Fig. 4.1
NEC—Various stages on plain abdominal radiograph. (a) Stage 1. Plain radiograph of the abdomen showing distended bowel loops. The distance between some bowel loops is increased suggesting bowel wall thickening and/or effusion. (b) Stage 2. Focused plain radiograph of the abdomen showing pneumatosis in the bowel loops of the right flank (arrows). (c) Stage 3. A pneumoperitoneum can be observed as an area of radiolucency below the diaphragm and superimposed to the liver (arrows)
Each stage will be managed accordingly through close observation, bowel decompression, or exploratory laparotomy [7].
4.2.1.2 Ultrasound
US is considered as a complementary imaging tool to the plain film of the abdomen. Its main advantages are that it is a radiation free technique, it can be performed at the bedside, and it can be repeated in order to monitor unstable clinical evolution. Its role in assessing NEC remains somewhat controversial but the technique does provide some additional information complementary to the findings on the plain abdominal radiograph. US provides direct images of the bowel and peritoneal cavity and may help to predict the need for surgery. High resolution transducers with 8–15 MHz frequency should be used. The use of a linear-array transducer is preferable for evaluating the bowel and a sectorial transducer can be used to detect free fluid or free abdominal air.
The examination is intended to assess bowel wall thickness, wall echogenicity, bowel peristalsis, intestinal pneumatosis, portal venous gas, free abdominal air or free fluid, and abscesses. Color Doppler US can be helpful to evaluate blood flow in the superior mesenteric artery and to verify bowel wall perfusion.
Bowel wall thickness greater than 2 mm should be considered as suspicious for NEC and is thought to correspond to mucosal edema and hemorrhage. It may represent the first feature of the disease. Conversely, thickness below 1 mm indicates abnormal thinning resulting from ischemia that may lead to perforation. Typically intestinal peristalsis is reduced. Some authors monitor abnormal and reduced peristalsis through color Doppler.
Intestinal pneumatosis or intramural gas corresponds to the presence of air within the serosal and submucosal layers. It is due to the passage of intramural gas into the injured intestinal wall. It corresponds to the passage from stage 1 to stage 2. It is most commonly observed in the distal ileum and colon. On US, intestinal pneumatosis appears as highly echogenic dots within the bowel wall. The amount of gas is variable, sometimes only a few foci, but sometimes it encircles the entire wall determining the “circle sign” (Fig. 4.2a). Intestinal pneumatosis should be differentiated from intraluminal air that usually moves within the bowel whereas pneumatosis tends to remain unchanged with time.
Fig. 4.2
NEC—US features. (a) Pneumatosis. Transverse scan in the midline below the liver. Bubbly hyperechogenicities can be observed within all bowel loops wall (determining the “circle sign”). They corresponding to pneumatosis. (b) Portal air. Oblique scan of the liver. Scattered hyperechogenic dots can be seen throughout the liver parenchyma corresponding to air bubbles within the portal system. (c) Effusion. Transverse scan of the right flank, echogenic fluid (in front of the right kidney (RK)) displaces the bowel loops to the midline
Portal venous gas possibly originates from the venous absorption of intestinal pneumatosis; its finding in the appropriate clinical setting should raise the suspicion of intestinal pneumatosis and of NEC of stage 2. On US, it appears as echogenic dots distributed within the distal portal branches (Fig. 4.2b). It can appear within a segmental area or the entire liver can appear dotted due to the presence of air. Portal venous gas should be differentiated from intrahepatic calcifications, presenting in asymptomatic neonates and related to different entities (e.g., congenital infections) or to air observed after the placement of intrahepatic umbilical catheters. Portal venous gas seems to be demonstrated earlier on US than on the plain film of the abdomen.
Free abdominal fluid and abscesses are common complications of NEC. Free abdominal fluid is a non-specific finding unless present in large amounts. Echogenic fluid or organized collections are more suspicious of complicated NEC and of bowel perforation. The presence of air within the collection is even more suspicious. Clearly, US is better than a plain film of the abdomen to demonstrate these complications (Fig. 4.2c).
Free abdominal air indicating bowel perforation can be observed on abdominal US as the reverberating artifact. However, this is more easily visualized on the plain film of the abdomen.
(Color) Doppler of the superior mesenteric artery is considered by some authors as useful in the evaluation of NEC. The mean diameter of the artery is 3 mm; the mean peak velocity is 57 ± 3 cm/s. However, during daily work Doppler evaluation of the artery is difficult due to abdominal air distension and to surrounding artifacts from various supporting equipment [9–13].
4.2.1.3 Late Complications of NEC (Presenting as Acute Abdominal Symptoms)
Intestinal strictures are a complication that occurs in up to 40% of neonates with a history of NEC. Strictures develop in patients with both medical and surgical management of their disease. The strictures may be symptomatic or asymptomatic (and discovered incidentally). They appear 4–6 weeks after the acute event. In symptomatic patients, a progressive distension of the abdomen, confirmed by a plain film of the abdomen, will raise the suspicion of a stricture and a contrast enema should be performed. In the absence of suspicion of perforation, a barium enema should be preferred as it might show more accurately the strictures. Water soluble enema should be preferred whenever there is a risk for perforation.
The strictures, defined as areas of persistent narrowing of the lumen on contrast enema with distension of the more proximal bowel, are typically observed at the splenic flexure or on the transverse colon; but may occur anywhere within the entire colon and small bowel (Fig. 4.3). Small bowel localization may be more difficult to demonstrate but is quite frequent. Upper GI opacification is very rarely performed in these patients as it is a time and radiation consuming technique [14, 15]. Conservative or surgical management will be decided on the basis of the clinical symptoms and the degree of narrowing on imaging.
Fig. 4.3
Post-NEC colonic strictures. Contrast enema showing a double stenosis at the junction between the descending colon and the sigmoid
4.2.2 Meconium: Ileus Equivalent of the Premature
A thick and sticky inspissated meconium can cause bowel obstruction as demonstrated in patients with cystic fibrosis or in the meconium plug syndrome. Intestinal obstruction due to intraluminal inspissated meconium is recognized as a distinct clinical entity affecting very low birth prematures and is known as the “meconium obstruction of the prematurity.” Its origin is unclear. Favoring factors include immature motility (with delayed passage of meconium), increased viscosity of the meconium, maternal diabetes, fetal hypoglycemia, and prenatal intestinal hypoperfusion. Sepsis and respiratory distress syndrome (with tracheal intubation) contribute to the intestinal dysmotility. If left untreated, ischemia of the distal bowel and subsequent perforation may occur [16, 17].
4.2.2.1 Imaging at Clinical Suspicion
Typically there is progressive abdominal distension in a baby that did pass some meconium at birth. Plain film of the abdomen will show, around the second week of life, multiple dilated loops suggestive of distal intestinal mechanical obstruction (Fig. 4.4a). In contrast to NEC, no associated pneumatosis is observed.
Fig. 4.4
Meconium ileus equivalent in a 4-week-old premature. (a) Plain film of the abdomen showing increased intestinal distension, especially in the right flank. (b) Water soluble enema showing persisting meconium in the colon. A filling of the terminal ileum is achieved indicating that the plug has been removed, thanks to the enema
4.2.2.2 Confirmative Imaging and Management
Contrast enema with iso-osmolar or slightly hyperosmolar water soluble enema under fluoroscopic control is the gold standard procedure. This agent is not only radio-opaque but would also dilute and mobilize the thick meconium. When performed, the contrast enema should reach the ileo-cecal valve and opacify the small bowel proximal to the site of obstruction (Fig. 4.4b). During and after the examination, hydration and fluid and electrolyte balance should be closely monitored.
Contrast enema may be difficult to organize and achieve in low birth or extremely low birth prematurely born and therefore alternative treatments can be proposed. First, contrast enema in the NICU had been advocated by some while others have tried to remove the obstruction under US guidance. Both methods encompass a higher risk of perforation and should be undertaken with extreme caution and only in exceptional cases. Finally, medications like N-Acetylcysteine have been used with variable rates of successes. Attempts at reduction should not be performed in case of suspected sepsis or perforation [18, 19].
4.2.3 “Spontaneous” Digestive Tract Perforation
Spontaneous intestinal perforation does occur (rarely) in full-term neonates. It is a distinct clinical entity from NEC. Its origin is unclear; associations have been reported with the maternal use of antibiotics, maternal chorioamnionitis, postnatal use of corticosteroids, indomethacin, and positive neonatal blood culture sepsis (staphylococcus). Spontaneous perforation also occurs as an early manifestation of Hirschsprung disease (see below). Perforation may occur either early within the first days of life or later within the two first weeks of life. The diagnosis is suspected, in the appropriate clinical setting, on the basis of early occurring pneumoperitoneum as demonstrated on the plain radiograph of the abdomen (Fig. 4.5). No other sign of NEC should be present. In cases of a gasless abdomen, extra-digestive air will be more difficult to demonstrate and in these circumstances US has been shown to provide additional information by demonstrating intraperitoneal echogenic free fluid [20, 21].
Fig. 4.5
Spontaneous pneumoperitoneum in 34 weeks premature on its second day of life. Plain film of the abdomen. A large area of radiolucency (arrows) is visible superimposed to the upper abdomen. The origin of the perforation was not found at exploratory surgery. Follow-up was uneventful
4.2.4 Hirschsprung Disease in the Premature
Previous reports have stated that Hirschsprung disease (HD) is uncommon in premature patients. More recent reports contradict these ancient data and show that the prevalence of HD is similar to that of full-term neonates. The diagnosis is based on the same imaging features as those described in full-term (Fig. 4.6): persistent abdominal distension on the abdominal radiograph and a transitional zone on radio-opaque enema. The diagnosis may be delayed due to intestinal dysmotility observed in the premature and to a delay in passing meconium (related to prematurity). Spontaneous pneumoperitoneum has been reported as the primary feature of HD in prematures [22, 23].
Fig. 4.6
Total Hirschsprung disease in a prematurely born (25 weeks at birth) aged 2 months. Contrast enema shows a relatively short colon without haustra (and without peristalsis at fluoroscopy). The small bowel loops are dilated as well (biopsy confirmed the involvement of the ileum as well)
4.3 Hepato-Biliary Complications
Hepatobiliary complications in the premature infant are mainly related to hepatic immaturity, to the consequences of total parenteral nutrition, to the consequences of the insertion of umbilical catheters, and to sepsis.
Ultrasound examination is the main imaging procedure performed to detect and follow these complications. In very few selected cases, CT may be used in order to confirm a large hematoma or abscess [24].
4.3.1 Complications of Total Parenteral Nutrition
Parenteral nutrition (PN) related liver disease develops in about 50% of infants with birth weight < 1000 g but falls to 7% in patients > 1500 g. Its prevalence is directly related to the duration of the parenteral nutrition (PN). The hepatic dysfunction may be related to immaturity of the neonatal liver. The components of the PN are the main causative factor in the development of liver disease.
Acalculous cholecystitis (see below), biliary sludge, gallbladder distension, and gallstones have been reported in neonates on long-term PN.
On US, the main sign of liver disease is non-specific hepatomegaly.
Echogenic sludge within the gallbladder may be visualized as early as 1 week after the starting of the PN (Fig. 4.7a). This sludge can disappear once the infant is fed orally. Yet, if the PN is continued, sludge may transform into sludge balls and into gallstones thereafter. These appear on US as echogenic masses within the gallbladder and acoustic shadowing is not the rule due to the soft nature of the balls. The sludge balls or gallstones may eventually migrate and induce (transient) biliary obstruction (Fig. 4.7b). Treatment will be conservative in most cases [25].
Fig. 4.7
Biliary tract obstruction by sludge in a premature under total PN displayed on US. (a) Sludge within the gallbladder. Sagittal scan of the liver and the gallbladder displaying echogenic sludge. (b) Sludge within the distended common bile duct (arrows). Sagittal scan through the bile duct and portal vein. Echogenic sludge is obstructing the common bile duct. The treatment was conservative and the dilatation resumed on follow-up
4.3.2 Acute Cholecystitis and Other Biliary Anomalies
Acute neonatal acalculous and calculus cholecystitis are uncommon events in neonates and premature infants, and their prevalence is unknown. Prematurity itself, some antibiotics, ischemia, and sepsis are favoring factors. On US, the gallbladder appears enlarged and non-depressible; its wall may appear thickened and edematous with fluid in the peri-vesicular space (Fig. 4.8). The differential diagnosis should include heart failure that causes a transient non-inflammatory wall thickening.
