Enteric duplication cysts in children: varied presentations, varied imaging findings

Abstract Enteric duplication cysts (EDCs) are rare congenital malformations formed during the embryonic development of the digestive tract. They are usually detected prenatally or in the first years of life. The size, location, type, mucosal pattern and presence of complications produce a varied clinical presentation and different imaging findings. Ultrasonography (US) is the most used imaging method for diagnosis. Magnetic resonance (MR) and computed tomography (CT) are less frequently used, but can be helpful in cases of difficult surgical approach. Conservative surgery is the treatment of choice. Pathology confirms the intestinal origin of the cyst, showing a layer of smooth muscle in the wall and an epithelial lining inside, resembling some part of the gastrointestinal tract (GT). We review the different forms of presentation of the EDCs, showing both the typical and atypical imaging findings with the different imaging techniques. We correlate the imaging findings with the surgical results and the final pathological features. Teaching Points • EDCs are rare congenital anomalies from the digestive tract with uncertain pathogenesis. • More frequently, diagnosis is antenatal, with most EDCs occurring in the distal ileum. • Ultrasonography is the method of choice for diagnosis of EDCs. • Complicated EDCs can show atypical imaging findings. • Surgery is necessary to avoid complications.

EDCs are believed to occur between the 4th and 8th weeks of embryonic development. Their aetiology is still unknown; several theories have been proposed to explain their pathophysiology, but no single hypothesis can justify all duplications, locations and associated anomalies. Split notochord theory is often postulated [8]. The luminal recanalisation theory explains duplications in those portions of the GT that have a solid stage, including the oesophagus, small bowel and colon; nevertheless, it does not explain duplications at other levels. Incomplete or partial twinning theory could explain the colorectal duplications that are associated with duplication of genital and urinary structures. Persistent embryonic diverticula theory suggests that small diverticula, usually transient along the antimesenteric border of the intestinal wall, persist and develop intestinal duplications, although most ECDs are in the mesenteric border. The intrauterine vascular accident theory suggests that gastrointestinal duplications arise from an intrauterine vascular accident during early fetal development and may be a valid explanation for isolated duplication. These different theories lead to think that the origin of EDCs can be multifactorial [1,2,4,9,10].
Associated anomalies such as spinal defects, cardiac or urinary malformations, are reported with an incidence rate of 16-26%. Other digestive anomalies are present in about 10% of cases. Therefore, once an EDC is found, a search for other anomalies is needed [6,[10][11][12].
EDCs must have three characteristics: an epithelial lining containing the mucosa of the alimentary tract, an envelope of smooth muscle, and the cyst must be closely attached to the GT by sharing a common wall (Fig. 1). The mucosal lining does not always correlate with the adjacent gastrointestinal tissue, but the duplications are named according to the part of the GT to which these are intimately attached. Ectopic gastric mucosa is found in 20-30% of these cysts, more frequently in oesophageal and small bowel duplications [13,14]. Prominent gastric mucosa can also be seen as a polypoid mass covering the base of the cyst, being transmural ( Fig. 2) [6]. Ectopic pancreatic mucosa is most common in gastric duplications [2].
Structurally, EDCs can be either cystic or tubular. Spherical cysts are the most common duplications (80%) and typically do not communicate with the adjacent lumen. Tubular duplication cysts (20%) run parallel to the GT, being communicated with it ( Fig. 3) [4,12,15,16]. Then, when a duplication cyst is tubular, the connection with GT must be demonstrated for surgical planning [17].
Atypical EDC is a non-communicating isolated duplication cyst completely separated from the bowel with no communication or shared wall. A vascular insult could have led to the isolation. They are extremely rare [19,20], especially multiple isolated EDCs, which are even rarer [19].
The size, location, type, mucosal pattern and presence of complications produce different clinical presentations and several imaging findings of the EDCs. Ultrasonography (US) is the most used imaging method for diagnosis of abdominal EDCs. Magnetic resonance (MR) and computed tomography (CT) are utilised for oesophageal EDCs and for helping in difficult surgical approaches.

Clinical presentations
The intrauterine presentation is increasing, mostly due to the improvement in prenatal screening US, routine secondtrimester screening and improved imaging resolution. However, prenatal diagnosis of EDCs is often difficult, and US identifies only 20-30% of them, and sometimes they are discovered by chance (Fig. 5) [21,22].
The natural history of EDCs is quite variable. The clinical presentation or onset symptoms of these malformations range from infancy and early childhood to adulthood. Almost 70% of EDCs present symptoms within the first year of life and 85% in the second one [3,10,14].
The signs and symptoms depend on the type and location of the duplication.
Oral and oesophageal cysts may cause respiratory distress or dysphagia. Retrosternal pain, haemoptysis and infection can occur in case of large cysts with rapid growth (Fig. 6) [6,23].
Gastric and intestinal duplications may produce nausea, vomiting, abdominal distention or palpable abdominal mass (Fig. 7). Recurrent abdominal pain is one of the most frequent forms of presentation and is usually attributed to high pressure inside the duplication cyst because of the accumulation of secretions. Intussusception is another complication in which the cyst serves as a head point and pain, obstruction or bleeding are possible forms of manifestation. Extrinsic compression of the adjacent bowel is also possible, which causes obstruction. However, the most serious complications are produced if gastric mucosa is present within the cyst, leading to inflammation, bleeding, ulceration and even perforation [6,9,13,14,24,25].

Imaging findings
US is the imaging method of choice in the diagnosis of EDCs; only limited in the evaluation of oesophageal EDCs. Postnatal thoraco-abdominal radiograph: the gastric line tip is seen (black arrow) confirming the oesophageal atresia. The absence of air in the abdomen indicates a type-I or -II oesophageal atresia (without fistula). Venous umbilical catheter (white arrow) Fig. 6 A 10-month-old boy with a congenital cardiopathy presents respiratory distress. a Chest Xray: a left cervicothoracic mass is suspected displacing the trachea to the right (arrows). b Chest US: cystic mass (M) with slightly echogenic content inside is seen next to the thymus (T). Its origin is unclear. c Coronal view SSFSE T2 MRI: a well-delineated and hyperintense lesion (star) is seen. d Transversal view of the lesion in a gadolinium-enhanced VIBE MRI confirms the cystic nature of the mass (star) next to the anterior oesophageal wall (arrow). e Thoracoscopic findings: a 6 × 4cm lesion with close contact with the trachea originated from the muscular wall of the oesophagus Transoesophageal ultrasound might be useful but is not routinely used [26,27].
New US signs are described according to the characteristics of the EDCs: -As an EDC contains the same multi-layered wall architecture as the normal GT, the sign Bfive-layered cyst wallî s proposed. It corresponds to the innermost hyperechoic mucosa, hypoechoic muscularis mucosa, hyperechoic submucosa, hypoechoic muscularis propia and the outermost hyperechoic serosa. Identification of all five layers in a cyst is pathognomonic of EDC. However, this sign is difficult to demonstrate and needs expertise and highresolution US (12)(13)(14)(15)(16)(17)(18) [27,29,30]. For this reason, the use of US linear probe is recommendable when the GT is examined. -An EDC shares wall with the adjacent GT. Therefore, the diagnosis is carried out if it is possible to demonstrate the BY^sonographic configuration of the muscle layer caused by the splitting of the shared muscularis propria between the cyst and the adjacent loop. This sign is not described for other abdominal cysts and reflects one of the histological characteristics of the EDCs (Fig. 9) [29,31].
US is a dynamic study and allows to visualise the peristalsis of the cyst wall. It appears as a transient change of the shape and contour of the cyst because of a concentric contraction of the cyst wall (Fig. 10) when the transductor stays still on the cyst for a while [2,27].
Complicated EDCs rarely present the classic five layers or double-wall sign. Ectopic rest of pancreatic tissue can produce enzymatic destruction of the mucosa with inflammation, as the muscular layer is hypoechoic (dashed-line arrow). A gastric duplication cyst was suspected. L liver, P pancreas, AO aorta. c Laparotomy: antral duplication cyst was found (arrow). S stomach Fig. 8 A 12-year-old girl with a gynaecological malformation and haematometrocolpos. a A hypointense lesion is seen (white arrow) next to the rectum in axial T1 weighted pelvic MR. b On T2-weighted pelvic MR, the cyst next to the left wall of the rectum is seen. c Sagittal plane of the T2 MRI showing the posterior location of the cyst (arrow). VG vagina, BL bladder, U uterus. Imaging findings of a rectal duplication cyst. Note the haemorrhagic content of the uterus and vagina because of haematometrocolpos well as loss of the wall layers showing a hyperaemic thick wall. In such cases, the BY configuration^sign helps in establishing the correct diagnosis of EDC (Fig. 12) [3,29,30]. If ectopic gastric mucosa produces haemorrhage and bleeding, fluid levels or echogenic debris can be seen. When infection occurs, ulceration of mucosa can appear, and internal debris may be seen. The transmural extension can produce important inflammatory changes in the surrounding mesentery fat (Figs. 13 and 14) [3,7,24]. Ileal EDC, near the ileocecal valve, can act as intussusception head, showing on US a cystic mass inside the intussusception requiring emergency treatment (Fig. 15) [2].
In case of atypical or isolated EDC, the pseudokidney sign is described when there is a complete loss of typical wall layers because of severe congestion, thus producing a thick hypoechoic rim with a hyperechoic central layer [32].
US prenatal diagnosis of EDCs includes the same signs as postnatal cyst: the double-wall sign and the presence of peristalsis. However, on the prenatal US, the Bdouble wall^is not always seen or can be partial [10,33,34], and Fig. 9 A 3-month-old boy with vomiting is admitted to the emergency room. a US shows a cystic round-shape lesion with the Bfive-layers sign^(between arrows). b The BY sign^is seen (long arrow). Star ileum, L liver. Laparoscopic findings: a noncomplicated ileal duplication cyst  it may require the differential diagnosis with other cystic lesions such as mesenteric, omental, ovarian and choledochal cysts. If it is possible to demonstrate the presence of peristalsis in the cyst wall, an intestinal origin is probed. MR imaging is suggested to have a supplemental value in the assessment of fetal abdominal cysts (Fig. 16) [10,35,36].
CT is not typically performed for evaluation of EDCs due to radiation. CT may depict the location and extension of the cyst, as well as complications, the associated anomalies and anatomical relationship with surrounding structures. At CT, an EDC manifests as a cystic mass with a thin and slightly enhancing wall adjacent to the gastrointestinal wall. A high attenuation inside the cyst may be Power Doppler US demonstrates the significant vascularisation in the cyst wall. c Surgical findings: a cystic tumour next to the ileocecal valve. Pathological findings: ileal duplication cyst with heterotopic pancreatic tissue Fig. 13 A 3-year-old boy with fever and abdominal pain is studied. a US shows a cystic mass (star) with internal debris and next to an ileal loop (L). b The lesion (star) is surrounded by echogenic mesenteric fat (*) as an inflammatory sign. Surgical findings: a 5-cm ileal complicated duplication cyst was found with gastric mucosa with haemorrhagic and ulcerated walls    Surgical findings: rectal duplication cyst with mucous and purulent content. Rectum muscular wall was oedematous and it was shared with the duplication cyst seen due to haemorrhage or proteinaceous material. A thick enhancing wall, air bubbles inside and cystsurrounding inflammation may indicate an EDC complicated by infection (Fig. 17) [1,11,12,15].
Like CT, MR is not routinely used as a diagnostic method for EDCs, especially due to sedation requirement. On MR imaging, most duplications have low signal intensity on T1-weighed images and very high intensity on T2weighted images (Fig. 18). Both CT and MR play a major role prior to surgery in establishing the relationship between the cyst and its adjacent structures [12], and in locations where US presents a limited use, particularly in oesophageal and rectal duplications [1,2,6,12].

Management
The main considerations in the management of EDCs are: the condition of the patient, the location of the cyst, whether it involves one or more anatomic locations, whether its structure is cystic or tubular, and if it is communicated with the true intestinal lumen.
With the widespread availability of antenatal diagnosis, EDCs are often diagnosed prenatally. The optimal time to perform the resection in children with antenatal diagnosis is not defined. These patients should undergo early investigation, followed by early resection even within the first 6 months of life [3,37,38].
Treatment of asymptomatic EDCs remains controversial. The clinical behaviour of EDCs is unpredictable. EDCs tend to increase in size gradually and can cause symptoms and important complications that might be fatal, such as obstruction, massive bleeding or even a potential risk for malignant transformation in the adulthood [13,14,17,39].
Early excision is associated with less morbidity and a shorter length of stay compared to excision in symptomatic patients. There are significant post-operative morbidities after resection of complicated EDCs, compared with its elective surgery. Cyst excision alone could be considered, but if there is a communication, sometimes a resection of the adjacent bowel is necessary. It is important to ensure that the cyst is entirely resected because recurrence or malignant changes may occur [40].
Currently, minimally invasive surgery is becoming the elective approach, and most of the cysts can be resected successfully, either thoracoscopically or laparoscopically, as long as an exhaustive imaging diagnosis is available [41].

Conclusions
EDCs are uncommon congenital abnormalities arising anywhere along the GT. Their clinical presentations vary according to the site of duplication; ileum appears as the most commonly involved. Nowadays, antenatal diagnosis is becoming more frequent. US is the method of choice to diagnose gastrointestinal EDCs. Although double-wall US sign in a cyst is the most typical for diagnosis of EDCs, the findings of the five layers sign or the BY configuration^of the muscular layer are more specific features. Complicated cysts present atypical imaging findings. CT and MR imaging can be required in oesophageal or rectal EDCs for planning complicated surgical approach. Surgery is necessary because of the severe complications they can develop. The diagnosis is confirmed by histological examination. Fig. 18 A 2-year-old girl with fever and abdominal pain. a Abdominal US view of a complex cystic lesion (white arrows) in the duodenal area, next to the liver (L). GB gallbladder. b Axial gadolinium-enhanced GRE T1 demonstrating the presence of a multilocular cystic mass (white arrows) with wall thickening. c Axial T2 MRI: the mass (white arrow) shows three cystic cavities inside, close to the anterior wall of the duodenum (dashed-line arrow) and lateral to the gallbladder (star). Surgical findings: multiple duodenal duplication cyst, without connection with the lumen and with ectopic gastric mucosa