Simona Faraci, Luigi Dall’Oglio, Paola de Angelis, and Douglas S. Fishman Endoscopic ultrasound (EUS) is a minimally invasive method that combines the advantages of ultrasound and endoscopy [1]. The main advantage of EUS compared to conventional gastrointestinal endoscopy is its unique capacity for detailed cross‐sectional examination of the walls of the esophagus, stomach, duodenum, and rectum and detection of extraluminal lesions or structures within the surrounding compartments (e.g., the mediastinum) and acquisition of biological material through EUS‐guided fine needle aspiration (EUS‐FNA) [2–4]. The wall of the digestive tract on EUS appears as several hyperechoic and hypoechoic layers. The distortion of one or more of these layers will reflect the depth, size, and nature of the lesions. Application of EUS falls into two main categories: diagnostic and interventional/therapeutic endosonography. The latter includes EUS‐FNA and therapeutic procedures. Over the last decade, innovations in EUS technology have significantly expanded utilization of EUS. Most EUS devices require an echo‐transmitting physical medium (water), interposed between the probe and the anatomical structures being studied. In linear EUS, a latex balloon should be attached to the distal end of the scope and filled with water. A similar approach applies for examination of the esophagus with front‐loading radial ultrasound probes. For the study of gastric lesions, water instead is injected directly into the stomach. For investigation of the duodenum and rectum, it is useful to combine the two techniques [5]. The ultrasound transducer may have a frequency ranging from a minimum of 5 MHz to a maximum of 20 MHz and the scan can be radial or sectoral (Table 16.1). Reported experience with standard EUS scopes and miniprobes in children is limited to a small series [6–8]. Only a few articles including approximately 50 cases are reported [9], partly because commercially available echo‐endoscopes have a distal end diameter of 11–14 mm for radial probes and 14 mm for linear probes, which cannot traverse easily and without trauma from the first to the second portion of the duodenum in small children. The use of adult echo‐endoscopes has been described in children >3 years with weight >15 kg [6]. In children less than 15 kg, the endobronchial ultrasound (EBUS) endoscope or miniprobes are a good and useful alternative. A recent multicenter study described the efficacy and safety of EBUS with transbronchial needle aspiration and endoscopic ultrasound with an echo‐bronchoscope‐guided FNA in children with mediastinal lymphadenopathy of undefined etiology [10]. Miniprobes can be used with standard endoscopes in small children when standard EUS scopes cannot be maneuvered through the narrowed esophageal or intestinal lumen [7,11–14]. The high‐frequency (12–25 MHz) ultrasound catheter probes (Figure 16.1) are designed to pass through the working channel of standard endoscopes, which is exceptionally important for EUS in small children and patients with luminal narrowing, making application of the linear echo‐endoscope with a rigid 5–12 mm tip questionable or impossible [15,16]. These devices provide excellent recognition of structures within 5–20 mm from the transducer and are very useful for examining the layers of the gastrointestinal wall. Table 16.1 Commercially available echo‐endoscopes and miniprobes The diagnostic potential of a standard high‐frequency ultrasound catheter probe is quite limited when the lesions are large or broad‐based. To insure high‐quality EUS scanning of large lesions with deep penetration into and/or beyond the wall of the GI tract, a low‐frequency 7.5 MHz front‐loading probe was developed [15,17] (Figure 16.2). Radial endoscopic ultrasonography allows complete examination of large areas of the gastrointestinal tract and adjacent organs with simple and rapid visualization of these structures. The direction of scanning is perpendicular to the longitudinal axis of the device, producing a full 360° field of view. The available high‐frequency miniaturized probes can be used with standard endoscopes for evaluation of stenotic areas or small superficial lesions. This method requires filling of the balloon at the tip of the echo‐endoscope with 1–7 mL of deaerated water and direct contact between the balloon and the wall of the GI tract. It is used primarily for evaluation of the esophagus and pancreatobiliary system and adjacent lesions. In this method, the deaerated water is pumped into the GI tract through the working channel of the echo‐endoscope until the lumen is adequately distended. The volume of water varies between 100 and 500 mL. This method is useful to evaluate the penetration depth of GI lesions, for example for cancer staging. This is a combination of the two methods and is useful for GI tract lesions and lesions of the papilla of Vater [18] (Figure 16.3). The linear echo‐endoscope has a curved laterally oriented transducer providing a 120° sector scanning ultrasound view (Figure 16.4). Although linear EUS is designed for one‐sided sectoral scanning, a complete 360° image can be achieved by clockwise and/or counterclockwise torques of the scope in small incremental steps. The working channel opens just above the transducer (Figure 16.5) which is ideal for safe and effective use of FNA procedures because the needle and the target lesion are within the same ultrasound view (Figure 16.6). The parallel orientation of the ultrasonic beam to the longitudinal axis of the instrument allows precise navigation of the FNA needle to the target lesion for cytological sampling or therapeutic manipulations (Figure 16.7). This technique is particularly important for the diagnosis and treatment of conditions including pancreatobiliary tumors, mediastinal lymph node in patients with suspected TB or sarcoidosis, and other pathology. The wide (3.8 mm) instrumental channel of some lineal echo‐endoscopes allows passage of accessories up to 10 Fr in diameter. The instruments with an electronic transducer have color Doppler and power Doppler signals. Needles for FNA are equipped with a handle connected to the operator channel of the echo‐endoscope. The needle flows inside a metal or plastic protective sheath, which simplifies manipulations. The needles are available in three sizes: 19, 22, and 25 G. The aspiration system consists of a negative pressure syringe connected to a tap, which is opened after having engaged the needle system [19,20]. An application of the color Doppler modality of the linear EUS scope with electronic transducer substantially reduces an accidental puncture of neighboring vessels. Once the needle has been advanced into the lesion safely, changing the penetration angle and rapid withdrawal of the needle are helpful for better tissue sampling. The collected specimen is placed in fixative solution for histology and other histochemical and cytogenetic studies. Under low‐frequency (7.5 MHz) EUS scanning, the walls of the esophagus, stomach, and rectum appear as five concentric layers that alternate according to the echogenicity. From the inside out, the first two hyper‐ and hypoechoic layers correspond to the mucosa and muscularis mucosa; the third hyperechoic layer is associated with the submucosa; the fourth hypoechoic layer represents muscularis propria; and the fifth hyperechoic layer is related to the serosa (Figure 16.8). Due to the relatively thin wall of the esophagus, it is not easy to distinguish mucosa and submucosa. In the stomach, the fourth layer (muscularis propria) may consist of two sublayers (inner circular muscle and outer longitudinal muscle) divided by a hyperechoic line. High‐frequency (20 MHz) probes provide a better resolution of the wall architecture (up to nine layers) at the expense of depth of scanning of the surrounding structures. In contrast, many vital structures are within the reach of a low‐frequency EUS. From the esophagus it is possible to study the posterior mediastinum: thoracic aorta, azygos vein, pulmonary arteries, and lymph nodes. EUS from the stomach provides access to the spleen, left adrenal gland, celiac tripod/axis, body and tail of pancreas, splenic vessels up to the portal vein, left lobe of liver and gallbladder. From the duodenum, the head of the pancreas, extrahepatic biliary ducts, major duodenal papilla, and right lobe of the liver can be visualized [21]. Endoscopic ultrasonography is a useful imaging technique that has applications for the pediatric population. In 2017, ESPGHAN‐ESGE released their guidelines for pediatric gastrointestinal endoscopy. The panel of experts emphasized that proposed recommendations for EUS in children have been made based on low quality of evidence [22]. Pancreaticobiliary and duodenal indications include differentiation between autoimmune pancreatitis and neoplasm [23]; assessment of anatomy of the pancreas in pancreatitis [24] and biliary anatomical abnormalities [25]; pancreatic pseudocyst drainage and duodenal duplication cyst assessment [26,27]. ESPGHAN‐ESGE suggested the following. Indications for EUS in children are summarized in Table 16.2. Table 16.2 Indications for EUS in children In children, esophageal and pancreatobiliary congenital anomalies comprise a higher percentage of indications for EUS than in adults. As mentioned above, successful application of EUS and EUS‐guided FNA has been reported in children with pancreatobiliary diseases [23–25], in whom noninvasive imaging modalities (i.e., US, MRCP, CT, etc.) were inconclusive. Esophageal strictures in children are predominantly benign and associated with many conditions including reflux and eosinophilic esophagitis, caustic ingestion, tuberculosis, post surgical (anastomotic), IgG4‐related esophagitis, radiation and drug‐induced esophageal injuries (Figures 16.9 and 16.10). In children with congenital esophageal stenosis, miniprobe EUS can distinguish between tracheobronchial remnants (TBR) and fibromuscular stenosis (FMS). In congenital esophageal stenosis with TBR, there are multiple echogenic regions in the muscle layer that represent aberrant cartilaginous remnants. Patients with TBR often require surgical resection because of the increased risk of perforation during dilation. In contrast, patients with FMS or membranous stenosis can be treated safely with esophageal dilation [12,23]. EUS is the best diagnostic test to distinguish between these conditions. High correlation between EUS miniprobe evidence of TBR and surgical findings has been documented [7]. Both high‐frequency miniprobe and three‐dimensional EUS have been used for preoperative evaluation of congenital esophageal stenosis in children [14]. After a pediatric endoscope is positioned just above the narrowed esophagus, the probe is inserted through the instrument channel and negotiated across the stricture. The miniprobe EUS procedure is performed using the direct contact method (Figure 16.11). Other structural abnormalities of the esophageal wall and submucosal lesions such as esophageal duplications, malignant lesions, and lymphomas are generally well defined by EUS [30–33]. EUS is considered the primary diagnostic tool in preoperative staging of esophageal carcinoma. Endoscopic treatment by mucosal EUS‐guided resection is used effectively to treat Barrett’s esophagus in adults. Barrett’s esophagus has no specific EUS characteristics but only a slight thickening of the mucosa. However, if complicated by severe dysplasia, it shows infiltration of the underlying layers and lymphadenopathy [34]. To study Barrett’s esophagus and other infiltrating lesions of the esophagus, it is necessary to utilize EUS at high frequency (e.g., 20 MHz). EUS features of esophageal lesions are listed in Table 16.3. Many studies have shown that EUS is superior to CT in the staging of gastric tumors and associated lymph nodes. The information from EUS helps to indicate the surgical intervention, type of surgery, and any adjuvant chemotherapy. EUS assesses the degree of infiltration of the neoplasm in early and advanced stages. In pediatric patients it is very useful both in the rare cases of mass and of lymphoma. Both the radial instrument and the miniprobe can be used in relation to age. Bowel or balloon filling is necessary for the study. Neoplastic lesions can infiltrate deeply into the gastric wall with complete disappearance of stratification [33] (Figures 16.12–16.14). Congenital anomalies are common in children, for example duodenal duplication (Figure 16.15). In congenital duodenal duplications, EUS may identify anomalous pancreatobiliary ducts that may not be as well defined by CT scan or MRCP [26,27]. This information is essential for choosing between surgical and endoscopic therapy. Table 16.3 EUS features in esophageal diseases The plicate hypertrophy of the stomach is amenable to study by EUS for differential diagnosis with lymphomas (Figure 16.16). In case of duodenal web, it is important to perform EUS before endoscopic dilation or dissection to evaluate the thickness of the web and the outlet of the biliary tract [33–35] (Figure 16.17). EUS features of the main lesions of the stomach are detailed in Table 16.4. Given its high accuracy and sensitivity, EUS is particularly effective in evaluating pancreatobiliary diseases. One of the important benefits of EUS is a reduction of unnecessary diagnostic ERCP [10,29,30]. The diagnosis of lithiasis or microlithiasis of the common bile duct by EUS is superior to conventional ultrasound technique (Figure 16.18). Table 16.4 EUS features in gastric pathology In children with chronic pancreatitis, EUS is more sensitive than CT scan, especially in the early stage of the disease, and helps to depict the focal or diffuse changes of the pancreatic parenchyma such as echogenic foci, interlobular septa, small cystic cavities, lobulated glandular margins, parenchymal heterogeneity, and pancreatic ducts/ectasia of collateral branches (Figure 16.19). In children with pancreatic pseudocysts, it is often necessary to perform an internal drainage through the stomach (Figure 16.20). For a detailed description of pancreatic cystogastrostomy see Chapter 38. Complications related to this intervention (perforation or bleeding) can be prevented by EUS. Table 16.5 EUS features of the cystic and mass lesions of the pancreas and biliary ducts EUS with FNA allows precise histological analysis and differential diagnosis of cystic lesions/tumors of the pancreas and biliary ducts (Table 16.5). Overall, current data support a high diagnostic value of EUS in many pancreatobiliary conditions including cholelithiasis, recurrent, chronic and autoimmune pancreatitis, idiopathic fibrosing pancreatitis, pancreas divisum, congenital anomalies, microlithiasis, pancreatic pseudocysts, and pancreatic mass lesions [19,35–43]. Therapeutic EUS with pancreatic fluid collection in children appears promising, although larger prospective studies will be needed for conclusion [44]. EUS and EUS‐guided interventions could alter clinical management in pediatric patients and should be considered in some challenging cases of pancreatobiliary disorders [45]. EUS is shown to be a safe and cost‐effective modality with both diagnostic and therapeutic capabilities in the pediatric population. It is now increasingly being recognized as a standard of care when evaluating pancreatobiliary conditions in children [40].
16
Endoscopic ultrasonography
Introduction
Instruments and technique
Ultrasound catheter probe (radial EUS)
Manufacturer
Type
Product
Max diameter (mm)
Insertion tube diameter (mm)
Channel size (mm)
Pentax
Radial
EG‐3670URK
n/a
12.1
2.4
Linear
EG‐3270UK
11.5
10.8
2.8
Linear
EG‐3870UTK
n/a
12.8
3.8
EBUS (Linear)
EB‐1970UK
6.3
n/a
2.0
Olympus
Mini‐probe
UM2R/3R
2.5
n/a
n/a
Radial
GF‐UE160‐AL5
13.8
11.8
2.2
Linear
GF‐UCT180
14.6
12.6
3.7
Linear
GF‐UC140P‐AL5
14.2
11.8
2.8
Linear
GF‐UC140‐AL5
14.6
12.6
3.7
Linear
TGF‐UC180J
14.6
12.6
3.7
EBUS
BF‐UC180F
n/a
6.2
2.2
Fujinon
Radial
EG‐580UR
n/a
11.4
2.8
Radial
EG‐530UR2
11.4
11.5
2.2
Linear
EG‐580UT
13.9
n/a
3.8
Linear
EG‐530UT2
13.9
12.1
3.8
EBUS
EB‐530US
6.7
6.3
2.0
Front‐loading ultrasound probe
Radial endoscopic ultrasonography
Balloon contact method
Water‐filling method
Balloon contact plus water‐filling method
Linear endoscopic ultrasonography
Appearance of the gastrointestinal wall on EUS images
Indications in children
Esophagus
Stomach
Duodenum
Pancreatobiliary
EUS features in pediatric diseases
Esophageal strictures
Stomach
Disease
Layer
Feature
Caustic stenosis
Mucosa/muscularis mucosa
Subversion and dissection of the layers
Congenital stenosis
Mucosa/muscularis mucosa
Thickening of the layers
Eosinophilic esophagitis
Mucosa
Thin wall, variable thickness
Achalasia
Muscularis mucosa
Thickening of the layers
Varices
Mucosa/submucosa
Anechoic, tortuous, color Doppler
Duplication cyst
Variable
Hypoechoic, roundish, variable inside
Barrett’s/esophageal cancer
Mucosa/submucosa/muscularis mucosa
Parietal thickening of esophagus with fusion of layers that involves the wall including muscle layers
Pancreatobiliary ducts
Disease
Layer
Feature
Leiomyoma
Mucosa/muscularis mucosa
Hypoechogenic, roundish, net margins
Lipoma
Submucosa
Echogenic, smooth margins
Cyst
Variable
Hypoechogenic, roundish
Aberrant pancreas
Submucosa/muscularis mucosa
Hypoechoic, mixed, bile ducts?
Varices
Mucosa/submucosa
Size, depth, tortuousity, color Doppler
Gastrointestinal stromal tumor
Muscularis mucosa
<3 cm hypoechoic, net margins; >3 cm cystic weakness, irregular margins
Lynphoma
Mucosa/submucosae/muscularis mucosa
Hypoechogenic
Disease
Features
Neuroendocrine tumors
Tiny, discrete, encapsulated, hypoechoic mass lesions, often along the anterior/posterior surface of pancreas. High vascularity on color Doppler. Large tumors show cystic and necrotic areas
Pseudocysts
Large and hypoechogenic. Well‐formed fibrous wall
Pancreatitis
Variable, heterogeneous with hypo‐ and hyperechogenic areas
Lithiasis of the common bile
Hyperechogenic lesions evident in the common bile duct
Portal hypertension
Use of Doppler