An external hypoechoic rim representing muscularis (arrows) and 2 hyperechoic layers of mucosa and submucosa (arrowhead) can be distinguished. B, Technetium Tc 99m pertechnetate scintigraphy shows a small focus of uptake in the right flank (arrow) compatible with the presence of heterotopic gastric mucosa in the Meckel diverticulum. * 2014 Lippincott Williams & Wilkins



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FIGURE 8. Enteric duplication cyst. A 3-month-old girl with palpable mass in the left flank. A, Transverse sonogram demonstrates an enteric duplication cyst in the left flank. The inner hyperechoic rim of mucosa-submucosa (white arrow) and outer hypoechoic rim representing the muscularis (black arrow) can be identified. B, Longitudinal sonogram of the same lesion. The close relation to the small bowel (SB) can be seen.

confirmed with technetium Tc 99m pertechnetate scintigraphy (Fig. 7B).14

Cystic Lesions Duplication Cysts Duplication cysts are rare congenital anomalies that can occur anywhere along the alimentary tract. In the bowel,

they can be found along the mesenteric border and most frequently involve the jejunum or ileum. In more than 70% of cases, clinical onset occurs before the patient is 2 years of age.16 Neonatal bowel obstruction, intussusception, palpable mass, acute abdominal pain, and hemorrhage are common presentations. On ultrasound, they typically have a spherical, ovoid, or dumbbell shape. They share a common muscular wall and blood supply with the bowel, but unlike the

FIGURE 9. Mesenteric cyst and mesenteric pseudocyst. A and B, A 2-week-old girl with palpable abdominal mass. Transverse sonogram of the right flank (A) demonstrates a large simple cyst. High-resolution sonogram of the same lesion (B) depicts a simple thin wall. The gut signature sign as seen in enteric duplication cysts is absent. C and D, A 4-year-old boy complaining of right iliac fossa pain. On sonography (C), a thick-walled cystic structure (arrows) is seen with intracystic fluid and echogenic material. Pathology proved the echogenic material to represent degenerate blood products and necrotic debris with the wall composed of densely hyalinized tissue without signs of epithelial lining. Transverse CT image of the pelvis after oral and intravenous contrast (D) shows the same pathologically proven nonpancreatic pseudocyst.

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Meckel diverticulum, they have a separate mucosal lining.16 On sonography, the wall of the cyst demonstrates an inner hyperechoic rim correlating to the mucosa-submucosa and an outer hypoechoic layer of muscularis propria (Fig. 8).17

Mesenteric Cysts A mesenteric cyst, also known as mesenteric lymphatic malformation, arises from the small or large bowel mesentery. It develops from a proliferation of lymphatic tissue that fails to communicate with the central lymphatic system. On ultrasound, they present as unilocular or multilocular, sharply defined cystic lesions with simple anechoic contents and possible internal septations. Variable attenuation of the internal echogenicity can be seen, depending on the composition of the internal fluid, which is predominantly chylous but can be serous or hemorrhagic (Fig. 9).17,18 The mesenteric pseudocyst is an acquired cyst of the mesentery that is nonpancreatic in origin. It is unrelated to pancreatitis, as opposed to the pancreatic pseudocyst. They represent sequelae from a mesenteric or omental hematoma


or abscess that did not completely resorb.18 On sonography, they frequently demonstrate intracystic echogenic debris and are often thick walled.19

ACQUIRED PATHOLOGIC FINDINGS Intussusception An intussusception is a process where a segment of bowel invaginates into itself. The intussuscipiens or ‘‘receiving loop’’ contains the infolded intussusceptum or ‘‘donor loop.’’ This intussusceptum has a central entering limb of bowel and a returning limb more peripherally, and the attached mesentery is dragged between the 2 limbs. The majority is of the ileocolic type and is typically located in the subhepatic region (Fig. 10A).20 The condition typically occurs in children between 6 months and 2 years of age with a classic clinical triad of acute colicky abdominal pain, ‘‘currant jelly’’ or bloody stools, and a palpable abdominal mass or vomiting.

FIGURE 10. Intussusception. Ultrasound imaging of 6 different patients presenting with a history of colicky abdominal pain and red stools. A, Transverse sonogram of the right upper quadrant demonstrates the typical subhepatic location of an ileocolic intussusception (Li = liver, Co = colon, Sb = small bowel, Ln = lymph node). Some enlarged lymph nodes act as likely lead point for the intussusception. B, Longitudinal sonogram shows the different layers of an intussusceptum, with the colon (Co) being the intussuscipiens and the small bowel (Sb) the intussusceptum. The mesentery (Me) is dragged along with the small bowel. Some fluid is seen within the colon lumen. C. Longitudinal sonogram of an intussusceptum showing the ‘‘pseudokidney sign.’’ Co = colon, Sb = small bowel. D, Transverse sonogram demonstrates the different components of the intussusception. Color Doppler demonstrates good flow in the intussuscipiens (colon, Co) but near absent flow in the intussusceptum (small bowel, Sb). Some fluid (F) is also seen trapped between the rings of the intussusception. Me = mesentery. E. Transverse sonogram of an intussusceptum showing a Meckel diverticulum (between arrows) as lead point. Co = colon, Sb = small bowel F, Small bowelYsmall bowel intussusception with concentric rings on transverse sonography in the left flank. Central hyperechoic mesentery is seen (Me). Intra-abdominal free fluid is also noted. * 2014 Lippincott Williams & Wilkins



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FIGURE 11. Appendicitis. A, A 13-year-old boy with right iliac fossa pain. Transverse sonography demonstrates the target sign with the inflamed appendix seen as a hypoechoic center, an inner hyperechoic ring, and an outer hypoechoic ring, measuring 10 mm. Two inflamed lymph nodes (LN) are seen in the adjacent mesentery. B, A 12-year-old girl with right iliac fossa pain. Longitudinal sonogram of the inflamed appendix demonstrates a noncompressible blind-ending tubular structure measuring 9.6 mm in thickness. Hyperechoic surrounding mesentery (arrowheads) is seen. C, Longitudinal color Doppler sonogram of the appendix in a 13-year-old boy with mild right iliac fossa complaints. Hyperemia in the muscular layer of the bowel wall is consistent with early-stage acute appendicitis. D, Transverse sonogram of the appendix in a 2-year-old boy with right iliac fossa pain and fever. An appendicolith is seen as a hyperechoic structure with acoustic shadow (fat arrow) inside the inflamed appendix. A hypoechoic collection (skinny arrow) surrounds the appendix, indicative of perforation. Note the inflamed hyperechoic surrounding mesentery (arrowhead).

Although childhood cases of intussusception are usual idiopathic, a lead point, such as polyps, Henoch-Scho¨nlein purpura (HSP), Meckel diverticulum, duplication cyst, or tumor, can sometimes be seen (Fig. 10E), especially in children outside the common age group.

Ultrasound has a high sensitivity (near 100%) for the diagnosis of intussusception. In the longitudinal plain, a loopwithin-loop structure can be seen consisting of 3 parallel hypoechoic bands separated by 2 hyperechoic bands. The outer bands represent the everted limb of the intussusceptum

FIGURE 12. Epiploic appendagitis. A 13-year-old boy with left iliac fossa pain. A and B, Sonographic images of the left iliac fossa. A hyperechoic noncompressible mass can be seen close to the sigmoid colon (Si) at the point of maximum tenderness, delineated by a hypoechoic band (arrowheads). Further scanning demonstrates the actual appendage (between arrows) within the inflamed omentum. C, Axial contrast-enhanced CT image of the same patient shows a fat-containing lesion (between arrows) that abuts the sigmoid (Si), consistent with an epiploic appendage. A central focal area of hyper attenuation is seen representing a small vessel. Surrounding mesenterial inflammation is present (between arrowheads).

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FIGURE 13. Crohn disease. Ultrasound images of the terminal ileum in 5 different patients with CD. A, Longitudinal sonogram of an acutely inflamed terminal ileum. The submucosa is thickened and hyperechoic. Power Doppler demonstrates hyperemia in the bowel wall. B, Longitudinal sonogram demonstrates a thickened and hypoechoic segment of bowel wall with loss of the normal bowel wall stratification. The adjacent mesentery is hyperechoic because of transmural inflammation. C, Color Doppler sonogram in a different patient shows lack of hyperemia of the thickened bowel wall, consistent with chronic, fibrotic stage of disease. D, Composed gray-scale sonogram shows different stages of bowel inflammation and destruction of normal bowel architecture. E, A focal stricture (arrow) can be seen in the bowel with prestenotic dilatation of an atonic and fluid-filled bowel loop.

FIGURE 14. Typhlitis. A 10-year-old neutropenic girl with right iliac fossa and flank pain. A and B, Gray-scale sonography (A) of the cecum demonstrates asymmetric, echogenic thickening of the mucosal wall (arrows). Color Doppler imaging of the same segment shows the segment to be diffusely hyperemic. C, Composed gray-scale sonogram of the same patient demonstrates that the acute inflammatory changes involve a long right colonic segment (arrows). Li = liver, Bl = bladder. * 2014 Lippincott Williams & Wilkins



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FIGURE 15. Graft-versus-host disease. A 10-year-old boy with known graft-versus-host disease after bone marrow transplantation. Longitudinal ultrasound (A) of the bowel demonstrates an atonic colon is seen with thickened wall and loss of haustration pattern. The normal stratification pattern of muscularis propria (arrowhead), mucosa (curved arrow), and submucosa (wider arrow) can still be identified. In addition, an echogenic layer is detected between the bowel wall and the bowel lumen, likely sloughed membrane (slender arrows). Transverse gray-scale (B) and correlated color Doppler (C) images of an affected segment of bowel demonstrate diffuse hyperemia.

and the intussuscipiens; the central hypoechoic band is the central limb of the intussusceptum. This appearance is also known as the sandwich sign. If the intussusception is curved or imaged obliquely with the mesentery only demonstrated on 1 side of the central limb, the ‘‘pseudokidney sign’’ occurs (Fig. 10C).21,22 Transverse imaging shows alternating concentric hypoechoic and echogenic layers of bowel referred to as the ‘‘target sign’’ or ‘‘donut sign.’’ Fluid trapped between the layers of the intussusception on ultrasound (Fig. 10D) and absence of color flow within the intussusception have been shown to correlate with a greater likelihood of failure at enema reduction and bowel ischemia. The finding of lymph nodes within the intussusception

(Fig. 10A) or the presence of a small amount of peritoneal free fluid does not change reduction rates.20

Inflammatory Appendicitis Appendicitis is the result of the obstruction of the appendiceal lumen. It occurs in all age groups with a higher incidence between 5 and 15 years. The classic presentation is periumbilical pain that migrates to the right lower quadrant at McBurney point over a period of 12 to 24 hours, with associated anorexia, leukocytosis, and often low-grade fever.20 On longitudinal ultrasound images, the inflamed appendix is seen as a blind-ending noncompressible tubular

FIGURE 16. Vasculitis. A and B, Ultrasound in an 8-year-old girl with known HSP. A thickened, edematous bowel wall can be identified on transverse sonography (A). Color Doppler imaging (B) in the same patient demonstrates hyperemia in the edematous bowel wall. C, A 2-year-old boy with known HSP vasculitis of the bowel. A small bowel intussusception (black arrow) is seen besides obstructed, fluid-filled bowel loops (white arrow) and free fluid (FF).

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FIGURE 17. Necrotizing enterocolitis. A, Longitudinal sonogram of the bowel in a 6-week-old boy suspected to have NEC. A small focus of intramural air can be identified in the bowel wall (arrow). Associated finding of ascites. B-D, A 2-month-old girl with NEC. Abdominal x-ray demonstrates multiple dilated bowel loops. Several bowel segments (arrows) demonstrate intramural air, better seen on the magnified view (C). In segments where intramural gas is present in the entire bowel circumference, a continuous echogenic ring (arrows) can be seen on ultrasound (D), called the ‘‘ring sign.’’ E and F, A 4-week-old boy with NEC. Ultrasound of the abdomen (E) demonstrates the presence of hyperechoic portovenous gas in the left liver lobe (arrows). Abdominal x-ray (F) shows the corresponding branching pattern of gas in the region of the left liver lobe (black arrowheads).

structure that is aperistaltic. An outer wall diameter greater than 6 mm under compression is generally accepted, although a recent study has proposed a new criterion of 7-mm maximal outer diameter or wall thickness of more than 1.7 mm (Fig. 11B).23 In the transverse plane, the target sign is seen with a hypoechoic centre, an inner hyperechoic ring, and an external thicker hypoechoic ring (Fig. 11A). Inflamed surrounding mesentery and periappendiceal fat may be seen as a hyperechoic halo sign surrounding the appendix. When ultrasound findings are ambiguous, color Doppler examination can be helpful in the diagnosis of early acute appendicitis, demonstrating hyperemia or increased flow in the hypoechoic muscular layer of the bowel wall (Fig. 11C). * 2014 Lippincott Williams & Wilkins

Increased flow in the mucosal layer, on the other hand, most likely represents enteritis. An appendicolith (Fig. 11D) can be seen in an inflamed appendix, but its presence alone is not a diagnostic criterion for appendicitis in the absence of appendiceal or periappendiceal inflammation.24 Perforation and abscess formation are the major complications of appendicitis.20,22

Epiploic Appendagitis Epiploic appendages arise from the serosal surface of the colon. Torsion of the appendages, resulting in venous occlusion and ischemia, is the cause of epiploic appendagitis.25 It is www.ultrasound-quarterly.com


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FIGURE 18. Burkitt lymphoma. A 10-year-old boy presenting with lower abdominal pain. A and B, Transverse color Doppler sonogram (A) and sagittal gray-scale sonogram (B) of the pelvis show a bowel segment with diffuse hypoechoic bowel wall thickening (arrows), surrounding an echogenic lumen (L) filled with fecal material and air bubbles. Bl = bladder, R = rectum. C and D, Axial (C) and coronal (D) CT scans after intravenous and oral contrast administration show the CT correlation for the bowel segment with diffuse wall thickening (arrows). The bowel lumen (L) is filled with oral contrast material. The rectum (R) is seen posterior to the affected segment. Bl = bladder.

predominantly encountered in adults, and diagnosis is most often made on computed tomography (CT), with only limited case reports described in children. Nonetheless, it should be

kept in mind when scanning a patient with symptoms resembling appendicitis because the treatment is conservative rather than surgical. Typical ultrasound findings are a hyperechoic,

FIGURE 19. Inflammatory myofibroblastic tumor. A 13-year-old boy with clinical signs of gastric outlet obstruction. A, Longitudinal sonogram of the pylorus region shows irregular wall thickening of the gastric antrum, pylorus, and proximal duodenum (between arrows). B, Axial CT after intravenous and oral contrast administration confirms the presence of irregular wall thickening at the site of the gastric outlet causing luminal narrowing. Findings are completely nonspecific. Pathology proved this nonspecific mass lesion to be an inflammatory myofibroblastic tumor.

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FIGURE 20. Polyps. A 10-year-old boy with known Peutz-Jeghers syndrome presenting with abdominal pain. A and B, Ultrasound imaging in this patient found a small bowelYsmall bowel intussusception as cause for the pain (not clearly shown). A polyp as lead point is seen (between arrows in image A, between calipers in image B). C, A barium follow-through study shows the presence of multiple endoluminal filling defects in the small bowel compatible with multiple small polyps (arrows).

noncompressible oval mass circumscribed by a hypoechoic line (Fig. 12). This mass generally stays fixed to the abdominal wall during breathing.26

Inflammatory Bowel Disease Crohn disease is an inflammatory bowel disease of unknown etiology that can affect any part of the gastrointestinal

tract. In 20% of cases, the disease first presents itself during childhood. It should therefore be kept in mind when examining a child with nonspecific abdominal symptoms. The normal thickness of the bowel wall has been described in several studies varying between 1.5 and 3.0 mm in the terminal ileum.27Y29 In early CD, the hyperechoic submucosa becomes thickened due to lymphedema. On ultrasound, the inflamed bowel appears

FIGURE 21. Duodenal hematoma. A 6-year-old girl with upper abdominal pain after trauma. A and B, Transverse (A) and longitudinal (B) sonograms demonstrate an atonic duodenal segment with the presence of a heterogeneous mass filling the complete lumen (between arrows). Small amount of intraluminal air is still seen (arrowhead). C, Coronal CT image after intravenous and oral contrast administration of the right upper quadrant shows a predominantly high-attenuation, unenhancing, hematoma occupying the lumen of the duodenum (between arrows) GB = gallbladder; DU = duodenum, contrast filled; PA = pancreas. * 2014 Lippincott Williams & Wilkins



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thick walled (Fig. 13A),30 is often noncompressible, and has reduced or absent peristalsis. Color Doppler can be helpful in demonstrating hyperemia (Fig. 13A). If transmural inflammation is present, it may cause fibrosis and edema in the adjacent mesentery that appears thickened and hyperechoic (Fig. 13B). Transmural deep ulcers can be seen as hyperechoic tracts perpendicular to the bowel wall or as hyperechoic gas within the bowel wall. Strictures are seen as rigid, thick-walled, bowel loops that are aperistaltic with dilatation of the bowel segment proximal to the stricture, also known as ‘‘upstream dilatation’’ (Fig. 13E). Fistulae can appear as hypoechoic tracts with gas inclusions connecting adjacent bowel loops. Chronic disease resulting in fibrosis leads to thickening of the bowel wall, which is hypoechoic, with the normal layers of the bowel wall becoming indistinct (loss of stratification) (Fig. 13B).27

Typhlitis Typhlitis, also known as neutropenic enterocolitis, is a necrotizing inflammatory disease of the ileocecal region and is a complication of severe neutropenia. The characteristic sonographic features are hypoechoic, asymmetric, and thickening of the mucosal wall with transmural inflammatory reaction (Fig. 14). Different patterns of echogenicity can be seen caused by edema, necrosis, or circumscript hemorrhages. Intramural air can be seen suggesting an infection with


anaerobic bacteria.31 Sonography is also helpful to look for complications of enterocolitis such as abscess formation. Color Doppler can be used to demonstrate hyperemia.

Graft Versus Host In acute graft-versus-host disease, donor lymphoid cells damage host tissues. Skin, liver, and gastrointestinal tract are target organs. Ultrasound can demonstrate marked bowel wall thickening involving both small bowel and colon, luminal narrowing, or haustral fold enlargement or loss. An additional double-lined echo can be seen next to the small bowel lumen (Fig. 15) when there is severe mucosal surface ulceration with coating of the mucosal surface by sloughed membranes.32

Vasculitis The most common pediatric vasculitis is HSP, with typically bowel wall thickening and edema on ultrasound (Figs. 16A, B). The vasculitis causes thrombosis of small blood vessels, which in turn can cause ischemia of the small bowel. Color Doppler is useful to differentiate inflammation, with readily visible color Doppler flow and arterial flow signal, from ischemia, where these findings are absent or barely visible.33 In patients with obstructive symptoms, 1 or more intussusceptions can be demonstrated, typically involving the small bowel (Fig. 16C).34

FIGURE 22. Bezoar. A 4-year-old girl with a habit of eating hair. A and B, Sonographic evaluation of the stomach shows an intraluminal mass distinct from the stomach wall with hyperechoic curved or ‘‘arclike’’ surface (arrows) casting a clear posterior acoustic shadow. C, Anteroposterior x-ray of the abdomen in the same patient shows the bezoar (arrows) in the stomach surrounded by gas.

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FIGURE 23. Focal omental infarct. A 5-year-old boy with right iliac fossa pain. A, Transverse gray-scale sonogram (A) demonstrates a triangular mass-like structure in the mesentery (between arrows). B, Color Doppler evaluation of the lesion demonstrates the avascular nature, compatible with a focal omental infarct.

Other vasculitides involving the bowel can occur, with a very variable presentation depending on which vessels are involved and whether the involvement is focal or diffuse. Presentation is mostly nonspecific as paralytic ileus, mesenteric ischemia, submucosal edema and hemorrhage, and bowel perforation or stricture.35

Infectious Necrotizing Enterocolitis Necrotizing enterocolitis (NEC) is believed to be the result of several factors leading to mucosal damage of the bowel in premature neonates, which leads in turn to intestinal ischemia and necrosis. Sonographic evaluation of the bowel wall can show an entire spectrum of appearances from nonspecific thickening and inflammation to thinning of the bowel wall in severe NEC implying ischemia. In severely affected cases, there may be a loss of peristaltic activity. The presence of intramural gas is considered a virtually pathognomonic sign of NEC (Fig. 17). If the bubbles of gas produce the appearance of a continuous echogenic ring, the term ‘‘circle sign’’ has been used (Fig. 17D).36 Other signs may include the presence of portovenous gas, free intraperitoneal gas, and abdominal free fluid. Doppler imaging can differentiate between hyperemic bowel loops that are still viable and absence of flow in necrotic loops.37

Neoplastic In a pediatric population, tumors of the gastrointestinal tract are rare, with benign neoplasms more common than malignant tumors. A wide range of benign neoplasms can be encountered including polyps, hemangiomas, neurofibromas, leiomyomas, gastrointestinal stromal tumors, and lipomas. Of the malignant lesions, lymphoma is the most commonly encountered, with other malignancies being much less frequent.38

Solid Malignancies Both Hodgkin disease and non-Hodgkin lymphoma can affect the bowel, with small bowel more frequently involved * 2014 Lippincott Williams & Wilkins

than colon. Of the non-Hodgkin lymphomas, Burkitt lymphoma is the most frequently encountered subtype in children, often boys between the ages of 5 and 10 years.39 It commonly involves the terminal ileum, and the presenting symptoms can easily be confused with those of appendicitis. On ultrasound, diffuse hypoechoic bowel wall thickening is seen, either due to lymphedema or tumor infiltration, with a central echogenic region caused by intraluminal air, bowel mucosa, or inspissated mucus (Fig. 18).39 Intussusception with the tumor as lead point is often the cause of obstruction in these patients. Burkitt lymphoma should therefore always be considered as a potential diagnosis in an older child presenting with intussusception. Bowel perforation, cavitation, or abscess formation can occur but are uncommon.40

Pseudotumor Inflammatory myofibroblastic tumor is a neoplasm characterized by spindle cell proliferation associated with an inflammatory infiltrate. It is overall accepted as being a benign entity that often behaves in an indolent manner but mimics malignancy. Recurrences and metastases have been reported, possibly leading to a reclassification of the tumor to uncertain malignant potential in the future.41 They can occur at any age or at any site, but because they have a predilection for the visceral soft tissues of children and adolescents, they should be kept in mind when encountering a nonspecific mass lesion (Fig. 19).42 Differential diagnosis with malignancy cannot be made on ultrasound, only on histology.

Polyps The most common type of polyp in the pediatric population is the isolated juvenile polyp that frequently occurs in the rectosigmoid colon. Peutz-Jeghers syndrome is much less common and presents with multiple hamartomatous polyps predominantly in the small bowel. These patients www.ultrasound-quarterly.com


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frequently present with an intussusception from a polyp lead point (Fig. 20).38

Miscellaneous Duodenal Hematoma Hematoma of the bowel can be either posttraumatic or spontaneous. Clinical presentation of patients with spontaneous intramural small bowel hematoma can vary from mild and vague abdominal pain to intestinal tract obstruction and acute abdomen. Although this diagnosis is most frequently made on CT, ultrasound combined with suggestive clinical information can demonstrate the presence of a bowel hematoma. Findings on ultrasound are generally a heterogeneous mass arising from the bowel wall (Fig. 21).43 Because the presence of a bowel-related mass is a nonspecific finding on ultrasound, reexamination of the patient within a few days may be helpful.44 The echogenicity of a hematoma varies rapidly over time, with hypoechoic appearance of acute blood and more hyperechoic clot formation and retraction evolving over the next days. This makes differentiating hematoma from neoplasm much more evident.

Gastric Bezoar A bezoar is composed of ingested foreign materials that accumulate within the gastrointestinal tract. Trichobezoars (composed of hair) and phytobezoars (composed of fruit and vegetable fibers) are the most common. On ultrasound, a bezoar is identified as an intraluminal mass with hyperechoic arclike (curved or ‘‘inverted U’’) surface and marked acoustic shadowing (Fig. 22). On color Doppler, the twinkling artifact, described behind highly reflecting structures and predominantly used for evaluation of kidney stones, can be seen as a rapidly changing mixture of red and blue.45 Associated signs of bowel obstruction may be noted.46

Focal Omental Infarct Omental infarction is a rare cause of acute abdominal pain in the pediatric population. The clinical picture is often similar to that of appendicitis because it is often right sided.47 Awareness of this entity is therefore crucial when performing sonography. On ultrasound, identification of a hyperechoic noncompressible mass just underneath the abdominal wall without evidence of vascularization can be seen (Fig. 23). The lesion is usually triangular and involves the inferior aspect of the right side of the omentum.48 The finding of a normal appendix can be helpful.

CONCLUSIONS Because high-resolution ultrasound is often the first imaging modality used for evaluation of the gastrointestinal tract in children, recognizing the key sonographic features of the different entities that can be encountered is crucial. This knowledge can help avoid further imaging with ionizing radiation and, when needed, aid toward choosing the correct additional imaging modality.

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Endoscopic sonography of the upper gastrointestinal tract.

Pediatric gynecologic sonography.

Sonography of the musculoskeletal system.

[Sonography of congenital abnormalities of the gastrointestinal tract].

Sonography of complications in pediatric renal allografts.

Abdominal ultrasonography of the pediatric gastrointestinal tract.

Modeling the gastrointestinal system.

The liver in pediatric gastrointestinal disease.

Evaluation of acute appendicitis by pediatric emergency physician sonography.

Pediatric gastrointestinal basidiobolomycosis mimicking malignancy.

The gastrointestinal system: a piece of cake.

The role of endoscopy in pediatric gastrointestinal bleeding.

Interpretability of the PedsQL™ Gastrointestinal Symptoms Scales and Gastrointestinal Worry Scales in Pediatric Patients With Functional and Organic Gastrointestinal Diseases.

Psychotropic medications for pediatric functional gastrointestinal disorders.

Psychotropic medications for pediatric functional gastrointestinal disorders.

Magnetic gastrointestinal anastomosis in pediatric patients.

Pediatric gastrointestinal PEComas: a diagnostic challenge.

Foreword: Immune dysregulation and pediatric gastrointestinal disorders.

Gastrointestinal tract filling defects in pediatric patients.

Sports injury of the pediatric musculoskeletal system.

Sonographic evaluation of hydronephrosis in the pediatric population: is well-tempered sonography necessary?

Sonography of the ankle.

Sonography of the eye.

Central nervous system regulation of gastrointestinal motility.