Prospective application of clinician-performed lung ultrasonography during the 2009 H1N1 influenza A pandemic: distinguishing viral from bacterial pneumonia
© Tsung et al.; licensee Springer. 2012
Received: 6 May 2012
Accepted: 14 June 2012
Published: 10 July 2012
Emergency department visits quadrupled with the initial onset and surge during the 2009 H1N1 influenza pandemic in New York City from April to June 2009. This time period was unique in that >90% of the circulating virus was surveyed to be the novel 2009 H1N1 influenza A according to the New York City Department of Health. We describe our experience using lung ultrasound in a case series of patients with respiratory symptoms requiring chest X-ray during the initial onset and surge of the 2009 H1N1 influenza pandemic.
We describe a case series of patients from a prospective observational cohort study of lung ultrasound, enrolling patients requiring chest X-ray for suspected pneumonia that coincided with the onset and surge of the 2009 H1N1 influenza pandemic.
Twenty pandemic 2009 H1N1 influenza patients requiring chest X-ray were enrolled during this time period. Median age was 6.7 years. Lung ultrasound via modified Bedside Lung Ultrasound in Emergency protocol assisted in the identification of viral pneumonia (n = 15; 75%), viral pneumonia with superimposed bacterial pneumonia (n = 7; 35%), isolated bacterial pneumonia only (n = 1; 5%), and no findings of viral or bacterial pneumonia (n = 4; 20%) in this cohort of patients. Based on 54 observations, interobserver agreement for distinguishing viral from bacterial pneumonia using lung ultrasound was ĸ = 0.82 (0.63 to 0.99).
Lung ultrasound may be used to distinguish viral from bacterial pneumonia. Lung ultrasound may be useful during epidemics or pandemics of acute respiratory illnesses for rapid point-of-care triage and management of patients.
This fourfold increase in patient volume presented logistical challenges for emergency departments . In response to mass casualty incident-type conditions and overcrowding, emergency departments in New York City added staffing and created alternate sites of care to accommodate the increased patient volume. Increased demand for chest radiography for those patients with more severe disease led to increased delays and length of stay for those patients with suspected, but non-severe pneumonia.
Study design and setting
We describe a subcohort of patients who required chest X-ray for suspected pneumonia and were enrolled into a prospective study of lung ultrasound for diagnosing pneumonia that coincided with the onset and surge of the 2009 H1N1 influenza pandemic from April to June 2009 [1, 2, 13]. We also describe the application of a modified Bedside Lung Ultrasound in Emergency (BLUE) protocol  with posterior thorax scanning (Figure 3) during the onset and surge of pandemic patients in an urban emergency department.
This study was approved by our institutional review board. The study population consisted of a convenience sample of patients who met predetermined inclusion criteria and in whom informed consent had been obtained and documented from the patient or guardian for enrollment into the study.
Selection of participants
Inclusion criteria consisted of patients < 21 years of age presenting to the emergency department with clinical suspicion of pneumonia requiring chest X-ray for evaluationWe excluded those patients who presented the following: (1) arrival in the emergency department with a chest X-ray, (2) a confirmed diagnosis of pneumonia by diagnostic imaging, or (3) hemodynamic instability.
Methods of measurement and outcome measures
Additional file 1: Title: Small subpleural consolidation. Description: Small subpleural consolidation consistent with viral lung ultrasound pattern. (MOV )
Additional file 2: Title: Confluent B-lines. Description: Confluent B-lines consistent with viral lung ultrasound pattern. (MOV )
Additional file 3: Title: Rt anterior middle lobe lung consolidation with air bronchograms. Description:Rt anterior middle lobe lung consolidation with air bronchograms consistent with bacterial pneumonia lung ultrasound pattern. (MOV )
Ultrasound images and videos were reviewed between two blinded investigator sonologists (enrolling sonologist and reviewing sonologist) to determine interobserver agreement by unweighted Cohens Kappa for viral pneumonia (small subpleural consolidation and/or B-lines), normal lung ultrasound pattern (A-lines), and bacterial pneumonia (lung consolidation with sonographic air bronchograms).
Characteristics of study subjects
6.7 years (IQR, 3.6 to 10.7)
Median US exam time (IQR)
6 min (IQR, 4 to 8)
History of fever
History of cough
Median time to CXR from request prior to pandemic (N = 20)
29 min (IQR, 18 to 43)
Median time to CXR from request during pandemic surge (N = 20)
98 min (IQR, 79 to 125)
Findings ( N = 20)
US - n ; % [95% CI]
CXR - n ; % [95% CI]
15; 75 [53 to 89]
8; 40 [22 to 61]
Bacterial pneumonia only
1; 5 [0 to 25]
5; 25 [11 to 47]
Antibiotics and oseltamivir
Viral and bacterial pneumonia
7; 35 [18 to 59]
3; 15 [3 to 38]
Antibiotics and oseltamivir
4; 20 [7 to 42]
7; 35 [18 to 59]
Discharge and observation
Cohen’s Kappa for distinguishing viral from bacterial pneumonia on lung ultrasound between two blinded sonologists
Cohen’s Kappa = 0.82
95% CI (0.63 to 0.99)
Additional file 4: Title: Confluent B-lines and lung consolidation with air bronchograms. Description: Viral and bacterial pneumonia lung ultrasound patterns. (MOV )
All patients in our series were recovering or recovered from their influenza illness on follow-up after 2 weeks. All admitted patients were subsequently confirmed with the 2009 H1N1 influenza A by the New York City Department of Health. Per hospital protocol for possible hospital admission, four of nine patients tested positive for influenza A by viral antigen testing, despite the New York City Department of Health reporting >90% of the circulating virus during this pandemic time period was the novel influenza A H1N1 . One infant in the cohort was co-infected with respiratory syncytial virus based on viral antigen testing. Three patients, all <5 years of age requiring hospital admission had evidence of both bacterial and viral pneumonia on ultrasound. The only patient requiring ICU admission, a 20-year-old female, was intubated after deteriorating during her ED stay with persistent hypotension and septic shock from a left lower lobe bacterial pneumonia. This patient initially presented with an influenza-like illness and acute abdominal pain.
To our knowledge, this is the first prospective series describing the use of lung ultrasound in children as a potential real-time diagnostic triage tool during a mass casualty-type incident due to an acute respiratory illness pandemic surge [17, 18]. Testa et al. have reported on similar lung ultrasound findings in adults during the 2009 H1N1 influenza A pandemic . Single case reports of clinician-performed lung ultrasound to monitor the progression of H1N1 influenza-associated ARDS  and point-of-care echocardiography to diagnose H1N1 influenza myocarditis  have been described. Retrospective reports of the role of ultrasound in mass casualty incidents during disasters such as earthquakes have also been described [21, 22]. Lichtenstein et al. described an algorithm using lung ultrasonography to distinguish between various respiratory pathologies of the lung . We modified Lichtenstein’s BLUE protocol  to recognize basic lung ultrasound patterns to distinguish between the normal unaffected lung, viral pneumonia pattern, and bacterial pneumonia (Figure 3). Scanning the posterior thorax was added to increase the sensitivity of the protocol . Point-of-care lung ultrasound was able to identify, in real-time, four groups of pandemic patients: viral pneumonia only (subpleural consolidations and/or B-lines or confluent B-lines), bacterial pneumonia only (lung consolidation with sonographic air bronchograms), both viral and bacterial pneumonia (Figure 7), and normal lungs (A-lines only). Our calculated Kappa was 0.82, which means that the interobserver agreement in distinguishing between these ultrasound findings was excellent.
These ultrasound findings facilitated triage and immediate decision making regarding the need for respiratory isolation in a negative pressure room without waiting for chest X-ray. Our median time to chest X-ray tripled (Table 1) during the pandemic compared to a time period prior to the pandemic. Our time to chest X-ray interpretation during the pandemic was longer than the median of 98 min reported by Zanobetti et al. in the study of emergency department lung ultrasound in non-pandemic conditions .
When lung consolidation with sonographic air bronchograms was visualized, point-of-care ultrasound facilitated the immediate decision to treat with antibiotics, without waiting for chest X-ray. Visualization of viral pneumonia on ultrasound may be useful to assist in the decision to initiate immediate empiric treatment with antiviral medication for future pandemic or epidemic influenza patients. In a large cohort of hospitalized H1N1 influenza A pandemic patients, only 73% of patients with radiographic evidence of pneumonia received antiviral drugs, whereas 97% received antibiotics . Better recognition of viral pneumonia by ultrasound may impact outcomes, as available data have shown treatment with antiviral medication reduces mortality in hospitalized patients with influenza, even when therapy is initiated after 48 h of illness onset .
Our sample size was limited by the inability to enroll during the surge of pandemic patients due to time and resource constraints. Selection bias from convenience sampling may have occurred because patients were more likely to have been enrolled at less busier or better staffed times. In general, the patients in this series had illnesses severe enough to warrant investigation with chest X-ray. Thus, information about less ill or asymptomatic pandemic patients is lacking.
Although our calculated interobserver agreement for lung ultrasound to distinguish between viral and bacterial pneumonia is high, the number of total observations was limited, and this is reflected in our wide 95% confidence intervals. However, it is notable that our point estimate Kappa for ultrasound is higher than the reported interobserver agreement for chest X-ray for pneumonia by pediatric radiologists, 0.51 (0.39 to 0.64) .
Due to the large numbers of patients presenting to our emergency department during the pandemic, only hospitalized patients (four patients in our series) were confirmed with 2009 H1N1 influenza A . Finding small subpleural consolidations and/or B-lines on ultrasound allows the recognition of viral pneumonia from bacterial pneumonia (lung consolidation with sonographic air bronchograms), but it is unknown if different viruses have unique lung ultrasound patterns (e.g., influenza A from RSV). We could not report test performance characteristics, such as sensitivity and specificity, as there was no practical reference gold standard for viral pneumonia at the time our study was conducted. Additionally, chest X-ray cannot be used as a gold standard for viral pneumonia. However, according to the New York City Department of Health, >90% of the circulating virus during this pandemic time period was the novel influenza A H1N1 .
Lung ultrasound may be used to distinguish viral from bacterial pneumonia with high interobserver agreement. Lung ultrasonography may be useful during epidemics or pandemics of acute respiratory illnesses for rapid point-of-care triage and management of patients.
JWT and VPS participated in the design of the study, coordinated the study, and performed the statistical analysis. JWT, DOK, and VPS participated in the patient enrollment and data collection and drafting of the manuscript. All authors read and approved the final manuscript.
- New York City Department of Health and Mental Hygiene: Community transmission of H1N1 flu appears to decline in New York City. 2009. Accessed 12 June 2010 http://www.nyc.gov/html/doh/html/pr2009/pr042–09.shtml Google Scholar
- Lessler J, Reich NG, Cummings DA, New York City Department of Health and Mental Hygiene Swine Influenza Investigation Team: Outbreak of 2009 pandemic influenza A (H1N1) at a New York City school. N Engl J Med 2009,361(27):2628–2636. 10.1056/NEJMoa0906089PubMedView ArticleGoogle Scholar
- Call SA, Vollenweider MA, Hornung CA, Simel DL, McKinney WP: Does this patient have influenza? JAMA 2005,293(8):987–997. 10.1001/jama.293.8.987PubMedView ArticleGoogle Scholar
- Lichtenstein DA, Meziere GA: Relevance of lung ultrasound in the diagnosis of acute respiratory failure: the BLUE protocol. Chest 2008,134(1):117–125. 10.1378/chest.07-2800PubMed CentralPubMedView ArticleGoogle Scholar
- Zanobetti M, Poggioni C, Pini R: Can chest ultrasonography replace standard chest radiography for evaluation of acute dyspnea in the ED? Chest 2011,139(5):1140–1147. 10.1378/chest.10-0435PubMedView ArticleGoogle Scholar
- Lichtenstein DA, Lascols N, Mezière G, Gepner A: Ultrasound diagnosis of alveolar consolidation in the critically ill. Intensive Care Med 2004,30(2):276–281. 10.1007/s00134-003-2075-6PubMedView ArticleGoogle Scholar
- Copetti R, Catarossi L: Ultrasound diagnosis of pneumonia in children. Radiol Med 2008,113(2):190–198. 10.1007/s11547-008-0247-8PubMedView ArticleGoogle Scholar
- Parlamento S, Copetti R, Di Bartolomeo S: Evaluation of lung ultrasound for the diagnosis of pneumonia in the ED. Am J Emerg Med 2009,27(4):379–384. 10.1016/j.ajem.2008.03.009PubMedView ArticleGoogle Scholar
- Volpicelli G, Frascisco M: Sonographic detection of radio-occult interstitial lung involvement in measles pneumonia. Am J Emerg Med 2009,27(1):e1-e3. 128PubMedView ArticleGoogle Scholar
- Lichtenstein D, Goldstein I, Mourgeon E, Cluzel P, Grenier P, Rouby JJ: Comparative diagnostic performances of auscultation, chest radiography, and lung ultrasonography in acute respiratory distress syndrome. Anesthesiology 2004,100(1):9–15. 10.1097/00000542-200401000-00006PubMedView ArticleGoogle Scholar
- 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(4):577–591. 10.1007/s00134-012-2513-4PubMedView ArticleGoogle Scholar
- Testa A, Soldati G, Copetti R, Giannuzzi R, Portale G, Gentiloni-Silveri N: Early recognition of the 2009 pandemic influenza A (H1N1) pneumonia by chest ultrasound. Crit Care 2012,16(1):R30. 10.1186/cc11201PubMed CentralPubMedView ArticleGoogle Scholar
- Shah VP, Tunik MG, Tsung JW: The feasibility of diagnosing pneumonia in children with point-of-care ultrasound. Pediatric Emerg Care 2009,25(10):711–712.Google Scholar
- Lichtenstein D, Meziere 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(5):1640–1646.PubMedView ArticleGoogle Scholar
- Lichtenstein DA: Ultrasound in the management of thoracic disease. Crit Care Med 2007,35(5 Suppl):S250-S261.PubMedView ArticleGoogle Scholar
- Weinberg B, Diakoumakis EE, Kass EG, Seife B, Zvi ZB: The air bronchogram: sonographic demonstration. AJR Am J Roentgenol 1986,147(3):593–595.PubMedView ArticleGoogle Scholar
- Peiris JS, Yuen KY, Osterhaus AD, Stöhr K: The severe acute respiratory distress syndrome. N Engl J Med 2003,349(25):2431–2441. 10.1056/NEJMra032498PubMedView ArticleGoogle Scholar
- Jain S, Kamimoto L, Bramley AM, Schmitz AM, Benoit SR, Louie J, Sugerman DE, Druckenmiller JK, Ritger KA, Chugh R, Jasuja S, Deutscher M, Chen S, Walker JD, Duchin JS, Lett S, Soliva S, Wells EV, Swerdlow D, Uyeki TM, Fiore AE, Olsen SJ, Fry AM, Bridges CB, Finelli L: Pandemic Influenza A (H1N1) Virus Hospitalizations Investigation Team (2009) Hospitalized patients with 2009 H1N1 Influenza in the United States, April-June 2009. N Engl J Med 2009, 361: 1935–1944. 10.1056/NEJMoa0906695PubMedView ArticleGoogle Scholar
- Peris A, Zagli G, Barbani F, Tutino L, Biondi S, di Valvasone S, Batacchi S, Bonizzoli M, Spina R, Miniati M, Pappagallo S, Giovannini V, Gensini GF: The value of lung ultrasound monitoring in H1N1 acute respiratory distress syndrome. Anaesthesia 2010,65(3):294–297. 10.1111/j.1365-2044.2009.06210.xPubMedView ArticleGoogle Scholar
- Bramante RM, Cirilli A, Raio CC: Point-of-care sonography in the emergency department diagnosis of acute H1N1 Influenza myocarditis. J Ultrasound Med 2010,29(9):1361–1364.PubMedGoogle Scholar
- Dan D, Mingsong L, Jie T, Xiaobo W, Zhong C, Yan L, Xiaojin L, Ming C: Ultrasonographic applications after mass casualty incident cause by Wenchuan earthquake. J Trauma 2010,68(6):1417–1420. 10.1097/TA.0b013e3181c9b301PubMedView ArticleGoogle Scholar
- Sarkisian AE, Khondarian RA, Amirbekian NM, Bagdasarian NB, Khojayan RL, Oganesian YT: Sonographic screening of mass casualties for abdominal and renal injuries following the 1988 Armenian earthquake. J Trauma 1991,31(2):247–250.PubMedView ArticleGoogle Scholar
- Volpicelli G, Noble VE, Liteplo A, Cardinale L: Decreased sensitivity of lung ultrasound limited to the anterior chest in emergency department diagnosis of cardiogenic pulmonary edema: a retrospective analysis. Crit Ultrasound J 2010,2(2):47–52. 10.1007/s13089-010-0037-0View ArticleGoogle Scholar
- McGeer A, Green KA, Plevneshi A, Shigayeva A, Siddiqi N, Raboud J, Low DE, Toronto Invasive Bacterial Diseases Network: Antiviral therapy and outcomes of influenza requiring hospitalization in Ontario, Canada. Clin Infect Dis 2007,45(12):1568–1575. 10.1086/523584PubMedView ArticleGoogle Scholar
- Johnson J, Kline JA: Intraobserver and interobserver agreement of the interpretation of pediatric chest radiographs. Emerg Radiol 2010,17(4):285–290. 10.1007/s10140-009-0854-2PubMedView ArticleGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.