G Model EURR-6752; No. of Pages 9
ARTICLE IN PRESS European Journal of Radiology xxx (2014) xxx–xxx
Contents lists available at ScienceDirect
European Journal of Radiology journal homepage: www.elsevier.com/locate/ejrad
Gastrointestinal ultrasound in neonates, infants and children Maria Luisa Lobo ∗ , Mariana Roque Servic¸o de Imagiologia Geral, Hospital de Santa Maria – Centro Hospitalar Lisboa Norte (CHLN), Av. Prof. Egas Moniz, 1649-035 Lisboa, Portugal
a r t i c l e
i n f o
Article history: Received 31 March 2014 Received in revised form 12 April 2014 Accepted 15 April 2014 Keywords: Ultrasound Gastrointestinal tract Pediatrics Neonates/children
a b s t r a c t Today US plays an important and increasing role in the assessment of many, partially age-specific conditions in the GI tract in neonates, infants and children. Knowledge of the potential capabilities of US and its restrictions together with a skillful performance of GI US examination can provide essential anatomic and functional diagnostic information in many pediatric GI disorders. The aim of this review is to highlight the potential of ultrasound (US) in the evaluation of the gastrointestinal (GI) tract in neonates, infants and children. Basic and potential applications of modern US tools in pediatric GI tract are addressed, the GI US examination technique is discussed – including some common and/or typical clinical applications of and indications for US. © 2014 Elsevier Ireland Ltd. All rights reserved.
1. Introduction Ultrasound (US) is an excellent imaging modality in the evaluation of the gastrointestinal (GI) tract in pediatric patients. Besides its well-established primordial diagnostic role in some typical pediatric GI conditions such as in hypertrophic pyloric stenosis (HPS) and intestinal intussusception, US diagnostic capabilities has been widely explored in several other GI tract diseases such as in acute appendicitis, inflammatory bowel disease (IBD), necrotizing enterocolitis (NEC), intestinal malrotation, gastro-oesophageal reflux (GER), and even in less conventional applications such as in patients with esophageal atresia and tracheoesophageal fistula. Furthermore, US is an excellent bedside high yield imaging tool for neonates, infants and children in intensive care units and it can also be used to guide therapeutic maneuvers like in reduction of intussusception or in enema for meconium ileus. Since its introduction in clinical practice, US technology along with computed imaging processing has greatly progressed allowing for higher resolution and better quality imaging with higher diagnostic reliability [1], thus with ongoing expanding clinical applications [2]. These modern approaches and the advent of high resolution transducers have made US an essential imaging technique in pediatric GI tract that has initially not been considered suitable for US assessment. The well known advantages of US, particularly its lack of ionizing radiation and easy access, together with the general good anatomic profile of young patients, makes
∗ Corresponding author. Tel.: +351 217805085; fax: +351 217805085. E-mail addresses: [email protected], [email protected] (M.L. Lobo), [email protected] (M. Roque).
this imaging technique an ideal one for the evaluation of the pediatric patient with GI tract complaints. Major limitations include its operator-dependency and reproducibility, apart from factors related to the patient such as painful abdomen, noncollaboration, obesity and interposition of large amount of gas. Some of these drawbacks can be overcome with a careful, dedicated and comprehensive technique examination using modern US capabilities [3]. The aim of this paper is to highlight the potential of US in the evaluation of the GI tract in neonates, infants and children. In this review we address basic and potential applications of modern US tools in pediatric GI tract, review the GI US examination technique, and discuss some common and/or typical clinical applications and indications of US in the evaluation of the GI tract in neonates, infants and children. The in depth discussion of all pathologic entities and all the detailed imaging findings is beyond the scope of this paper.
2. Potential applications of modern US tools in the pediatric GI tract In the last decades, advances in US technology have greatly improved the quality of GI US imaging with a consequent positive impact on its diagnostic yield. Improvement in US probes, particularly high-resolution linear probes, with new piezoelectric material incorporated and broadband techniques permit better spatial resolution in the near-field and better penetration in the far-field, whereas improvement in contrast resolution can now be achieved with recent US modes like image compounding, speckle/noise reduction filters and (tissue) harmonic imaging [1–3].
http://dx.doi.org/10.1016/j.ejrad.2014.04.016 0720-048X/© 2014 Elsevier Ireland Ltd. All rights reserved.
Please cite this article in press as: Lobo ML, Roque M. Gastrointestinal ultrasound in neonates, infants and children. Eur J Radiol (2014), http://dx.doi.org/10.1016/j.ejrad.2014.04.016
G Model EURR-6752; No. of Pages 9
ARTICLE IN PRESS M.L. Lobo, M. Roque / European Journal of Radiology xxx (2014) xxx–xxx
2
Endoscopic US is another emerging field in adult GI tract imaging, although with limited experience and applicability in the pediatric population, partially due to lack of dedicated pediatric transducers [13].
3. Gastrointestinal US technique and how to improve pediatric GI US examination
Fig. 1. Extended field of view. US imaging documentation of a long segment of the colon in a patient with colitis due to Crohn’s disease. Courtesy: M. Riccabona, Graz.
Likewise, progress in Doppler techniques allows better depiction and quantification of even slow flow of small vessels within the normal and pathological GI structures [1,3,4]. With the use of US contrast agents (US-CA) and contrast specific US modes, contrast-enhanced US (ce-US) enables further characterization of flow dynamics and enhancement pattern in real time [1,3,5]. Although limited research has been conducted in the pediatric population, mainly because currently available (US-CA) have not been approved for pediatric use yet, some studies have pointed out its potential benefit in the evaluation of the pediatric GI tract, for instances in the assessment of disease activity in IBD [5,6,7]. In pediatric abdominal blunt trauma intravenous ce-US seems to improve the detection of solid organ lesions compared unenhanced US, but it is limited in the identification of bowel or mesenteric traumatic lesions [1]. Potential benefit from the non-vascular use of US-CA have also been referred in the literature [2,3], as in ce-US evaluation of GER [8]. Extended field of view or panoramic US can be extremely useful in GI US, particularly in the evaluation of the bowel (Fig. 1). The reconstruction of a wide image by correlating data from consecutive images adding these frames together to one large picture allows demonstration of large segments of the bowel and to make correct length measurements [1,3,9]. Volume US or three-dimensional US (3DUS) has been shown to improve volume assessment, and has the potential to improve documentation and comparison between different studies [1,10]. Clinical experience with 3DUS in the pediatric GI tract is limited, with few reports in the literature related to the calculation of gastric volume in GER disease or in tumor volume assessment. Recording US video clips is another useful option in GI US imaging that allows, in addition to the conventional review of the real time images, documentation of gastric motility and bowel peristalsis as well as air bubbles movement in GI fistulous sinus tracts or in bowel perforation, e.g. in premature babies with NEC. US elastography is an emerging US application in various abdominal clinical fields for assessment of “stiffness” of a tissue. Growing experience has been obtained in liver diseases as well as on oncology, particularly in adult population [1]. Recently extended applications have also been explored, including the GI tract particularly in IBD. In the GI tract, specific challenges rise from the anatomy and physiology of the bowel with thin wall, non-constant boundary conditions and intrinsic contractility, although pathological conditions are often related with increased bowel wall thickness and decreased bowel peristalsis [11,12].
For any US examination the choice of adequate transducers and adjustment of basic parameters as well as the choice of US modality is fundamental to obtain a proper image quality. In general, the optimal transducer should have the highest possible frequency still allowing to penetrate to the targeted anatomical area thus offering best spatial resolution. After initial evaluation of the entire abdominal cavity that can be performed with a curved array transducer, the individual structures of GI tract are then specifically examined with a high resolution linear probe which allows detailed visualization of the oesophageal-, gastric- and bowel wall as well as of the relevant surrounding structures [3,14]. Not infrequently, curved array (and sometimes sector) probes may also be needed in order to obtain a better access window to image deeper structures in older children (like the oesophago-gastric junction, the sigmoid colon and rectum) or to allow for a broader field of view. In addition to the conventional transabdominal US approach, other less common approaches might be necessary, and should be included, in specific situations such as the suprasternal and mediastinal US approach to visualize the upper oesophagus in oesophageal atresia [15] or the perineal US approach to evaluate the anal canal or the distal rectal pouch location [16] and its distance to the skin surface in anorectal or in cloacal malformations. When imaging the bowel by US, a methodic and systematic analysis is crucial to facilitate a thorough evaluation of the various intestinal segments as complete as possible. As mentioned before, extended field of view imaging can be helpful to document large segments of diseased bowel and recording US cine loop clips is useful to demonstrate normal or abnormal GI motility. Bowel gas interposition is a well known limitation to US examinations, but with a careful and proper bowel US technique this obstacle can often be at least partially overcome. Particularly gentle graded compression is the essential technique in US of the GI tract, as it displaces undesirable gas, shortens the distance to the skin surface and isolates the bowel loops while displacing adjacent ones [3,17,18]. Furthermore, it helps to localize the origin of pain (“sonopalpation”) and to assess the bowel compressibility, which is an important sign in the evaluation of the bowel. The adjuvant use of posterior manual compression [3,19] can also be helpful, particularly for the evaluation of the right iliac fossa. Changing patient position is another easy way to move disturbing air/gas away from the area to examine. GI luminal filling after oral intake of water or another liquid meal or with oral or rectal administration of saline fluid (hydrosonography) is particularly useful to optimize US evaluation of the GI tract [14,20,21]. These techniques have been applied to several pediatric conditions for decades. In addition to improve visualization with the distension obtained, it also helps to displace gas/air and, in the upper GI tract it enables to verify pylorus channel opening or to confirm the duodenal or duodeno-jejunal junction position. Moreover, in small patients and particularly in critical ill neonates, a small bowel follow-through can be performed and followed by US. Furthermore, filling techniques are the basis for therapeutic maneuvers under US guidance as in the non-surgical reduction of an ileocolic intussusception or in the attempt to resolve meconium ileus using an enema.
Please cite this article in press as: Lobo ML, Roque M. Gastrointestinal ultrasound in neonates, infants and children. Eur J Radiol (2014), http://dx.doi.org/10.1016/j.ejrad.2014.04.016
G Model EURR-6752; No. of Pages 9
ARTICLE IN PRESS M.L. Lobo, M. Roque / European Journal of Radiology xxx (2014) xxx–xxx
Since the 1990s, the US evaluation of the small bowel with a non-absorbable anechoic oral contrast, such as isotonic polyethylene glycol (PEG), also known as small intestine ce-US (SICUS), has shown advantages over conventional bowel US in various adulthood intestinal pathologies [14,20,22]. In Crohn’s disease it was found to be comparable to ileo-colonoscopy, wireless capsule endoscopy, and small-bowel sonography in the assessment of the number, site, extension, and postoperative recurrence of small bowel lesions; but only few studies have specifically addressed the pediatric population [14,22,23]. Particularly important, SICUS seems advantageous in the depiction of proximal small bowel lesions, a commonly affected GI intestinal segment in younger patients which is less accurately assessed by non-contrast bowel US [14,20,23]. Although SICUS has been shown to be a more reliable technique with improved sensitivity and specificity compared with conventional bowel US in the evaluation of patients with suspected or known Crohn’s disease [20], it is a time consuming examination (mean duration of 30–40 min) which is in discordance with the expected advantages of US as a simple, practical and rapid examination [14,22]. Thus, in clinical practice the decision to perform SICUS is usually case-based according to the clinical context and the experience of the operator, and the availability and applicability of the contrast agent.
4. Indications and some clinical applications of GI US in neonates, infants and children 4.1. Upper GI tract In neonates with oesophageal atresia, usually diagnosed with frontal and lateral radiograms, US can give additional valuable information to the surgeon. Besides the role of abdominal and cardiac US to search for associated abnormalities, mediastinal US allows the characterization of the length, morphology and structure of the wall of the blind upper oesophageal pouch which can be improved by the administration of small amount of saline fluid through the oesophageal tube [15]; sometimes even a tracheaoesophageal fistula may be recognized by US. Moreover, the definition of the anatomic position of the aortic arch is crucial to plan the surgical approach. With a superior abdominal US approach the cardia and the adjacent distal oeosophagus are often easily depicted, although visualization of the entire distal esophageal length behind the heart is difficult and restricted [15]. In neonates and infants with suspected gastro-oesophageal reflux disease (GERD) US is a widely available, non-invasive and sensitive method that can provide both useful anatomical and functional information [24–28] (Fig. 2), although it’s role is still controversial and debated [24,25]. The complex issue of GER and GERD is related to many factors, including the nonspecific nature of symptoms in young children, the difficult distinction between physiological and pathological GER, and the impasse to establish a cause-effect relationship between GER and symptoms or complications related to GERD [24,25]. Nevertheless, US is considered by many authors as a first noninvasive imaging tool in a child with vomiting, particular in patients younger than 2 years of age, as it can provide alternative diagnosis other than GER and rule out gastric outlet obstruction [24]. More important than the detection of GER per se, one can correlate those with the occurrence of clinical symptoms. Furthermore, US can give information on functional aspects such as the oesophageal clearance of the gastric content refluxed, the opening of the gastro-oesophageal junction, the gastric emptying, and can potentially detect an associated hiatal hernia [26,27]. Anatomic details of the gastro-oesophageal structure, like the length of the abdominal oesophagus and the gastro-oesophageal angle (“His angle”), can be assessed and seem to have high sensitivity and high
3
Fig. 2. GER. Longitudinal US section of the epigastric region showing opening of the cardia and reflux of gastric content into the lower esophagus.
positive predictive value for GER [24,28]. Colour Doppler sonography (CDS) may increase the sensitivity of US for detection of GER although it might be sometimes difficult to apply due to artifacts caused by the cardiac movement [8]; it definitely is a good tool for documentation if no video clips can be stored [29]. US is generally considered the modality of choice to confirm or exclude the diagnosis of hypertrophic pyloric stenosis (HPS). The diagnosis of HPS is based on US morphological and dynamic findings with the most significant criteria being a thickened pyloric muscle (greater than 3 mm) and the lack of luminal opening of the pyloric channel [30–32] (Fig. 3). The usually distended stomach, seen as an indirect sign of gastric outlet obstruction, must be interpreted according to the time of the last meal. Changing the patient position may be necessary to improve visualization of the pylorus
Fig. 3. HPS. Longitudinal US section of the pylorus. Thickened hypoechoic pyloric muscle (A x. . .x) and elongated pyloric channel (B X. . .X) with persistent nonopening of the lumen on real time US.
Please cite this article in press as: Lobo ML, Roque M. Gastrointestinal ultrasound in neonates, infants and children. Eur J Radiol (2014), http://dx.doi.org/10.1016/j.ejrad.2014.04.016
G Model EURR-6752; No. of Pages 9
ARTICLE IN PRESS M.L. Lobo, M. Roque / European Journal of Radiology xxx (2014) xxx–xxx
4
Fig. 4. Gastric duplication cyst. Transverse US section of the right upper abdomen showing the typical “gut signature” wall of an abdominal cyst in a 6 month old infant with profuse vomiting (a). After filling the stomach with a small amount of saline fluid it was possible to document its close relation with the anterior wall of the anthropyloric region causing obstruction of the gastric outlet (b).
channel that might be hidden by a distended stomach. It is also important to analyze the pylorus channel over time, which will allow the differentiation between HPS and pylorospasm, a transient phenomenon that may have similar morphological and measurements features with HPS. In doubtful or equivocal cases, a repeated US examination several hours later may clarify the diagnosis and nowadays the need of other diagnostic imaging tools is extremely rare [30,31]. US may also serve for follow-up in conservatively treated patients [32]. Gastric duplication cysts are usually easily to recognize when they exhibit the typical US features of a cystic structure with a thick layered wall. Filling the stomach with fluid is helpful to define the close relationship of the cyst with the gastric wall. If located in the antro-pyloric region they often cause a gastric outlet obstruction (Fig. 4). Other gastric conditions may be first suspected during an abdominal US performed in a child with vomiting, epigastric pain or nonspecific abdominal complains, either by causing focal or diffuse thickening of the gastric wall such as eosinophilic gastritis, chronic granulomatous disease and tumoral and pseudotumoral conditions, or by the presence of an endoluminal abnormality such as polyps (Fig. 5), bezoars or ingested foreign body. Also infiltrating (e.g. lymphoma) or tumorous (e.g. leiomyoma) stomach wall conditions may be depictable by US. After US evaluation of the oesophago-gastric junction, the stomach and the pylorus, the next step is to follow the duodenum to look at the position of the third part of the duodenum (D3) normally passing between the abdominal aorta and the superior mesenteric artery, and to identify the duodeno-jejunal junction on the left side of the aorta.
of the mesenteric vessels (the “whirlpool sign”) with a pseudotumorous aspect, must lead to emergent surgery to prevent intestinal ischemia, necrosis and perforation [34]. Diagnosis of neonatal bowel obstruction, or confirmation of a suspected prenatal diagnosis, is usually based on clinical and radiological signs on abdominal plain film occurring with a delay of at least 12–24 h; in some partial or very distal obstruction it may present even later. Besides the search for associated malformations, US can contribute with important additional information [35,37], such as: early diagnosis of a mechanical occlusion (e.g. malrotation with volvolus); assessment of the colon size and its content (e.g. normal colon in proximal small bowel atresia; microcolon with abnormal hyperechogenic meconium in distal small bowel atresia and in meconium ileus, or with hydrocolon in meconium plug syndrome and small left colon syndrome) which is a main marker to assume the probable location of the obstruction thus indicating the need to perform a contrast enema in case of lower bowel obstruction such as in meconium ileus or in meconium plug syndrome; occasional detection of the cause of obstruction, either intrinsic (e.g. duodenal web) or extrinsic (e.g. GI duplication cyst or
4.2. Small and large bowel An abnormal relationship between the superior mesenteric artery and the superior mesenteric vein should raise suspicion of a intestinal malrotation, although a normal position does not exclude the presence of abnormal midgut rotation [33,34]. In addition, a normal retroperitoneal position of D3 is said to be a more reliable sign to exclude malrotation than does the position of the mesenteric vessels [35,36]. US screening for intestinal malrotation in an asymptomatic pediatric patient aims at preventing future obstructive or ischemic complications or completing a US work-up for unspecific complaints, whereas the sonografic diagnosis of malrotation with acute volvulus, on US seen by the characteristic twist
Fig. 5. Gastric polyp. Axial US section of the stomach after oral intake of water revealing a gastric polypoid lesion in a 15 years old male with Peutz–Jeghers syndrome.
Please cite this article in press as: Lobo ML, Roque M. Gastrointestinal ultrasound in neonates, infants and children. Eur J Radiol (2014), http://dx.doi.org/10.1016/j.ejrad.2014.04.016
G Model EURR-6752; No. of Pages 9
ARTICLE IN PRESS M.L. Lobo, M. Roque / European Journal of Radiology xxx (2014) xxx–xxx
5
Fig. 6. Anorectal malformation. Perineal US approach in longitudinal (a) and axial (b) planes in a neonate with imperforated anus. The dilated colon is seen coming down below the level of the pubo-coccigeal line, with the anal blind end pouch located within a few millimeters from the perineal surface.
annular pancreas); presence of free intraperitoneal fluid and/or air, and signs of vascular compromise indicating of bowel ischemia and perforation. In addition to its diagnostic role, US can also be used for therapeutical purpose to guide enema reduction of meconium ileus – or meconium plug equivalent – which is particularly useful as a bedside procedure in critically ill preterm babies in the neonatal intensive care unit who cannot be brought to the fluoroscopic suit [38]. In anorectal malformations perineal US can help defining the type of malformation (Fig. 6). The distance between the rectal cul-de-sac and the perineum can be reliably measured by using a transperineal approach, and US may identify the location and course of the urorectal fistula [16,35,37]. The role of US in necrotizing enterocolitis has been increasingly recognized [39–42], with higher sensitivity than plain films in the detection of early changes such as wall thickening and disturbed bowel wall perfusion, intestinal pneumatosis and portal pneumatosis [38] (Fig. 7) as well as early signs of perforation [39,40]. It has also been suggested that US findings are useful in predicting outcome [41,42]. US may also be useful in the diagnosis of post-enterocolitis stenosis [40]. In suspicion of bowel obstruction in older children, US may help to differentiate between mechanical or functional intestinal occlusion, may detect the transition zone, and may show worrying signs related to vascular compromise of the involved bowel. Bowel wall thickening is the hallmark of intestinal diseases. Bowel wall thickness increases with age [43], and in the pediatric population bowel wall thickness greater than 2.5 mm and 2 mm respectively for the small and large bowel are considered abnormal [43]. A careful and attentive abdominal US examination in a child with unclear clinical symptoms may reveal not only a thickened bowel wall, but also the location and extension of the involved segments, their vascular features on CDS, and the presence of extramural signs of disease such as hyperechogenicity of surrounding fat planes, abscesses and fistulas [3–5,17,20,23]; abnormal bowel wall stratification and abnormal peristalsis should also be noted. Although US signs are generally nonspecific, the correlation of the US findings with the clinical history and laboratorial data often permits to narrow the differential diagnosis, thus directing further additional imaging in a more efficient way. The role of US in inflammatory bowel disease (IBD), and particularly in Crohn’s disease, has been thoroughly evaluated in adults and to a limited extent in children [17,18,44–48]. Most published studies have found bowel US a valuable tool in patients with suspected or known IBD. Although US has a good negative predictive value for Crohn’s disease in patients with a clinical suspicion of IBD
allowing for more invasive diagnostic procedures to be postponed [17,46], its main application is in the follow-up of patients with known IBD to monitor treatment and to ensure early detection of intra-abdominal complications in relapse [7,17,46]. Assessment of vascularity with CDS provides additional information about disease activity [4,5,7,47,48] and it may help to distinguish between inflammatory and fibrotic bowel stenosis [5], although its exact role has yet to be defined [7,46,48] (Fig. 8). US has become the modality of choice to accurately diagnose or exclude intestinal intussusception [49]. Moreover, US can determine the location and the type of the intussusception (idiopathic versus secondary to the presence of a lead point, or ileo-ileal intussusception), which has a decisive impact on the therapeutic approach, as well as signs related to nonsurgical reduction success [50,51]. Typical signs of ileocolic intussusception include the “target” or “doghnut” sign and the “pseudokidney” sign respectively on transverse and longitudinal planes (Fig. 9a). Transient and asymptomatic small bowel intussusceptions are relatively common and should not be confused with ileocolic intussusception that needs urgent reduction. The former are usually encountered around the periumbilical region, are smaller (less than 2 cm) in diameter, do not exhibit the hyperechoic central core (Fig. 9b), and tend to resolve spontaneously within a few minutes [51]. In ileocolic intussusception, a small amount of intraperitoneal free fluid can often be seen, and should not preclude a nonsurgical reduction attempt. On the other hand, the presence of trapped fluid within the intussusception and the absence of flow on CDS in the intussuscetum wall raise the suspicion of vascular compromise of the bowel, and are related to lower success rate of nonsurgical reduction [50,51]. Although these signs are not considered absolute contraindications to attempt nonsurgical reduction, when present a nonsurgical reduction should be performed with extremely caution due to the high risk of perforation [51]. US guidance of hydrostatic or air enema reduction of intestinal ileocolic intussusception has been successfully used for therapeutic purpose in many centers [51]. Appendicitis is the most common pediatric surgical emergency [52–54]. For the last decades, imaging has become an important diagnostic contributor to timely improve reliability of diagnosis and to lower the rate of unnecessary appendectomies, although the exact place of the different imaging modalities is still a matter of debate [55,56]. US should be encouraged and promoted as it can often provide a reliable contribution to the diagnosis by supporting or, more rarely, excluding appendicitis, and by helping in the differential diagnosis – thus avoiding unnecessary radiation exposure from CT in a significant number of patients in whom imaging is needed [54–56] (Fig. 10a). Typical findings include
Please cite this article in press as: Lobo ML, Roque M. Gastrointestinal ultrasound in neonates, infants and children. Eur J Radiol (2014), http://dx.doi.org/10.1016/j.ejrad.2014.04.016
G Model EURR-6752; No. of Pages 9
ARTICLE IN PRESS M.L. Lobo, M. Roque / European Journal of Radiology xxx (2014) xxx–xxx
6
Fig. 7. Necrotizing enterocolitis. Thickened small bowel loops with intestinal pneumatosis seen as hyperechoic dots within the bowel wall; peritoneal free fluid and pneumoperitoneum (a). Axial plan of the liver showing mulitple hyperechoic dots in a linear arrangement extending to the periphery of the liver parenchymal due portal pneumatosis (b). Courtesy: M. Riccabona, Graz.
an enlarged (outer diameter greater than 6 mm usually is used as cut-off), non compressible and tender appendix, sometimes with an appendicolith, with surrounding infiltration of the periappendicular fat; on CDS increased vascularity of the appendicular wall is seen in early inflammatory phases, whereas no flow can be detected if the appendix is necrotic or perforated; other secondary changes include peri-appendicular free fluid or collected fluid [52,54]. Imaging is not always necessary in every patient suspected for appendicitis, especially in boys presenting with an
obvious clinical picture. On the contrary, US is particularly valuable in girls in whom ovarian conditions must be considered in the differential diagnosis, which might be difficult to achieve clinically [55]. Except for lymphoma, tumors of the small and large bowel are rare in children. Burkitt lymphoma is the most frequent subtype of non-Hodgkin lymphoma occurring in children, and it frequently affects the GI tract, most commonly the terminal ileum [57]. Typically it has a rapidly growing rate and can present with intestinal
Fig. 8. Active Crohn’s disease. Long segment of a bowel loop with narrowed lumen and marked thickening of the intestinal wall, with ill defined outer border (a); small hyperechoic dots are seen within the wall due to deep ulcers (b); on CDS bowel wall hyperemia and prominent vasa recta are seen; also note extramural changes (c); thickened and hyperechoic mesenteric fat with various small round hypoechoic lymph nodes (d).
Please cite this article in press as: Lobo ML, Roque M. Gastrointestinal ultrasound in neonates, infants and children. Eur J Radiol (2014), http://dx.doi.org/10.1016/j.ejrad.2014.04.016
G Model EURR-6752; No. of Pages 9
ARTICLE IN PRESS M.L. Lobo, M. Roque / European Journal of Radiology xxx (2014) xxx–xxx
7
Fig. 9. Intestinal intussusception. Axial US plane of the abdominal right quadrant showing typical features of ileocolic intussusception in an 18 month old infant with crampy abdominal pain (a). Axial US section of the abdominal left quadrant incidentally depicting a transient small bowel intussusception in an asymptomatic patient (b).
obstruction due to secondary intussusception. On US it is usually seen as a mass with low or heterogeneous echogenicity with low vascularity seen on CDS [57]. Several other intestinal conditions may first come to attention during an abdominal US examination, including pathologies resulting from intraluminal conditions such as polyps or abnormal intestinal content (like in cystic fibrosis), bowel wall involvement in various inflammatory (e.g. benign lymphoid hyperplasia), infectious (e.g. viral or bacterial enterocolitis, tuberculous ileocolitis) (Fig. 10b,c), infiltrative and haematologic (e.g. Henoch–Schonlein purpura, hemolytic-uremic syndrome, graft versus host disease, neutropenic colitis) or traumatic disorders, as well as others such as hernias, Meckel’s diverticulum, duplication cysts and other tumor and tumor-like conditions. 4.3. Peritoneal cavity The evaluation of the peritoneal cavity is part of a general abdominal US examination, and it should not be limited to merely search for the presence or absence of peritoneal free or collected fluid. Small amounts of pneumoperitoneum can be depicted by US, easier to see in front of the liver with a linear transducer (tip: avoid transducer pressure). Peritoneal (and scrotal) calcifications can be seen in meconium peritonitis in neonates. Thickening and hyperechogenicity of the mesenteric or omental fat can be the initial clue
to an inflammatory or infectious abdominal process, directing ones attention to the neighboring GI tract segment. Mesenteric lymphadenitis is a common cause for abdominal pain in children, sometimes mimicking acute appendicitis. It is usually a self-limiting disorder due to inflammation of mesenteric lymph nodes caused by different types of bacteria, mycobacteria and viruses [58]. On US using the “sonopalpation” technique, tenderness over a cluster of enlarged mesenteric lymph nodes can be detected. It is important to search for or rule out other conditions causing abdominal pain, as the diagnosis of mesenteric lymphadenitis is generally one of exclusion [58,59]. It should be noted that some mesenteric lymph nodes are commonly seen in pediatric patients on abdominal US, even in asymptomatic children, and not necessarily related to any pathological process [59]. Peritoneal cavity and bowel tumors and tumor-like conditions are rare in children, including benign and malignant etiologies such as (veno-) lymphatic malformations [60], cysts of mesothelial origin, peritoneal primary or secondary malignancies. US is usually the first imaging modality in the evaluation of a child presenting with an abdominal mass, and after a careful examination exclusion of its relation to a solid organ or retroperitoneal origin is usually possible (sometimes supplemented by a “sonographic hydrocolon” to reliably identify the bowel), thus differentiating a GI tract condition from the peritoneal cavity origin.
Fig. 10. Acute abdominal pain. Acute appendicitis with a tender, noncompressible, thickened appendix and the hyperechoic surrounding mesenteric fat on US (a). Infectious enteritis with dilated and thickened walled small bowel loops with small amounts of peritoneal free fluid (b). Follicular lymphoid hyperplasia with gross appendiceal enlargement and thickened, hypoechoic, nodular intermediate wall layer that is hypervascular on CDS, and protrusion of the base of the appendix into the caecum (c).
Please cite this article in press as: Lobo ML, Roque M. Gastrointestinal ultrasound in neonates, infants and children. Eur J Radiol (2014), http://dx.doi.org/10.1016/j.ejrad.2014.04.016
G Model EURR-6752; No. of Pages 9
ARTICLE IN PRESS M.L. Lobo, M. Roque / European Journal of Radiology xxx (2014) xxx–xxx
8
5. Conclusion US is the major imaging tool in the evaluation of the GI-tract in neonates, infants and children – either in clinical routine or with urgent context. With a dedicated and carefully performed US examination of the GI tract using adequate equipment and modern techniques, US can provide important and even essential diagnostic information in many pediatric GI tract conditions. Whilst limitations of US technique should be kept in mind, pediatric GI tract US should be encouraged and promoted thus making use of its huge diagnostic capabilities, helping to avoid and/or limit the need of more aggressive investigations, including those using ionizing radiation.
Conflict of interest There is no financial or other interest concerning the reported topic.
References [1] Dumitriu D, Galloy MA, Claudon M. New techniques in pediatric ultrasound. Ultrasound Clin 2010;5:153–69. [2] Coley BD. The future of pediatric US. Pediatr Radiol 2011;41:S220–7. [3] Darge K, Anupindi S, Keener H, Rompel O. Ultrasound of the bowel in children: how we do it. Pediatr Radiol 2010;40:528–36. [4] Spalinger J, Patriquin H, Miron MC, Marx G, Herzog D, Dubois J, et al. Doppler US in patients with Crohn disease: vessel density in the diseased bowel reflects disease activity. Radiology 2000;217:787–91. [5] Kratz W, von Tirpitz C, Mason R, Reinshagen M, Adler G, Moller P, et al. Contrast-enhanced power Doppler sonography of the intestinal wall in the differentiation of hypervascularized and hypovascularized intestinal obstructions in patients with Crohn’s disease. J Ultrasound Med 2002;21:149–57. [6] Thomson M, Rao P, Berger L, Rawat D. Graded compression and power Doppler ultrasonography versus endoscopy to assess paediatric Crohn disease activity pre- and post-treatment. JPGN 2012;54:404–8. [7] Maconi G, Radice E, Greco S, Bianchi Porro G. Bowel ultrasound in Crohn’s disease. Best Pract Res Clin Gastroenterol 2006;20:93–112. [8] Hirsch W, Kedar R, Preiss U. Color doppler in the diagnosis of the gastroesophageal reflux in children: comparison with pH measurements and B-mode ultrasound. Pediatr Radiol 1996;26:232–5. [9] Sauerbrei EE. Extended field-of-view sonography: utility in clinical practice. J Ultrasound Med 1999;18:335–41. [10] Riccabona M. Pediatric three-dimensional ultrasound: basics and potential clinical value. Clin Imaging 2005;29:1–5. [11] Havre R, Gilja OH. Elastography and strain rate imaging of the gastrointestinal tract. Eur J Radiol 2014;83:438–41. [12] Dillman JR, Stidham RW, Higgins PD, Moons DS, Johnson LA, Rubin JM. US elastography – derived shear wave velocity helps distinguish acutely inflamed from fibrotic bowel in a Crohn disease animal model. Radiology 2013;267:757–66. [13] Attila T, Adler DG, Hilden K, Faigel DO. EUS in pediatric patients. Gastrointest Endosc 2009;70:892–8. [14] Maconi G, Radice E, Bareggi E, Porro GB. Hydrosonography of the gastrointestinal tract. Am J Roentgenol 2009;193:700–8. [15] Gassner I, Geley TE. Sonographic evaluation of oesophageal atresia and tracheooesophageal fistula. Pediatr Radiol 2005;35:159–64. [16] Kim IO, Han TI, Kim WS, Yeon KM. Transperineal ultrasonography in imperforate anus: identification of the internal fistula. J Ultrasound Med 2000;19:211–6. [17] Alison M, Kheniche A, Azoulay R, Roche S, Sebag G, Belarbi N. Ultrasonography of Crohn disease in children. Pediatr Radiol 2007;37:1071–82. [18] Tarján Z, Tóth G, Györke T, Mester A, Karlinger K, Makó EK. Ultrasound in Crohn’s disease of the small bowel. Eur J Radiol 2000;35:176–82. [19] Lee JH, Jeong YK, Hwang JC, Ham SY, Yang SO. Graded compression sonography with adjuvant use of a posterior manual compression technique in the sonographic diagnosis of acute appendicitis. AJR 2002;178:863–6. [20] Pallotta N, Tomei E, Viscido A, Calabrese E, Marcheggiano A, Caprilli R, et al. Small intestine contrast ultrasonography. An alternative to radiology in the assessment of small bowel disease. Inflamm Bowel Dis 2005;11:146–53. [21] Cohen HL, Haller JO, Mestel AL, Coren SC, Schechter S, Eaton DH. Neonatal duodenum: fluid-aided US examination. Radiology 1987;164:805–9. [22] Parente F, Greco S, Molteni M, Anderloni A, Sampietro GM, Danelli PG, et al. Oral contrast enhanced bowel ultrasonography in the assessment of small intestine Crohn’s disease. A prospective comparison with conventional ultrasound, X-ray studies, and ileocolonoscopy. Gut 2004;53:1652–7. [23] Pallotta N, Civitelli F, Di Nardo G, Vincoli G, Aloi M, Viola F, et al. Small intestine contrast ultrasonography in pediatric Crohn’s disease. J Pediatr 2013;163:778–84.
[24] Savino A, Cecamore C, Matronola MF, Verrotti A, Mohn A, Chiarelli F, et al. US in the diagnosis of gastroesophageal reflux in children. Pediatr Radiol 2012;42:515–24. [25] Vandenplas Y, Rudolph CD, Di Lorenzo C, Hassal E, Liptak G, Mazur L, et al. Pediatric gastroesophageal reflux clinical guidelines practice guidelines: joint recommendations of the North American Society for Pediatric Gastroenterology, Hepatology, and Nutricion (NASPGHAN) and the European Society for Pediatric Gastroenterology, Hepatology, and Nutrition (ESPGHAN). J Pediatr Gastroenterol Nutr 2009;49:498–547. [26] Riccabona M, Maurer U, Lackner H, Uray E, Ring E. The role of sonography in the evaluation of gastro-oesophageal reflux – correlation to pH-metry. Eur J Pediatr 1992;151:655–7. [27] Gomes H, Hornoy P, Liehn JC. Ultrasonography and gastric emptying in children: validation of a sonographic method and determination of physiological and pathological patterns. Pediatr Radiol 2003;33:522–9. [28] Koumanidou C, Vakaki M, Pitsoulakis G, Anagnostara A, Mirilas P. Sonographic measurement of the abdominal esophagus length in infancy: a diagnostic tool for gastroesophageal reflux. Am J Roentgenol 2004;183:801–7. [29] Riccabona M, Schwinger W. The role of colour Doppler sonography in the assessment of gastro-oesophageal reflux in infants, German [Stellenwert der Farbdopplersonographie beim gastroösophagealen Reflux im Säuglingsalter]. Ultraschall Klin Prax 1993;8:131–4. [30] Riccabona M. Ultrasonography for hypertrophc pyloric stenosis–prognostic assessment based on sonographic criteria, German [Sonographie bei der hypertrophen Pylorusstenose – Versuch einer prognostischen Aussage anhand sonographischer Kriterien]. WiKliWo 1990;102:13–5. [31] Hernanz-Schulman M. Pyloric stenosis: role of imaging. Pediatr Radiol 2009;39:S134–9. [32] Riccabona M, Weitzer C, Lindbichler F, Mayr J. Sonography and color Doppler sonography for monitoring conservatively treated infant hypertrophic pyloric stenosis. JUM 2001;20:997–1002. [33] Dufour D, Delaet MH, Dassonville M, Cadranel S, Perlmutter N. Midgut malrotation, the reliability of sonographic diagnosis. Pediatr Radiol 1992;22: 21–3. [34] Pracros JP, Sann L, Genin G, Tran-Minh VA, Morin de Finfe CH, Forey, et al. Ultrasound diagnosis of midgut volvulus: the “whirlpool” sign. Pediatr Radiol 1992;22:18–20. [35] Yousefzadeh DK. The position of the duodenojejunal junction: the wrong horse to bet on in diagnosing or excluding malrotation. Pediatr Radiol 2009;39:S172–7. [36] Menten R, Reding R, Godding V, Dumitriu D, Clapuyt P. Sonographic assessment of the retroperitoneal position of the third portion of the duodenum: an indicator of normal intestinal rotation. Pediatr Radiol 2012;42:941–5. [37] Veyrac C, Baud C, Prodhomme O, Saguintaah M, Couture A. US assessment of neonatal bowel (necrotizing enterocolitis excluded). Pediatr Radiol 2012;42:S107–14. [38] Riccabona M, Haim M, Kutschera J. Sonografically guided reduction of meconium ileus in preterm neonates. Eur Radiol 2006;16(Suppl. 1):284. [39] Kim WY, Kim WS, Kim IO, Kwon TH, Chang W, Lee EK. Sonographic evaluation of neonates with early-stage necrotizing enterocolitis. Pediatr Radiol 2005;35:1056–61. [40] Epelman M, Daneman A, Navarro OM, Morag I, Moore AM, Kim JH, et al. Necrotizing enterocolitis: review of state-of-the-art imaging findings with pathologic correlation. Radiographics 2007;27:285–305. [41] Silva CT, Daneman A, Navarro OM, Moore AM, Moineddin R, Gerstle JT, et al. Correlation of sonographic findings and outcome in necrotizing enterocolitis. Pediatr Radiol 2007;37:274–82. [42] Muchantef K, Epelman M, Darge K, Kirpalani H, Laje P, Anupindi SA. Sonographic and radiographic imaging features of the neonate with necrotizing enterocolitis: correlating findings with outcomes. Pediatr Radiol 2013;43: 1444–52. [43] Haber HP, Stern M. Intestinal ultrasonography in children and young adults: bowel wall thickness is age dependent. J Ultrasound Med 2000;19:315–21. [44] Bremner AR, Griffiths M, Argent JD, Fairhurst JJ, Beattie RM. Sonographic evaluation of inflammatory bowel disease: a prospective, blinded, comparative study. Pediatr Radiol 2006;36:947–53. [45] Haber HP, Busch A, Ziebach R, Dette S, Ruck P, Stern M. Ultrasonographic findings correspond to clinical, endoscopic, and histologic findings in inflammatory bowel disease and other enterocolitides. J Ultrasound Med 2002;21: 375–82. [46] Di Nardo G, Aloi M, Oliva S, Civitelli F, Casciani E, Cucchiara S. Investigation of small bowel in pediatric Crohn’s disease. Inflamm Bowel Dis 2012;8:1760–76. [47] Castiglione F, Mainenti PP, De Palma GD, Testa A, Bucci L, Pesce G, et al. Noninvasive diagnosis of small bowel Crohn’s disease: direct comparison of bowel sonography and magnetic resonance enterography. Inflamm Bowel Dis 2013;19:991–8. [48] Magalhaes J, Leite S, Cotter J. Contrast-enhanced ultrasonography for assessment of activity of Crohn’s disease: the future? J Crohns Colitis 2013;7:e607. [49] Verschelden P, Filiatrault D, Garel L, Grignon A, Perreault G, Boisvert J, et al. Intussusception in children: reliability of US in diagnosis-a prospective study. Radiology 1992;184:741–4. [50] Del-Pozo G, Albillos JC, Tejedor D, Calero R, Rasero M, de-la-Calle U, et al. Intussusception in children: current concepts in diagnosis and enema reduction. Radiographics 1999;19:299–319. [51] Daneman A, Navarro O. Intussusception. Part 2: An update on the evolution of management. Pediatr Radiol 2004;34:97–108.
Please cite this article in press as: Lobo ML, Roque M. Gastrointestinal ultrasound in neonates, infants and children. Eur J Radiol (2014), http://dx.doi.org/10.1016/j.ejrad.2014.04.016
G Model EURR-6752; No. of Pages 9
ARTICLE IN PRESS M.L. Lobo, M. Roque / European Journal of Radiology xxx (2014) xxx–xxx
[52] Quigley AJ, Stafrace S. Ultrasound assessment of acute appendicitis in paediatric patients: methodology and pictorial overview of findings seen. Insights Imaging 2013;4:741–51. [53] Linam LE, Munden M. Sonography as the first line of evaluation in children with suspected acute appendicitis. J Ultrasound Med 2012;31:1153–7. [54] Trout AT, Sanchez R, Ladino-Torres MF. Reevaluating the sonographic criteria for acute appendicitis in children: a review of the literature and a retrospective analysis of 246 cases. Acad Radiol 2012;19(11):1382–94. [55] Strouse PJ. Pediatric appendicitis: an argument for US. Radiology 2010;255:8–13. [56] Hernanz-Schulman M. CT and US in the diagnosis of appendicitis: an argument for CT. Radiology 2010;255:3–7.
9
[57] Phillips GS, Pruthi S. Acquired lesions of the small intestines. In: Coley BD, editor. Caffey’s pediatric diagnostic imaging. Philadelfia: Elsevier; 2013. p. 1091–106. [58] Simanovsky N, Hiller N. Importance of sonographic detection of enlarged abdominal lymph nodes in children. J Ultrasound Med 2007;26:581–4. [59] Karmazyn B, Werner EA, Rejaie B, Applegate KE. Mesenteric lymph nodes in children: what is normal. Pediatr Radiol 2005;35:774–7. [60] Kalmar PI, Petnehazy T, Wießpeiner U, Beer M, Hauer AC, Till H, et al. Large, segmental, circular vascular malformation of the small intestine (in a female toddler with hematochezia): unusual presentation in a child. BMC Pediatr 2014;14:55, http://dx.doi.org/10.1186/1471-2431-14-55.
Please cite this article in press as: Lobo ML, Roque M. Gastrointestinal ultrasound in neonates, infants and children. Eur J Radiol (2014), http://dx.doi.org/10.1016/j.ejrad.2014.04.016
ARTICLE IN PRESS European Journal of Radiology xxx (2014) xxx–xxx
Contents lists available at ScienceDirect
European Journal of Radiology journal homepage: www.elsevier.com/locate/ejrad
Gastrointestinal ultrasound in neonates, infants and children Maria Luisa Lobo ∗ , Mariana Roque Servic¸o de Imagiologia Geral, Hospital de Santa Maria – Centro Hospitalar Lisboa Norte (CHLN), Av. Prof. Egas Moniz, 1649-035 Lisboa, Portugal
a r t i c l e
i n f o
Article history: Received 31 March 2014 Received in revised form 12 April 2014 Accepted 15 April 2014 Keywords: Ultrasound Gastrointestinal tract Pediatrics Neonates/children
a b s t r a c t Today US plays an important and increasing role in the assessment of many, partially age-specific conditions in the GI tract in neonates, infants and children. Knowledge of the potential capabilities of US and its restrictions together with a skillful performance of GI US examination can provide essential anatomic and functional diagnostic information in many pediatric GI disorders. The aim of this review is to highlight the potential of ultrasound (US) in the evaluation of the gastrointestinal (GI) tract in neonates, infants and children. Basic and potential applications of modern US tools in pediatric GI tract are addressed, the GI US examination technique is discussed – including some common and/or typical clinical applications of and indications for US. © 2014 Elsevier Ireland Ltd. All rights reserved.
1. Introduction Ultrasound (US) is an excellent imaging modality in the evaluation of the gastrointestinal (GI) tract in pediatric patients. Besides its well-established primordial diagnostic role in some typical pediatric GI conditions such as in hypertrophic pyloric stenosis (HPS) and intestinal intussusception, US diagnostic capabilities has been widely explored in several other GI tract diseases such as in acute appendicitis, inflammatory bowel disease (IBD), necrotizing enterocolitis (NEC), intestinal malrotation, gastro-oesophageal reflux (GER), and even in less conventional applications such as in patients with esophageal atresia and tracheoesophageal fistula. Furthermore, US is an excellent bedside high yield imaging tool for neonates, infants and children in intensive care units and it can also be used to guide therapeutic maneuvers like in reduction of intussusception or in enema for meconium ileus. Since its introduction in clinical practice, US technology along with computed imaging processing has greatly progressed allowing for higher resolution and better quality imaging with higher diagnostic reliability [1], thus with ongoing expanding clinical applications [2]. These modern approaches and the advent of high resolution transducers have made US an essential imaging technique in pediatric GI tract that has initially not been considered suitable for US assessment. The well known advantages of US, particularly its lack of ionizing radiation and easy access, together with the general good anatomic profile of young patients, makes
∗ Corresponding author. Tel.: +351 217805085; fax: +351 217805085. E-mail addresses: [email protected], [email protected] (M.L. Lobo), [email protected] (M. Roque).
this imaging technique an ideal one for the evaluation of the pediatric patient with GI tract complaints. Major limitations include its operator-dependency and reproducibility, apart from factors related to the patient such as painful abdomen, noncollaboration, obesity and interposition of large amount of gas. Some of these drawbacks can be overcome with a careful, dedicated and comprehensive technique examination using modern US capabilities [3]. The aim of this paper is to highlight the potential of US in the evaluation of the GI tract in neonates, infants and children. In this review we address basic and potential applications of modern US tools in pediatric GI tract, review the GI US examination technique, and discuss some common and/or typical clinical applications and indications of US in the evaluation of the GI tract in neonates, infants and children. The in depth discussion of all pathologic entities and all the detailed imaging findings is beyond the scope of this paper.
2. Potential applications of modern US tools in the pediatric GI tract In the last decades, advances in US technology have greatly improved the quality of GI US imaging with a consequent positive impact on its diagnostic yield. Improvement in US probes, particularly high-resolution linear probes, with new piezoelectric material incorporated and broadband techniques permit better spatial resolution in the near-field and better penetration in the far-field, whereas improvement in contrast resolution can now be achieved with recent US modes like image compounding, speckle/noise reduction filters and (tissue) harmonic imaging [1–3].
http://dx.doi.org/10.1016/j.ejrad.2014.04.016 0720-048X/© 2014 Elsevier Ireland Ltd. All rights reserved.
Please cite this article in press as: Lobo ML, Roque M. Gastrointestinal ultrasound in neonates, infants and children. Eur J Radiol (2014), http://dx.doi.org/10.1016/j.ejrad.2014.04.016
G Model EURR-6752; No. of Pages 9
ARTICLE IN PRESS M.L. Lobo, M. Roque / European Journal of Radiology xxx (2014) xxx–xxx
2
Endoscopic US is another emerging field in adult GI tract imaging, although with limited experience and applicability in the pediatric population, partially due to lack of dedicated pediatric transducers [13].
3. Gastrointestinal US technique and how to improve pediatric GI US examination
Fig. 1. Extended field of view. US imaging documentation of a long segment of the colon in a patient with colitis due to Crohn’s disease. Courtesy: M. Riccabona, Graz.
Likewise, progress in Doppler techniques allows better depiction and quantification of even slow flow of small vessels within the normal and pathological GI structures [1,3,4]. With the use of US contrast agents (US-CA) and contrast specific US modes, contrast-enhanced US (ce-US) enables further characterization of flow dynamics and enhancement pattern in real time [1,3,5]. Although limited research has been conducted in the pediatric population, mainly because currently available (US-CA) have not been approved for pediatric use yet, some studies have pointed out its potential benefit in the evaluation of the pediatric GI tract, for instances in the assessment of disease activity in IBD [5,6,7]. In pediatric abdominal blunt trauma intravenous ce-US seems to improve the detection of solid organ lesions compared unenhanced US, but it is limited in the identification of bowel or mesenteric traumatic lesions [1]. Potential benefit from the non-vascular use of US-CA have also been referred in the literature [2,3], as in ce-US evaluation of GER [8]. Extended field of view or panoramic US can be extremely useful in GI US, particularly in the evaluation of the bowel (Fig. 1). The reconstruction of a wide image by correlating data from consecutive images adding these frames together to one large picture allows demonstration of large segments of the bowel and to make correct length measurements [1,3,9]. Volume US or three-dimensional US (3DUS) has been shown to improve volume assessment, and has the potential to improve documentation and comparison between different studies [1,10]. Clinical experience with 3DUS in the pediatric GI tract is limited, with few reports in the literature related to the calculation of gastric volume in GER disease or in tumor volume assessment. Recording US video clips is another useful option in GI US imaging that allows, in addition to the conventional review of the real time images, documentation of gastric motility and bowel peristalsis as well as air bubbles movement in GI fistulous sinus tracts or in bowel perforation, e.g. in premature babies with NEC. US elastography is an emerging US application in various abdominal clinical fields for assessment of “stiffness” of a tissue. Growing experience has been obtained in liver diseases as well as on oncology, particularly in adult population [1]. Recently extended applications have also been explored, including the GI tract particularly in IBD. In the GI tract, specific challenges rise from the anatomy and physiology of the bowel with thin wall, non-constant boundary conditions and intrinsic contractility, although pathological conditions are often related with increased bowel wall thickness and decreased bowel peristalsis [11,12].
For any US examination the choice of adequate transducers and adjustment of basic parameters as well as the choice of US modality is fundamental to obtain a proper image quality. In general, the optimal transducer should have the highest possible frequency still allowing to penetrate to the targeted anatomical area thus offering best spatial resolution. After initial evaluation of the entire abdominal cavity that can be performed with a curved array transducer, the individual structures of GI tract are then specifically examined with a high resolution linear probe which allows detailed visualization of the oesophageal-, gastric- and bowel wall as well as of the relevant surrounding structures [3,14]. Not infrequently, curved array (and sometimes sector) probes may also be needed in order to obtain a better access window to image deeper structures in older children (like the oesophago-gastric junction, the sigmoid colon and rectum) or to allow for a broader field of view. In addition to the conventional transabdominal US approach, other less common approaches might be necessary, and should be included, in specific situations such as the suprasternal and mediastinal US approach to visualize the upper oesophagus in oesophageal atresia [15] or the perineal US approach to evaluate the anal canal or the distal rectal pouch location [16] and its distance to the skin surface in anorectal or in cloacal malformations. When imaging the bowel by US, a methodic and systematic analysis is crucial to facilitate a thorough evaluation of the various intestinal segments as complete as possible. As mentioned before, extended field of view imaging can be helpful to document large segments of diseased bowel and recording US cine loop clips is useful to demonstrate normal or abnormal GI motility. Bowel gas interposition is a well known limitation to US examinations, but with a careful and proper bowel US technique this obstacle can often be at least partially overcome. Particularly gentle graded compression is the essential technique in US of the GI tract, as it displaces undesirable gas, shortens the distance to the skin surface and isolates the bowel loops while displacing adjacent ones [3,17,18]. Furthermore, it helps to localize the origin of pain (“sonopalpation”) and to assess the bowel compressibility, which is an important sign in the evaluation of the bowel. The adjuvant use of posterior manual compression [3,19] can also be helpful, particularly for the evaluation of the right iliac fossa. Changing patient position is another easy way to move disturbing air/gas away from the area to examine. GI luminal filling after oral intake of water or another liquid meal or with oral or rectal administration of saline fluid (hydrosonography) is particularly useful to optimize US evaluation of the GI tract [14,20,21]. These techniques have been applied to several pediatric conditions for decades. In addition to improve visualization with the distension obtained, it also helps to displace gas/air and, in the upper GI tract it enables to verify pylorus channel opening or to confirm the duodenal or duodeno-jejunal junction position. Moreover, in small patients and particularly in critical ill neonates, a small bowel follow-through can be performed and followed by US. Furthermore, filling techniques are the basis for therapeutic maneuvers under US guidance as in the non-surgical reduction of an ileocolic intussusception or in the attempt to resolve meconium ileus using an enema.
Please cite this article in press as: Lobo ML, Roque M. Gastrointestinal ultrasound in neonates, infants and children. Eur J Radiol (2014), http://dx.doi.org/10.1016/j.ejrad.2014.04.016
G Model EURR-6752; No. of Pages 9
ARTICLE IN PRESS M.L. Lobo, M. Roque / European Journal of Radiology xxx (2014) xxx–xxx
Since the 1990s, the US evaluation of the small bowel with a non-absorbable anechoic oral contrast, such as isotonic polyethylene glycol (PEG), also known as small intestine ce-US (SICUS), has shown advantages over conventional bowel US in various adulthood intestinal pathologies [14,20,22]. In Crohn’s disease it was found to be comparable to ileo-colonoscopy, wireless capsule endoscopy, and small-bowel sonography in the assessment of the number, site, extension, and postoperative recurrence of small bowel lesions; but only few studies have specifically addressed the pediatric population [14,22,23]. Particularly important, SICUS seems advantageous in the depiction of proximal small bowel lesions, a commonly affected GI intestinal segment in younger patients which is less accurately assessed by non-contrast bowel US [14,20,23]. Although SICUS has been shown to be a more reliable technique with improved sensitivity and specificity compared with conventional bowel US in the evaluation of patients with suspected or known Crohn’s disease [20], it is a time consuming examination (mean duration of 30–40 min) which is in discordance with the expected advantages of US as a simple, practical and rapid examination [14,22]. Thus, in clinical practice the decision to perform SICUS is usually case-based according to the clinical context and the experience of the operator, and the availability and applicability of the contrast agent.
4. Indications and some clinical applications of GI US in neonates, infants and children 4.1. Upper GI tract In neonates with oesophageal atresia, usually diagnosed with frontal and lateral radiograms, US can give additional valuable information to the surgeon. Besides the role of abdominal and cardiac US to search for associated abnormalities, mediastinal US allows the characterization of the length, morphology and structure of the wall of the blind upper oesophageal pouch which can be improved by the administration of small amount of saline fluid through the oesophageal tube [15]; sometimes even a tracheaoesophageal fistula may be recognized by US. Moreover, the definition of the anatomic position of the aortic arch is crucial to plan the surgical approach. With a superior abdominal US approach the cardia and the adjacent distal oeosophagus are often easily depicted, although visualization of the entire distal esophageal length behind the heart is difficult and restricted [15]. In neonates and infants with suspected gastro-oesophageal reflux disease (GERD) US is a widely available, non-invasive and sensitive method that can provide both useful anatomical and functional information [24–28] (Fig. 2), although it’s role is still controversial and debated [24,25]. The complex issue of GER and GERD is related to many factors, including the nonspecific nature of symptoms in young children, the difficult distinction between physiological and pathological GER, and the impasse to establish a cause-effect relationship between GER and symptoms or complications related to GERD [24,25]. Nevertheless, US is considered by many authors as a first noninvasive imaging tool in a child with vomiting, particular in patients younger than 2 years of age, as it can provide alternative diagnosis other than GER and rule out gastric outlet obstruction [24]. More important than the detection of GER per se, one can correlate those with the occurrence of clinical symptoms. Furthermore, US can give information on functional aspects such as the oesophageal clearance of the gastric content refluxed, the opening of the gastro-oesophageal junction, the gastric emptying, and can potentially detect an associated hiatal hernia [26,27]. Anatomic details of the gastro-oesophageal structure, like the length of the abdominal oesophagus and the gastro-oesophageal angle (“His angle”), can be assessed and seem to have high sensitivity and high
3
Fig. 2. GER. Longitudinal US section of the epigastric region showing opening of the cardia and reflux of gastric content into the lower esophagus.
positive predictive value for GER [24,28]. Colour Doppler sonography (CDS) may increase the sensitivity of US for detection of GER although it might be sometimes difficult to apply due to artifacts caused by the cardiac movement [8]; it definitely is a good tool for documentation if no video clips can be stored [29]. US is generally considered the modality of choice to confirm or exclude the diagnosis of hypertrophic pyloric stenosis (HPS). The diagnosis of HPS is based on US morphological and dynamic findings with the most significant criteria being a thickened pyloric muscle (greater than 3 mm) and the lack of luminal opening of the pyloric channel [30–32] (Fig. 3). The usually distended stomach, seen as an indirect sign of gastric outlet obstruction, must be interpreted according to the time of the last meal. Changing the patient position may be necessary to improve visualization of the pylorus
Fig. 3. HPS. Longitudinal US section of the pylorus. Thickened hypoechoic pyloric muscle (A x. . .x) and elongated pyloric channel (B X. . .X) with persistent nonopening of the lumen on real time US.
Please cite this article in press as: Lobo ML, Roque M. Gastrointestinal ultrasound in neonates, infants and children. Eur J Radiol (2014), http://dx.doi.org/10.1016/j.ejrad.2014.04.016
G Model EURR-6752; No. of Pages 9
ARTICLE IN PRESS M.L. Lobo, M. Roque / European Journal of Radiology xxx (2014) xxx–xxx
4
Fig. 4. Gastric duplication cyst. Transverse US section of the right upper abdomen showing the typical “gut signature” wall of an abdominal cyst in a 6 month old infant with profuse vomiting (a). After filling the stomach with a small amount of saline fluid it was possible to document its close relation with the anterior wall of the anthropyloric region causing obstruction of the gastric outlet (b).
channel that might be hidden by a distended stomach. It is also important to analyze the pylorus channel over time, which will allow the differentiation between HPS and pylorospasm, a transient phenomenon that may have similar morphological and measurements features with HPS. In doubtful or equivocal cases, a repeated US examination several hours later may clarify the diagnosis and nowadays the need of other diagnostic imaging tools is extremely rare [30,31]. US may also serve for follow-up in conservatively treated patients [32]. Gastric duplication cysts are usually easily to recognize when they exhibit the typical US features of a cystic structure with a thick layered wall. Filling the stomach with fluid is helpful to define the close relationship of the cyst with the gastric wall. If located in the antro-pyloric region they often cause a gastric outlet obstruction (Fig. 4). Other gastric conditions may be first suspected during an abdominal US performed in a child with vomiting, epigastric pain or nonspecific abdominal complains, either by causing focal or diffuse thickening of the gastric wall such as eosinophilic gastritis, chronic granulomatous disease and tumoral and pseudotumoral conditions, or by the presence of an endoluminal abnormality such as polyps (Fig. 5), bezoars or ingested foreign body. Also infiltrating (e.g. lymphoma) or tumorous (e.g. leiomyoma) stomach wall conditions may be depictable by US. After US evaluation of the oesophago-gastric junction, the stomach and the pylorus, the next step is to follow the duodenum to look at the position of the third part of the duodenum (D3) normally passing between the abdominal aorta and the superior mesenteric artery, and to identify the duodeno-jejunal junction on the left side of the aorta.
of the mesenteric vessels (the “whirlpool sign”) with a pseudotumorous aspect, must lead to emergent surgery to prevent intestinal ischemia, necrosis and perforation [34]. Diagnosis of neonatal bowel obstruction, or confirmation of a suspected prenatal diagnosis, is usually based on clinical and radiological signs on abdominal plain film occurring with a delay of at least 12–24 h; in some partial or very distal obstruction it may present even later. Besides the search for associated malformations, US can contribute with important additional information [35,37], such as: early diagnosis of a mechanical occlusion (e.g. malrotation with volvolus); assessment of the colon size and its content (e.g. normal colon in proximal small bowel atresia; microcolon with abnormal hyperechogenic meconium in distal small bowel atresia and in meconium ileus, or with hydrocolon in meconium plug syndrome and small left colon syndrome) which is a main marker to assume the probable location of the obstruction thus indicating the need to perform a contrast enema in case of lower bowel obstruction such as in meconium ileus or in meconium plug syndrome; occasional detection of the cause of obstruction, either intrinsic (e.g. duodenal web) or extrinsic (e.g. GI duplication cyst or
4.2. Small and large bowel An abnormal relationship between the superior mesenteric artery and the superior mesenteric vein should raise suspicion of a intestinal malrotation, although a normal position does not exclude the presence of abnormal midgut rotation [33,34]. In addition, a normal retroperitoneal position of D3 is said to be a more reliable sign to exclude malrotation than does the position of the mesenteric vessels [35,36]. US screening for intestinal malrotation in an asymptomatic pediatric patient aims at preventing future obstructive or ischemic complications or completing a US work-up for unspecific complaints, whereas the sonografic diagnosis of malrotation with acute volvulus, on US seen by the characteristic twist
Fig. 5. Gastric polyp. Axial US section of the stomach after oral intake of water revealing a gastric polypoid lesion in a 15 years old male with Peutz–Jeghers syndrome.
Please cite this article in press as: Lobo ML, Roque M. Gastrointestinal ultrasound in neonates, infants and children. Eur J Radiol (2014), http://dx.doi.org/10.1016/j.ejrad.2014.04.016
G Model EURR-6752; No. of Pages 9
ARTICLE IN PRESS M.L. Lobo, M. Roque / European Journal of Radiology xxx (2014) xxx–xxx
5
Fig. 6. Anorectal malformation. Perineal US approach in longitudinal (a) and axial (b) planes in a neonate with imperforated anus. The dilated colon is seen coming down below the level of the pubo-coccigeal line, with the anal blind end pouch located within a few millimeters from the perineal surface.
annular pancreas); presence of free intraperitoneal fluid and/or air, and signs of vascular compromise indicating of bowel ischemia and perforation. In addition to its diagnostic role, US can also be used for therapeutical purpose to guide enema reduction of meconium ileus – or meconium plug equivalent – which is particularly useful as a bedside procedure in critically ill preterm babies in the neonatal intensive care unit who cannot be brought to the fluoroscopic suit [38]. In anorectal malformations perineal US can help defining the type of malformation (Fig. 6). The distance between the rectal cul-de-sac and the perineum can be reliably measured by using a transperineal approach, and US may identify the location and course of the urorectal fistula [16,35,37]. The role of US in necrotizing enterocolitis has been increasingly recognized [39–42], with higher sensitivity than plain films in the detection of early changes such as wall thickening and disturbed bowel wall perfusion, intestinal pneumatosis and portal pneumatosis [38] (Fig. 7) as well as early signs of perforation [39,40]. It has also been suggested that US findings are useful in predicting outcome [41,42]. US may also be useful in the diagnosis of post-enterocolitis stenosis [40]. In suspicion of bowel obstruction in older children, US may help to differentiate between mechanical or functional intestinal occlusion, may detect the transition zone, and may show worrying signs related to vascular compromise of the involved bowel. Bowel wall thickening is the hallmark of intestinal diseases. Bowel wall thickness increases with age [43], and in the pediatric population bowel wall thickness greater than 2.5 mm and 2 mm respectively for the small and large bowel are considered abnormal [43]. A careful and attentive abdominal US examination in a child with unclear clinical symptoms may reveal not only a thickened bowel wall, but also the location and extension of the involved segments, their vascular features on CDS, and the presence of extramural signs of disease such as hyperechogenicity of surrounding fat planes, abscesses and fistulas [3–5,17,20,23]; abnormal bowel wall stratification and abnormal peristalsis should also be noted. Although US signs are generally nonspecific, the correlation of the US findings with the clinical history and laboratorial data often permits to narrow the differential diagnosis, thus directing further additional imaging in a more efficient way. The role of US in inflammatory bowel disease (IBD), and particularly in Crohn’s disease, has been thoroughly evaluated in adults and to a limited extent in children [17,18,44–48]. Most published studies have found bowel US a valuable tool in patients with suspected or known IBD. Although US has a good negative predictive value for Crohn’s disease in patients with a clinical suspicion of IBD
allowing for more invasive diagnostic procedures to be postponed [17,46], its main application is in the follow-up of patients with known IBD to monitor treatment and to ensure early detection of intra-abdominal complications in relapse [7,17,46]. Assessment of vascularity with CDS provides additional information about disease activity [4,5,7,47,48] and it may help to distinguish between inflammatory and fibrotic bowel stenosis [5], although its exact role has yet to be defined [7,46,48] (Fig. 8). US has become the modality of choice to accurately diagnose or exclude intestinal intussusception [49]. Moreover, US can determine the location and the type of the intussusception (idiopathic versus secondary to the presence of a lead point, or ileo-ileal intussusception), which has a decisive impact on the therapeutic approach, as well as signs related to nonsurgical reduction success [50,51]. Typical signs of ileocolic intussusception include the “target” or “doghnut” sign and the “pseudokidney” sign respectively on transverse and longitudinal planes (Fig. 9a). Transient and asymptomatic small bowel intussusceptions are relatively common and should not be confused with ileocolic intussusception that needs urgent reduction. The former are usually encountered around the periumbilical region, are smaller (less than 2 cm) in diameter, do not exhibit the hyperechoic central core (Fig. 9b), and tend to resolve spontaneously within a few minutes [51]. In ileocolic intussusception, a small amount of intraperitoneal free fluid can often be seen, and should not preclude a nonsurgical reduction attempt. On the other hand, the presence of trapped fluid within the intussusception and the absence of flow on CDS in the intussuscetum wall raise the suspicion of vascular compromise of the bowel, and are related to lower success rate of nonsurgical reduction [50,51]. Although these signs are not considered absolute contraindications to attempt nonsurgical reduction, when present a nonsurgical reduction should be performed with extremely caution due to the high risk of perforation [51]. US guidance of hydrostatic or air enema reduction of intestinal ileocolic intussusception has been successfully used for therapeutic purpose in many centers [51]. Appendicitis is the most common pediatric surgical emergency [52–54]. For the last decades, imaging has become an important diagnostic contributor to timely improve reliability of diagnosis and to lower the rate of unnecessary appendectomies, although the exact place of the different imaging modalities is still a matter of debate [55,56]. US should be encouraged and promoted as it can often provide a reliable contribution to the diagnosis by supporting or, more rarely, excluding appendicitis, and by helping in the differential diagnosis – thus avoiding unnecessary radiation exposure from CT in a significant number of patients in whom imaging is needed [54–56] (Fig. 10a). Typical findings include
Please cite this article in press as: Lobo ML, Roque M. Gastrointestinal ultrasound in neonates, infants and children. Eur J Radiol (2014), http://dx.doi.org/10.1016/j.ejrad.2014.04.016
G Model EURR-6752; No. of Pages 9
ARTICLE IN PRESS M.L. Lobo, M. Roque / European Journal of Radiology xxx (2014) xxx–xxx
6
Fig. 7. Necrotizing enterocolitis. Thickened small bowel loops with intestinal pneumatosis seen as hyperechoic dots within the bowel wall; peritoneal free fluid and pneumoperitoneum (a). Axial plan of the liver showing mulitple hyperechoic dots in a linear arrangement extending to the periphery of the liver parenchymal due portal pneumatosis (b). Courtesy: M. Riccabona, Graz.
an enlarged (outer diameter greater than 6 mm usually is used as cut-off), non compressible and tender appendix, sometimes with an appendicolith, with surrounding infiltration of the periappendicular fat; on CDS increased vascularity of the appendicular wall is seen in early inflammatory phases, whereas no flow can be detected if the appendix is necrotic or perforated; other secondary changes include peri-appendicular free fluid or collected fluid [52,54]. Imaging is not always necessary in every patient suspected for appendicitis, especially in boys presenting with an
obvious clinical picture. On the contrary, US is particularly valuable in girls in whom ovarian conditions must be considered in the differential diagnosis, which might be difficult to achieve clinically [55]. Except for lymphoma, tumors of the small and large bowel are rare in children. Burkitt lymphoma is the most frequent subtype of non-Hodgkin lymphoma occurring in children, and it frequently affects the GI tract, most commonly the terminal ileum [57]. Typically it has a rapidly growing rate and can present with intestinal
Fig. 8. Active Crohn’s disease. Long segment of a bowel loop with narrowed lumen and marked thickening of the intestinal wall, with ill defined outer border (a); small hyperechoic dots are seen within the wall due to deep ulcers (b); on CDS bowel wall hyperemia and prominent vasa recta are seen; also note extramural changes (c); thickened and hyperechoic mesenteric fat with various small round hypoechoic lymph nodes (d).
Please cite this article in press as: Lobo ML, Roque M. Gastrointestinal ultrasound in neonates, infants and children. Eur J Radiol (2014), http://dx.doi.org/10.1016/j.ejrad.2014.04.016
G Model EURR-6752; No. of Pages 9
ARTICLE IN PRESS M.L. Lobo, M. Roque / European Journal of Radiology xxx (2014) xxx–xxx
7
Fig. 9. Intestinal intussusception. Axial US plane of the abdominal right quadrant showing typical features of ileocolic intussusception in an 18 month old infant with crampy abdominal pain (a). Axial US section of the abdominal left quadrant incidentally depicting a transient small bowel intussusception in an asymptomatic patient (b).
obstruction due to secondary intussusception. On US it is usually seen as a mass with low or heterogeneous echogenicity with low vascularity seen on CDS [57]. Several other intestinal conditions may first come to attention during an abdominal US examination, including pathologies resulting from intraluminal conditions such as polyps or abnormal intestinal content (like in cystic fibrosis), bowel wall involvement in various inflammatory (e.g. benign lymphoid hyperplasia), infectious (e.g. viral or bacterial enterocolitis, tuberculous ileocolitis) (Fig. 10b,c), infiltrative and haematologic (e.g. Henoch–Schonlein purpura, hemolytic-uremic syndrome, graft versus host disease, neutropenic colitis) or traumatic disorders, as well as others such as hernias, Meckel’s diverticulum, duplication cysts and other tumor and tumor-like conditions. 4.3. Peritoneal cavity The evaluation of the peritoneal cavity is part of a general abdominal US examination, and it should not be limited to merely search for the presence or absence of peritoneal free or collected fluid. Small amounts of pneumoperitoneum can be depicted by US, easier to see in front of the liver with a linear transducer (tip: avoid transducer pressure). Peritoneal (and scrotal) calcifications can be seen in meconium peritonitis in neonates. Thickening and hyperechogenicity of the mesenteric or omental fat can be the initial clue
to an inflammatory or infectious abdominal process, directing ones attention to the neighboring GI tract segment. Mesenteric lymphadenitis is a common cause for abdominal pain in children, sometimes mimicking acute appendicitis. It is usually a self-limiting disorder due to inflammation of mesenteric lymph nodes caused by different types of bacteria, mycobacteria and viruses [58]. On US using the “sonopalpation” technique, tenderness over a cluster of enlarged mesenteric lymph nodes can be detected. It is important to search for or rule out other conditions causing abdominal pain, as the diagnosis of mesenteric lymphadenitis is generally one of exclusion [58,59]. It should be noted that some mesenteric lymph nodes are commonly seen in pediatric patients on abdominal US, even in asymptomatic children, and not necessarily related to any pathological process [59]. Peritoneal cavity and bowel tumors and tumor-like conditions are rare in children, including benign and malignant etiologies such as (veno-) lymphatic malformations [60], cysts of mesothelial origin, peritoneal primary or secondary malignancies. US is usually the first imaging modality in the evaluation of a child presenting with an abdominal mass, and after a careful examination exclusion of its relation to a solid organ or retroperitoneal origin is usually possible (sometimes supplemented by a “sonographic hydrocolon” to reliably identify the bowel), thus differentiating a GI tract condition from the peritoneal cavity origin.
Fig. 10. Acute abdominal pain. Acute appendicitis with a tender, noncompressible, thickened appendix and the hyperechoic surrounding mesenteric fat on US (a). Infectious enteritis with dilated and thickened walled small bowel loops with small amounts of peritoneal free fluid (b). Follicular lymphoid hyperplasia with gross appendiceal enlargement and thickened, hypoechoic, nodular intermediate wall layer that is hypervascular on CDS, and protrusion of the base of the appendix into the caecum (c).
Please cite this article in press as: Lobo ML, Roque M. Gastrointestinal ultrasound in neonates, infants and children. Eur J Radiol (2014), http://dx.doi.org/10.1016/j.ejrad.2014.04.016
G Model EURR-6752; No. of Pages 9
ARTICLE IN PRESS M.L. Lobo, M. Roque / European Journal of Radiology xxx (2014) xxx–xxx
8
5. Conclusion US is the major imaging tool in the evaluation of the GI-tract in neonates, infants and children – either in clinical routine or with urgent context. With a dedicated and carefully performed US examination of the GI tract using adequate equipment and modern techniques, US can provide important and even essential diagnostic information in many pediatric GI tract conditions. Whilst limitations of US technique should be kept in mind, pediatric GI tract US should be encouraged and promoted thus making use of its huge diagnostic capabilities, helping to avoid and/or limit the need of more aggressive investigations, including those using ionizing radiation.
Conflict of interest There is no financial or other interest concerning the reported topic.
References [1] Dumitriu D, Galloy MA, Claudon M. New techniques in pediatric ultrasound. Ultrasound Clin 2010;5:153–69. [2] Coley BD. The future of pediatric US. Pediatr Radiol 2011;41:S220–7. [3] Darge K, Anupindi S, Keener H, Rompel O. Ultrasound of the bowel in children: how we do it. Pediatr Radiol 2010;40:528–36. [4] Spalinger J, Patriquin H, Miron MC, Marx G, Herzog D, Dubois J, et al. Doppler US in patients with Crohn disease: vessel density in the diseased bowel reflects disease activity. Radiology 2000;217:787–91. [5] Kratz W, von Tirpitz C, Mason R, Reinshagen M, Adler G, Moller P, et al. Contrast-enhanced power Doppler sonography of the intestinal wall in the differentiation of hypervascularized and hypovascularized intestinal obstructions in patients with Crohn’s disease. J Ultrasound Med 2002;21:149–57. [6] Thomson M, Rao P, Berger L, Rawat D. Graded compression and power Doppler ultrasonography versus endoscopy to assess paediatric Crohn disease activity pre- and post-treatment. JPGN 2012;54:404–8. [7] Maconi G, Radice E, Greco S, Bianchi Porro G. Bowel ultrasound in Crohn’s disease. Best Pract Res Clin Gastroenterol 2006;20:93–112. [8] Hirsch W, Kedar R, Preiss U. Color doppler in the diagnosis of the gastroesophageal reflux in children: comparison with pH measurements and B-mode ultrasound. Pediatr Radiol 1996;26:232–5. [9] Sauerbrei EE. Extended field-of-view sonography: utility in clinical practice. J Ultrasound Med 1999;18:335–41. [10] Riccabona M. Pediatric three-dimensional ultrasound: basics and potential clinical value. Clin Imaging 2005;29:1–5. [11] Havre R, Gilja OH. Elastography and strain rate imaging of the gastrointestinal tract. Eur J Radiol 2014;83:438–41. [12] Dillman JR, Stidham RW, Higgins PD, Moons DS, Johnson LA, Rubin JM. US elastography – derived shear wave velocity helps distinguish acutely inflamed from fibrotic bowel in a Crohn disease animal model. Radiology 2013;267:757–66. [13] Attila T, Adler DG, Hilden K, Faigel DO. EUS in pediatric patients. Gastrointest Endosc 2009;70:892–8. [14] Maconi G, Radice E, Bareggi E, Porro GB. Hydrosonography of the gastrointestinal tract. Am J Roentgenol 2009;193:700–8. [15] Gassner I, Geley TE. Sonographic evaluation of oesophageal atresia and tracheooesophageal fistula. Pediatr Radiol 2005;35:159–64. [16] Kim IO, Han TI, Kim WS, Yeon KM. Transperineal ultrasonography in imperforate anus: identification of the internal fistula. J Ultrasound Med 2000;19:211–6. [17] Alison M, Kheniche A, Azoulay R, Roche S, Sebag G, Belarbi N. Ultrasonography of Crohn disease in children. Pediatr Radiol 2007;37:1071–82. [18] Tarján Z, Tóth G, Györke T, Mester A, Karlinger K, Makó EK. Ultrasound in Crohn’s disease of the small bowel. Eur J Radiol 2000;35:176–82. [19] Lee JH, Jeong YK, Hwang JC, Ham SY, Yang SO. Graded compression sonography with adjuvant use of a posterior manual compression technique in the sonographic diagnosis of acute appendicitis. AJR 2002;178:863–6. [20] Pallotta N, Tomei E, Viscido A, Calabrese E, Marcheggiano A, Caprilli R, et al. Small intestine contrast ultrasonography. An alternative to radiology in the assessment of small bowel disease. Inflamm Bowel Dis 2005;11:146–53. [21] Cohen HL, Haller JO, Mestel AL, Coren SC, Schechter S, Eaton DH. Neonatal duodenum: fluid-aided US examination. Radiology 1987;164:805–9. [22] Parente F, Greco S, Molteni M, Anderloni A, Sampietro GM, Danelli PG, et al. Oral contrast enhanced bowel ultrasonography in the assessment of small intestine Crohn’s disease. A prospective comparison with conventional ultrasound, X-ray studies, and ileocolonoscopy. Gut 2004;53:1652–7. [23] Pallotta N, Civitelli F, Di Nardo G, Vincoli G, Aloi M, Viola F, et al. Small intestine contrast ultrasonography in pediatric Crohn’s disease. J Pediatr 2013;163:778–84.
[24] Savino A, Cecamore C, Matronola MF, Verrotti A, Mohn A, Chiarelli F, et al. US in the diagnosis of gastroesophageal reflux in children. Pediatr Radiol 2012;42:515–24. [25] Vandenplas Y, Rudolph CD, Di Lorenzo C, Hassal E, Liptak G, Mazur L, et al. Pediatric gastroesophageal reflux clinical guidelines practice guidelines: joint recommendations of the North American Society for Pediatric Gastroenterology, Hepatology, and Nutricion (NASPGHAN) and the European Society for Pediatric Gastroenterology, Hepatology, and Nutrition (ESPGHAN). J Pediatr Gastroenterol Nutr 2009;49:498–547. [26] Riccabona M, Maurer U, Lackner H, Uray E, Ring E. The role of sonography in the evaluation of gastro-oesophageal reflux – correlation to pH-metry. Eur J Pediatr 1992;151:655–7. [27] Gomes H, Hornoy P, Liehn JC. Ultrasonography and gastric emptying in children: validation of a sonographic method and determination of physiological and pathological patterns. Pediatr Radiol 2003;33:522–9. [28] Koumanidou C, Vakaki M, Pitsoulakis G, Anagnostara A, Mirilas P. Sonographic measurement of the abdominal esophagus length in infancy: a diagnostic tool for gastroesophageal reflux. Am J Roentgenol 2004;183:801–7. [29] Riccabona M, Schwinger W. The role of colour Doppler sonography in the assessment of gastro-oesophageal reflux in infants, German [Stellenwert der Farbdopplersonographie beim gastroösophagealen Reflux im Säuglingsalter]. Ultraschall Klin Prax 1993;8:131–4. [30] Riccabona M. Ultrasonography for hypertrophc pyloric stenosis–prognostic assessment based on sonographic criteria, German [Sonographie bei der hypertrophen Pylorusstenose – Versuch einer prognostischen Aussage anhand sonographischer Kriterien]. WiKliWo 1990;102:13–5. [31] Hernanz-Schulman M. Pyloric stenosis: role of imaging. Pediatr Radiol 2009;39:S134–9. [32] Riccabona M, Weitzer C, Lindbichler F, Mayr J. Sonography and color Doppler sonography for monitoring conservatively treated infant hypertrophic pyloric stenosis. JUM 2001;20:997–1002. [33] Dufour D, Delaet MH, Dassonville M, Cadranel S, Perlmutter N. Midgut malrotation, the reliability of sonographic diagnosis. Pediatr Radiol 1992;22: 21–3. [34] Pracros JP, Sann L, Genin G, Tran-Minh VA, Morin de Finfe CH, Forey, et al. Ultrasound diagnosis of midgut volvulus: the “whirlpool” sign. Pediatr Radiol 1992;22:18–20. [35] Yousefzadeh DK. The position of the duodenojejunal junction: the wrong horse to bet on in diagnosing or excluding malrotation. Pediatr Radiol 2009;39:S172–7. [36] Menten R, Reding R, Godding V, Dumitriu D, Clapuyt P. Sonographic assessment of the retroperitoneal position of the third portion of the duodenum: an indicator of normal intestinal rotation. Pediatr Radiol 2012;42:941–5. [37] Veyrac C, Baud C, Prodhomme O, Saguintaah M, Couture A. US assessment of neonatal bowel (necrotizing enterocolitis excluded). Pediatr Radiol 2012;42:S107–14. [38] Riccabona M, Haim M, Kutschera J. Sonografically guided reduction of meconium ileus in preterm neonates. Eur Radiol 2006;16(Suppl. 1):284. [39] Kim WY, Kim WS, Kim IO, Kwon TH, Chang W, Lee EK. Sonographic evaluation of neonates with early-stage necrotizing enterocolitis. Pediatr Radiol 2005;35:1056–61. [40] Epelman M, Daneman A, Navarro OM, Morag I, Moore AM, Kim JH, et al. Necrotizing enterocolitis: review of state-of-the-art imaging findings with pathologic correlation. Radiographics 2007;27:285–305. [41] Silva CT, Daneman A, Navarro OM, Moore AM, Moineddin R, Gerstle JT, et al. Correlation of sonographic findings and outcome in necrotizing enterocolitis. Pediatr Radiol 2007;37:274–82. [42] Muchantef K, Epelman M, Darge K, Kirpalani H, Laje P, Anupindi SA. Sonographic and radiographic imaging features of the neonate with necrotizing enterocolitis: correlating findings with outcomes. Pediatr Radiol 2013;43: 1444–52. [43] Haber HP, Stern M. Intestinal ultrasonography in children and young adults: bowel wall thickness is age dependent. J Ultrasound Med 2000;19:315–21. [44] Bremner AR, Griffiths M, Argent JD, Fairhurst JJ, Beattie RM. Sonographic evaluation of inflammatory bowel disease: a prospective, blinded, comparative study. Pediatr Radiol 2006;36:947–53. [45] Haber HP, Busch A, Ziebach R, Dette S, Ruck P, Stern M. Ultrasonographic findings correspond to clinical, endoscopic, and histologic findings in inflammatory bowel disease and other enterocolitides. J Ultrasound Med 2002;21: 375–82. [46] Di Nardo G, Aloi M, Oliva S, Civitelli F, Casciani E, Cucchiara S. Investigation of small bowel in pediatric Crohn’s disease. Inflamm Bowel Dis 2012;8:1760–76. [47] Castiglione F, Mainenti PP, De Palma GD, Testa A, Bucci L, Pesce G, et al. Noninvasive diagnosis of small bowel Crohn’s disease: direct comparison of bowel sonography and magnetic resonance enterography. Inflamm Bowel Dis 2013;19:991–8. [48] Magalhaes J, Leite S, Cotter J. Contrast-enhanced ultrasonography for assessment of activity of Crohn’s disease: the future? J Crohns Colitis 2013;7:e607. [49] Verschelden P, Filiatrault D, Garel L, Grignon A, Perreault G, Boisvert J, et al. Intussusception in children: reliability of US in diagnosis-a prospective study. Radiology 1992;184:741–4. [50] Del-Pozo G, Albillos JC, Tejedor D, Calero R, Rasero M, de-la-Calle U, et al. Intussusception in children: current concepts in diagnosis and enema reduction. Radiographics 1999;19:299–319. [51] Daneman A, Navarro O. Intussusception. Part 2: An update on the evolution of management. Pediatr Radiol 2004;34:97–108.
Please cite this article in press as: Lobo ML, Roque M. Gastrointestinal ultrasound in neonates, infants and children. Eur J Radiol (2014), http://dx.doi.org/10.1016/j.ejrad.2014.04.016
G Model EURR-6752; No. of Pages 9
ARTICLE IN PRESS M.L. Lobo, M. Roque / European Journal of Radiology xxx (2014) xxx–xxx
[52] Quigley AJ, Stafrace S. Ultrasound assessment of acute appendicitis in paediatric patients: methodology and pictorial overview of findings seen. Insights Imaging 2013;4:741–51. [53] Linam LE, Munden M. Sonography as the first line of evaluation in children with suspected acute appendicitis. J Ultrasound Med 2012;31:1153–7. [54] Trout AT, Sanchez R, Ladino-Torres MF. Reevaluating the sonographic criteria for acute appendicitis in children: a review of the literature and a retrospective analysis of 246 cases. Acad Radiol 2012;19(11):1382–94. [55] Strouse PJ. Pediatric appendicitis: an argument for US. Radiology 2010;255:8–13. [56] Hernanz-Schulman M. CT and US in the diagnosis of appendicitis: an argument for CT. Radiology 2010;255:3–7.
9
[57] Phillips GS, Pruthi S. Acquired lesions of the small intestines. In: Coley BD, editor. Caffey’s pediatric diagnostic imaging. Philadelfia: Elsevier; 2013. p. 1091–106. [58] Simanovsky N, Hiller N. Importance of sonographic detection of enlarged abdominal lymph nodes in children. J Ultrasound Med 2007;26:581–4. [59] Karmazyn B, Werner EA, Rejaie B, Applegate KE. Mesenteric lymph nodes in children: what is normal. Pediatr Radiol 2005;35:774–7. [60] Kalmar PI, Petnehazy T, Wießpeiner U, Beer M, Hauer AC, Till H, et al. Large, segmental, circular vascular malformation of the small intestine (in a female toddler with hematochezia): unusual presentation in a child. BMC Pediatr 2014;14:55, http://dx.doi.org/10.1186/1471-2431-14-55.
Please cite this article in press as: Lobo ML, Roque M. Gastrointestinal ultrasound in neonates, infants and children. Eur J Radiol (2014), http://dx.doi.org/10.1016/j.ejrad.2014.04.016
