Applied Radiology

Sonographers are generally reluctant to examine the esophagus, stomach, and intestinal tract because of the presumed technical challenges. However, it has been found that sonography often is useful in evaluating gastrointestinal wall disorders in the pediatric population. This pictorial essay demonstrates the sonographic appearance of selected pediatric gastrointestinal disorders. These entities are presented in order of anatomic position, from cranial to caudal. The advantages and limitations of sonography, as compared to contrast studies, will be discussed, as well as examination techniques and common pitfalls.

Hiatal hernia

Sonography may be more sensitive than a contrast study for detecting small hiatal hernias.1 The preferred method for scanning is to place the transducer in the subxiphoid area in order to scan the distal esophagus and the gastroesophageal junction in longitudinal and transverse planes (figure 1). Demonstration of the stomach often can be improved after the oral ingestion of water, as it will provide a sonolucent window. Sonography also may be used to detect gastroesophageal reflux, though this examination can be quite labor intensive.2 Reflux occurs when there is retrograde flow of fluid or gas from the stomach into the distal esophagus. If fluid refluxes forcefully from the stomach into the distal esophagus, the sonographic appearance of this fluid may be seen as ranging from anechoic to mildly echogenic or "cloudy", due to the turbulent flow.

Gastric wall thickening

There is a broad differential diagnosis for gastric wall thickening. It includes (but is not limited to) lymphoma, carcinoma, hypertrophic gastritis, Crohn's disease, peptic ulcer disease, prosta- glandin-induced antral foveolar hyperplasia, and chronic granulomatous disease of childhood. Additionally, diffuse gastric rugal hypertrophy is a hallmark of Menetriers' disease (figure 2), though this appearance is nonspecific.

During the sonographic exam, it is helpful to use the left lobe of the liver as an acoustic window, although the ante-rior abdominal wall can serve this purpose as well. Left coronal imaging is useful in studying the gastric fundus as it is juxtaposed with the splenic hilum. Examining the fundus with the patient in the left lateral decubitus position also can be helpful, as this will cause intraluminal gas to shift towards the gastric antrum.

Normal gastric wall thickness generally ranges between 2.5 and 3.5 mm.3,4 However, one must be aware that apparent thickening of the gastric wall may be seen when the stomach is collapsed. Furthermore, retained intraluminal debris may be present and should not be mistaken for a focal lesion.

Hypertrophic pyloric stenosis/gastric outlet obstruction

Sonography is the procedure of choice for the diagnosis of hypertrophic pyloric stenosis. It is preferred over an upper gastrointestinal examination because the abnormal pyloric muscle mass that is the hallmark of this condition is able to be directly visualized. In this disorder, thickening of the antropyloric muscle and elongation of the antropyloric canal are the two most important diagnostic criteria. A pyloric muscle thickness of 4 mm or greater was originally considered to be diagnostic,5 but more recent work has suggested

3 mm as the upper limit.6 An antropyloric canal length of 12 mm or greater is currently considered to be diagnostic.

Pyloric stenosis manifests sonographically on transverse images with a typical "donut" or "bulls-eye" appearance (figure 3).7 The outer hypoechoic layer of the "bulls eye" consists of the pyloric muscle mass, whereas the inner hyperechoic layer corresponds to the mucosal layer. Longitudinal imaging will reveal the typical elongated antropyloric canal, as well as any thickening of the antropyloric muscle. Sonography will detect any fluid that may be trapped between the mucosal folds of the antropylorus and these findings should correspond to the classic "string" or "double-track" signs of contrast radiography.

In patients suspected of having pyloric stenosis, sonography is best performed with the patient in the right posterior oblique position. This maneuver allows intraluminal fluid to fill the antrum, providing more of an acoustic window. One should be careful not to overfill the stomach with fluid, however, because the distended stomach may prevent optimal measurement of pyloric length and thickness.8 In this situation, the antropylorus is displaced posteriorly, and transverse imaging may underestimate its length. If the stomach is too distended, excess fluid can be aspirated through a nasogastric tube. Once the stomach is emptied, the hypertrophied pyloric muscle mass may become more palpable, and its maximum longitudinal dimension will be in line with the transverse plane of imaging.

Patients with classic hypertrophic pyloric stenosis are treated surgically with pyloromyotomy. However, some symptomatic patients will present with minimal pyloric muscle thickening that does not meet the criteria for this diagnosis. In these patients, the pyloric muscle usually measures between 2 to 3 mm. These patients are treated initially with an antispasmodic agent, such as metoclopramide. If symptoms persist, a reexamination should be performed, as some of these patients eventually may progress to fulfill the criteria for hypertrophic pyloric stenosis. One should not be overzealous in diagnosing hypertrophic pyloric stenosis in these transitional cases. If it is missed on the initial ultrasound, it will likely be detected during a follow-up ultrasound or during an upper gastrointestinal examination. However, if pyloric stenosis is misdiagnosed, a surgical procedure may be performed unneccesarily.

The most common cause of gastric outlet obstruction in an infant is pylorospasm, often caused by milk allergy. Sonography will reveal elongation of the antropyloric canal and thickening of the contracted pyloric muscle. The pyloric muscle thickening is generally less than 3 mm in these cases. Further observation should eventually show relaxation of the pylorus and passage of fluid into the duodenum.

Other less common causes of gastric outlet obstruction also can be detected with sonography. Gastric diaphragms are hyperechoic congenital membranes that extend across the gastric antrum, either partially or completely obstructing the stomach. Gastric antral thickening and/or edema due to peptic ulcer disease, prostaglandin-induced antral foveolar hyperplasia, eosinophilic gastritis, and other causes (see preceding section) also may cause gastric outlet obstruction.

Enteric duplication cyst

Presence of gastric duplication cysts is another possible cause of gastric outlet obstruction. These cysts may clinically mimic hypertrophic pyloric stenosis, though they have a completely different sonographic appearance. The normal bowel wall typically demonstrates an inner echogenic mucosal layer and an outer hypoechoic muscular layer. Therefore, the presence of a cystic lesion with this type of wall architecture is virtually pathognomonic for an enteric duplication cyst (figure 4). However, one should be aware that a similar appearance may be present in any cyst in which bleeding has occurred, with resultant fibrin deposition along the cyst wall. In some duplication cysts, peristalsis may be observed in the cyst wall, thus confirming the diagnosis.9

Duodenal hematoma

Bowel hematomas generally manifest as eccentric intramural thickening of the bowel wall. The sonographic appearance varies, depending on the age of the lesion. Fresh hematomas often are hyperechoic, but they eventually become hypoechoic as liquefaction occurs (figure 5). During its evolution, the hematoma may have either a unilocular or multilocular appearance.10 In cases of blunt abdominal trauma, the duodenum is the most commonly injured segment of the gastrointestinal tract due to its relatively fixed position and its juxtaposition to the lumbar vertebrae.

Two common scenarios that can lead to a duodenal hematoma are seat belt injuries sustained during a motor vehicle accident and the battered child syndrome. Duodenal hematomas also may develop spontaneously in coagulopathic patients.11 If a duodenal hematoma is detected in a patient without a plausible history of non-accidental abdominal trauma or a known coagulopathy, the possibility of child abuse should be raised. Obtaining a skeletal survey would be a reasonable first step in determining a possible abusive cause of the hematoma. However, when a suspected child abuse victim presents with a low hematocrit or symptoms of gastric outlet obstruction such as vomiting, the possibility of a duodenal hematoma with or without concomitant solid organ injury should be suspected.

Duodenal obstruction

Duodenal stenosis and duodenal atresia are common causes of intrinsic congenital duodenal obstruction. Plain abdominal radiographs may be diagnostic in patients with duodenal atresia, demonstrating a characteristic "double-bubble" sign which represents the dilated and gas-filled stomach and duodenal bulb. In patients with combined duodenal and esophageal atresia, plain films may not display these diagnostic signs because air can not enter the stomach or duodenum unless there is an associated tracheoesophageal fistula. Sonography can be useful in these rare cases, as it is able to directly visualize the distended and fluid-filled proximal duodenum, stomach, and distal esophagus.12

Sonography may in some cases have the ability to directly visualize the site and/or cause of duodenal obstruction. In addition, if bowel perforation distal to a proximal obstruction is present, plain radiographs may not demonstrate free intraperitoneal air. In these cases, sonography may demonstrate free intraperitoneal fluid, raising the suspicion for bowel perforation, thus making it a better choice as a screening examination.

Another cause of duodenal obstruction that can be detected sonographically is a duodenal diaphragm (figure 6). In this entity, the distal duodenum is stretched into a "windsock" configuration. Extrinsic causes of duodenal obstruction such as an annular pancreas or a mesenteric mass also may be seen with ultrasound.

Midgut volvulus

Reversal of the normal relationship between the superior mesenteric artery and vein suggests the diagnosis of midgut malrotation, with or without migdgut volvulus (figure 7). However, some patients with midgut volvulus may have a normal relationship between the superior mesenteric artery and vein.13 It has been reported that the presence of mesenteric vessels swirling in a clockwise direction (the so-called "whirlpool" sign) is highly specific for midgut volvulus,14 but not all patients will display this finding. Because of this, an upper gastrointestinal examination remains the gold standard for detecting midgut volvulus. However, sonography may suggest the possibility of midgut volvulus in patients for whom this diagnosis is unsuspected. If an ultrasound examination reveals a reversed relationship between the superior mesenteric artery and vein, then confirmation should be achieved with an upper gastrointestinal examination.

Small bowel wall thickening

The differential diagnosis of small bowel wall thickening is extensive and includes (but is not limited to) Crohn's disease, tuberculosis, lymphoma, Henoch-Schönlein purpura, and graft-versus-host disease. With sonography, the thickened bowel wall can be visualized directly, rather than inferred indirectly as with plain abdominal radiographs or contrast studies. Normal small bowel wall thickness should not exceed 3 mm.15 Although a specific diagnosis often may not be possible based on the ultrasound findings alone, in conjunction with the clinical history, physical exam, and laboratory findings, sonography may be quite suggestive.

Classically, patients with Crohn's disease manifest sonographically with thickening of the wall of the terminal ileum. There usually is increased blood flow to this region, which can be detected with color-flow Doppler imaging. These findings are nonspecific, however, and can be seen with other entities such as tuberculosis, Yersinia enterocolitica infection, and lymphoma.

Henoch-Schönlein purpura is an idiopathic systemic vasculitis, with bowel involvement usually limited to the duodenum and jejunum (figure 8), although ileal and colonic involvement also can be seen. The bowel may be the initial site of presentation, prior to any vessel or skin abnormalities. Circumferential echogenic small bowel wall thickening often is present, resulting from intramural hemorrhage. In addition, Henoch-Schönlein purpura may be associated with intussusception and, therefore, examination of the entire intestinal tract can be extremely helpful. Significant ascites may be present and other organ systems may also be affected. For example, the kidneys may demonstrate increased echogenicity as a result of hemorrhagic nephritis.

In patients with graft-versus-host disease, diffuse circumferential thickening of the bowel wall can be seen (figure 9). The bowel loops are often fluid-filled and, unlike in Henoch-Schönlein purpura, there is no bowel wall nodularity or active peristaltic activity. Contrast studies characteristically demonstrate a bland, tubular, "toothpaste-like" pattern.

Intestinal lymphangiectasia is associated with diffusely nodular bowel wall thickening (figure 10). The appearance is nonspecific, however, as other disorders such as giardiasis, strongyloidiasis, and cystic fibrosis can give a similar picture.

Appendicitis

When searching for appendicitis, a graded-compression method should be used.16 Normal gas-filled bowel loops can be displaced from the right lower quadrant with steady compression on the transducer, allowing visualization of the inflamed appendix which, unlike the normal appendix, is not compressible. The demonstration of an appendicolith is not necessary to make the diagnosis of appendicitis, though it is a suggestive sign (figure 11). If perforation has occurred, the appendix becomes decompressed and may be more difficult to detect. The presence of an abscess in the right lower quadrant, which will manifest sonographically as a complex fluid collection, can be a clue that the appendix has perforated. However, a small amount of free fluid can be seen around the appendix in the absence of perforation.

Sonography is the initial imaging modality of choice in the evaluation of suspected appendicitis. However, exclusion of appendicitis requires visualization of the entire length of a normal appendix, which may not always be possible. For example, patient discomfort may prevent a satisfactory examination. The maximal outer diameter of the appendix should not exceed 6 mm.16,17 If the clinical question of appendicitis persists despite an apparently normal sonogram, other imaging modalities such as computed tomography or a contrast enema may be required.

Mesenteric adenitis

Mesenteric adenitis is a common cause of abdominal pain in children, symptoms of which may be similar to those of appendicitis. The etiology usually is viral, though it also can be seen with Yersinia enterocolitica infections. Mesenteric adenitis is a diagnosis of exclusion and should be made only when other entities such as appendicitis have been ruled out. Sonographically, it manifests as multiple enlarged mesenteric lymph nodes (figure 12) which often show increased blood flow on color Doppler imaging. Mild bowel wall thickening also may be associated with this disorder.

Prior to the advent of ultrasound, the primary diagnosis of mesenteric adenitis could only be made intraoperatively or histologically, as appendicitis could not be excluded with confidence radiographically or clinically. However, with ultrasound's current capabilities, the diagnosis of appendicitis and other entities can be excluded, and the presence of multiple enlarged mesenteric lymph nodes can suggest mesenteric adenitis as a primary diagnosis. In this situation, the patient can be safely observed without the fear of ongoing appendicitis or appendiceal perforation. If the patient's symptoms persist or worsen, a repeat sonogram can be performed.

Intussusception

A patient with an intussusception classically presents with crampy abdominal pain, "currant jelly" stools, vomiting, and a palpable abdominal mass. Those presenting in this manner can most likely proceed to enema reduction for diagnosis and therapy, bypassing an ultrasound examination altogether. Not all patients with intussusception will present in this manner, however, and therefore sonography is an important diagnostic tool, demonstrating both a high sensitivity and specificity for this disorder.18 In the hands of an experienced sonographer, a meticulously-performed ultrasound exam which is normal, combined with a normal abdominal plain film, may obviate the need for a contrast enema. Abdominal radiographs of patients with suspected intussusception may demonstrate an obstructive pattern, with gas-filled loops of bowel filling the abdomen. This appearance should not discourage the use of sonography, as the retroperitoneum can be used as an acoustic window in order to examine the colon.

Classically, longitudinal imaging of an intussusception reveals a hypoechoic mass with bright central echoes, the so-called "pseudo-kidney" sign. Trans-verse imaging reveals a characteristic "donut" configuration. The bright central echoes correspond to trapped intestinal contents, as well as mucosa and mesentery, while the hypoechoic outer layer corresponds to the edematous wall of the intussusception. On occasion, an enlarged mesenteric lymph node can be seen within the lumen of the intussuscipiens (figure 13). If there is a pathologic lead point such as a cyst or tumor, it also may be demonstrated sonographically.19 With the current generation of high resolution scanners, longitudinal scanning may show the telescoping of one bowel loop into another as multiple parallel layers of varying echogenicity, while transverse imaging may reveal multiple concentric rings.

As mentioned previously, if an intussusception is strongly suspected, the study of choice is an enema examination rather than sonography because an enema examination can be both diagnostic and therapeutic. An enema reduction can be performed using barium, gastrografin, saline, or air. Currently, air reduction is the most popular method, though these agents all are effective. However, if perforation occurs during attempted reduction, using barium as the contrast agent may result in barium peritonitis, whereas this complication would not occur with any of the other agents. Sonography may play a greater role in the management of patients with intussusception when ultrasound-guided reduction with a normal saline enema becomes a more accepted practice.

An enema reduction is contraindicated if there are clinical signs of peritonitis or radiographic signs of free intraperitoneal air. Patients with these signs will require surgical management. Sonography can sometimes be helpful in predicting whether non-surgical reduction of an intussusception will be successful. The finding of excessive free fluid and/or diminished or absent perfusion in the intussusception by color Doppler imaging suggest that attempts at non-surgical reduction will fail.

Large bowel wall thickening

The differential diagnosis of large bowel wall thickening is extensive and there is considerable overlap with the differential diagnosis for small bowel wall thickening. Included in the list are inflammatory bowel disease, infectious colitis, neutropenic colitis (typhlitis), necrotizing enterocolitis, pseudomembranous colitis, lymphoma, Henoch-Schönlein purpura, and hemolytic-uremic syndrome. These diseases often are indistinguishable from each other based on the sonographic appearance alone and all can manifest with colonic wall thickening. The normal colonic wall should not exceed 5 mm in thickness.20

The sonographic manifestations of necrotizing enterocolitis are varied and include bowel wall thickening, aperistaltic bowel loops, and portal venous gas (figure 14). Intramural bowel gas can sometimes be directly visualized, and sonography may be more sensitive than plain films in this regard. After bowel perforation, ascites with a fluid/debris level may be present. It has been reported that detecting increased flow velocity in the celiac and superior mesenteric arteries with Doppler sonography is an early sign of necrotizing enterocolitis.21 Abdominal radiographs in patients with this disorder range from an ileus pattern to a complete absence of bowel gas. Sonography can be especially useful in patients with a gasless abdomen, as the fluid-filled loops of bowel act as a natural acoustic window.

The ultrasound appearance of typhlitis is marked edematous thickening of the cecal wall associated with polypoid thickening of the mucosa (figure 15).22 In the clinical setting of neutropenia, the results are consistent with typhlitis. Sonography is preferred over contrast examinations in neutropenic patients because of the risk of bacteremia during a contrast enema. Furthermore, sonography is superior to a contrast enema in distinguishing typhlitis from pathology in adjacent organs (e.g., appendicitis). While a contrast enema may not be able to distinguish typhlitis from appendicitis, these entities have completely different sonographic features.

Hemolytic-uremic syndrome is a disease of unknown etiology characterized by microangiopathic hemolytic anemia, renal failure, and thrombocytopenia. It manifests sonographically as marked colonic wall thickening (figure 16). The appearance is nonspecific, and sonography is useful primarily as an adjunct to the history, physical examination, and laboratory studies.

Imperforate anus

While sonography is not necessary in order to make the diagnosis of imperforate anus, it can be helpful to further characterize the nature of the anomaly (figure 17). Sonography can directly visualize the location of the distal end of the hindgut, which can be important for surgical planning. The distance from the rectal pouch to the perineum is measured with longitudinal midline images through the perineum, usually obtained while the patient is in the lithotomy position. A perineum-to-pouch distance of less than 1.5 cm suggests a low imperforate anus.23

Alternatively, the "M" line of Cremin can be drawn.24 This line roughly corresponds to the level of the puborectalis muscle. Hindgut termination above this line suggests that the patient has a high imperforate anus, whereas termination below this line suggests a low imperforate anus. The "M" line of Cremin is drawn through the junction of the lower third and the upper two thirds of the ischia and parallels the pubococcygeal line (a line drawn from the midpubic bone to the sacrococcygeal junction).

Patients with imperforate anus have an increased risk of associated genitourinary tract and spinal cord abnormalities and ultrasound can be useful in their detection as well. It should be emphasized that a radiographic study of the rectum can underestimate or overestimate the true location of the most distal aspect of the rectal pouch: straining may make a high pouch appear to be low, and a mucous plug may make a low pouch appear to be high.

Conclusion

Sonography in conjunction with plain abdominal radiographs often is useful in the evaluation of suspected bowel pathology in the pediatric population. In many cases, it may obviate the need for contrast examinations. We recommend initial evaluation with sonography rather than a contrast study in the following cases:

• Gasless abdomen on plain abdominal radiograph.

• Physical examination or abdominal radiograph suspicious for abdominal mass.

• Debilitated patient condition such that contrast examination may be dangerous (e.g., risk of bacteremia in a neutropenic patient or intubated neonate who can not be transported to the radiology department).

• Initial evaluation of suspected appendicitis.

However, there are situations in which we recommend a contrast study for definitive diagnosis, such as suspected midgut malrotation and volvulus, for which an upper gastrointestinal study should be performed immediately, or for treatment of intussusception. AR

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Dr. Chang, Dr. Lim-Dunham, and Dr. Yousefzadeh are with the Department of Radiology at the University of Chicago Hospitals in Chicago, IL.