CC BY-NC-ND 4.0 · Ultrasound Int Open 2021; 07(01): E14-E24
DOI: 10.1055/a-1474-8013
Review

Gastrointestinal Ultrasound in Functional Disorders of the Gastrointestinal Tract - EFSUMB Consensus Statement

1   Gastroenterology Unit, Department of Biomedical and Clinical Sciences, "L.Sacco" University Hospital, Milano, Italy
,
Trygve Hausken
2   Department of Medicine, University of Bergen, Bergen, Norway
,
3   Department Allgemeine Innere Medizin, Kliniken Hirslanden Beau-Site, Salem und Permanence, Bern, Switzerland
,
Nadia Pallotta
4   Department of Internal Medicine and Medical Specialties, Sapienza University of Rome, Roma, Italy
,
Ioan Sporea
5   Department of Gastroenterology, University of Medicine and Pharmacy, Victor Babes Timisoara, Timisoara, Romania
6   Department of Gastroenterology, Universitatea de Vest din Timisoara, Timisoara, Romania
,
Dieter Nurnberg
7   Brandenburg Institute for Clinical Ultrasound (BICUS) – Medical University Brandenburg “Theodor Fontane”, Faculty of Medicine and Philosophy and Faculty of Health Sciences Brandenburg, Neuruppin, Germany
,
Klaus Dirks
8   Gastroenterology and Internal Medicine, Rems-Murr-Klinikum Winnenden, Winnenden, Germany
,
Laura Romanini
9   Department of Radiology, Radiologia 1, Hospital of Cremona, Cremona, Italy
,
Carla Serra
10   Internal Medicine and Gastroenterology, University of Bologna, Hospital of Bologna Sant’Orsola-Malpighi Polyclinic, Bologna, Italy
,
Barbara Braden
11   Translational Gastroenterology Unit, Oxford University Hospitals NHS Foundation Trust, Oxford, UK
,
Zeno Sparchez
12   3rd Medical Department, University of Medicine and Pharmacy, Cluj-Napoca, Romania
,
Odd Helge Gilja
13   Haukeland University Hospital, Haukeland University Hospital, and Department of Clinical Medicine, University of Bergen, Bergen, Norway
› Author Affiliations

Abstract

Abdominal ultrasonography and intestinal ultrasonography are widely used as first diagnostic tools for investigating patients with abdominal symptoms, mainly for excluding organic diseases. However, gastrointestinal ultrasound (GIUS), as a real-time diagnostic imaging method, can also provide information on motility, flow, perfusion, peristalsis, and organ filling and emptying, with high temporal and spatial resolution. Thanks to its noninvasiveness and high repeatability, GIUS can investigate functional gastrointestinal processes and functional gastrointestinal diseases (FGID) by studying their behavior over time and their response to therapy and providing insight into their pathophysiologic mechanisms. The European Federation of Societies for Ultrasound in Medicine and Biology (EFSUMB) has established a Task Force Group consisting of GIUS experts, which developed clinical recommendations and guidelines on the role of GIUS in several acute and chronic gastrointestinal diseases. This review is dedicated to the role of GIUS in assisting the diagnosis of FGID and particularly in investigating patients with symptoms of functional disorders, such as dysphagia, reflux disorders, dyspepsia, abdominal pain, bloating, and altered bowel habits. The available scientific evidence of GIUS in detecting, assessing, and investigating FGID are reported here, while highlighting sonographic findings and its usefulness in a clinical setting, defining the actual and potential role of GIUS in the management of patients, and providing information regarding future applications and research.

Supplementary Material



Publication History

Received: 10 October 2020

Accepted after revision: 01 April 2021

Article published online:
28 May 2021

© 2021. The Author(s). This is an open access article published by Thieme under the terms of the Creative Commons Attribution-NonDerivative-NonCommercial-License, permitting copying and reproduction so long as the original work is given appropriate credit. Contents may not be used for commercial purposes, or adapted, remixed, transformed or built upon. (https://creativecommons.org/licenses/by-nc-nd/4.0/).

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  • References

  • 1 Ødegaard S, Gilja OH, Gregersen H. Editors of book: Basic and New Aspects of Gastrointestinal Ultrasonography. 2005: 1-502 Publisher: World Scientific; Singapore: ISBN 981-238-845-1
  • 2 Nylund K, Maconi G, Hollerweger A. et al. EFSUMB Recommendations and Guidelines for Gastrointestinal Ultrasound. Ultraschall Med 2017; 38: 273-284
  • 3 Hollerweger A, Maconi G, Ripolles T, Nylund K, Higginson A, Serra C. et al. Gastrointestinal ultrasound (GIUS) in intestinal emergencies. An EFSUMB position paper. Ultraschall Med 2020; DOI: 10.1055/a-1147-1295.
  • 4 Dietrich CF, Hollerweger A, Dirks K. et al. EFSUMB Gastrointestinal Ultrasound (GIUS) Task Force Group: Celiac sprue and other rare gastrointestinal diseases ultrasound features. Med Ultrason 2019; 21: 299-315
  • 5 Nuernberg D, Saftoiu A, Barreiros AP. et al. EFSUMB Recommendations for Gastrointestinal Ultrasound Part 3: Endorectal, Endoanal and Perineal Ultrasound. Ultrasound Int Open 2019; 5: E34-E51
  • 6 Dirks K, Calabrese E, Dietrich CF. et al. EFSUMB Position Paper: Recommendations for Gastrointestinal Ultrasound (GIUS) in Acute Appendicitis and Diverticulitis. Ultraschall Med 2019; 40: 163-175
  • 7 Maconi G, Nylund K, Ripolles T. et al. EFSUMB Recommendations and Clinical Guidelines for Intestinal Ultrasound (GIUS) in Inflammatory Bowel Diseases. Ultraschall Med 2018; 39: 304-313
  • 8 Turley R, Cohen S. Impact of voice and swallowing problems in the elderly. Otolaryngol Head Neck Surg 2009; 140: 33-36
  • 9 Blyth KM, McCabe P, Madill C, Ballard KJ. Ultrasound in dysphagia rehabilitation: a novel approach following partial glossectomy. Disabil Rehabil 2017; 39: 2215-2227
  • 10 Lee YS, Lee KE, Kang Y, Yi TI, Kim JS. Usefulness of Submental Ultrasonographic Evaluation for Dysphagia Patients. Ann Rehabil Med 2016; 40: 197-205
  • 11 Achille G, Castellana M, Russo S, Montepara M, Giagulli VA, Triggiani V. Zenker Diverticulum: A Potential Pitfall in Thyroid Ultrasound Evaluation: A Case Report and Systematic Review of Literature. Endocr Metab Immune Disord Drug Targets 2019; 19: 95-99
  • 12 Cui XW, Ignee A, Baum U, Dietrich CF. Feasibility and usefulness of using swallow contrast-enhanced ultrasound to diagnose Zenker's diverticulum: preliminary results. Ultrasound Med Biol 2015; 41: 975-981
  • 13 Takebayashi S, Matsui K, Ozawa Y, Nozawa T, Fujioka E. Cervical esophageal motility: evaluation with US in progressive systemic sclerosis. Radiology 1991; 179: 389-393.
  • 14 Zuber-Jerger I, Müller A, Kullmann F, Gelbmann CM, Endlicher E, Müller-Ladner U, Fleck M. Gastrointestinal manifestation of systemic sclerosis--thickening of the upper gastrointestinal wall detected by endoscopic ultrasound is a valid sign. Rheumatology (Oxford) 2010; 49: 368-372
  • 15 Nam IC, Choi H, Kim ES, Mo EY, Park YH, Sun DI. Characteristics of thyroid nodules causing globus symptoms. Eur Arch Otorhinolaryngol 2015; 272 (05) 1181-1188
  • 16 Järvenpää P, Ilmarinen T, Geneid A. et al. Work-up of globus: assessing the benefits of neck ultrasound and videofluorography. Eur Arch Otorhinolaryngol 2017; 274: 931-937
  • 17 Eskander A, Monteiro E, O'Connell D, Taylor SM. Canadian Association of Head and Neck Surgical Oncology (CAHNSO). Head and Neck Surgical Oncology Choosing Wisely Campaign: imaging for patients with hoarseness, fine needle aspiration for neck mass, and ultrasound for odynophagia. J Otolaryngol Head Neck Surg 2018; 47: 2
  • 18 Eckardt VF, Schmitt T, Kanzler G. Transabdominal ultrasonography in achalasia. Scand J Gastroenterol 2004; 39 (07) 634-647 DOI: 10.1080/00365520410005478;. PMID: 15370683
  • 19 Minella R, Minelli R, Rossi E, Cremone G, Tozzi A. Gastroesophageal and gastric ultrasound in children: the state of the art. J Ultrasound 2020; DOI: 10.1007/s40477-020-00471-w. Epub ahead of print. PMID: 32361921
  • 20 Savino A, Cecamore C, Matronola MF, Verrotti A, Mohn A, Chiarelli F, Pelliccia P. US in the diagnosis of gastroesophageal reflux in children. Pediatr Radiol. 2012; 42(5):515-524. DOI: 10.1007/s00247-012-2344-z.. Epub 2012 Mar 9. PMID: 22402830
  • 21 Barone M, Di Lernia P, Carbonara M, Ladisa R, Donno A, Amoruso A, Di Leo A, Francavilla A. Sliding gastric hiatal hernia diagnosis by transabdominal ultrasonography: an easy, reliable and non-invasive procedure. Scand J Gastroenterol 2006; 41 (07) 851-855 DOI: 10.1080/00365520500453408.. PMID: 16785200
  • 22 Gilja OH. Ultrasound of the stomach--the EUROSON lecture 2006. Ultraschall Med 2007; 28: 32-39
  • 23 Gilja OH, Hatlebakk JG, Odegaard S. et al. Advanced imaging and visualization in gastrointestinal disorders. World J Gastroenterol 2007; 13: 1408-1421
  • 24 Pallotta N, Cicala M, Frandina C, Corazziari E. Antro-pyloric Contractile Patterns and Transpyloric Flow After Meal Ingestion in Humans. Am J Gastroenterol 1998; 93: 2513-2522
  • 25 Hveem K, Sun WM, Hebbard G, Horowitz M, Doran S, Dent J. Relationship between ultrasonically detected phasic antral contractions and antral pressure. Am J Physiol Gastrointest Liver Physiol 2001; 281: G95-G101
  • 26 Savoye-Collet C, Savoye G, Smout A. Determinants of transpyloric fluid transport: a study using combined real-time ultrasound, manometry, and impedance recording. Am J Physiol Gastrointest Liver Physiol 2003; 285 (06) G1147-G1152
  • 27 Hausken T, Mundt M, Samsom M. Low antroduodenal pressure gradients are responsible for gastric emptying of a low-caloric liquid meal in humans. Neurogastroenterol Motil 2002; 14 (01) 97-105
  • 28 Hveem K, Svebak S, Hausken T, Berstad A. Effect of mental stress and cisapride on autonomic nerve functions in functional dyspepsia. Scand J Gastroenterol 1998; 33: 123-127
  • 29 Ahluwalia NK, Thompson DG, Mamtora H, Hindle J. Evaluation of gastric antral motor performance in patients with dysmotility-like dyspepsia using real-time high-resolution ultrasound. Neurogastroenterol Motil 1996; 8: 333-338
  • 30 Gilja OH, Heimdal A, Hausken T. et al. Strain during gastric contractions can be measured using Doppler Ultrasonography. Ultrasound Med Biol 2002; 28: 1457-1465
  • 31 Ahmed AB, Matre K, Hausken T, Gregersen H, Gilja OH. Rome III subgroups of functional dyspepsia exhibit different characteristics of antral contractions measured by strain rate imaging - a pilot study. Ultraschall Med 2012; 33: E233-40
  • 32 Bolondi L, Bortolotti M, Santi V, Calletti T, Gaiani S, Labo G. Measurement of gastric emptying time by real-time ultrasonography. Gastroenterology 1985; 89: 752-759
  • 33 Gentilcore D, Hausken T, Horowitz M, Jones KL. Measurements of gastric emptying of low- and high-nutrient liquids using 3D ultrasonography and scintigraphy in healthy subjects. Neurogastroenterol Motil 2006; 18: 1062-1068
  • 34 Duan LP, Zheng ZT, Li YN. A study of gastric emptying in non-ulcer dyspepsia using a new ultrasonographic method. Scand J Gastroenterol 1993; 28: 355-360
  • 35 Sogabe M, Okahisa T, Tsujigami K. et al. Ultrasonographic assessment of gastric motility in diabetic gastroparesis before and after attaining glycemic control. J Gastroenterol 2005; 40: 583-590
  • 36 Hausken T, Gilja OH, Undeland KA, Berstad A. Timing of postprandial dyspeptic symptoms and transpyloric passage of gastric contents. Scand J Gastroenterol 1998; 33: 822-827
  • 37 Gilja OH, Lunding J, Hausken T, Gregersen H. Gastric accommodation assessed by ultrasonography. World J Gastroenterol 2006; 12: 2825-2829
  • 38 Gilja OH, Hausken T, Wilhelmsen I, Berstad A. Impaired accommodation of proximal stomach to a meal in functional dyspepsia. Dig Dis Sci 1996; 41: 689-696
  • 39 Steinsvik EK, Hausken T, Gilja OH. The ultrasound meal accommodation test in 509 patients with functional gastrointestinal disorders. Scand J Gastroenterol 2016; 51: 788-794
  • 40 Storlid EL, Hausken T, Lied GA, Gilja OH, Hatlebakk JG. Gastric accommodation in healthy subjects studied by ultrasound, manometry, and impedancemetry. Neurogastroenterol Motil 2018; 30: e13249
  • 41 Gilja OH, Thune N, Matre K, Hausken T, Odegaard S, Berstad A. In vitro evaluation of three-dimensional ultrasonography in volume estimation of abdominal organs. Ultrasound Med Biol 1994; 20: 157-165
  • 42 Gilja OH, Detmer PR, Jong JM. et al. Intragastric distribution and gastric emptying assessed by three-dimensional ultrasonography. Gastroenterology 1997; 113: 38-49
  • 43 Steinsvik EK, Valeur J, Hausken T, Gilja OH. Postprandial Symptoms in Patients With Functional Dyspepsia and Irritable Bowel Syndrome: Relations to Ultrasound Measurements and Psychological Factors. J Neurogastroenterol Motil 2020; 26: 96-105
  • 44 Gilja OH, Heimdal A, Hausken T. et al. Strain during gastric contractions can be measured using Doppler ultrasonography. Ultrasound Med Biol 2002; 28: 1457-65
  • 45 Soncini M, Stasi C, Usai Satta P. et al. AIGO. IBS clinical management in Italy: The AIGO survey. Dig Liver Dis 2019; 51: 782-789
  • 46 Francis CY, Duffy JN, Whorwell PJ, Martin DF. Does routine abdominal ultrasound enhance diagnostic accuracy in irritable bowel syndrome?. Am J Gastroenterol 1996; 91: 1348-1350
  • 47 Dilillo D, Zuccotti GV, Galli E. et al. Noninvasive testing in the management of children with suspected inflammatory bowel disease. Scand J Gastroenterol 2019; 54: 586-591
  • 48 Novak KL, Jacob D, Kaplan GG, Boyce E, Ghosh S, Ma I, Lu C, Wilson S, Panaccione R. Point of Care Ultrasound Accurately Distinguishes Inflammatory from Noninflammatory Disease in Patients Presenting with Abdominal Pain and Diarrhea. Can J Gastroenterol Hepatol 2016; 2016: 4023065
  • 49 O'Connor OJ, McSweeney SE, McWilliams S, O'Neill S, Shanahan F, Quigley EM, Maher MM. Role of radiologic imaging in irritable bowel syndrome: evidence-based review. Radiology. 2012; 262 (02) 485-494 DOI: 10.1148/radiol.11110423. Epub 2011 Dec 9. PMID: 22156992
  • 50 Crade M, Pham V. Ultrasound examination of the sigmoid colon: possible new diagnostic tool for irritable bowel syndrome. Ultrasound Obstet Gynecol 2006; 27: 206-209
  • 51 Smereczyński A, Starzyńska T, Kołaczyk K. Ultrasound of selected pathologies of the small intestine. J Ultrason 2013; 13: 155-166
  • 52 von Volkmann HL, Nylund K, Tronstad RR. et al. An activating gucy2c mutation causes impaired contractility and fluid stagnation in the small bowel. Scand J Gastroenterol 2016; 1-8
  • 53 Hollerweger A, Macheiner P, Hubner E. et al. Colonic diverticulosis: a comparison between sonography and endoscopy. Ultraschall Med 2002; 231: 41-46
  • 54 Derchi LE, Musante F, Biggi E, Cicio GR, Oliva L. Sonographic appearance of fecal masses. J Ultrasound Med 1985; 4: 573-575
  • 55 Bijoś A, Czerwionka-Szaflarska M, Mazur A, Romañczuk W. The usefulness of ultrasound examination of the bowel as a method of assessment of functional chronic constipation in children. Pediatr Radiol 2007; 37: 1247-1252
  • 56 Yabunaka K, Matsumoto M, Yoshida M. et al. Assessment of rectal feces storage condition by a point-of-care pocket-size ultrasound device for healthy adult subjects: A preliminary study. Drug Discov Ther 2018; 12: 42-46
  • 57 Lakshminarayanan B, Kufeji D, Clayden G. A new ultrasound scoring system for assessing the severity of constipation in children. Pediatr Surg Int 2008; 24: 1379-1384
  • 58 Yabunaka K, Matsuo J, Hara A. et al. Sonographic Visualization of Fecal Loading in Adults: Comparison With Computed Tomography. Journal of Diagnostic Medical Sonography 2015; 31: 86-92