Neonatal gastrointestinal imaging

European Journal of Radiology 60 (2006) 171–186

Neonatal gastrointestinal imaging Padma Rao ∗ Department of Radiology, Royal Children’s Hospital and the University of Melbourne, Flemington Road, Parkville, Melbourne, Vic. 3052, Australia Received 10 July 2006; received in revised form 10 July 2006; accepted 12 July 2006

Abstract Radiological imaging is an important part of the evaluation and management of neonates with suspected anomalies of the gastrointestinal tract. Clinical presentation is often non-specific, commonly with abdominal distension and vomiting for which the underlying cause may or may not be clinically apparent. In a proportion of patients, the clinical assessment alone may suffice in providing the diagnosis and no further imaging is necessary. The reader must have an understanding of the normal radiographic appearances of the gastrointestinal tract in neonates and appreciate normal variants and differences to adults. In certain cases, the abdominal radiograph alone is diagnostic. In others, sonography and contrast studies are useful adjunct investigations and the indications for CT and MRI are few, but specific. Appropriate radiological investigation will help to establish the diagnosis and guide surgical intervention whilst also avoiding unnecessary radiation. Some of the conditions require transfer to specialist paediatric institutions for care. Thus, in some circumstances it is appropriate for imaging to be delayed and performed at the specialist centre with early referral often essential for the continued well being of the child. © 2006 Elsevier Ireland Ltd. All rights reserved. Keywords: Neonate; Congenital disorders; Gastrointestinal tract; Imaging studies

1. Introduction Imaging plays an important role in the diagnosis and management of gastrointestinal (GI) disorders in both full term and preterm neonates. Imaging serves to help direct management, establish a diagnosis and look for associated anomalies. The type of imaging selected depends not only on the clinical scenario but also on a desire to minimise unnecessary radiation exposure in small babies. Clinical presentation in neonates is often non-specific. Common presentations include abdominal distension and vomiting, which may, for example, be present in mechanical obstruction, sepsis or necrotising enterocolitis (NEC). Thus, two babies may present with the same symptoms and signs but have different underlying pathology. The initial radiological investigation is usually the plain abdominal radiograph (aXR), and in some conditions ultrasound (US). Knowledge of the general principles of aXR interpretation in the neonate is essential. This article serves to highlight some common neonatal GI disorders that the radiologist may encounter and to help guide appropriate investigations to elucidate the cause. The ∗

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rarer, more esoteric conditions are beyond the scope of this article. 2. Obstruction In the normal term neonate air enters the stomach soon after the first breath and proceeds into the proximal small intestine within minutes. It is seen in the distal small bowel by 3 h, the caecum at 6 h and the rectum by 24 h. The bowel gas pattern in normal neonates differs from older children in that the differentiation into the typical appearances of small and large bowel has not yet occurred making it difficult to accurately determine the level of obstruction. Causes of neonatal obstruction can be broadly categorised into high GI and low GI. High GI includes obstruction to the level of, and including the proximal jejunum and the diagnosis can often be made by aXR alone. Presentation is usually with vomiting which is bilious if the obstruction is distal to the ampulla of Vater. Distal GI obstruction includes those from the mid–distal jejunum to the anus, produces less classical radiographic appearances, and usually requires further radiological investigations before a diagnosis can be made. These neonates may present also with abdominal distension and vomiting, but failure to pass meconium is the key to the diagnosis. Two conditions that mimic obstruction are paralytic ileus and

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infants post resuscitation. Paralytic ileus tends to present with uniform dilatation of the bowel loops to the level of the rectum. Post resuscitation, the bowel loops are distended with gas only and thus air fluid levels are absent. In mechanical obstruction, there is variation in the calibre of the bowel loops with dilatation of the bowel proximal to and collapsed bowel distal to the obstruction. Investigation of the neonate with suspected obstruction usually involves chest and aXR and contrast studies. US can be very useful such as to confirm hypertrophic pyloric stenosis and duplication, mesenteric, omental and choledochal cysts. 2.1. Oesophageal atresia and tracheooesophageal fistula This is a common condition occurring in approximately 2.5 per 10,000 live births. The incidence in Caucasians is double that in the non-white population, and is increased in the offspring of a parent who had tracheo-oeophageal fistula (TOF) as well as in siblings, especially twins [1,2]. The classification of oesophageal atresia (OA) and TOF is based on their anatomic and radiographic appearance (Fig. 1). The fistula usually presents above the carina [3]. Clinical presentation is early after birth with cyanosis, respiratory difficulty, excessive oral secretions and drooling. The diagnosis may be suspected on antenatal US in the presence of maternal polyhydramnios, absence of the stomach bubble and a distended fluid filled proximal oesophageal pouch. Post-

natal chest radiograph may demonstrate the distended air filled oesophageal pouch and a nasogastric tube sited abnormally high. The aXR demonstrates a completely gasless abdomen in the absence of a distal fistula, but if a fistula is present varying amounts of abdominal gas may be present. It is important for the surgeon to know the position of the aortic arch. The site and number of fistulae present can be identified via fluoroscopic upper GI contrast study using non-ionic water soluble contrast. The H-type fistula usually runs an upwardly oblique course (Fig. 2) and is frequently only confirmed in the prone position. In the case of suspected OA alone without associated fistula, positive contrast is not recommended due to the high possibility of aspiration. Negative contrast using air alone is preferred. US has been utilised in the diagnosis and evaluation of OA and TOF [4]. The blind upper oesophageal pouch is well seen in OA. In OA with isolated TOF, detection of air bubbles in the soft tissues between the trachea and oesophagus or ascending in the oesophagus confirms the fistula. Post-operative complications include anastamotic stricture, which is more common than anastamotic leak (15%) or recurrent fistula (3–14%). Other rarer complications include vocal cord dysfunction, gastro-oesophageal reflux and peptic oesophagitis, tracheomalacia, oesophageal dysmotility and failure to thrive. Approximately 50% of patients with OA and TOF have additional anomalies which account for the major cause of mortality and which require further more dedicated imaging [5];

Fig. 1. Classification of oesophageal atresia and tracheooesophageal fistula.

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Fig. 3. US upper abdomen/pylorus in a 3-week-old neonate who presented with a 4 day history of vomiting. There are classical US features of pyloric stenosis. x–x demarcates the pyloric canal. y–y demarcates the pyloric muscle.

Fig. 2. Upper GI contrast study in a 1-day-old neonate with oesophageal atresia. The tip of the nasogastric tube lies in the proximal oesophageal pouch. Proximal fistula (A) passes obliquely upwards from proximal oesophageal pouch to trachea. Distal fistula (B) passes caudally from trachea to distal oesophagus.

in 15–30% VACTERL syndrome is present [2]. Other associations include Down syndrome, trisomy 18, CHARGE syndrome, hypertrophic pyloric stenosis, malrotation, Meckel’s diverticulum, pulmonary hypoplasia and agenesis and congenital stenosis of the more distal oesophagus. 2.2. Gastric outlet obstruction Hypertrophic pyloric stenosis (HPS) was first described by Hirschsprung in 1888. A genetic component exists especially through the maternal line and postnatal factors such as seasonal variations and smoking also play a part [6] as may impaired neuronal nitric oxide synthase synthesis in the myenteric plexus [7]. Pyloric tumours have been detected on antenatal imaging, both US and MRI [8,9]. Clinically, the baby usually presents with non-bilious vomiting after feeds that rapidly become projectile in nature. With time, the baby loses weight and becomes dehydrated. A pyloric mass or “tumour” is felt along with visible peristalsis. Classical cases do not require further imaging. The aXR, typically demonstrates a distended gastric air bubble. However, in the presence of vomiting or a nasogastric tube, the

stomach may be deflated. In an atypical age group or where the clinical findings do not confirm the diagnosis, US can help diagnose pyloric stenosis (Fig. 3). US criteria applied to infants of 6 weeks and older include: muscle thickness >3 mm, pyloric channel length >14 mm, pyloric thickness (serosa to serosa) >10 mm, failure of the pylorus to open with pyloric elongation and displacement, as well as retrograde or hyperperistaltic gastric contractions. A pyloric ratio, which is the ratio of the wall thickness to the pyloric diameter, above 0.27 is stated to be 96% sensitive for the diagnosis [10]. The standard measurements above are not always applicable to neonates in whom real time assessment to look for passage of fluid from the stomach into the duodenum becomes more important. Gastric atresia is very rare. There may be a complete atresia with no connection between the oesophagus and duodenum, or complete atresia with a fibrous band connecting the atretic ends. The third type is of a gastric membrane or diaphragm which may perforate thus resulting in incomplete obstruction [11]. On upper GI contrast study, congenital antropyloric webs are evident as linear filling defects resulting in a “pseudo double bulb” appearance whereby the barium outlines the space between the antrum and pylorus before the duodenal bulb [12]. If the stomach is filled with clear fluid the membrane can be detected on US. 2.3. Duodenal obstruction Duodenal obstruction may be broadly categorised into intrinsic and extrinsic causes (Table 1). Duodenal atresia results from a failure of recanalisation of the gut after the 6th week of gestation [13]. Incidence is approximately 1 in 3400 live births. In 65%, the atresia occurs just distal to the ampulla of Vater. Thus, the usual presentation is with bile stained vomiting, occasionally with jaundice and haematemesis. Associated anomalies are common in duodenal atresia occurring in 80%. Twenty to 25% have congenital heart disease and 30% have Down syndrome. Ten percent have oesophageal atresia and malrotation is present in 20–40%. In 45%, the neonates

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Table 1 Causes of duodenal obstruction Intrinsic Duodenal atresia Duodenal stenosis Duodenal web/diaphragm/windsock deformity Extrinsic Ladd’s bands resulting from midgut volvulus Midgut volvulus complicating malrotation Annular pancreas Preduodenal portal vein Duodenal duplication Duodenal haematoma

are premature. Annular pancreas is present in 20–40% with the obstructing element being the duodenal atresia not the annular pancreas [14]. If the obstruction is due to an intraluminal membrane the child does not always present in the neonatal period. Over time, they undergo stretching and eventually present as an intraluminal diverticulum (windsock duodenum). The diagnosis may be made on antenatal US with the double bubble of the dilated stomach and duodenum evident; there is associated polyhydramnios in 50%. Postnatally, the aXR is often diagnostic with a classical “double bubble” sign and no distal air (Fig. 4), but may be gasless if vomiting has occurred. Contrast studies

Fig. 4. Abdominal radiograph in a 2-day-old neonate with duodenal atresia demonstrating a markedly dilated stomach and duodenal bulb giving the classical “double bubble” appearance.

are usually unnecessary as the level of obstruction is readily outlined by air acting as negative contrast; however, in delayed presentation contrast studies are indicated to exclude midgut volvulus. In duodenal stenosis, a small amount of air or contrast is evident distal to the stenotic segment. Rarely, gas can be seen more distally in the small intestine in complete atresia where a Y-shaped bile duct inserts both proximal and distal to the atresia [15]. The preduodenal portal vein (persistent left vitelline vein) is a rare condition whereby the portal vein lies in an abnormal position anterior to the duodenum and causes compression. It results from persistence of the left/inferior vitelline vein due to derangement of normal situs asymmetry [16]. In over 85% of patients, the primary obstruction is due to an associated obstructing duodenal lesion such as an intraluminal membrane or web and not to the abnormal position of the vein [16]. Malrotation is a term that includes a spectrum of anomalies of intestinal rotation and mesenteric fixation ranging from complete non-rotation to the classical malrotation and reverse rotation. It can occur as an isolated anomaly or in association with conditions such as diaphragmatic hernia, gastroschisis and omphalocele. Other recognised associations of malrotation include duodenal atresia or stenosis, omphalocele, Meckel’s diverticulum, polysplenia, asplenia and situs ambiguous. There is also an increased incidence of renal anomalies. The commonest type is incomplete rotation where the arrest of rotation occurs at 180◦ . This results in abnormal shortening of the mesenteric root which predisposes to twisting or volvulus. When this occurs, the duodeno-jejunal (DJ) flexure is located to the right of the midline or anterior to the superior mesenteric artery (SMA), there is no ligament of Treitz and the jejunum descends to the right of the midline [17]. Peritoneal bands, (Ladds bands), may develop as an attempt to fix the malpositioned high riding caecum to the posterior abdominal wall beneath the liver and are associated with further more proximal bands between the duodenum and jejunum compressing and kinking the DJ flexure. If volvulus occurs, ischaemia and infarction of the bowel supplied by the SMA can result. Midgut volvulus is a clinical emergency which, if not diagnosed and treated, can result in gut necrosis and death. Presentation is usually early in life, but is delayed in 15–20% or asymptomatic and discovered incidentally in 10%. Clinically, the child presents shocked with abdominal distension, bilious vomiting and blood stained stools. The aXR may be normal or even gasless particularly if vomiting has occurred, or it may show signs of duodenal obstruction. Ischaemia induced by volvulus may result in bowel wall thickening and pneumatosis, often associated with distal bowel dilatation and ascites [14]. Duodenal obstruction or a sick, unstable neonate presenting with bilious vomiting after the immediate postnatal period should be assumed to be due to midgut volvulus unless proven otherwise. In most centres, upper GI contrast studies are still performed to confirm malrotation and midgut volvulus. Water-soluble nonionic contrast medium (300 mg/ml) is preferred but barium is still acceptable. The normal duodenum is a retroperitoneal struc-

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Fig. 5. (a) Upper GI contrast study in a 1-day-old neonate with bilious vomiting demonstrating malrotation with the duodenum and jejunum descending on the right and the classical “cork screw” appearance of contrast in the duodenum in midgut volvulus. There is dilatation of the more proximal duodenum due to relative obstruction caused by the twist. (b) US study in a neonate presenting acutely with abdominal distension and bilious vomiting demonstrating the “whirlpool sign” of midgut volvulus. Courtesy of M. Riccabona, Graz, Austria.

ture and on the right lateral view courses posteriorly giving a reverse ‘C’ shape [18]. When supine the duodenum normally crosses the midline and ascends so that the DJ flexure fixes to the left of the spine at the same level as the pylorus. If malrotated, the proximal duodenum courses abnormally anteriorly and the duodenum and proximal jejunum descend on the right of the midline. In midgut volvulus, the duodenum may be partially or completely obstructed, in the latter with a “beaked” tapering of the obstructed duodenum. In intermittent obstruction, which is more common, contrast enters the jejunum giving the characteristic “corkscrew” appearance due to the clockwise twisting around the SMA (Fig. 5a). US is being increasingly used in the investigation of suspected midgut volvulus. US findings in malrotation include reversal of the normal relationship of the SMA and SMV. The SMA lies to the right of the SMV, and in midgut volvulus the SMV and its mesentery are seen to rotate clockwise around the artery, the “whirlpool sign” [19,20] (Fig. 5b). Associated findings include a distended, hyperperistaltic proximal duodenum with tapering anterior to the spine, peritoneal fluid and oedematous bowel loops. Midgut volvulus is a surgical emergency and prompt surgical referral is of utmost importance. US is not the primary imaging tool to assess for malrotation alone. If the route of the fluid filled duodenum and jejunum can be followed across the midline and the superior mesenteric vessels are normally sited, this would suggest normal gut rotation. 2.4. Omphalocele (exomphalos) and gastroschisisis Both conditions are detected on antenatal US and both need to be managed in tertiary specialist paediatric centres. Postnatally, imaging aids in the detection of associated abnormalities and post-operative complications, mainly relying on US and GI contrast studies [21].

2.5. Small bowel atresia and stenosis Atresia of the small intestine often occurs as an isolated anomaly or can be associated with other atresias; stenosis is less common than complete atresia. The acquired forms are preceded by a prenatal intrauterine ischaemic episode. There are four types of atresia (Fig. 6). Jejunoileal atresia is the commonest cause of neonatal small bowel obstruction. The incidence is about 1 in 750 live births. There is a high association with prematurity and gastroschisis [22]. Two familial forms of atresia are recognised. One is a variant of type 3, also known as “apple peel” or “Christmas tree” atresia [23]. This form is associated with prematurity, biliary atresia, pelviureteric junction obstruction and imperforate anus. The second familial form, usually of type 1 or 2, are multiple atresias with intraluminal calcifications which can occur anywhere in the GI tract. The insult usually occurs during the first trimester and thus is associated with biliary dilatation and congenital heart disease. Approximately, 30% involve the proximal jejunum, 20% the distal jejunum, 15% the proximal ileum and 35% the distal ileum. Atresia can occur at multiple sites, involve both the jejunum and ileum, and be associated with colonic atresia [22]. Antenatal US may suggest the diagnosis in the presence of dilated fluid filled loops of bowel and polyhydramnios but findings at this time are non-specific. Postnatal clinical presentation is commonly with bilious vomiting if the atresia is proximal, and abdominal distension and failure to pass meconium with the more distal atresias. However, meconium may still be passed if the atresia is in the jejunum and occurred late in intrauterine life. aXR demonstrates small bowel obstruction. A few loops in the left upper quadrant suggest a high jejunal atresia, the “triple bubble” sign, whereas, a low ileal atresia usually results in more numerous uniformly dilated loops. Large almost cystic appearing dilated areas are either due to grossly distended small

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Fig. 6. Classification of small bowel atresia.

intestine proximal to the atresia or a pseudocyst associated with localised perforation (Fig. 7). With the more distal atresias, the foetal colon does not receive sufficient small intestine contents to assume and maintain its normal calibre. At birth, the colon is non-used, narrow and non-distensible, a microcolon (Fig. 8). Microcolons are also associated with meconium ileus, colonic atresia and in 30% of patients with total colonic aganglionosis. Fluoroscopic contrast enema or US guided saline enema demonstrate the microcolon and if reflux into the small bowel occurs, may demonstrate the level of the atresia. Perforation in utero occurs in 10–15% of low atresia and results in meconium peritonitis evident on the aXR as speckled peritoneal calcification; if a patent processus is present, scrotal calcification can occur. 2.6. Abdominal cystic lesions These are frequently detected postnatally when investigating for abdominal distension or obstruction. The diagnosis is usually made with US. The main differentials in the neonatal period include duplication cysts, mesenteric and omental cysts, lymphangiomas and, in females, ovarian cysts. Intestinal duplication cysts usually occur during early second trimester or late first trimester from abnormal canalisation of the bowel. The most common location is around the terminal ileum and ileo-caecal valve, followed by the oesophagus, duodenum and stomach. Duplication cysts contain both mucosal and

muscle layers. The thickness of the cyst wall is the same as the calibre of normal bowel wall. Enteric duplications are usually spherical, localised masses and do not communicate with the bowel lumen. However, they can be tubular and run parallel to the bowel, and this type is more likely to communicate with the lumen. They usually occur along the mesenteric border of the intestine and share a common blood supply. The more common presentations are with obstruction and abdominal distension, but pain, perforation, ulceration, haemorrhage, volvulus and respiratory distress can all occur depending on the size and the location. Multiple duplication cysts are present in 20%. Distal ileal cysts may cause intussusception. Forty percent of enteric duplications present by one month of age and 85% are diagnosed within the first year of life [24]. The aXR may be normal or, if large enough, the cyst may cause mass effect with displacement of adjacent bowel loops. There may be features of obstruction or wall calcification. US clearly demonstrates abdominal duplication cysts which are anechoic unless complicated by haemorrhage or infection or inspissated mucoid material [25]. The wall demonstrates an inner echogenic line of mucosa and an outer hypoechoic muscle layer, the “bowel wall signature” (Fig. 9). Peristalsis of the cyst wall may occur. Further imaging after US is rarely necessary with surgical intervention being the next step. Oesophageal duplication cysts may occur as isolated entities or in combination with other bronchopulmonary foregut anomalies. On imaging they can look identical to a bronchogenic

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Fig. 9. Two-week-old neonate presenting with abdominal distension and vomiting. Ultrasound of the abdomen demonstrates a well defined anechoic cyst containing mobile particulate matte. The wall of the cyst demonstrates an inner echogenic layer of mucosa and an outer hypoechoic layer (arrow)—the signature sign of a duplication cyst.

Fig. 7. Chest and abdominal radiographs in a 2-day-old neonate with oesophageal atresia and jejunal atresia. Markedly dilated small bowel loops are consistent with a jejunal atresia. Gas present within the stomach and small bowel signifies the presence of an associated tracheooesophageal fistula.

Fig. 8. Lower GI contrast study in a 3-day-old neonate with ileal atresia. Contrast via a rectal catheter outlines the small calibre microcolon (large arrow) and is seen to fill the entire colon and outline the appendix. Markedly dilated obstructed loops of small bowel exist proximal to this (arrow heads) confirmed at operation to be ileal atresia.

cyst, differing only in site and histology. Ten to 15% of all gastroenteric duplications are intrathoracic, located next to the oesophagus. They are often asymptomatic but may cause respiratory distress or dysphagia. The diagnosis is usually made on cross-sectional imaging (Fig. 10). They are cystic and avascular. Nuclear medicine Tc 99m pertechnetate confirms the presence of gastric mucosa. Gastric duplications are a much rarer entity. They typically arise along the greater curve of the stomach, often antral. They present with vomiting and bleeding leading to melena or haematemesis. The larger cysts usually result from abnormal separation of the endoderm and notochord and the smaller cysts from persistent vacuoles within the primitive foregut. Gastric duplications usually communicate with the lumen of the stomach. On US, the cyst is typically intramural and anechoic. Lymphangiomas, mesenteric and omental cysts are rare, forming a spectrum of disease, occurring in about one in 20,000 of the paediatric population [26]. Mesenteric cysts are four to five times more common than omental cysts. Cystic lym-

Fig. 10. Axial contrast enhanced CT through the upper chest demonstrating two well defined low density cystic structures in the posterior mediastinum. The larger cyst lying to the left of the aortic arch was confirmed to be a bronchogenic cyst. The smaller cyst in the subcarinal region is an oesophageal duplication cyst (arrow).

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phangiomas are histologically different from mesenteric cysts in that they have an endothelial lining, foam cells and thin walls that contain lymphatic spaces, lymphoid tissue and smooth muscle. Mesenteric cysts, however, lack smooth muscle and lymphatic spaces and the cells lining the cysts are cuboidal or columnar [27]. Mesenteric cysts are situated anywhere in the mesentery of the gut, most commonly in the small bowel mesentery (60%), and can extend into the retroperitoneum. Omental cysts are confined to the lesser or greater omentum [28]. Lymphangiomas are more diffuse and cross anatomical spaces. The ileal and colonic cysts contain serous fluid and the jejunal cysts chylous fluid. Presentation varies from being asymptomatic and found incidentally, to vague abdominal pain or to life threatening events from obstruction, volvulus, infarction, rupture and haemorrhage. On US, the cysts are fluid filled and anechoic with thin walls. Internal echoes imply complication from debris, haemorrhage or infection. Further cross sectional imaging to delineate extent has previously relied on CT, but nowadays, if needed, MRI would be the investigation of choice. Ovarian cysts are relatively common in the female neonate resulting from maternal hormonal stimulation. They are often very large at presentation and present remote to the pelvis making it difficult to confirm their ovarian origin. Haemorrhage into the cyst may occur. Serial US follows their resolution, sometimes US guided puncture may be suggested. 2.7. Meconium ileus This is a condition whereby there is distal intestinal obstruction due to inspissation and impaction of thick meconium in the distal ileum. It constitutes approximately 20% of neonatal intestinal obstruction in term infants, and is almost invariably associated with patients with cystic fibrosis. Conversely, 15% of cystic fibrosis neonates present with intestinal obstruction secondary to meconium ileus. Clinically, the neonate presents within the first day of life with abdominal distension, bilious vomiting and failure to pass meconium [29]. The aXR demonstrates gas filled loops of bowel consistent with a low gut obstruction. A “soap bubble” appearance is sometimes evident due to a mixture of air and meconium. Due to the viscosity of the meconium, air fluid levels are commonly absent [30]. Both antenatal and postnatal US demonstrate abnormal bowel dilatation and echogenic bowel contents. Conventional water soluble contrast enema under fluoroscopic guidance, or saline enema under US guidance are performed to demonstrate the level of obstruction and the unused microcolon. Contrast outlines the multiple filling defects in the terminal ileum due to the inspissated meconium plugs. The more proximal small bowel loops are dilated (Fig. 11). The contrast enema serves two purposes: diagnostic and therapeutic. The hyperosmolarity of conventional contrast medium serves to loosen up the plugs and aid their passage. If required, the procedure can be repeated the following day, so long as there is progressive clinical improvement as monitored by the passage of meconium and reduction in the degree of abdominal distension. An overall success rate of 60% has been reported and a perforation rate of

Fig. 11. Lower GI contrast study in a term neonate with presenting with failure to pass meconium and increasing abdominal distension. Contrast outines a small calibre colon and multiple filling defects in the terminal ileum due to inspissated meconium plugs (arrow). The proximal small bowel loops are dilated.

3–10%. If repeated enema is unsuccessful, surgical intervention is required. Complications of meconium ileus include meconium peritonitis from bowel perforation, and volvulus. A localised perforation can result in a “meconium pseudocyst”. If the perforation persists postnatally, pneumoperitoneum or ascites can result. 2.8. Colonic obstruction The main colonic pathologies encountered in the neonate resulting in obstruction are colonic atresia, anal atresia, Hirschsprungs disease and meconium plug syndrome. Neonatal intussusception can occur but it is extremely rare [31]. It is usually caused by a lead point such as a Meckel’s diverticulum, polyp or tumour. Colonic atresia occurs secondary to a vascular insult in utero. It occurs in approximately 1 in 40,000 live births and is less common than ileal atresia [2,32]. It may occur in isolation or be associated with a more proximal atresia. Clinically, it is often difficult to distinguish from ileal atresia presenting as low gastrointestinal obstruction with abdominal distension and failure to pass meconium. A microcolon exists distal to the atresia and contrast fails to pass from the microcolon into the proximal dilated colon. Colonic atresias are classified in much the same way as ileal atresias (see Fig. 7). Colonic atresia is associated with Hirschsprung’s, especially short segment disease. Meconium plug syndrome is a transient disorder of the neonatal colon characterised by delayed passage of meconium and proximal dilatation of the bowel. Distal obstruction is due to colonic dysmotility and associated with a large meconium plug in the rectosigmoid or more proximal colon. The colon itself is of normal calibre and can appear normal or distended proximal to, and of small calibre distal to the plug. The rectum is distensible. The aXR is non-specific demonstrating dilated gas filled loops of

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bowel with air fluid levels. There may be a soap bubble appearance of meconium in the collapsed left colon. Air fluid levels are often absent before 48 h of life. Contrast enema performed with water soluble non-ionic contrast medium is again both diagnostic and therapeutic. The colon contains a large filling defect due to the presence of a plug and a small left colon distally. Digital examination or passage of the catheter and contrast serve to precipitate plug passage resulting in relief of symptoms. If there is persistence of abdominal distension and/or failure to evacuate, a rectal biopsy is needed to exclude Hirschsprung’s disease. Small left colon syndrome is a subtype of meconium plug syndrome. The clinical presentation and outcomes are very similar to patients with meconium plug syndrome [33]. Approximately 50% of cases occur in association with maternal diabetes mellitius. Contrast enema demonstrates an apparent transition zone at the splenic flexure. There is a normal sized sigmoid colon but a small left (descending) colon mimicking a microcolon, which becomes a normal size again around the splenic flexure. Therefore, the abnormality is limited to the descending colon. Natural history of the disorder is that there is a gradual improvement in clinical and radiological findings within hours to days and once a normal bowel pattern is established, it remains normal. Hirschsprung’s disease is a disorder of the bowel resulting from absence of normal ganglion cells in the intermuscular (Auerbach’s) and submucosal (Meissner’s) plexuses. It is due to abnormal arrested neural crest migration. Aganglionosis is described to always affect the rectum and extend proximally in a continuous fashion for a variable distance. However, some authors have described the very rare condition of skip lesions in Hirschsprung’s [34]. Short segment disease is the most common accounting for 80–90% of cases and involves the distal sigmoid and rectum with the transition zone to normal bowel occurring in the rectosigmoid. Eighty percent of these cases are male. Long segment disease accounts for the remaining 10%. Down syndrome is said to occur in 6–16% of Hirschsprung’s cases. In this group of patients, the incidence of enterocolitis is increased and they have a worse prognosis for bowel continence post surgery [35]. Clinical suspicion of Hirschsprung’s should arise when there is failure to pass meconium in the first 24–48 h of life. The abdomen becomes distended and bile stained vomiting may occur. The spectrum of the disease is variable with some neonates severely affected and developing enterocolitis soon after birth. In others, the onset is more insidious resulting with difficulties with stooling. If the diagnosis is missed, in later life the child may develop severe chronic constipation with marked proximal bowel dilatation. The disease may be complicated by malabsorption and protein losing enteropathy. The aXR often has non-specific appearances, and the differential would include any cause of neonatal low bowel obstruction. A small gas filled rectum in the presence of marked proximal colonic dilatation is classical except in cases where prior digital examination has introduced rectal air. Colonic perforation leading to pneumoperitoneum complicates approximately 4% of infants affected usually in the long segment or total colonic disease. Definitive diagnosis is made by rectal biopsy using suction biopsy 2 cms above the dentate line. If ganglion cells are present, Hirschsprung’s disease is effectively 100% excluded, except for

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Fig. 12. Lower GI contrast study demonstrating long segment Hirschsprung’s disease. The rectum, sigmoid and distal descending colons are of small calibre. The transition zone (arrowed) is between the aganglionic distal segment and dilated proximal colon.

the rare case of zonal aganglionosis [34]. Contrast enema is the radiological investigation of choice, used not only to help confirm the diagnosis but also to delineate the level of the transition zone (Fig. 12). Care must be taken not to overfill and artificially distend the rectum and sigmoid colons thus masking the transition zone. Classical signs of Hirschsprung’s disease on contrast enema include: small, irregular, non-distensible rectum; reversal of the rectosigmoid ratio; detection of the transition zone (which is the junction between the normal sized distal aganglionic segment and the proximal dilated bowel), demonstrated in 65% of cases; note that the pathological transition zone is usually more proximal to the radiographic one [36]; irregular, uncoordinated contractions in the aganglionic segment seen in 20%; thickening and nodularity of the colonic mucosa proximal to the transition zone; and – in equivocal cases – the non-specific finding of retention of barium on delayed radiographs taken at 24 h post study. 2.9. Anorectal anomalies The classification of anorectal anomalies is complex and currently undergoing evaluation and change, some classifications emphasising the pure anatomy and others concentrating on the required surgical approach [37–39]. Historically, anorec-

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tal malformations have been subdivided into high (supralevator), intermediate or low (infralevator) as determined by the relationship of the distal rectal pouch to the pelvic floor formed by the puborectalis muscle. The incidence of anorectal malformations is approximately 1 in 5000 live births, with a male to female ratio of 6:4. Patients with high anorectal malformations have a greater risk of associated anomalies than those with low lesions. Female patients frequently have a rectovaginal fistula. If the fistula is large, meconium can pass per vagina with resultant decompression of the bowel. The vaginal and urethral orifices may be separate or single—the urogenital sinus abnormality where the urethra enters anteriorly and the bowel posteriorly. This is associated with obstruction of the vagina and subsequent hydrometrocolpos. In males, the fistula enters the prostatic urethra or the bladder. In low anorectal malformations, the bowel passes through the levator sling formed by the puborectalis muscle. Fistulae to the lower vagina, urethra or perineum anterior to the expected anal site can occur. There may be an obstructing membrane. Meconium may appear in the scrotum. There is a lower incidence of associated GU anomalies. In the intermediate category, the imperforate anus terminates at the level of the levator sling. The incidence of associated anomalies falls between that for high and low anorectal malformations. Associated lumbosacral and genitourinary anomalies are common and may occur in isolation or as part of the VACTERL spectrum. The main renal anomalies are horseshoe kidney, crossed fused ectopia, renal agenesis and renal hypoplasia. Fifteen percent of patients have associated cardiovascular anomalies, frequently ventricular septal defects. Imaging of anorectal malformations serves to identify the lesion itself, any direct complications and the more distant associations. aXRs demonstrate distal bowel obstruction +/− calcified intraluminal meconium resulting from the mixing of urine and meconium. Gas present within the bladder or vagina signify the presence of an associated fistula. Various radiographic methods have been devised to determine the position of the terminal colon including the invertogram, the prone cross table lateral, and assessing the position of the terminal colon to certain bony landmarks [40–42]. Each are fraught with inaccuracies. Several studies have suggested US to determine the position of the terminal colon by measuring the distance between the anal dimple and the terminal colon [43]. The true distance can be altered if too much pressure is applied whilst scanning, and in the presence of a large fistula the colon may decompress and be difficult to visualise. The infracoccygeal approach to US of the perineum can estimate the rectal pouch-perineal distance and is useful in determining the position of the terminal colon relative to the levator sling. A distance of less than 1.5 cm indicates a low lesion, and a pouch that terminates above the base of the bladder indicates a high lesion [44]. US measurements are also subject to inaccuracies due to movement between the atretic bowel and pelvic floor. More recently anal endosonography has been described as a technique for assessing anorectal malformations post repair, providing an alternative approach to MRI [45]. In reality, however, a thorough clinical examination by an experienced specialist along with contrast studies form the mainstay of the evaluation of a neonate with an anorectal malformation.

Fig. 13. Micturating cystourethrogram in a male neonate during the voiding phase demonstrating the presence of a low rectourethral fistula (arrow).

Contrast studies include a micturating cystourethrogram (MCUG) to assess for fistulae between the bladder and bowel and confirm associated vesico-ureteric reflux. In females, water soluble contrast placed in the vagina may aid demonstration of the fistula as may contrast placed into the rectum if present. However, both the latter are “low pressure” systems compared with the bladder, and the MCUG has been found to give the highest yield (Fig. 13). Imaging of the spinal and renal anomalies has historically been carried out with plain radiographs and US. Nowadays, with the newer high field strength magnets, MRI is playing an increasing role as it can detect both spinal and genitourinary anomalies. In addition, MRI is the optimum technique for demonstrating the pelvic floor musculature. It can accurately define the relationship of the bowel to the levator sling [46]. In low anorectal malformations, the sphincter muscle complex (puborectalis and the external anal sphincter) is well developed. In intermediate or high malformations, development of one or both components of the sphincter muscle complex may be deficient and this has an important impact on post operative bowel continence. CT invertograms have been performed to evaluate the relationship of the colon to the levator sling, although given the high radiation dose we do not recommend this procedure. 3. Necrotising enterocolitis The term NEC is generally used to describe the often severe enterocolitis that occurs in premature babies. The incidence varies between 1 and 3 cases per 1000 live births. The aetiology remains uncertain, but its development has been strongly associated with the presence of hypoxia, infection, intensive treatment,

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hyperosmolar and enteric feeds, decreased mucus production and gut motility and the poor immune response of the premature infant, all of which may contribute to the breakdown of the intestinal mucosal barrier. The vast majority of cases of NEC occur in premature infants weighing less than 2000 g, but it has been known to affect stressed, sick term babies [47]. Pathologically, there is inflammation of the intestine which begins in the mucosa and extends transmurally. The disease usually affects the distal ileum and proximal colon first, and involvement may be patchy or diffuse and continuous. The age of onset is usually within the first two weeks of life, although in premature babies onset may be delayed. Clinical presentation is varied and often non-specific; symptoms include abdominal distension, feed intolerance, vomiting, bile stained aspirates, diarrhoea and bloody stools. Mortality rate in untreated cases is high ranging from 20% to 40%. Radiology is used to confirm suspected cases, check for complications of NEC and to monitor the course of the disease [48]. Serial aXR is the initial investigation. US including Doppler can also be used to assess SMA perfusion, search for free air, and assess bowel wall thickness, structure and vascularity. Early NEC cases demonstrate symmetrical loss of bowel gas pattern with non-specific gaseous distension with increasing separation of bowel loops. Later, more florid signs include pneumatosis, portal venous gas and pneumoperitoneum. Pneumatosis intestinalis has been said to be pathognomic of NEC in premature babies. It may be cystic (submucosal) or linear (subserosal)

Fig. 15. Abdominal radiograph in a premature sick neonate demonstrates the classical “football sign” of a large pneumoperitoneum. Air outlines the falciform ligament (arrows).

Fig. 14. Abdominal radiograph of a premature baby presenting with increasing abdominal distension. Multiple gas filled dilated loops of bowel are present. Curvilinear lucencies consistent with subserosal pneumatosis inestinalis parallel the bowel (arrow). Faint branching lucencies evident in the right upper quadrant in the liver consistent with associated portal venous gas.

(Fig. 14). The cystic pneumatosis may be difficult to differentiate from meconium mixed with air, although a bubbly stool pattern is rare within the first few weeks of life. Pneumatosis is commonest in the distal ileum and proximal colon. There is poor correlation between the extent of pneumatosis and disease severity [48]. Bowel affected by NEC is prone to perforation. If large, this may be evident on the supine radiograph (Fig. 15). However, a cross table lateral is a sensitive method to detect small amounts of free gas. The signs of pnemoperitoneum are the same whatever the cause. The presence of perforation has been said to be an indication for surgery. However, only 60% of patients with surgically proven pneumoperitoneum demonstrate radiologically detectable free gas. Another so-called pathognomic sign of NEC is portal venous gas (Fig. 14). The incidence of portal venous gas varies between 10% and 30% and often occurs transiently. It occurs following dissection of intramural pneumatosis into the lymphatics to the mesenteric venous axis. It is evident on the aXR as linear branching radiolucencies extending peripherally from the porta hepatis, and is sometimes more evident on a cross table lateral view. On US, portal venous gas is evident as echogenic mobile foci within the portal vein causing spiky Doppler changes. Although considered a bad prognostic sign,

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portal venous gas is not invariably associated with a fatal outcome, and may persist radiologically after clinical improvement. Ascites is a further sign of perforation or impending perforation. Detection of ascites on aXR is difficult and US is the preferred method for detecting small amounts of free fluid. The “persistent loop” sign is thought to be a marker for advanced disease. This sign refers to a dilated loop of bowel that remains unchanged in appearance over 24–36 h. Contrast studies may be performed to evaluate for strictures as a delayed complication of NEC. Strictures may be single or multiple and they occur in approximately 20% of patients whether treated medically or surgically. The commonest site is in the descending colon and splenic flexure. NEC strictures have been known to resolve spontaneously, particularly if they occur soon after the onset of acute NEC [49]. Usual treatment is surgical but there have been attempts to dilate the strictures with angioplasty balloon catheters post proximal bowel diversion. Contrast studies are also used to evaluate the distal defunctionalised colon post diversion surgery with ileostomy or colostomy, prior to reanastamosis. Further complications of NEC include lymphoid hyperplasia, enteroenteric fistulae, adhesions, malabsorption and enterocysts in children with multiple strictures which refers to a stagnant loop between two strictures. 4. Miscellaneous conditions Several conditions of the liver and spleen present because the child is symptomatic or because they form part of a more widespread syndrome; some important entities are listed below. 4.1. Patent ductus venosus The ductus venosus is present in utero. It usually closes within the first few days after birth but in neonates with congenital heart disease or sick neonates, it may remain patent. The normal mechanism of closure is by intraluminal connective tissue deposition which becomes evident on US as an illdefined area of increased echogenicity with detectable flow on Doppler US. 4.2. Portal vein anomalies These may be symptomatic or discovered incidentally during investigations for other conditions. A congenital intrahepatic portohepatic venous shunt is an abnormal communication between a branch of the portal vein and a hepatic vein. Most undergo spontaneous closure at around 2–3 years of life. The congenital portocaval fistula is also known as congenital absence of the portal vein because the intrahepatic portal branches are not visible [50,51]. A type 1 shunt is a congenital absence of the portal vein with complete diversion of the portal blood into the inferior vena cava. In type 2, the portal vein is present and intact but portal blood diverts through a side to side extrahepatic shunt into the IVC. The “Abernethy malformation” refers to the congenital diversion of portal blood away from the liver by either mechanism [51]. It may occur in isolation but, in females, is frequently associated with other congenital conditions such as biliary atresia and cardiac anomalies. The

connection between the portal vein and IVC may be intrahepatic or extrahepatic and is occasionally via the ductus venosus. As a result, portal venous blood bypasses the liver resulting in metabolic abnormalities producing a combination of symptoms and signs of both liver disease and pulmonary disease [52]. Congenital arterioportal fistulae usually present acutely outside the neonatal period with anaemia, ascites, gastrointestinal bleeding, heart failure or diarrhoea. The abnormal vascular connections are usually well demonstrated on US. Further imaging is not usually required. Premature or sick neonates frequently have umbilical venous and arterial catheters in situ. An umbilical venous catheter left in situ over an extended period of time predisposes to left portal vein thrombosis. In most cases, the clots resolve without clinical sequelae and the portal vein recanalises. However, in the long term, this may be evident as an ill-defined area of calcification both on US and plain radiography. 4.3. Splenic anomalies Splenic anomalies are often asymptomatic and thus not detected unless investigated for other pathology. They may be detected in the neonatal period when they form part of the heterotaxy spectrum, with either asplenia or polysplenia. Three important clinical associations are the increased risk of congenital heart disease, immunodeficiency and the increased risk of malrotation with midgut volvulus. Other anomalies associated with polysplenia include a preduodenal portal vein, bilateral left sidedness of the lungs and bronchi and azygos continuation of the IVC. Absence of the gallbladder and biliary atresia are also associated. The congenital heart disease is usually of the noncyanotic type with left to right shunts. However, in asplenia, the congenital heart disease is usually more complex and cyanotic. Other splenic anomalies, such as accessory and wandering spleens do not usually declare themselves until later childhood if at all. 4.4. Biliary tract abnormalities Biliary tract abnormalities in the neonate usually present with pain and jaundice. Jaundice is a common occurrence in the newborn, found in about 60% of term infants and a greater proportion of premature. The aetiology is varied (Table 2), but prolonged jaundice that persists beyond 4 weeks of age is due to biliary atresia or neonatal hepatitis in most cases [53]. Biliary atresia is the commonest cause of neonatal cholestasis and accounts for about 50% of all cases and over 90% of the extrahepatic causes. It may be focal, intrahepatic or extrahepatic with obliteration of varying parts of the biliary tree secondary to acquired progressive inflammation. Eight different anatomical types of biliary atresia have been described (Fig. 16). Biliary atresia may occur as an isolated entity or be part of the “noncardiac polysplenia syndrome” [53,54]. The aetiology of neonatal hepatitis is varied. It is commonly associated with viruses such as hepatitis B or cytomegalovirus, and is associated with various syndromes and metabolic disorders. Mechanical obstruction of the common bile duct by inspissated secretions or a bile plug has been described in neonates on

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Fig. 16. Classification of the anatomical types of biliary atresia.

total parenteral nutrition, premature, infection, intestinal abnormalities and in Rhesus and ABO incompatibility. If persistent, surgical intervention is required. Choledochal cysts are congenital dilatations of the extrahepatic bile ducts and present variably from birth to old age. They are four times more common in females. Their aetiology is uncertain. It is also unknown as to whether those occurring in the neonatal period have a different aetiology to those occurring in older children. There is a high association of choledochal cysts with biliary atresia. Five types of choledochal cysts have been described (Fig. 17). Type 5, or Caroli’s disease, is associated with autosomal recessive polycystic kidney disease and congenital hepatic fibrosis. Jaundice is often the first visible clinical sign. Blood, stool and urine tests help to determine whether the problem is obstructive (cholestatic) or non-obstructive. US is usually the initial imaging procedure in the evaluation of a patient with neonatal jaundice [55]. The patient should be adequately fasted for a period of at least 4 h and a high frequency or linear probe used. US often demonstrates non-specific findings but is diagnostic in duplication cyst, choledochal cyst and Caroli’s disease (Fig. 18).

A diagnosis of biliary atresia cannot usually be made with US alone. Although visualisation of a normal sized gallbladder has been said to favour neonatal hepatitis, 20% of patients with biliary atresia have a normal sized gallbladder which also empties after a feed. However, in the presence of a suggestive clinical picture, an absent or small gallbladder in the fasting state, a gallbladder with irregular and echogenic walls or a large gallbladder that does not empty post feed are highly suggestive of biliary atresia. The “triangular cord sign” corresponds to the fibrous remnant of the obliterated biliary ducts [56]. It is evident as a triangular or tubular echogenic density at the porta hepatis and immediately cranial to the portal vein bifurcation. It has been quoted as being a very sensitive and specific indicator of biliary atresia. However, the sign is often difficult to demonstrate and has been said to be present in other causes of neonatal liver fibrosis. US is also valuable in assessing for associated anomalies and to make an overall assessment of hepatic vascularity. Nuclear medicine scintigraphy with 99m-Technetium EHIDA should be performed in those suspected of having biliary atresia. Normally, the isotope is rapidly cleared from the blood

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Fig. 17. Classification of the types of choledochal cyst.

stream and binds to the biliary radicles. Hepatic excretion usually commences within 5 min and is normally visible in the biliary tree and intestines by 15 min. There is complete clearance from the liver by 40 min post injection. In early biliary atresia prior to cirrhosis, there is rapid extraction of radionuclide from the blood stream which persists and accumulates in the hepatic parenchyma with failure of excretion into the gut. The gallbladder is never visualised because the hepatic duct above the insertion of the cystic duct is never patent. Images taken 6 and 24 h post injection demonstrate increasingly dense liver activity, increased renal clearance of isotope and no activity in the gut. Thus, visualisation of isotope activity within the gut excludes the diagnosis of biliary atresia. In severe or late biliary atresia, hepatocyte function eventually deteriorates resulting in sluggish

tracer uptake by the hepatocytes. Patients with neonatal hepatitis often have decreased parenchymal extraction and clearance of radioisotope from the blood stream but tracer does reach the intestines. Cystic fibrosis, diarrhoeal illness and panhypopituitarism have been reported to cause false positive results. Conventional endoscopic retrograde cholangio-pancreatography (ERCP) is very rarely used to make the diagnosis of biliary atresia. It is invasive, requires general anaesthetic and is difficult to perform. Magnetic resonance cholangiopancreatography (MRCP), particularly with the newer high field strength magnets, is becoming a more reliable and available imaging tool to evaluate the hepatobiliary system [57,58]. Demonstration of normal major intrahepatic and extrahepatic biliary ducts and a gallbladder on heavily T2 weighted images excludes the diagno-

P. Rao / European Journal of Radiology 60 (2006) 171–186 Table 2 Causes of neonatal jaundice Bile duct abnormalities Extrahepatic

Choledochal cyst Duodenal duplication Cholelithiasis Perforation

Intra- and extrahepatic

Biliary atresia

Intrahepatic

Transient neonatal cholestasis Sclerosing cholangitis Alagilles syndrome Metabolic disorders, e.g. cystic fibrosis, alpha 1 antitrypsin def, galactosemia, tyrosinemia

Infections

Cytomegalovirus Bacterial sepsis Syphilis

Toxic

Drugs TPN

Miscellaneous

Bile plug syndrome Neonatal hepatitis Breast milk jaundice

Fig. 18. US of the upper abdomen in a neonate with a large choledochal cyst. There is marked cystic dilatation of the common bile duct (labelled).

sis of biliary atresia. In some neonates, liver biopsy and/or percutaneous/intraoperative cholangio-pancreatography is required for a definitive answer. Neonatal cholelithiasis is uncommon and usually associated with infants on total parenteral nutrition or who are stressed or dehydrated. Underlying predisposing factors such as haemolytic disease, cystic fibrosis or pancreatitis are extremely rare in this age group and are relatively more common in older children. 5. Summary This article covers the major and more common gastrointestinal problems occurring in the neonate. The reader must be familiar with the normal radiological appearances in the neonate and be aware of the differences to adults. Whilst imaging plays an

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