Prospective application of clinician-performed lung ultrasonography during the 2009 H1N1 influenza A pandemic: distinguishing viral from bacterial pneumonia

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 [4] 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.

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.

Enrolled patients had a screening history and physical examination performed at the time of triage to determine eligibility into the study. After informed consent was obtained, enrolled patients had clinical exam findings documented on a standardized form and underwent point-of-care lung ultrasound examination. An ultrasound machine with a linear array transducer at 7.5 to 10 MHz (Sonosite Micromaxx, Bothell, WA, USA) was used to image the lungs in perpendicular planes (transverse, parasagittal, and coronal) in the midclavicular line anteriorly and posteriorly on the chest and the midaxillary line from the axillae to diaphragm (Figure 4).

Using a six-zone lung ultrasound scanning protocol similar to that described by Copetti et al. [7], we defined and classified patients as positive or negative for viral pneumonia based on the presence of small subpleural consolidations usually <0.5 cm (Figure 5 and Additional file 1) and/or individual B-lines or confluent B-lines (echogenic vertical lines arising from the pleural line to the bottom of the ultrasound screen; Figure 6 and Additional file 2) [7]. These ultrasound findings are similar to those described in interstitial syndrome which is defined as three or more B-lines in a given lung region [10, 14, 15]. A-lines (horizontal, reverberation artifacts of the pleural line; Figure 7 left) which indicate areas of the normal lung were also noted when present [10, 14]. Patients were classified as positive or negative for bacterial pneumonia based on the presence or absence of lung consolidation with air bronchograms [6, 7, 16] seen on ultrasound (Figures 7 right, 8, and Additional file 3). A clinical course with follow-up after 2 weeks (via electronic medical record and telephone interview) was used to determine disposition and outcomes of enrolled patients. Clinicians performing and interpreting ultrasound were blinded to chest X-ray results, and when performed per hospital protocol for possible admission, viral antigen testing results. Bacterial pneumonia on chest X-ray (posterior-anterior and lateral views) was classified based on the attending pediatric radiologist reading for ‘consolidation, ‘infiltrate, or ‘pneumonia. For analysis purposes only, viral pneumonia on chest X-ray was defined as ‘peri-bronchial cuffing, ‘peri-bronchial thickening, or ‘increased interstitial markings identified by the pediatric radiologist. Pediatric radiologists were blinded to the lung ultrasound results.

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).

Patient demographic and study characteristics are presented in Table 1. Twenty pandemic 2009 H1N1 influenza patients requiring chest X-ray (CXR) were enrolled during this time period.

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) [25].

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 [1]. 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 [1].