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DOI: 10.1055/a-1978-5575
Best Practice Recommendations for the Safe use of Lung Ultrasound
Empfehlungen zur sicheren Anwendung des Ultraschalls an der Lunge- Abstract
- Zusammenfassung
- Introduction
- Current literature status concerning lung ultrasound safety
- Best Practice Recommendations
- References
Abstract
The safety of ultrasound is of particular importance when examining the lungs, due to specific bioeffects occurring at the alveolar air-tissue interface. Lung is significantly more sensitive than solid tissue to mechanical stress. The causal biological effects due to the total reflection of sound waves have also not been investigated comprehensively.
On the other hand, the clinical benefit of lung ultrasound is outstanding. It has gained considerable importance during the pandemic, showing comparable diagnostic value with other radiological imaging modalities.
Therefore, based on currently available literature, this work aims to determine possible effects caused by ultrasound on the lung parenchyma and evaluate existing recommendations for acoustic output power limits when performing lung sonography.
This work recommends a stepwise approach to obtain clinically relevant images while ensuring lung ultrasound safety. A special focus was set on the safety of new ultrasound modalities, which had not yet been introduced at the time of previous recommendations.
Finally, necessary research and training steps are recommended in order to close knowledge gaps in the field of lung ultrasound safety in the future.
These recommendations for practice were prepared by ECMUS, the safety committee of the EFSUMB, with participation of international experts in the field of lung sonography and ultrasound bioeffects.
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Zusammenfassung
Die Sicherheit des Ultraschalls ist bei der Untersuchung der Lunge von besonderer Bedeutung, da spezifische Wechselwirkungsmechanismen an der alveolaren Luft-Gewebe-Grenze auftreten. Lungengewebe ist dabei deutlich empfindlicher gegenüber mechanischen Kräften als solides Gewebe. Die ursächlichen biologischen Effekte, basierend auf Totalreflektion von Schallwellen, sind zudem nur unzureichend untersucht.
Andererseits ist der klinische Nutzen des Lungenultraschalls beträchtlich und hat aufgrund der Pandemiesituation einen erheblichen Stellenwert dazugewonnen. Dabei erweist sich dieser bisweilen dem anderer radiologischer Bildgebungsverfahren als ebenbürtig.
Deshalb widmet sich diese Arbeit, basierend auf derzeit verfügbaren Literaturquellen, dem Einfluss von Schalleffekten auf das Lungenparenchym und evaluiert bestehende Empfehlungen zur Schalldruckreduzierung bei der Durchführung der Lungensonografie.
Es wird ein Vorgehen empfohlen, um klinisch relevante Bilder zu erhalten und gleichzeitig die Ultraschallsicherheit zu gewährleisten. Ein besonderes Augenmerk liegt auf der Sicherheit neuer Ultraschall-Modalitäten, welche zum Zeitpunkt früherer Empfehlungen noch nicht berücksichtigt waren.
Abschließend werden notwendige Forschungs- und Ausbildungsschritte empfohlen, um Wissenslücken auf dem Gebiet des Lungenultraschalls in Zukunft schließen zu können.
Diese Empfehlungen für die Praxis wurden von ECMUS, dem Sicherheitskomitee der EFSUMB, unter Mitwirkung von internationalen Experten auf dem Gebiet der Lungensonografie und biologischer Ultraschallwechselwirkung, erstellt.
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Introduction
This best practice recommendation gives an overview of current statements and novel findings regarding the safety aspects on the interaction of ultrasound on lung tissue. Based on these data, a best practice recommendation is given to minimise potential risks during routine lung ultrasound applications.
The use of sonography on lung tissue is a valuable Point of Care diagnostic covering almost all medical disciplines [1] [2] [3] [4] which is currently summarised by an international consensus [5]. However, due to total reflection at the air-tissue interface, such as occurs during pleural sonography, potential bio-effects of this interaction should be considered. Consideration of these bio-effects should always be balanced with the clinical benefits of using a non-ionising imaging modality such as sonography.
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Current literature status concerning lung ultrasound safety
Ultrasound, when used under diagnostic exposure conditions, can cause pulmonary capillary haemorrhage (PCH) in peripheral lung which has been investigated extensively on several animal models [6]. Lung ultrasound (LUS) induced PCH has not been investigated in humans on a pathological level such as in animals. In contrast, observational safety studies in children [7] and during transoesophageal sonography [8] showed no complications including no symptomatic pulmonary haemorrhage.
In large animal models, it was clearly shown that PCH occurred over an acoustic output range that is typical of that emitted during clinical sonographic B-mode (brightness mode) imaging [9]. In addition, it has been shown that sonographic modes with longer pulses such as those used in Doppler induce PCH at lower output levels (low Mechanical Index (MI)) [10]. In addition, shear wave elastography (SWE) and acoustic radiation force impulse (ARFI) sonography techniques emit push pulses with higher intensity and longer durations, that induce reliable PCH on direct pleural exposure as shown in pre-clinical studies [11] [12].
Even though ultrasound induced PCH seems to be a threshold phenomenon, reduction of scan duration, independent of scanning mode, significantly decreases the likelihood of PCH induction and its extent [13] [14]. In obese patients, PCH is much less likely to occur during lung sonography due to the high attenuation of the soft tissue of the chest wall [15].
Earlier statements of the British Medical Ultrasound Society (BMUS) and American Institute of Ultrasound in Medicine (AIUM) point to the likelihood of PCH induction at MI values greater than 0.3 [16] [17].
Sonography induced PCH was shown to be limited to a peripheral depth of 1–2 mm and is related to the size of the transducer. PCH is asymptomatic, does not cause alveolar rupture and does not require interventions [18] [19]. Diagnostic concerns arise, however, due to the fact that PCH can generate LUS signs such as the vertical hyperechoic artefacts (B Lines) and White Lung Syndrome (WLS) and may lead to an incorrect presentation of LUS artefacts and therefore diagnosis [11] [13].
To the best of our knowledge, there is no literature on LUS safety in diseased lung nor regarding effects of contrast enhanced sonography on lung. Due to lower MI values, typically used during contrast enhanced ultrasound (CEUS), it may not affect the lung. But studies are required to prove the safety of CEUS on lung tissue.
Therapeutic ultrasound applications are emerging, where focal ablation in proximity to lung is performed [20]. Pre-clinical animal studies showed PCH induction in lung tissue during shock wave treatment of liver [21] and heart tissue at peak negative pressures (PNP) above 1.5 MPa. Such values are similar to diagnostic ultrasound thresholds [22], however due to the use of higher intensities and lower frequencies than in diagnostic sonography, PCH may arise on a larger surface. Even though the lung is not directly targeted, pre-focal and post-focal intensities may expose the lung surface above the PCH threshold. Therefore, treatment planning should consider a sufficient safety margin between focal position and lung during application of therapeutic ultrasound in proximity to lung.
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Best Practice Recommendations
Scan Settings and Preparation
A LUS specific Pre-Set should be used or scanner settings in line with the guidelines should be set up prior to any LUS examination [23] [24]. LUS specific Pre-Sets are nowadays available on modern scanners but cover a wide acoustic output range (0.4–1.4 MI). Therefore, the initial output should be adjusted (MI ≤ 0.4) independent of PreSet configuration before any lung examination.
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Safety Indices during applications
Independent of mode, sonography of the lung with an MI value of less than or equal to 0.4 can be performed safely without limits on exposure time. Use overall gain and TGC (time gain compensation) for optimal imaging adjustments. For specific diagnostic imaging requirements, the output can be increased up to an MI value of 0.7.
In clinical cases where adiposity may limit the field of view, or acoustic obstacles exist in the sonication path, a maximal MI value of 1.0 should not be exceeded in order to minimise the probability of cavitation. In such cases, justified by diagnostic needs, the operator should be aware of the likelihood of PCH induction falsifying diagnostic findings.
The use of the ALARA (As Low As Reasonable Achievable) principle is strongly recommended whenever LUS is performed. When exceeding the initial MI value and depending on the examination requirements, exposure times should be kept as short as possible (1–2 breath cycles).
The use of Doppler during LUS should be applied with an MI ≤ 0.5 and with exposure times as short as possible.
SWE and ARFI sonography techniques should be performed only if the region of interest (ROI-where the shear wave is generated) is located in consolidated, peripheral lung tissue, avoiding direct pleural exposure.
Lung sonography in the neonate should always be performed with the lowest MI value possible and not exceeding 0.4. The use of Doppler as well as SWE and ARFI should not be applied on neonatal subjects until further studies have shown that it is safe to use for this vulnerable patient class.
A summary of output setting recommendations is shown in [Table 1].
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Education and Future directions
Specific teaching and education for lung sonography should include principles of safety indices and their recommended limits for lung sonography.
The safety profile of SWE and ARFI when applied to lung tissues requires more scientific evaluation to prove its diagnostic safety record before further recommendation.
No lung specific safety index has been introduced to date. However, most of the research literature shows good correlation of PCH thresholds with MI, even though current research would suggest that cavitation is not the cause of PCH [25]. A specific safety index for lung is justified which should include TI (Thermal Index), MI and pulse duration but requires evaluation in future studies [18] [26].
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Conflict of Interest
Prof. Demi is cofounder of UltraAI (Trento, IT); received funding from the European Institute for Innovation and Technology, Fondazione Valorizzazione Ricerca Trentina, the National Research Council (CNR), and Esaote(IT).
Dr Wolfram receives Funding from the Federal Ministry of Education and Research (BMBF, Germany).
Acknowledgment
The authors thank the support of the BMUS Physics & Safety Committee as well as Dr Lesser (Gera, Germany).
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References
- 1 Mathis G. Pneumonia: Does Ultrasound Replace Chest X-Ray?. Praxis 1994; 107 (23) 1283-1287
- 2 Soldatia G, Demi M, Smargiassic A. et al. The role of ultrasound lung artefacts in the diagnosis of respiratory diseases. Exp Rev Resp Med 2019; 13 (02) 163-172
- 3 Soldati G, Demi M. The use of lung ultrasound images for the differential diagnosis of pulmonary and cardiac interstitial pathology. J Ultrasound 2017; 20 (02) 91-96
- 4 Gutsche H, Lesser T, Wolfram F. et al. Significance of Lung Ultrasound in Patients with Suspected COVID-19 Infection at Hospital Admission. Diagnostics 2021; 11 (06) 921
- 5 Demi L, Wolfram F, Klersy C. et al. New International Guidelines and Consensus on the Use of Lung Ultrasound. J Ultrasound Med 2022;
- 6 Rott H. Lung hemorrhage caused by diagnostic ultrasound. Review of the literature. Ultraschall in Med 1997; 18 (05) 226-228
- 7 Jagła M, Krzeczek O, Buczyńska A. et al. The safety of pulmonary ultrasonography in the neonatal intensive care unit. Dev Period Med 2018; 22 (01) 75-80
- 8 Meltzer R, Adsumelli R, Risher W. et al. Lack of Lung Hemorrhage in Humans After Intraoperative Transesophageal Echocardiography with Ultrasound Exposure Conditions Similar to Those Causing Lung Hemorrhage in Laboratory Animals. J Am Echocardiography 1998; 11 (01) 57-60
- 9 Miller D, Dong Z, Dou C. et al. Pulmonary capillary hemorrhage induced by diagnostic ultrasound in ventilated rats. Ultrasound Med Biol 2017; 44 (08) 1810-1817
- 10 Miller D, Dong Z, Dou C. et al. Pulmonary Capillary Hemorrhage Induced by Different Imaging Modes of Diagnostic Ultrasound. Ultrasound Med Biol 2018; 44 (05) 1012-1021
- 11 Miller D, Dong Z, Dou C. et al. Pulmonary Capillary Hemorrhage Induced by Super Sonic Shear Wave Elastography in Rats. Ultrasound Med Biol 2019; 45 (11) 2993-3004
- 12 Takayama N, Ishiguro Y, Taniguchi N. et al. The effect of ultrasound with acoustic radiation force on rabbit lung tissue: a preliminary study. J Med Ultrason 2001; 43 (04) 481-485
- 13 Miller D, Dong Z, Dou C. et al. Influence of scan duration on pulmonary capillary hemorrhage induced by diagnostic ultrasound. Ultrasound in Med. & Biol 2016; 42 (08) 1942-1950
- 14 Abramowicz J, Bagley J, Church C. et al. Medical Ultrasound Safety/Fourth Edition. Part Three: Implementing ALARA. 2020
- 15 Patterson B, Miller D. Experimental measurements of ultrasound attenuation in human chest wall and assessment of the mechanical index for lung ultrasound. Ultrasound Med Biol 2020; 46 (06) 1442-1454
- 16 British Medical Ultrasound Society. BMUS. [Online]. 2009 [cited 2021. Available from: https://www.bmus.org/policies-statements-guidelines/safety-statements/
- 17 American Institute of Ultrasound in Medicine A. Official Statements. [Online]. 2015 [cited 2021. Available from: https://www.aium.org/officialStatements/67
- 18 Miller D. Mechanism for induction of pulmonary capillary hemorrhage by diagnostic ultrasound : Review and consideration of acoustical pleural surface pressure. Ultrasound Med Biol 2016; 42 (12) 2743-2757
- 19 Miller D, Suresh M, Dou C. et al. Characterization of ultrasound-induced pulmonary capillary hemorrhage in rats. Microvasc Res 2014; 93: 42-45
- 20 Tsang S, Wing MaK, Hoi SheW. et al. High-intensity focused ultrasound ablation of liver tumors in difficult locations. Int J Hyperthermia 2021; 38 (02) 56-64
- 21 Knott E, Longo K, Swietlik J. et al. Hepatic Ablation with Robotically Assisted Sonic Therapy (RAST) Through Full Rib Coverage in a Porcine Model. In ITSU EUFUS. Barcelona: International Society for Therapeutic Ultrasound; 2019
- 22 Jang K, Tu T, Nagle M. et al. Molecular and histological effects of MR-guided pulsed focused ultrasound to the rat heart. J Transl Med 2017; 15 (01) 252
- 23 Gargani L, Volpicelli G. How I do it: lung ultrasound. Cardiovasc Ultrasound 2014; 12 (25)
- 24 Liu J, Guo G, Kurepa D. et al. Specification and guideline for technical aspects and scanning parameter settings of neonatal lung ultrasound examination. J Matern Fetal Neonatal Med 2021; 35 (05) 1003-1016
- 25 OʼBrien W, Frizzell L, Weigel R. et al. Ultrasound-induced lung hemorrhage is not caused by inertial cavitation. J Acoust Soc Am 2000; 108 (03) 1290-1297
- 26 Church C, OʼBrien W. Evaluation of the Threshold for Lung Hemorrhage by Diagnostic Ultrasound and a Proposed New Safety Index. Ultrasound Med Biol 2007; 33 (05) 810-818
Correspondence
Publication History
Received: 21 July 2022
Accepted: 14 November 2022
Accepted Manuscript online:
14 November 2022
Article published online:
03 March 2023
© 2023. Thieme. All rights reserved.
Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany
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References
- 1 Mathis G. Pneumonia: Does Ultrasound Replace Chest X-Ray?. Praxis 1994; 107 (23) 1283-1287
- 2 Soldatia G, Demi M, Smargiassic A. et al. The role of ultrasound lung artefacts in the diagnosis of respiratory diseases. Exp Rev Resp Med 2019; 13 (02) 163-172
- 3 Soldati G, Demi M. The use of lung ultrasound images for the differential diagnosis of pulmonary and cardiac interstitial pathology. J Ultrasound 2017; 20 (02) 91-96
- 4 Gutsche H, Lesser T, Wolfram F. et al. Significance of Lung Ultrasound in Patients with Suspected COVID-19 Infection at Hospital Admission. Diagnostics 2021; 11 (06) 921
- 5 Demi L, Wolfram F, Klersy C. et al. New International Guidelines and Consensus on the Use of Lung Ultrasound. J Ultrasound Med 2022;
- 6 Rott H. Lung hemorrhage caused by diagnostic ultrasound. Review of the literature. Ultraschall in Med 1997; 18 (05) 226-228
- 7 Jagła M, Krzeczek O, Buczyńska A. et al. The safety of pulmonary ultrasonography in the neonatal intensive care unit. Dev Period Med 2018; 22 (01) 75-80
- 8 Meltzer R, Adsumelli R, Risher W. et al. Lack of Lung Hemorrhage in Humans After Intraoperative Transesophageal Echocardiography with Ultrasound Exposure Conditions Similar to Those Causing Lung Hemorrhage in Laboratory Animals. J Am Echocardiography 1998; 11 (01) 57-60
- 9 Miller D, Dong Z, Dou C. et al. Pulmonary capillary hemorrhage induced by diagnostic ultrasound in ventilated rats. Ultrasound Med Biol 2017; 44 (08) 1810-1817
- 10 Miller D, Dong Z, Dou C. et al. Pulmonary Capillary Hemorrhage Induced by Different Imaging Modes of Diagnostic Ultrasound. Ultrasound Med Biol 2018; 44 (05) 1012-1021
- 11 Miller D, Dong Z, Dou C. et al. Pulmonary Capillary Hemorrhage Induced by Super Sonic Shear Wave Elastography in Rats. Ultrasound Med Biol 2019; 45 (11) 2993-3004
- 12 Takayama N, Ishiguro Y, Taniguchi N. et al. The effect of ultrasound with acoustic radiation force on rabbit lung tissue: a preliminary study. J Med Ultrason 2001; 43 (04) 481-485
- 13 Miller D, Dong Z, Dou C. et al. Influence of scan duration on pulmonary capillary hemorrhage induced by diagnostic ultrasound. Ultrasound in Med. & Biol 2016; 42 (08) 1942-1950
- 14 Abramowicz J, Bagley J, Church C. et al. Medical Ultrasound Safety/Fourth Edition. Part Three: Implementing ALARA. 2020
- 15 Patterson B, Miller D. Experimental measurements of ultrasound attenuation in human chest wall and assessment of the mechanical index for lung ultrasound. Ultrasound Med Biol 2020; 46 (06) 1442-1454
- 16 British Medical Ultrasound Society. BMUS. [Online]. 2009 [cited 2021. Available from: https://www.bmus.org/policies-statements-guidelines/safety-statements/
- 17 American Institute of Ultrasound in Medicine A. Official Statements. [Online]. 2015 [cited 2021. Available from: https://www.aium.org/officialStatements/67
- 18 Miller D. Mechanism for induction of pulmonary capillary hemorrhage by diagnostic ultrasound : Review and consideration of acoustical pleural surface pressure. Ultrasound Med Biol 2016; 42 (12) 2743-2757
- 19 Miller D, Suresh M, Dou C. et al. Characterization of ultrasound-induced pulmonary capillary hemorrhage in rats. Microvasc Res 2014; 93: 42-45
- 20 Tsang S, Wing MaK, Hoi SheW. et al. High-intensity focused ultrasound ablation of liver tumors in difficult locations. Int J Hyperthermia 2021; 38 (02) 56-64
- 21 Knott E, Longo K, Swietlik J. et al. Hepatic Ablation with Robotically Assisted Sonic Therapy (RAST) Through Full Rib Coverage in a Porcine Model. In ITSU EUFUS. Barcelona: International Society for Therapeutic Ultrasound; 2019
- 22 Jang K, Tu T, Nagle M. et al. Molecular and histological effects of MR-guided pulsed focused ultrasound to the rat heart. J Transl Med 2017; 15 (01) 252
- 23 Gargani L, Volpicelli G. How I do it: lung ultrasound. Cardiovasc Ultrasound 2014; 12 (25)
- 24 Liu J, Guo G, Kurepa D. et al. Specification and guideline for technical aspects and scanning parameter settings of neonatal lung ultrasound examination. J Matern Fetal Neonatal Med 2021; 35 (05) 1003-1016
- 25 OʼBrien W, Frizzell L, Weigel R. et al. Ultrasound-induced lung hemorrhage is not caused by inertial cavitation. J Acoust Soc Am 2000; 108 (03) 1290-1297
- 26 Church C, OʼBrien W. Evaluation of the Threshold for Lung Hemorrhage by Diagnostic Ultrasound and a Proposed New Safety Index. Ultrasound Med Biol 2007; 33 (05) 810-818