Ultrasound of extravascular lung water: a new standard for pulmonary congestion

Eugenio Picano, Patricia A Pellikka, Eugenio Picano, Patricia A Pellikka

Abstract

Extravascular lung water (EVLW) is a key variable in heart failure management and prognosis, but its objective assessment remains elusive. Lung imaging has been traditionally considered off-limits for ultrasound techniques due to the acoustic barrier of high-impedance air wall. In pulmonary congestion however, the presence of both air and water creates a peculiar echo fingerprint. Lung ultrasound shows B-lines, comet-like signals arising from a hyper-echoic pleural line with a to-and-fro movement synchronized with respiration. Increasing EVLW accumulation changes the normal, no-echo signal (black lung, no EVLW) into a black-and-white pattern (interstitial sub-pleural oedema with multiple B-lines) or a white lung pattern (alveolar pulmonary oedema) with coalescing B-lines. The number and spatial extent of B-lines on the antero-lateral chest allows a semi-quantitative estimation of EVLW (from absent, ≤5, to severe pulmonary oedema, >30 B-lines). Wet B-lines are made by water and decreased by diuretics, which cannot modify dry B-lines made by connective tissue. B-lines can be evaluated anywhere (including extreme environmental conditions with pocket size instruments to detect high-altitude pulmonary oedema), anytime (during dialysis to titrate intervention), by anyone (even a novice sonographer after 1 h training), and on anybody (since the chest acoustic window usually remains patent when echocardiography is not feasible). Cardiologists can achieve much diagnostic gain with little investment of technology, training, and time. B-lines represent 'the shape of lung water'. They allow non-invasive detection, in real time, of even sub-clinical forms of pulmonary oedema with a low cost, radiation-free approach.

Keywords: Lung; Oedema; Ultrasound; Water.

© The Author 2016. Published by Oxford University Press on behalf of the European Society of Cardiology.

Figures

Figure 1
Figure 1
The recommended protocol for evaluating B-lines is performed by scanning 28-region protocol on the anterior chest with the patient in the supine position.,,
Figure 2
Figure 2
From left to right panels, the normal lung, then increasing severity of pulmonary oedema. From top to bottom, the corresponding pathology (first row), schematic ultrasound pattern (second row), and in vivo ultrasound texture (bottom). The increase in relative content of water, and decrease of content of air in the lung (middle panel), reshapes the texture of clinical image (last row) from normal, A-lines to abnormal B-lines (water and air mix).,
Figure 3
Figure 3
A very good correlation (R = 0.91 in both cases) is shown between B-lines and extravascular lung water evaluated experimentally by gravimetry in pigs with acute lung injury induced by oleic acid (left panel) and clinically by thermodilution in patients with acute lung injury-acute respiratory distress syndrome (right panel).,
Figure 4
Figure 4
Sequence of events in a pig model of acute respiratory distress syndrome. B-lines occur early (already significantly increased at 15 min); only at a later stage (at 90 min) were changes in haemogasanalytic parameters significant. ALI, acute lung injury; ARDS, acute respiratory distress syndrome.
Figure 5
Figure 5
Lung ultrasound (third right intercostal space) at rest (upper panel) and immediately after exercise (lower panel). The exercise-induced appearance of B-lines eclipses the normal pattern of A-lines present at rest.
Figure 6
Figure 6
Outdoor stress echo with lung ultrasound for the diagnosis of subclinical pulmonary oedema. A typical image of lung ultrasound before (left panel, normal) and soon after (right panel, B-lines) apnoea diving. Scan is made by a sonographer on the boat supporting divers in Red Sea.

References

    1. Gheorghiade M, Follath F, Ponikowski P, Barsuk JH, Blair JE, Cleland JG, Dickstein K, Drazner MH, Fonarow GC, Jaarsma T, Jondeau G, Sendon JL, Mebazaa A, Metra M, Nieminen M, Pang PS, Seferovic P, Stevenson LW, van Veldhuisen DJ, Zannad F, Anker SD, Rhodes A, McMurray JJ, Filippatos G. Assessing and grading heart failure in acute heart failure: a scientific statement from the acute heart failure committee of the Heart failure association of the European Society of cardiology and endorsed by the European Society of Intensive Care medicine. Eur J Heart Failure 2010;12:423–433.
    1. Lichtenstein D, Mézière G, Biderman P, Gepner A, Barré O. The comet-tail artifact. An ultrasound sign of alveolar-interstitial syndrome. Am J Respir Crit Care Med 1997;156:1640–1646.
    1. Jambrik Z, Monti S, Coppola V, Agricola E, Mottola G, Miniati M, Picano E. Usefulness of ultrasound lung comets as a nonradiologic sign of extravascular lung water. Am J Cardiol 2004;93:1265–1270.
    1. Picano E, Frassi F, Agricola E, Gligorova S, Gargani L, Mottola G. Ultrasound lung comets: a clinically useful sign of extravascular lung water. J Am Soc Echocardiogr 2006;19:356–363.
    1. Volpicelli G, Elbarbary M, Blaivas M, Lichtenstein DA, Mathis G, Kirkpatrick AW, Melniker L, Gargani L, Noble VE, Via G, Dean A, Tsung JW, Soldati G, Copetti R, Bouhemad B, Reissig A, Agricola E, Rouby JJ, Arbelot C, Liteplo A, Sargsyan A, Silva F, Hoppmann R, Breitkreutz R, Seibel A, Neri L, Storti E, Petrovic T, International Liaison Committee on Lung Ultrasound (ILC-LUS) for International Consensus Conference on Lung Ultrasound (ICC-LUS). International evidence-based recommendations for point-of-care lung ultrasound. Intensive Care Med 2012;38:577–591.
    1. Soldati G, Inchingolo R, Smargiassi A, Sher S, Nenna R. Ex-vivo lung sonography: morphologic – ultrasound relationship. Ultrasound Med Biol 2012;38:1169–1170.
    1. Spinelli A, Vinci B, Tirella A, Matteucci M, Gargani L, Ahluwalia A, Domenici C, Picano E, Chiarelli P. Realization of a poro-elastic ultrasound replica of pulmonary tissue. Biomatter 2012;2:37–42.
    1. Rademacher N, Pariaut R, Pate J, Saelinger C, Kearney MT, Gaschen L. Transthoracic lung ultrasound in normal dogs and dogs with cardiogenic pulmonary edema: a pilot study. Vet Radiol Ultrasound 2014;55:447–452.
    1. Jambrik Z, Gargani L, Adamicza A, Kaszaki J, Varga A, Forster T, Boros M, Picano E. B-lines quantify the lung water content: a lung ultrasound versus lung gravimetry study in acute lung injury. Ultrasound Med Biol 2010;36:2004–2010.
    1. Gargani L, Lionetti V, Di Cristofano G, Bevilacqua G, Recchia FA, Picano E. Early detection of acute lung injury uncoupled to hypoxemia in pigs using ultrasound lung comets. Crit Care Med 2007;35:2769–2774.
    1. Agricola E, Bove T, Oppizzi M, Marino G, Zangrillo A, Margonato A, Picano E. Ultrasound comet-tail images. A comparative study with wedge pressure and extravascular lung water. Chest 2005;127:1690–1695.
    1. Enghard P, Rademacher S, Nee J, Hasper D, Engert U, Jörres A, Kruse JM. Simplified lung ultrasound protocol shows excellent prediction of extravascular lung water in ventilated intensive care patients. Crit Care 2015;19:36.
    1. Volpicelli G, Caramello V, Cardinale L, Mussa A, Bar F, Frascisco MF. Bedside ultrasound of the lung for the monitoring of acute decompensated heart failure. Am J Emerg Med 2008;28:585–591.
    1. Baldi G, Gargani L, Abramo A, D'Errico L, Caramella D, Picano E, Giunta F, Forfori F. Lung water assessment by lung ultrasonography in intensive care: a pilot study. Intensive Care Med 2013;39:74–84.
    1. Gargani L, Frassi F, Soldati G, Tesorio P, Gheorghiade M, Picano E. Ultrasound lung comets for the differential diagnosis of acute cardiogenic dyspnoea: a comparison with natriuretic peptides. Eur J Heart Fail 2008;10:70–77.
    1. Liteplo AS, Marill KA, Villen T, Miller RM, Murray AF, Croft PE, Capp R, Noble VE. Emergency thoracic ultrasound in the differentiation of the etiology of shortness of breath (ETUDES): sonographic B-lines and N-terminal pro-brain-type natriuretic peptide in diagnosing congestive heart failure. Acad Emerg Med 2009;16:201–210.
    1. Prosen G, Klemen P, Štrnad M, Grmec S. Combination of lung ultrasound (a comet-tail sign) and N-terminal pro-brain natriuretic peptide in differentiating acute heart failure from chronic obstructive pulmonary disease and asthma as cause of acute dyspnea in prehospital emergency setting. Crit Care 2011;15:R114; 10.1186/cc10140.
    1. Miglioranza MH, Gargani L, Sant'Anna RT, Rover MM, Martins VM, Mantovani A, Weber C, Moraes MA, Feldman CJ, Kalil RA, Sicari R, Picano E, Leiria TL. Lung ultrasound for the evaluation of pulmonary congestion in outpatients: a comparison with clinical assessment, natriuretic peptides, and echocardiography. JACC Cardiovasc Imaging 2013;6:1141–1151.
    1. Volpicelli G, Skurzak S, Boero E, Carpinteri G, Tengattini M, Stefanone V, Luberto L, Anile A, Cerutti E, Radeschi G, Frascisco MF. Lung ultrasound predicts well extravascular lung water but is of limited usefulness in the prediction of wedge pressure. Anesthesiology 2014;121:320–327.
    1. Lichtenstein D. Lung ultrasound in the critically ill. Review. Annals Intensive Care 2014;4:1–12.
    1. Al Deeb M, Barbic S, Featherstone R, Dankoff J, Barbic D. Point-of-care ultrasonography for the diagnosis of acute cardiogenic pulmonary edema in patients presenting with acute dyspnea: a systematic review and meta-analysis. Acad Emerg Med 2014;21:843–852.
    1. Pivetta E, Goffi A, Lupia E, Tizzani M, Porrino G, Ferreri E, Volpicelli G, Balzaretti P, Banderali A, Iacobucci A, Locatelli S, Casoli G, Stone MB, Maule MM, Baldi I, Merletti F, Cibinel GA, SIMEU Group for Lung Ultrasound in the Emergency Department in Piedmont. Lung ultrasound-implemented diagnosis of acute decompensated heart failure in the ED: a SIMEU Multicenter Study. Chest 2015;148:202–210.
    1. Frassi F, Gargani L, Tesorio P, Raciti M, Mottola G, Picano E. Prognostic value of extravascular lung water assessed with ultrasound lung comets by chest sonography in patients with dyspnea and/or chest pain. J Card Fail 2007;13:830–835.
    1. Gustafsson M, Alehagen U, Johansson P. Imaging congestion with a pocket ultrasound device: prognostic implications in patients with chronic heart failure. J Card Fail 2015;21:548–554.
    1. Platz E, Lewis EF, Uno H, Peck J, Pivetta E, Merz AA, Hempel D, Wilson C, Jhund PS, Cheng S, Solomon SD. Detection and prognostic value of pulmonary congestion by lung ultrasound in ambulatory heart failure patients. Eur Heart J 2016;37:1244–1251.
    1. Bedetti G, Gargani L, Sicari R, Gianfaldoni ML, Molinaro S, Picano E. Comparison of prognostic value of echocardiographic risk score with the Thrombolysis in Myocardial Infarction (TIMI) and Global Registry in Acute Coronary Events (GRACE) risk scores in acute coronary syndrome. Am J Cardiol 2010;106:1709–1716.
    1. Zoccali C, Torino C, Tripepi R, Tripepi G, D'Arrigo G, Postorino M, Gargani L, Sicari R, Picano E, Mallamaci F, on behalf of the Lung US in CKD Working Group. Pulmonary congestion predicts cardiac events and mortality in ESRD. J Am Soc Nephrol 2013;24:639–646.
    1. Gargani L, Pang PS, Frassi F, Miglioranza MH, Dini FL, Landi P, Picano E. Persistent pulmonary congestion before discharge predicts rehospitalization in heart failure: a lung ultrasound study. Cardiovasc Ultrasound 2015;13:40.
    1. Coiro S, Rossignol P, Ambrosio G, Carluccio E, Alunni G, Murrone A, Tritto I, Zannad F, Girerd N. Prognostic value of residual pulmonary congestion at discharge assessed by lung ultrasound imaging in heart failure. Eur J Heart Fail 2015;17:1172–1181.
    1. Facchini C, Malfatto G, Giglio A, Facchini M, Parati G, Branzi G. Lung ultrasound and transthoracic impedance for noninvasive evaluation of pulmonary congestion in heart failure. J Cardiovasc Med (Hagerstown) 2015[Epub ahead of print].
    1. Noble VE, Murray AF, Capp R, Sylvia-Reardon MH, Steele DJ, Liteplo A. Ultrasound assessment for extravascular lung water in patients undergoing hemodialysis. Time course for resolution. Chest 2009;135:1433–1439.
    1. Agricola E, Picano E, Oppizzi M, Marino G, Zangrillo A, Margonato A. Assessment of stress-induced pulmonary interstitial edema by chest ultrasound during exercise echocardiography and its correlation with left ventricular function. J Am Soc Echocardiogr 2006;19:457–463.
    1. Scali MC, Simionuc A, Mandoli GE, Dini FL, Marzilli M, Picano E. The added value of exercise-echocardiography in heart failure patients: assessing dynamic changes in extravascular lung water. Eur Heart J Cardiovascul Imaging 2015;16 (suppl 2):S102–S129.
    1. Pratali L, Rimoldi SF, Rexhaj E, Hutter D, Faita F, Salmòn CS, Villena M, Sicari R, Picano E, Allemann Y, Scherrer U, Sartori C. Exercise induces rapid interstitial lung water accumulation in patients with chronic mountain sickness. Chest 2012;141:953–958.
    1. Fagenholz PJ, Gutman JA, Murray AF, Noble VE, Thomas SH, Harris NS. Chest ultrasonography for the diagnosis and monitoring of high-altitude pulmonary edema. Chest 2007;131:1013–1018.
    1. Pratali L, Cavana M, Sicari R, Picano E. Frequent subclinical high-altitude pulmonary edema detected by chest sonography as ultrasound lung comets in recreational climbers. Crit Care Med 2010;38:1818–1823.
    1. Frassi F, Pingitore A, Cialoni D, Picano E. Chest sonography detects lung water accumulation in healthy elite apnea divers. J Am Soc Echocardiogr 2008;21:1150–1155.
    1. Boussuges A, Coulange M, Bessereau J, Gargne O, Ayme K, Gavarry O, Fontanari P, Joulia F. Ultrasound lung comets induced by repeated breath-hold diving, a study in underwater fishermen. Scand J Med Sci Sports 2011;21:e384–e392.
    1. Picano E, Pellikka PA. Stress echo applications beyond coronary artery disease. Eur Heart J 2014;35:1033–1040.
    1. Picano E, Vañó E, Rehani MM, Cuocolo A, Mont L, Bodi V, Bar O, Maccia C, Pierard L, Sicari R, Plein S, Mahrholdt H, Lancellotti P, Knuuti J, Heidbuchel H, Di Mario C, Badano LP. The appropriate and justified use of medical radiation in cardiovascular imaging: a position document of the ESC Associations of Cardiovascular Imaging, Percutaneous Cardiovascular Interventions and Electrophysiology. Eur Heart J 2014;35:665–672.
    1. Bedetti G, Gargani L, Corbisiero A, Frassi F, Poggianti E, Mottola G. Evaluation of ultrasound lung comets by hand-held echocardiography. Cardiovasc Ultrasound 2006;4:34.
    1. Chiem AT, Cham CH, Ander DS, Kobylivker AN, Manson WC. Comparison of expert and novice sonographers’ performance in focused lung ultrasonography in dyspnea (FLUID) to diagnose patients with heart failure syndrome. Acad Emer Med 2015;22:564–573.
    1. Gargani L, Doveri M, D'Errico L, Frassi F, Bazzichi ML, Delle Sedie A, Scali MC, Monti S, Mondillo S, Bombardieri S, Caramella D, Picano E. Ultrasound lung comets in systemic sclerosis: a chest sonography hallmark of pulmonary interstitial fibrosis. Rheumatology (Oxford) 2009;48:1382–1387.
    1. Frasure SE, Matilsky DK, Siadecki SD, Platz E, Saul T, Lewis EF. Impact of patient positioning on lung ultrasound findings in acute heart failure. Eur Heart J Acute Cardiovasc Care 2015;4:326–332.
    1. Gargani L, Volpicelli G. How I do it: lung ultrasound. Cardiovasc Ultrasound 2014;12:25.
    1. Brattain LJ, Telfer BA, Liteplo AS, Noble VE. Automated B-line scoring on thoracic sonography. J Ultrasound Med 2013;32:2185–2190.
    1. Lancellotti P, Price S, Edvardsen T, Cosyns B, Neskovic AN, Dulgheru R, Flachskampf FA, Hassager C, Pasquet A, Gargani L, Galderisi M, Cardim N, Haugaa KH, Ancion A, Zamorano JL, Donal E, Bueno H, Habib G. The use of echocardiography in acute cardiovascular care: recommendations of the European Association of Cardiovascular Imaging and the Acute Cardiovascular care Association. Eur Heart J Cardiov Imaging 2015;16:119–146.
    1. Mebazaa A, Yilmaz MB, Levy P, Ponikowski P, Peacock WF, Laribi S, Ristic AD, Lambrinou E, Masip J, Riley JP, McDonagh T, Mueller C, deFilippi C, Harjola VP, Thiele H, Piepoli MF, Metra M, Maggioni A, McMurray J, Dickstein K, Damman K, Seferovic PM, Ruschitzka F, Leite-Moreira AF, Bellou A, Anker SD, Filippatos G. (2015) Recommendations management on pre-hospital and hospital of acute heart failure: a consensus paper of the Heart Failure Association of the European Society of Cardiology, the European Society of Emergency Medicine and the Society of Academic Emergency Medicine. Eur Heart J 2015;17:544–558.
    1. Lancellotti P, Pellikka PA, Budts W, Chaudry F, Donal E, Dulgheru R, Edvarsen T, Garbi M, Ha JW, Kane G, Kreeger J, Mertens L, Pibarot P, Picano E, Ryan T, Tsutsui J, Varga A. Recommendations for the clinical use of stress echocardiography in non-ischemic heart disease: joint document of the European Association of Cardiovascular imaging and the American Society of Echocardiography. Eur Heart J Cardiov Imaging 2016.
    1. Sicari R, Galderisi M, Voigt JU, Habib G, Zamorano JL, Lancellotti P, Badano LP. The use of pocket-size imaging devices: a position statement of the European Association of Echocardiography. Eur J Echocardiogr 2011;12:85–87.

Source: PubMed

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