Ultrasound in the evaluation of necrotic bowel in children: A pictorial essay

Abstract

Necrotic bowel is a serious condition involving death of gastrointestinal tissue. The diagnosis is difficult to make clinically, and plain radiography is often inconclusive. Ultrasonography is an inexpensive, portable and readily available complementary diagnostic tool. In some cases, ultrasonography can detect features of necrotic bowel earlier than plain radiography or when plain radiography is equivocal and does not correlate with the clinical findings. This pictorial essay aims to compare the ultrasonography features of normal bowel and necrotic bowel in children. The role of ultrasonography and the ultrasonographic features of necrotic bowel will be illustrated by discussing some of the causes of necrotic bowel in children. Correlation with plain radiographs and pathological specimens is made. Frequent causes of necrotic bowel in neonates include necrotising enterocolitis, malrotation with small bowel volvulus and incarcerated inguinal hernias. Causes in older children include intussusception, complications of Meckel’s diverticulum, post-surgical adhesions, internal hernias and vasculitic abnormalities. Ultrasonography features suggestive of necrotic bowel include persistently dilated loops of aperistaltic bowel, increase or decrease of bowel wall thickness, intramural or portal venous gas, loss of bowel wall perfusion, and free intraperitoneal gas and fluid. The diagnosis of necrotic bowel may be made earlier on ultrasonography than on abdominal radiographs alone. This pictorial essay will familiarise the reader with the role of ultrasonography and the ultrasonographic features of necrotic bowel through a wide range of conditions that may cause necrotic bowel in children. Familiarity with these findings will facilitate timely imaging diagnosis of necrotic bowel before complications develop.

Keywords

Paediatric necrotic bowel ultrasound features pneumoperitoneum intramural gas

Introduction

Necrotic bowel (NB) is a difficult diagnosis to make clinically. Although most patients are usually septic and very ill, symptoms are very variable, depending on the cause and the acuteness of onset of the underlying pathology.

Typically, these patients are first evaluated with plain abdominal radiographs (AXRs). In the absence of prior abdominal surgery, the detection of free intraperitoneal gas on AXR is the most definitive sign that perforation has occurred in patients with suspected NB. However, when AXRs are inconclusive or do not correlate with clinical findings – particularly in the early stages of NB – ultrasonography (US) may be a more sensitive and thus appropriate complementary investigation.^1,2

US is an increasingly available modality that may be used in paediatric outpatient clinics, accident and emergency departments as well as in hospitals without an established paediatric radiology service. However, it is operator dependent and requires experience. Therefore, the sonologist should be familiar with the US findings and potential pitfalls in the imaging of NB.

This pictorial essay will familiarise the reader with the US features of NB through a wide range of conditions that may cause NB in children. The role of US in the evaluation of these patients will be discussed.

Ultrasound findings in normal bowel

Faingold et al. described the US features of normal bowel in 30 neonates. Normal bowel wall thickness ranged from 1.1 to 2.6 mm with no significant difference in mean thickness between different abdominal quadrants. A prominent hypoechoic halo, thought to represent the muscularis propria, was representative of normal bowel echogenicity. In normal patients, intramural gas, portal venous gas, pneumoperitoneum or intraperitoneal free fluid was not seen. Peristalsis with a minimum of 10 contractions per minute in all quadrants was noted. Allowing for limitations of acoustic windows due to abundant bowel gas, bowel perfusion was detected.^3–6 Figure 1 illustrates some of these findings in a normal child as a baseline for comparison with the patients with NB.

Figure 1.

Ultrasonographic appearances of normal bowel. This nine-year-old girl presented with abdominal pain. (a) US of the bowel loops (arrow) showed no mural thickening, increased echogenicity or intramural gas. Mural thickness in a loop of bowel is better assessed when it contains hypoechoic fluid as shown. (b) Preserved bowel perfusion was demonstrated (arrow). Bowel peristalsis was observed under real-time ultrasound.

Figure 2.

This two-day-old neonate presented with bilious vomiting. (a) US of the duodenal loops shows increased echogenicity and thickening of the bowel wall with no perfusion (arrow). These findings are suspicious for bowel gangrene which was found at surgery. (b) Plain AXR shows subtle mottled lucencies in a loop of bowel in the left upper abdomen (arrow). Some of these lucencies have a linear appearance whilst others appear as tiny bubbles. These findings are suspicious for intramural gas. (c) Spot image from an upper GI contrast study shows complete obstruction at the third part of the duodenum (arrow) which is diagnostic of malrotation with bowel obstruction.

Ultrasound findings in NB

Ultrasound findings that are suspicious for NB are persistently dilated loops of aperistaltic bowel or bowel demonstrating sluggish peristalsis, bowel wall thickening or thinning, intramural gas, portal venous gas, pneumoperitoneum, free fluid and loss of bowel wall perfusion.^3,7

The normal echogenicity of bowel wall is lost with bowel wall thickening or thinning. As such, it is difficult to resolve the thickened hyperechoic bowel wall from the echogenic contents of intraluminal material. This is also known as the greyscale ‘zebra’ or ‘herringbone’ pattern.⁷ Faingold et al. defined bowel wall thinning to be less than 1 mm. However, abnormal thinning must be differentiated from apparent thinning due to stretching of the bowel wall due to fluid distension. In apparent thinning, the normal bowel echogenicity is preserved (see Table 1).^3,7

Table 1.

Ultrasound features of normal versus necrotic bowel

Feature	Normal bowel	Necrotic bowel
Bowel wall thickness	<3 mm	Markedly thinned or ≥3 mm
Bowel wall echogenicity	Preserved	Loss of normal ‘gut signature’ (well-delineated stratified echogenic layers)
Peristalsis	Present	Sluggish or absent
Free intraperitoneal fluid	Absent	Present
Intramural gas	Absent	Present
Portal venous gas	Absent	Present
Pneumoperitoneum	Absent	Present

In experienced hands, US may be more sensitive and specific in detecting NB than AXR. Faingold et al. found that the sensitivity of AXR in detecting free intraperitoneal gas as a marker of NB in patients with severe NEC was 40%, compared to the 100% sensitivity for the absence of perfusion as a marker of NB on US.³ In addition, bowel perforation may manifest as free intraperitoneal gas or fluid.⁸

On US, intramural gas is seen as intramural hyperechoic, granular foci with posterior reverberation artefacts.⁹ Intramural gas needs to be differentiated from intraluminal gas. Unlike intraluminal gas, intramural gas does not change in position with changes in the patient’s position, abdominal compression with the transducer, peristalsis or respiratory movement.¹⁰ Portal venous gas is seen as mobile intraluminal echogenic foci within the main portal vein or linear branching echogenic foci reaching the periphery of the liver.⁷

Advantages of US over plain radiography in the detection of NB include the ability to demonstrate intraperitoneal free fluid, mural thickening, bowel wall perfusion and subtle intramural gas, portal venous gas and pneumoperitoneum that may not be seen on plain radiographs.⁷ As such, the diagnosis of NB may be made earlier with complementary US than on AXRs alone.^1,2 If NB is detected before pneumoperitoneum occurs, it can prevent significant morbidity and mortality in young children.

The most frequent causes of NB in the neonatal period are necrotising enterocolitis (NEC), malrotation and incarcerated inguinal hernia. In older children, causes include intussusception, complications of Meckel’s diverticulum, postsurgical adhesions, internal hernias and vasculitic abnormalities. Regardless of the cause of NB, the ultrasonographic features of NB are the same. The role of US in the evaluation of NB and ultrasonographic features of NB will be illustrated by discussing some of the more common causes of NB in children.

Malrotation with midgut volvulus

In malrotation, there is congenital abnormal shortening of the mesenteric root within the peritoneal cavity. This predisposes the patient to midgut volvulus (Figure 2).¹¹ Malrotation may present in the early neonatal period with persistent bilious vomiting. Timely diagnosis of malrotation when it is complicated by midgut volvulus is crucial in reducing morbidity and mortality. Diagnostic delay may lead to NB. An upper gastrointestinal contrast study remains the definitive investigation of choice in the diagnosis of malrotation.^12,13

In cases when the typical history of bilious vomiting is not elicited or noticed by the patient’s parents or clinicians, AXR followed by US may be the only initial investigations the patient receives. In these cases, US may be a helpful screening tool. US may depict features of NB, pointing clinicians to the possibility of malrotation with volvulus as the cause of the patient’s symptoms. In such cases, an upper gastrointestinal contrast study should not be further delayed.

NEC

NEC is a common gastrointestinal abnormality that typically affects the premature neonate. The clinical presentation is non-specific and includes abdominal distension and feed intolerance. NEC is indistinguishable from neonatal sepsis.⁷ The aetiology and pathophysiology of NEC are complex and multifactorial and outside the scope of this paper.⁷ Patients with suspected NEC are typically evaluated with AXR in the first instance. There may be fixed dilatation of the same bowel loops in serial AXRs. AXR may show intramural, portal venous or free intraperitoneal gas (Figure 3). US for further evaluation may be considered especially if there is clinical deterioration with no evidence of free gas on AXR.⁷ US has the advantage over AXR in that it can provide real-time evaluation of mural thickening, absence of bowel peristalsis, lack of bowel wall perfusion and free intraperitoneal gas or fluid.⁷

Figure 3.

Eight-day-old premature neonate (35 weeks’ gestational age) developed septic shock and bowel distension. (a) Plain AXR shows persistently dilated bowel loops throughout the abdomen. No definite intramural, free intraperitoneal or portal venous gas is seen. (b, c) US shows the presence of intramural gas as hyperechoic, granular foci with posterior reverberation artefacts (arrows). Intraluminal gas is also seen (thin arrow) and can be distinguished from intramural gas by its location. Peritoneal fluid is also noted (*). (d) US shows hyperechogenicity of the valvulae conniventes (arrow) known as the ‘zebra’ or ‘herringbone’ pattern. (e) Portal venous gas is also noted (arrow). A large amount of clear peritoneal fluid was found at surgery. Two areas of NB with impending perforation were noted in the jejunum, 90 cm from the DJ junction and in the terminal ileum, 15 cm from the ileocaecal valve.

In the clinical setting of NEC, the presence of intramural gas is pathognomonic for NEC. Intramural or portal venous gas may be present only transiently in NEC. It is important to note that the amount of intramural or portal venous gas does not necessarily correlate with the clinical severity of NEC.⁷

Meckel’s diverticulum

Meckel’s diverticulum is a congenital abnormality resulting from incomplete closure of the vitelline duct. It may present with intestinal obstruction or gastrointestinal bleeding.¹⁴ In the absence of bowel obstruction, Meckel’s diverticula are diagnosed using Tc-99 m nuclear medicine studies, usually following episodes of unexplained bleeding per rectum. Meckel’s diverticula themselves are infrequently visualised at ultrasonography. They may cause bowel obstruction due to an omphalomesenteric band resulting in volvulus and closed loop bowel obstruction, which can be inferred at ultrasonography (Figure 4).

Figure 4.

Four-year-old girl with acute onset of abdominal pain and vomiting. (a, b) US shows bowel wall thickening with a layered appearance (thin arrow). Intramural hyperechoic linear foci are due to intramural gas (arrows). Free intraperitoneal fluid is also noted (*). (c) Plain radiograph shows multiple loops of dilated bowel in the central abdomen. (d) At surgery a Meckel’s diverticulum was discovered with adhesions, causing an internal hernia and bowel gangrene. Intra-operative photograph shows purple, dusky, gangrenous bowel on the left with normal pinkish bowel to the right of the picture corroborating the findings noted on imaging.

Adhesions causing bowel strangulation and necrosis

In patients with prior abdominal surgery presenting with symptoms of bowel obstruction, bowel obstruction secondary to adhesions is the main diagnostic consideration. Depending on the type of prior abdominal surgery, the risk of developing adhesive complication varies, with small bowel and abdominal wall surgery having the highest risk.¹⁵ On US or plain radiographs, persistent or progressively dilated loops of bowel are often seen (Figure 5), suggesting obstruction. Sonographic features of small bowel obstruction include dilated bowel loops >3 cm, length of dilated segment >10 cm and increased peristalsis in the dilated segment.^16,17 If obstruction is severe or prolonged, the presence of free fluid between dilated small bowel loops, aperistalsis and wall thickening >3 mm in a fluid-filled dilated segment suggests NB.^16,17

Figure 5.

Six-month old infant with a previous history of abdominal surgery presented with vomiting of blood and abdominal distension. (a, b) Plain radiographs done 24 hours apart show increasing bowel dilatation (arrow) and (c, d) US shows the presence of a focal loop of dilated bowel corresponding to the findings on the AXR (arrows). Free intraperitoneal fluid is also noted (*). At surgery an adhesion band was noted causing volvulus of the terminal ileum resulting in 53 cm of NB.

Ileo-colic intussusception with necrotic terminal ileum

Ileo-colic intussusception refers to the telescoping of a loop of distal ileum into the ascending colon. The aetiology of ileo-colic intussusception is varied but in the majority of cases, no fixed anatomical lead point is found. As such, some authors surmise that these ‘idiopathic’ intussusceptions may be the result of lymphoid hyperplasia. In other patients, lead points include gastrointestinal polyps, duplication cysts or Meckel’s diverticula.¹⁸ Patients typically present with colicky abdominal pain and bloody stools. On US, the affected bowel loops show a bowel-in-bowel appearance with mural thickening (Figure 6). Lymphoid hyperplasia, polyps or cysts within the intussusception are easily demonstrable. Bowel perfusion may be normal or reduced. It is important to note that the presence of transmural blood flow does not exclude NB.¹⁹

Figure 6.

2.5-month-old infant with intussusception. (a, b) Cross section and longitudinal US images show the presence of an intussusception with a thick and oedematous bowel wall. Transmural blood flow was seen within the bowel wall (arrow). Air enema reduction was attempted but was unsuccessful. At surgical reduction, an ileo-colic intussusception was identified. Eighteen centimetre of the terminal ileum was gangrenous and was resected. This case illustrates a potential pitfall in that the presence of transmural blood flow in the bowel wall does not exclude bowel gangrene. (a, b labelled) Intussuscipiens (dotted green line) and intussusceptum (solid green line).

Henoch–Schönlein purpura (HSP)

HSP is an immune-mediated vasculitis in which IgA complexes are deposited in the small vessels, commonly affecting children. Patients often present with a palpable purpura, abdominal pain and gastrointestinal bleeding. Intussusception, bowel obstruction and NB are rare.²⁰ AXR may show non-specific findings of bowel wall thickening (‘thumbprinting’) or evidence of bowel obstruction. US is a useful adjunct as it allows for direct visualisation of bowel wall thickening²¹ and intussusception, usually ileoileal, may also be identified (Figure 7). In the appropriate clinical setting, these imaging findings are suggestive of the diagnosis.

Figure 7.

Three-year five-month-old child with HSP on steroids, presented with abdominal pain. (a, b) US shows the presence of an intussusception with thickened bowel wall without bowel perfusion (arrows). Free intraperitoneal fluid was noted (*). Although it was suspected that the intussusception was ileoileal, a confirmatory/therapeutic air enema reduction was performed which did not reveal an ileo-colic intussusception. The patient’s symptoms gradually worsened over a period of 36 hours. Repeat US examinations over this period of time showed the intussusception to be persistent. In view of these findings and the patient’s worsening clinical condition, surgery was performed. This revealed the presence of an ileoileal intussusception and HSP involving the small bowel with haemorrhagic infarction. (a, b labelled) Intussuscipiens (dotted green line) and intussusceptum (solid green line).

Inguinal hernia

Inguinal region hernias mostly comprise direct and indirect inguinal hernias and femoral hernias. Indirect inguinal hernias arise medial to the inferior epigastric artery (IEA), whereas direct inguinal hernias originate lateral to the IEA in Hesselbach’s triangle. Femoral hernias tend to occur inferior to the inguinal ligament and along the medial aspect of the femoral vein.²² In children, inguinal hernias are almost always due to a patent processus vaginalis. Bowel-containing hernias can be distinguished by the presence of peristalsis, intramural gas or the ‘gut signature’ appearance of bowel wall within the hernia sac. These can be complicated by incarceration (Figure 8) with subsequent bowel obstruction and NB and should be evaluated for reducibility and bowel viability.²² The risk factors for obstruction include right-sided hernia, young age and male gender.²³

Figure 8.

Two-month-old infant with left inguinal swelling and redness. (a) Longitudinal and (b) transverse US images show the presence of a narrow necked (paired arrows) thick-walled incarcerated inguinal hernia containing bowel (arrow) without transmural blood flow. A loop of necrotic small bowel was found at surgery within the hernia sac.

Conclusion

In the appropriate clinical setting, NB should be suspected if the following features are noted on US: aperistaltic bowel or bowel showing sluggish peristalsis, abnormally thickened echogenic bowel wall, abnormal thinning of bowel wall, intramural gas, portal venous gas, free intraperitoneal gas or fluid, and loss of bowel wall perfusion. It is important to note that the presence of blood flow in the bowel wall does not exclude NB. To make a confident diagnosis of NB, an experienced sonologist is recommended as ultrasound is a highly operator-dependent modality. Sonologists need to be familiar with these findings to facilitate timely imaging diagnosis of NB before complications develop.