Abstract
Key Words
Introduction
World Health Organization (WHO). Coronavirus disease 2019 (COVID-19) Situation Report 51. 2020 March 11. Available at: https://www.who.int/emergencies/diseases/novel-coronavirus-2019/situation-reports. Accessed March 11, 2020.
- Gupta A
- Madhavan MV
- Sehgal K
- Nair N
- Mahajan S
- Sehrawat TS
- Bikdeli B
- Ahluwalia N
- Ausiello JC
- Wan EY
- Freedberg DE
- Kirtane AJ
- Parikh SA
- Maurer MS
- Nordvig AS
- Accili D
- Bathon JM
- Mohan S
- Bauer KA
- Leon MB
- Krumholz HM
- Uriel N
- Mehra MR
- Elkind MSV
- Stone GW
- Schwartz A
- Ho DD
- Bilezikian JP
- Landry DW.
- 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 evidence-based recommendations for point-of-care lung ultrasound.
- Bonadia N
- Carnicelli A
- Piano A
- Buonsenso D
- Gilardi E
- Kadhim C
- Torelli E
- Petrucci M
- Di Maurizio L
- Biasucci DG
- Fuorlo M
- Forte E
- Zaccaria R
- Franceschi F.
Methods
Study design
Lung US scanning technique

Lung ultrasound findings
- 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 evidence-based recommendations for point-of-care lung ultrasound.
- •A-pattern: A-lines without other artifacts, 0 points (Fig. 2)Fig. 2A-Pattern. The red arrows indicates the posterior pleural reverberations (A-Lines)
- •Isolated B-lines: one or no more than three distant, well-isolated B-lines, 1 point (Fig. 3)Fig. 3Isolated B-line. The red arrow indicates an isolated B-line moving from the pleural line.
- •Isolated subpleural consolidation: in a context of A-pattern, presence of one consolidation <2 cm with a posterior vertical artifact, extending to the bottom of the screen without fading and moving synchronously with lung sliding, 1.5 points (Fig. 4)Fig. 4Isolated subpleural consolidation. The red arrow indicates an isolated subpleural consolidation.
- •Non-confluent B-lines: multiple B-lines that do not completely erase A-lines, 2 points (Fig. 5).Fig. 5Non-confluent B-lines. Red arrows indicate two B-lines moving from the pleural line, non-completely erasing the posterior pleural reverberations (green arrow).
- •Confluent B-lines: multiple B-lines that completely erase A-lines, 3 points (Fig. 6)Fig. 6Multiple confluent B-lines completely erasing the posterior pleural reverberation of the pleural line. The red arrow indicates the pleural line with a “with-lung” appearance.
- •Confluent subpleural consolidations (CSpCs): multiple consolidations <2 cm in depth with a posterior vertical artifact, 4 points (Fig. 7)Fig. 7Multiple subpleural consolidations. Red arrows indicate the thickening of the irregular pleural line with a posterior “with-lung appearance” because of erasure of the pleural reverberation.
- •Parenchymal consolidation >2 cm: subpleural consolidation >2 cm in-depth, 5 points (Fig. 8)Fig. 8Large subpleural consolidation. The red arrow indicates the pulmonary consolidation and the “hepatic-like” aspect of the lung. The green arrow indicates the air bronchograms: hyperechogenic artifact caused by the presence of trapped air.
- •Pleural effusion: anechoic fluid within the pleural space, 0 points (Fig. 9).Fig 9The red arrow indicates the anechoic free fluid in the thoracic cavity, above the diaphragm on the right side of the body. The red star indicates the liver.
Lung US severity index
Lung artifact | Chest area | |||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
R1 | L1 | R2 | L2 | R3 | L3 | R4 | L4 | R5 | L5 | R6 | L6 | |
A-Pattern (0 points) | ||||||||||||
Isolated B-lines (1 point) | ||||||||||||
Isolated subpleural consolidation (1.5 points) | ||||||||||||
Non-confluent B-lines (2 points) | ||||||||||||
Confluent B-lines (3 points) | ||||||||||||
Confluent subpleural consolidations (4 points) | ||||||||||||
Parenchymal consolidation >2 cm (5 points) | ||||||||||||
Pleural effusion (0 points) | ||||||||||||
rLUSS | ||||||||||||
rLUHS | ||||||||||||
rLUSI | ||||||||||||
LUSI: | points | |||||||||||
How to use it: 1. Each column identifies a specific thoracic area: enter in each empty box all the lung ultrasound lesion(s) found in each area. 2. Calculate (i) rLUSS as the sum of the corresponding points of all patterns found in each area; (ii) rLUHS as the number of different patterns found in each area; and (iii) rLUSI as rLUSS/rLUHS. 3. LUSI is the sum of all rLUSI values. |
Statistical analysis
Results
Clinical characteristics of all patients
All patients | COVID-19 patients | ||||||
---|---|---|---|---|---|---|---|
Total N = 159 | No COVID-19 (N = 58) | COVID-19 (N = 101) | p Value | Survived to hospital admission(N = 82) | In-hospital death (N = 19) | p Value | |
Demographics | |||||||
Men, N (%) | 105 (66) | 34 (58.6) | 71 (70.3) | 0.135 | 55 (67.1) | 16 (84.2) | 0.133 |
Age, mean (SD), y | 64.59 (16.63) | 65.4 (19.51) | 64.13 (14.85) | 0.67 | 61 (14) | 79 (8) | <0.001 |
Vital signs, mean (SD) | |||||||
Heart rate, ppm | 93.9 (18.28) | 98.45 (20.49) | 91.33 (16.46) | 0.02 | 89 (15) | 99 (19) | 0.02 |
Respiratory rate/min | 20.63 (5.51) | 21.84 (6.35) | 19.94 (4.87) | 0.06 | 19 (4) | 23 (6) | 0.02 |
Systolic blood pressure, mm Hg | 123.51 (18.45) | 126.27 (22.5) | 121.95 (15.61) | 0.2 | 122 (14) | 121 (20) | 0.69 |
Diastolic blood pressure, mm Hg | 73.5 (10.09) | 73.95 (11.11) | 73.25 (9.51) | 0.68 | 74 (9) | 71 (10) | 0.17 |
Body temperature,°C | 37.61 (0.98) | 37.47 (1.04) | 37.7 (0.94) | 0.16 | 37.7 (.9) | 37.7 (1) | 0.84 |
Anion blood gas analysis, mean (SD) | |||||||
pH | 7.44 (0.05) | 7.43 (0.05) | 7.46 (0.04) | <0.001 | 7.47 (0.004) | 7.42 (0.06) | <0.001 |
pCO2 | 36.28 (6.41) | 38.9 (7.76) | 34.9 (5.12) | <0.001 | 35 (5) | 34 (7) | 0.65 |
pO2 | 89.99 (33.99) | 97.1 (38.21) | 86.3 (31.14) | 0.06 | 90 (32) | 70 (21) | <0.001 |
Lactate | 1.06 (0.5) | 1.14 (0.61) | 1.03 (0.43) | 0.24 | 0.97 (0.34) | 1.3 (0.65) | 0.04 |
P/F | 281 (104.18) | 318 (109.25) | 261 (96.33) | <0.001 | 284 (76) | 172 (117) | <0.001 |
HCO3 | 25 (3.83) | 25 (4.53) | 24 (3.41) | 0.18 | 25.24 (3) | 22.39 (4.14) | <0.001 |
Lung ultrasound characteristics | |||||||
No. of lung US scans, mean (SD) | 23.77 (7.02) | 21.41 (5.74) | 25.12 (7.18) | 0.001 | 25.78 (7.53) | 22.26 (4.61) | 0.054 |
Length of lung US scan, mean (SD), min | 8.05 (2.88) | 7.53 (2.66) | 8.35 (2.98) | 0.087 | 8.49 (3.06) | 7.74 (2.6) | 0.49 |
Areas with A-pattern, median (IQR), N | 11 (10–12) | 12 (11–12) | 11 (9–12) | 0.01 | 11 (10–12) | 9 (6.75–11) | <0.001 |
Areas with isolated B-lines, median (IQR), N | 2 (1–4) | 2 (0.75–4) | 2 (1–4) | 0.46 | 3 (1–5) | 1 (0.75–4) | 0.053 |
Areas with isolated subpleural consolidations, median (IQR) | 1 (0–2) | 1 (0–2) | 1 (0–2) | 0.095 | 2 (0–3) | 0 (0–2) | 0.107 |
Areas with non-confluent B-lines, median (IQR), N | 0 (0–2) | 0.5 (0–2) | 0 (0–2) | 0.85 | 0 (0–2) | 2 (0–3.25) | 0.04 |
Areas with confluent B-lines, median (IQR), N | 0 (0–1.25) | 0 (0–0.25) | 0 (0–2) | 0.014 | 0 (0–1) | 1.5 (0–3) | 0.013 |
Areas with confluent subpleural consolidations, median (IQR), N | 4 (2–6) | 2 (0–4) | 5 (3–7) | <0.001 | 5 (3–6) | 6.5 (4.75–8.25) | 0.014 |
Areas with pulmonary consolidation >2 cm, median (IQR), N | 0 (0–1) | 0 (0–1) | 0 (0–1) | 0.89 | 0 (0–1) | 0 (0–1.25) | 0.56 |
Areas with pleural effusion, median (IQR), N | 0 (0–1) | 0 (0–1.5) | 0 (0–1) | 0.38 | 0 (0–1) | 1 (0–2) | 0.29 |
Lung Ultrasound Severity Score, mean (SD) | 29.95 (18.25) | 22.62 (18.37) | 34.16 (16.89) | <0.001 | 32.33 (15.84) | 43.21 (18.67) | 0.009 |
Lung Ultrasound Severity Index, mean (SD) | 13.96 (9.25) | 10.08 (8.92) | 16.14 (8.71) | <0.001 | 14.56 (7.6) | 22.91 (10.08) | <0.001 |
Lung Ultrasound Heterogeneity Score, mean (SD) | 21.64 (5.53) | 19.84 (5.72) | 22.67 (5.17) | 0.002 | 22.79 (5.11) | 22.79 (4.98) | 0.92 |
Outcomes | |||||||
Total deaths, N (%) | 23 (14.5) | 4 (6.9) | 19 (18.8) | 0.04 |
Lung US characteristics of all patients
AUROC (95% CI) | Cutoff | Sensitivity (%) | Specificity (%) | Odds ratio (95% CI) | |
---|---|---|---|---|---|
In relation to in-hospital mortality | |||||
LUSI | 0.805 (0.735–0.864) | 14 | 90.91 | 65.67 | 1.14 (1.076–1.207) |
3.63 | 95 | 15.67 | |||
26 | 40.91 | 95 | |||
LUSS | 0.733 (0.657–0.8) | 37 | 65.22 | 73.53 | 1.045 (1.018–1.073) |
11 | 95 | 16.9 | |||
57 | 20.87 | 95 | |||
LUHS | 0.576 (0.495–0.654) | 20 | 69.57 | 48.53 | 1.037 (0.958–1.122) |
13 | 95 | 8.31 | |||
31 | 4 | 95 | |||
In relation to in-hospital mortality, COVID-19 patients only | |||||
LUSI | 0.76 (0.66–0.84) | 24 | 63.16 | 90 | 1.124 (1.052–1.2) |
0 | 95 | 1.23 | |||
30 | 21 | 95 | |||
LUSS | 0.69 (059–0.78) | 37 | 68.42 | 68.29 | 1.042 (1.009–1.076) |
0 | 95 | 1.22 | |||
58 | 21.58 | 95 | |||
LUHS | 0.51 (0.41–0.61) | 20 | 68.42 | 37.8 | 1.005 (0.913–1.108) |
12 | 95 | 2.38 | |||
31 | 5.26 | 95 | |||
In relation to COVID-19 diagnosis | |||||
LUSI | 0.72 (0.64–0.78) | 13 | 63 | 75 | 1.09 (1.042–1.141) |
2 | 95 | 14.8 | |||
26 | 14.8 | 95 | |||
LUSS | 0.69 (0.62–0.76) | 26 | 68.32 | 68.97 | 1.04 (1.019–1.062) |
7 | 95 | 24.14 | |||
52 | 14.65 | 95 | |||
LUHS | 0.65 (0.57–0.73) | 17 | 88.12 | 37.93 | 1.11 (1.036–1.181) |
14 | 95 | 20.78 | |||
31 | 4.85 | 95 |
In-hospital deaths related to lung US characteristics in patients with COVID-19
Discussion
- Wu C
- Chen X
- Cai Y
- Xia J
- Zhou X
- Xu S
- Huang H
- Zhang L
- Zhou X
- Du C
- Zhang Y
- Song J
- Wang S
- Chao Y
- Yang Z
- Xu J
- Zhou X
- Chen D
- Xiong W
- Xu L
- Zhou F
- Jiang J
- Bai C
- Zheng J
- Song Y.
- 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 evidence-based recommendations for point-of-care lung ultrasound.
- Bar S
- Lecourtois A
- Diouf M
- Goldberg E
- Bourbon C
- Arnaud E
- Domisse L
- Dupont H
- Gosset P.
- Zieleskiewicz L
- Markarian T
- Lopez A
- Taguet C
- Mohammedi N
- Boucekine M
- Baumstarck K
- Besch G
- Mathon G
- Duclos G
- Bouvet L
- Michelet P
- Allaouchiche B
- Chaumoître K
- Di Bisceglie M
- Leone M
Comparative study of lung ultrasound and chest computed tomography scan in the assessment of severity of confirmed COVID-19 pneumonia.
- Mongodi S
- Orlando A
- Arisi E
- Tavazzi G
- Santangelo E
- Caneva L
- Pozzi M
- Pariani E
- Bettini G
- Maggio G
- Perlini S
- Preda L
- Iotti GA
- Mojoli F.
- Islam N
- Ebrahimzadeh S
- Salameh J-P
- Kazi S
- Fabiano N
- Treanor L
- Absi M
- Hallgrimson Z
- Leeflang MMG
- Hooft L
- van der Pol CB
- Prager R
- Hare SS
- Dennie C
- Spijker R
- Deeks JJ
- Dinnes J
- Jenniskens K
- Korevaar DA
- Cohen JF
- Van den Bruel A
- Takwoingi Y
- van de Wijgert J
- Damen JAAG
- Wang J
- McInnes MDF.
- Bar S
- Lecourtois A
- Diouf M
- Goldberg E
- Bourbon C
- Arnaud E
- Domisse L
- Dupont H
- Gosset P.
- Bonadia N
- Carnicelli A
- Piano A
- Buonsenso D
- Gilardi E
- Kadhim C
- Torelli E
- Petrucci M
- Di Maurizio L
- Biasucci DG
- Fuorlo M
- Forte E
- Zaccaria R
- Franceschi F.
- Haak SL
- Renken IJ
- Jager LC
- Lameijer H
- van der Kolk BBY.
- Lichter Y
- Topilsky Y
- Taieb P
- Banai A
- Hochstadt A
- Merdler I
- Gal Oz A
- Vine J
- Goren O
- Cohen B
- Sapir O
- Granot Y
- Mann T
- Friedman S
- Angel Y
- Adi N
- Laufer-Perl M
- Ingbir M
- Arbel Y
- Matot I
- Szekely Y
- Islam N
- Ebrahimzadeh S
- Salameh J-P
- Kazi S
- Fabiano N
- Treanor L
- Absi M
- Hallgrimson Z
- Leeflang MMG
- Hooft L
- van der Pol CB
- Prager R
- Hare SS
- Dennie C
- Spijker R
- Deeks JJ
- Dinnes J
- Jenniskens K
- Korevaar DA
- Cohen JF
- Van den Bruel A
- Takwoingi Y
- van de Wijgert J
- Damen JAAG
- Wang J
- McInnes MDF.
- 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 evidence-based recommendations for point-of-care lung ultrasound.
Limitations
Conclusions
Conflict of interest disclosure
Acknowledgments
References
- ACR recommendations for the use of chest radiography and computed tomography (CT) for suspected COVID-19 infection.Author, Reston, VA2020 (Available at:) (Accessed February 1, 2021)
- The association of lung ultrasound images with COVID-19 infection in an emergency room cohort [e-pub ahead of print].Anaesthesia. 2020; (Accessed February 1, 2021)https://doi.org/10.1111/anae.15175
- BLUE protocol ultrasonography in emergency department patients presenting with acute dyspnea.Am J Emerg Med. 2019; 37: 2020-2027
- Lung ultrasound findings are associated with mortality and need for intensive care admission in COVID-19 patients evaluated in the emergency department.Ultrasound Med Biol. 2020; 46: 2927-2937
- Chest sonography: A useful tool to differentiate acute cardiogenic pulmonary edema from acute respiratory distress syndrome.Cardiovasc Ultrasound. 2008; 29: 6-16
- The species severe acute respiratory syndrome-related coronavirus: Classifying 2019-nCoV and naming it SARS-CoV-2.Nat Microbiol. 2020; 5: 536-544
- Lung ultrasound score to monitor COVID-19 pneumonia progression in patients with ARDS.PLoS One. 2020; 15e0236312
- Clinical characteristics of Covid-19 in New York City.N Engl J Med. 2020; 382: 2372-2374
- Extrapulmonary manifestations of COVID-19.Nat Med. 2020; 26: 1017-1032
- Diagnostic accuracy of point-of-care lung ultrasound in COVID-19 [e-pub ahead of print].Emerg Med J. 2020; (Nov 18. Accessed February 1, 2021)https://doi.org/10.1136/emermed-2020-210125
- Early clinical and CT manifestations of coronavirus disease 2019 (COVID-19) pneumonia.Am J Roentgenol. 2020; 17: 1-6
- Thoracic imaging tests for the diagnosis of COVID-19.Cochrane Database Syst Rev. 2021; 9CD013639
- Lung ultrasound predicts clinical course and outcomes in COVID-19 patients.Intensive Care Med. 2020; 46: 1873-1883
- Lung ultrasound score in establishing the timing of intubation in COVID-19 interstitial pneumonia: A preliminary retrospective observational study.PLoS One. 2020; 15e0238679
- CLUE: COVID-19 lung ultrasound in emergency department.Emerg Med Australas. 2020; 32: 694-696
- Modified lung ultrasound score for assessing and monitoring pulmonary aeration.Ultraschall Med. 2017; 38: 530-537
- Lung ultrasound in patients with acute respiratory failure reduces conventional imaging and health care provider exposure to COVID-19.Ultrasound Med Biol. 2020; 46: 2090-2093
- Feasibility of using point-of-care lung ultrasound for early triage of COVID-19 patients in the emergency room.Emerg Radiol. 2020; 10: 1-8
- Lung ultrasound in COVID-19 pneumonia: Correlations with chest CT on hospital admission.Respiration. 2020; 99: 617-624
- Lung ultrasound in the emergency department—A valuable tool in the management of patients presenting with respiratory symptoms during the SARS-CoV-2 pandemic.BMC Emerg Med. 2020; 20: 96
- Thoracic ultrasound and SARS-COVID-19: A pictorial essay.J Ultrasound. 2020; 23: 217-221
- Use of lung ultrasound to differentiate coronavirus disease 2019 (COVID-19) Pneumonia from community-acquired pneumonia.Ultrasound Med Biol. 2020; 46: 2651-2658
- Our Italian experience using lung ultrasound for identification, grading and serial follow-up of severity of lung involvement for management of patients with COVID-19.Echocardiography. 2020; 37: 625-627
- International evidence-based recommendations for point-of-care lung ultrasound.Intensive Care Med. 2012; 38: 577-591
- Clinical characteristics of 138 hospitalized patients with 2019 novel coronavirus-infected pneumonia in Wuhan, China.JAMA. 2020; 323: 1061-1069
- Point-of-care ultrasound induced changes in management of unselected patients in the emergency department—A prospective single-blinded observational trial.Scand J Trauma Resusc Emerg Med. 2020; 28: 47
World Health Organization (WHO). Coronavirus disease 2019 (COVID-19) Situation Report 51. 2020 March 11. Available at: https://www.who.int/emergencies/diseases/novel-coronavirus-2019/situation-reports. Accessed March 11, 2020.
- Risk factors associated with acute respiratory distress syndrome and death in patients with coronavirus disease 2019 pneumonia in Wuhan, China.JAMA Intern Med. 2020; 180: 934-943
- Saliva or Nasopharyngeal Swab Specimens for Detection of SARS-CoV-2.N Engl J Med. 2020; 383: 1283-1286
- Lung ultrasound findings in patients with COVID-19 pneumonia.Crit Care. 2020; 24: 174
- Lung ultrasonography in pregnant women during the COVID-19 pandemic: An interobserver agreement study among obstetricians.Ultrasonography. 2020; 39: 340-349
- Point-of-care lung ultrasound findings in patients with COVID-19 pneumonia.Am J Trop Med Hyg. 2020; 102: 1198-1202
- Lung ultrasound score in evaluating the severity of coronavirus disease 2019 (COVID-19) pneumonia.Ultrasound Med Biol. 2020; 46: 2938-2944
- Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: A retrospective cohort study.Lancet. 2020; 395: 1054-1062
- Comparative study of lung ultrasound and chest computed tomography scan in the assessment of severity of confirmed COVID-19 pneumonia.Intensive Care Med. 2020; 46: 1707-1713
- The appropriate use of testing for COVID-19.West J Emerg Med. 2020; 21: 470-472
Article info
Publication history
Footnotes
S.S. takes responsibility for the content of the article. All authors substantially contributed to the design of the work and the acquisition of data. M.D.S. analyzed the data, while S.S., G.G., and V.B. take responsibility for the integrity of the data and the accuracy of the data analysis. M.D.S., M.T.M. and S.S. drafted the article, and all authors revised it critically for important intellectual content, and questions related to the accuracy and integrity of any part of the work were investigated and resolved. All authors approved the final version of the article.