Ultrasonography of the Lung

Abstract

Background High diagnostic accuracy, increasing clinical experience and technical improvements are good reasons to consider lung ultrasound (US) for the assessment of pleural and pulmonary diseases. In the emergency room and in intensive care, it is well acknowledged, but application in other settings is rare. The aim of this review is to update potential users in general radiology about the diagnostic scope of lung US and to encourage more frequent use of this generally underestimated lung imaging modality.

Method Literature review was done independently by the two authors in MEDLINE (via PubMed) covering a time span from 2002 until 2017 using free text and Medical Subject Headings/MeSH. Article selection for the bibliography was based on consensus according to relevance and evidence.

Results and Conclusion The technical prerequisites include a standard ultrasound unit with a suitable transducer. Pleural effusion and pneumothorax, atelectasis, interstitial edema, pneumonia, exacerbated chronic obstructive pulmonary disease/asthma and pulmonary embolism can be distinguished by particular ultrasound signs, artifacts and their combinations. A highly standardized selection of access points and terminology for the description of imaging findings contributes to high diagnostic accuracy even in challenging patients and settings. Besides the assessment of acute respiratory failure in the emergency room, lung US may be used for monitoring interstitial fluid accumulation in volume therapy and for the diagnosis of pneumonia or the assessment of pleural effusion and pleurisy in a routine outpatient setting. Last but not least, the increasing concerns about medical radiation exposure warrant a more extensive use of this sometimes underestimated modality as a cost-, time- and radiation-saving alternative or valuable adjunct to the standard imaging modalities.

Key Points: 

• Lung US is a safe, quick and readily available method with options for dynamic imaging of respiratory function.

• Proper selection of technical parameters customized to the clinical question and standardized terminology for the precise description and interpretation of the imaging signs regarding patient history determine its diagnostic accuracy.

• In dyspnea lung US differentiates pneumothorax, lung edema, pneumonia, pulmonary embolism, atelectasis and pleural effusion.

• In intensive care, lung US allows monitoring of lung ventilation and fluid administration.

• It saves radiation exposure in serial follow-up, in pregnancy and pediatric radiology.

Citation Format

• Radzina M, Biederer J, Ultrasonography of the Lung. Fortschr Röntgenstr 2019; 191: 909 – 923

Zusammenfassung

Hintergrund Eine hohe diagnostische Treffsicherheit, zunehmende klinische Erfahrung und technische Verbesserungen machen den Ultraschall der Lunge zu einer interessanten Alternative für die Untersuchung pleuraler und pulmonaler Erkrankungen. Im Schockraum und auf der Intensivstation ist der Ultraschall etabliert. Ziel dieses Artikels ist, weitere potenzielle Anwender in der Radiologie mit der diagnostischen Reichweite der Methode vertraut zu machen und zu einer breiteren Anwendung dieses in der thorakalen Bildgebung häufig unterschätzten Verfahrens anzuregen.

Methode Die Literaturrecherche erfolgte in der Datenbank MEDLINE (via PubMed) im Suchzeitraum von 2002 bis 2017 mittels Freitext- und Schlagwortsuche (Medical Subject Headings/MeSH) durch 2 unabhängige Reviewer. Die Auswahl der Artikel erfolgte im Konsensus entsprechend Relevanz und Evidenzgrad.

Ergebnisse und Schlussfolgerung Die technischen Voraussetzungen sind mit einem modernen Ultraschallgerät und einem geeigneten Schallkopf erfüllt. Während Pathologien der Thoraxwand und der Pleura (z. B. Pleuraerguss) im B-Bild gut erkennbar sind, erfolgt die Beurteilung der pulmonalen Pathologie jenseits der Pleuralinie meist indirekt anhand typischer Artefakte und Zeichen. Diese erlauben z. B. die Unterscheidung von hämodynamischem Lungenödem, Pneumonie, Lungenembolie, exazerbierter COPD/Asthma oder Pneumothorax. Standardisierte Zugangswege und eine exakte Terminologie tragen wesentlich zur diagnostischen Genauigkeit und Reproduzierbarkeit der Methode auch in anspruchsvollen Situationen und bei erschwerten Untersuchungsbedingungen bei. Im Schockraum erlaubt der Lungen-Ultraschall eine sichere und schnelle Identifizierung des interstitiellen Lungenödems bei Patienten in Atemnot. Beim ambulanten Einsatz erlaubt die Sonografie eine schnelle und sichere Differenzierung von Pleuraerguss, Pleuritis und Pneumonie. Nicht zuletzt die Reduzierung der diagnostischen Strahlenexposition spricht für einen breiteren Einsatz dieser häufig unterschätzten Methode als kosten-, zeit- und strahlensparende Alternative oder als wertvolle Ergänzung zu den etablierten Standardverfahren.

Kernaussagen: 

• Der Lungen-US ist eine einfach verfügbare, sichere Methodik mit Optionen zur dynamischen Beurteilung der Atemmechanik.

• Eine an die Fragestellung angepasste Untersuchungstechnik und die standardisierte Beschreibung und Interpretation typischer Zeichen und Artefakte in Zusammenschau mit der klinischen Fragestellung bestimmen die diagnostische Sicherheit.

• Bei Dyspnoe lassen sich Pneumothorax, Lungenödem, Pneumonie, Lungenembolie, Atelektasen und Pleuraergüsse differenzieren.

• Lungenventilation und Infusionstherapie lassen sich mittels Lungen-US steuern.

• Bei Verlaufskontrollen, Schwangerschaft und Kindern wird eine Strahlenexposition vermieden.

Key words

thorax - ultrasound - pleura - pneumonia - lung

• References

• 1 Mohanty K, Blackwell J, Egan T. et al. Characterization of the Lung Parenchyma Using Ultrasound Multiple Scattering. Ultrasound Med Biol 2017; 43: 993-1003
• 2 Nelson M, Stankard B, Greco J. et al. Point of Care Ultrasound Diagnosis of Empyema. J Emerg Med 2016; 51: 140-143
• 3 Moreno-Aguilar G, Lichtenstein D. Lung ultrasound in the critically ill (LUCI) and the lung point: a sign specific to pneumothorax which cannot be mimicked. Crit Care Lond Engl 2015; 19: 311
• 4 Soldati G, Testa A, Sher S. et al. Occult traumatic pneumothorax: diagnostic accuracy of lung ultrasonography in the emergency department. Chest 2008; 133: 204-211
• 5 012-019k_S3_Polytrauma_Schwerverletzten-Behandlung_2016-10.pdf. o. J.
• 6 Volpicelli G, Elbarbary M, Blaivas M. et al. International evidence-based recommendations for point-of-care lung ultrasound. Intensive Care Med 2012; 38: 577-591
• 7 Lichtenstein DA, Mezière GA. Relevance of lung ultrasound in the diagnosis of acute respiratory failure: the BLUE protocol. Chest 2008; 134: 117-125
• 8 Mittal AK, Gupta N. Intraoperative lung ultrasound: A clinicodynamic perspective. J Anaesthesiol Clin Pharmacol 2016; 32: 288-297
• 9 Reissig A, Copetti R, Mathis G. et al. Lung ultrasound in the diagnosis and follow-up of community-acquired pneumonia: a prospective, multicenter, diagnostic accuracy study. Chest 2012; 142: 965-972
• 10 Lichtenstein D. Novel approaches to ultrasonography of the lung and pleural space: where are we now?. Breathe Sheff Engl 2017; 13: 100-111
• 11 Soldati G, Smargiassi A, Mariani AA. et al. Novel aspects in diagnostic approach to respiratory patients: is it the time for a new semiotics?. Multidiscip Respir Med 2017; 12: 15
• 12 Gargani L, Volpicelli G. How I do it: Lung ultrasound. Cardiovasc Ultrasound 2014; 12: 25
• 13 Bourcier JE, Braga S, Garnier D. Lung Ultrasound Will Soon Replace Chest Radiography in the Diagnosis of Acute Community-Acquired Pneumonia. Curr Infect Dis Rep 2016; 18: 43
• 14 Doerschug KC, Schmidt GA. Intensive care ultrasound: III. Lung and pleural ultrasound for the intensivist. Ann Am Thorac Soc 2013; 10: 708-712
• 15 Jambrik Z, Monti S, Coppola V. et al. Usefulness of ultrasound lung comets as a nonradiologic sign of extravascular lung water. Am J Cardiol 2004; 93: 1265-1270
• 16 Umbrello M, Formenti P, Longhi D. et al. Diaphragm ultrasound as indicator of respiratory effort in critically ill patients undergoing assisted mechanical ventilation: a pilot clinical study. Crit Care 2015; 19: 161
• 17 Lichtenstein DA. BLUE-protocol and FALLS-protocol: two applications of lung ultrasound in the critically ill. Chest 2015; 147: 1659-1670
• 18 Lichtenstein DA, Menu Y. A bedside ultrasound sign ruling out pneumothorax in the critically ill. Lung sliding. Chest 1995; 108: 1345-1348
• 19 Na MJ. Diagnostic tools of pleural effusion. Tuberc Respir Dis 2014; 76: 199-210
• 20 Lichtenstein DA. Lung ultrasound in the critically ill. Ann Intensive Care 2014; 4: 1
• 21 Volpicelli G, Boero E, Stefanone V. et al. Unusual new signs of pneumothorax at lung ultrasound. Crit Ultrasound J 2013; 5: 10
• 22 Lichtenstein D, Mezière G, Biderman P. et al. The “lung point”: an ultrasound sign specific to pneumothorax. Intensive Care Med 2000; 26: 1434-1440
• 23 Lichtenstein DA, Mezière G, Lascols N. et al. Ultrasound diagnosis of occult pneumothorax. Crit Care Med 2005; 33: 1231-1238
• 24 Lichtenstein DA, Lascols N, Mezière G. et al. Ultrasound diagnosis of alveolar consolidation in the critically ill. Intensive Care Med 2004; 30: 276-281
• 25 Lichtenstein D, Mezière G, Seitz J. The dynamic air bronchogram. A lung ultrasound sign of alveolar consolidation ruling out atelectasis. Chest 2009; 135: 1421-1425
• 26 Karabinis A, Saranteas T, Karakitsos D. et al. The“cardiac-lung mass” artifact: an echocardiographic sign of lung atelectasis and/or pleural effusion. Crit Care 2008; 12: R122
• 27 Lichtenstein DA, Lascols N, Prin S. et al. The “lung pulse”: an early ultrasound sign of complete atelectasis. Intensive Care Med 2003; 29: 2187-2192
• 28 Soldati G, Smargiassi A, Mariani AA. et al. Novel aspects in diagnostic approach to respiratory patients: is it the time for a new semiotics?. Multidiscip Respir Med 2017; 12: 15
• 29 Pesenti A, Musch G, Lichtenstein D. et al. Imaging in acute respiratory distress syndrome. Intensive Care Med 2016; 42: 686-698
• 30 Wierzejski W, Adamski J, Weigl W. et al. Modern methods of assessment of lung aeration during mechanical ventilation. Anaesthesiol Intensive Ther 2012; 44: 226-231
• 31 Dietrich CF, Mathis G, Blaivas M. et al. Lung B-line artefacts and their use. J Thorac Dis 2016; 8: 1356-1365
• 32 Lichtenstein D, Mezière G, Biderman P. et al. The comet-tail artifact: an ultrasound sign ruling out pneumothorax. Intensive Care Med 1999; 25: 383-388
• 33 Chiesa AM, Ciccarese F, Gardelli G. et al. Sonography of the normal lung: Comparison between young and elderly subjects. J Clin Ultrasound JCU 2015; 43: 230-234
• 34 Martelius L, Süvari L, Janér C. et al. Lung Ultrasound and Static Lung Compliance during Postnatal Adaptation in Healthy Term Infants. Neonatology 2015; 108: 287-292
• 35 Lichtenstein D, Meziere G, Biderman P. et al. The comet-tail artifact: an ultrasound sign of alveolar-interstitial syndrome. Am J Respir Crit Care Med 1997; 156: 1640-1646
• 36 Volpicelli G, Mussa A, Garofalo G. et al. Bedside lung ultrasound in the assessment of alveolar-interstitial syndrome. Am J Emerg Med 2006; 24: 689-696
• 37 Lo Giudice V, Bruni A, Corcioni E. et al. Ultrasound in the evaluation of interstitial pneumonia. J Ultrasound 2008; 11: 30-38
• 38 Lichtenstein D, Mezière G. A lung ultrasound sign allowing bedside distinction between pulmonary edema and COPD: the comet-tail artifact. Intensive Care Med 1998; 24: 1331-1334
• 39 Volpicelli G, Cardinale L, Garofalo G. et al. Usefulness of lung ultrasound in the bedside distinction between pulmonary edema and exacerbation of COPD. Emerg Radiol 2008; 15: 145-151
• 40 Li H, Li YD, Zhu WW. et al. High-Resolution Transthoracic Ultrasonography for Assessment of Pleural Lines in Patients With Dyspnea With CT Comparison: An Observational Study: High-Resolution TUS of Lung Pathology. J Ultrasound Med 2017; 36: 707-716
• 41 Martelius L, Heldt H, Lauerma K. B-Lines on Pediatric Lung Sonography: Comparison With Computed Tomography. J Ultrasound Med 2016; 35: 153-157
• 42 Copetti R, Soldati G, Copetti P. Chest sonography: a useful tool to differentiate acute cardiogenic pulmonary edema from acute respiratory distress syndrome. Cardiovasc Ultrasound 2008; 6: 16
• 43 Lichtenstein D, Mauriat P. Lung ultrasound in the critically ill neonate. Curr Pediatr Rev 2012; 8: 217-223
• 44 Copetti R, Cattarossi L. The “double lung point”: an ultrasound sign diagnostic of transient tachypnea of the newborn. Neonatology 2007; 91: 203-209
• 45 Zieleskiewicz L, Contargyris C, Brun C. et al. Lung ultrasound predicts interstitial syndrome and hemodynamic profile in parturients with severe preeclampsia. Anesthesiology 2014; 120: 906-914
• 46 Alzahrani SA, Al-Salamah MA, Al-Madani WH. et al. Systematic review and meta-analysis for the use of ultrasound versus radiology in diagnosing of pneumonia. Crit Ultrasound J 2017; 9: 6
• 47 Brito V, Niederman MS. Pneumonia complicating pregnancy. Clin Chest Med 2011; 32: 121-132
• 48 Di Marco F, Adelaide Roggi M, Terraneo S. et al. Lung ultrasound as first line imaging tool in pregnant women with respiratory symptoms. Eur Respir J 2015; 46: OA494
• 49 Riccabona M. Ultrasound of the chest in children (mediastinum excluded). Eur Radiol 2008; 18: 390-399
• 50 Deganello A, Rafailidis V, Sellars ME. et al. Intravenous and Intracavitary Use of Contrast-Enhanced Ultrasound in the Evaluation and Management of Complicated Pediatric Pneumonia. J Ultrasound Med Off J Am Inst Ultrasound Med 2017; 36: 1943-1954
• 51 Gutierrez M, Gomez-Quiroz LE, Clavijo-Cornejo D. et al. Ultrasound in the interstitial pulmonary fibrosis. Can it facilitate a best routine assessment in rheumatic disorders?. Clin Rheumatol 2016; 35: 2387-2395
• 52 Tardella M, Gutierrez M, Salaffi F. et al. Ultrasound in the assessment of pulmonary fibrosis in connective tissue disorders: correlation with high-resolution computed tomography. J Rheumatol 2012; 39: 1641-1647
• 53 Sperandeo M, De Cata A, Molinaro F. et al. Ultrasound signs of pulmonary fibrosis in systemic sclerosis as timely indicators for chest computed tomography. Scand J Rheumatol 2015; 44: 389-398
• 54 Barskova T, Gargani L, Guiducci S. et al. Lung ultrasound for the screening of interstitial lung disease in very early systemic sclerosis. Ann Rheum Dis 2013; 72: 390-395
• 55 Gutierrez M, Salaffi F, Carotti M. et al. Utility of a simplified ultrasound assessment to assess interstitial pulmonary fibrosis in connective tissue disorders – preliminary results. Arthritis Res Ther 2011; 13: R134
• 56 Raso R, Tartarisco G, Matucci Cerinic M. et al. A soft computing-based B-line analysis for objective classification of severity of pulmonary edema and fibrosis. JACC Cardiovasc Imaging 2015; 8: 495-496
• 57 Baria MR, Shahgholi L, Sorenson EJ. et al. B-Mode Ultrasound Assessment of Diaphragm Structure and Function in Patients With COPD. Chest 2014; 146: 680-685
• 58 He L, Zhang W, Zhang J. et al. Diaphragmatic motion studied by M-mode ultrasonography in combined pulmonary fibrosis and emphysema. Lung 2014; 192: 553-561
• 59 Zanforlin A, Smargiassi A, Inchingolo R. et al. Ultrasound in obstructive lung diseases: the effect of airway obstruction on diaphragm kinetics. A short pictorial essay. J Ultrasound 2015; 18: 379-384
• 60 Vilmann P, Clementsen P, Colella S. et al. Combined endobronchial and esophageal endosonography for the diagnosis and staging of lung cancer: European Society of Gastrointestinal Endoscopy (ESGE) Guideline, in cooperation with the European Respiratory Society (ERS) and the European Society of Thoracic Surgeons (ESTS). Endoscopy 2015; 47: 545-559
• 61 Caroli G, Dell’Amore A, Cassanelli N. et al. Accuracy of transthoracic ultrasound for the prediction of chest wall infiltration by lung cancer and of lung infiltration by chest wall tumours. Heart Lung Circ 2015; 24: 1020-1026
• 62 Wang S, Yang W, Zhang H. et al. The Role of Contrast-Enhanced Ultrasound in Selection Indication and Improveing Diagnosis for Transthoracic Biopsy in Peripheral Pulmonary and Mediastinal Lesions. BioMed Res Int 2015; 2015: 1-8
• 63 Sperandeo M, Rea G, Grimaldi MA. et al. Contrast-enhanced ultrasound does not discriminate between community acquired pneumonia and lung cancer. Thorax 2017; 72: 178-180
• 64 Laursen CB, Naur TMH, Bodtger U. et al. Ultrasound-guided Lung Biopsy in the Hands of Respiratory Physicians: Diagnostic Yield and Complications in 215 Consecutive Patients in 3 Centers. J Bronchol Interv Pulmonol 2016; 23: 220-228
• 65 Reissig A, Heyne JP, Kroegel C. Sonography of lung and pleura in pulmonary embolism: sonomorphologic characterization and comparison with spiral CT scanning. Chest 2001; 120: 1977-1983
• 66 Mathis G, Blank W, Reissig A. et al. Thoracic ultrasound for diagnosing pulmonary embolism: a prospective multicenter study of 352 patients. Chest 2005; 128: 1531-1538
• 67 Bartelt S, Trenker C, Görg C. et al. Contrast-enhanced ultrasound of embolic consolidations in patients with pulmonary embolism: A pilot study. J Clin Ultrasound JCU 2016; 44: 129-135