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Objectives: The study goal was to concurrently evaluate agree- versus 62% (p < 0.001), respectively. Relaxing the agreement def-
ment of a 9-point pulmonary ultrasound protocol and portable inition to a matching CT finding being present anywhere within the
chest radiograph with chest CT for localization of pathology to the correct lung (“lung-specific” agreement), not necessarily the spe-
correct lung and also to specific anatomic lobes among a diverse cific mapped lobe, showed improved agreement for both pulmo-
group of intubated patients with acute respiratory failure. nary ultrasound and portable chest radiograph respectively (right
Design: Prospective cohort study. lung: 92.5% vs 65.7%; p < 0.001 and left lung: 83.6% vs 71.6%;
Setting: Medical, surgical, and neurologic ICUs at a 670-bed p = 0.097). The highest lobe-specific agreement was for the find-
urban teaching hospital. ing of atelectasis/consolidation for both pulmonary ultrasound
Patients: Intubated adults with acute respiratory failure having and portable chest radiograph (96% and 73%, respectively). The
chest CT and portable chest radiograph performed within 24 lowest lobe-specific agreement for pulmonary ultrasound was
hours of intubation. normal lung (79%) and interstitial process for portable chest ra-
Interventions: A 9-point pulmonary ultrasound examination per- diograph (29%). Lobe-specific agreement differed most between
formed at the time of intubation. pulmonary ultrasound and portable chest radiograph for interstitial
Measurements and Main Results: Sixty-seven patients had pul- findings (86% vs 29%, respectively). Pulmonary ultrasound had
monary ultrasound, portable chest radiograph, and chest CT the lowest agreement with CT for findings in the left lower lobe
performed within 24 hours of intubation. Overall agreement of (82.1%). Pleural effusion agreement also differed between pul-
pulmonary ultrasound and portable chest radiograph findings monary ultrasound and portable chest radiograph (right: 99% vs
with correlating lobe (“lobe-specific” agreement) on CT was 87% 87%; p = 0.009 and left: 99% vs 85%; p = 0.004).
Conclusions: A clinical, 9-point pulmonary ultrasound protocol
1
Department of Graduate Medical Education, Abbott Northwestern Hos- strongly agreed with specific CT findings when analyzed by both
pital, Minneapolis, MN. lung- and lobe-specific location among a diverse population of
2
Department of Critical Care, Abbott Northwestern Hospital, Minneapolis, MN. mechanically ventilated patients with acute respiratory failure; in
3
Consulting Radiologists, Ltd., Minneapolis, MN. this regard, pulmonary ultrasound significantly outperformed port-
4
Department of Care Delivery Research, Allina Health, Minneapolis, MN. able chest radiograph. (Crit Care Med 2019; XX:00–00)
5
University of Minnesota Medical School, Minneapolis, MN. Key Words: critical care; lung; point-of-care; radiography;
Supplemental digital content is available for this article. Direct URL cita- respiratory insufficiency; ultrasonography
tions appear in the printed text and are provided in the HTML and PDF
versions of this article on the journal’s website (http://journals.lww.com/
ccmjournal).
Dr. Tierney received funding from personally purchased stock options and
A
disclosed he is a member of Medical Advisory Boards for Echonous and cute respiratory failure (ARF) requiring mechanical
Bay Labs. The remaining authors have disclosed that they do not have any ventilatory support is the most common reason for
potential conflicts of interest.
ICU admission and has high mortality (1, 2). Initial
This work was performed at Abbott Northwestern Hospital, Minneap-
olis, MN. misdiagnosis of ARF etiology is common and increases mor-
For information regarding this article, E-mail: david.tierney@allina.com tality (3). With the broad differential of diseases causing ARF,
Copyright © 2019 by the Society of Critical Care Medicine and Wolters efficiency of diagnosis is not only related to accuracy of the
Kluwer Health, Inc. All Rights Reserved. chest imaging modality, but also its ability to anatomically lo-
DOI: 10.1097/CCM.0000000000004124 calize a process and monitor for change with treatment.
Portable chest radiograph (pCXR) lacks the sensitivity and this study were a subset from a larger (n = 250), previously
specificity of CT (4–6), yet may be favored in some settings due published study evaluating a protocolized 9-location PU ex-
to speed, lower cost and radiation, and risk associated with ICU amination in patients with ARF requiring mechanical venti-
patient transport especially with technologically complex support lation (20). Patients were included in the current study if, in
modes such as extracorporeal membrane oxygenation (ECMO) addition to their PU at the time of intubation, they underwent
(7, 8). Pulmonary ultrasound (PU) has demonstrated the ben- pCXR and chest CT within 24 hours of the PU. The protocol
efits of pCXR’s portability, speed, and lower cost while approach- was approved by the institutional review board (Schulman
ing accuracy of chest CT for pneumonia, interstitial processes, Associates IRB, number 4080-2E).
acute respiratory distress syndrome (ARDS), pleural effusion, and
pneumothorax (9–15). The Society of Critical Care Medicine and Imaging and Classification
international guidelines support incorporation of point-of-care Details of the full PU examination protocol have been described
ultrasound (POCUS) in diagnosis of these conditions (16, 17). In previously (20). Presence of normal lung, quantified B-line cat-
addition to its initial diagnostic ability, POCUS offers clinicians a egory (B1–B3), atelectasis/consolidation, and pleural effusion
radiation-free tool to repeatedly reassess for progression or regres- was registered in nine anatomically chosen (to approximate
sion of pulmonary findings in real-time at the bedside which can lobar anatomy) and clinically applicable PU zones (Fig. 1).
further aid in tailoring treatment and differential diagnosis. The surface area examined within each zone was limited to
The majority of research reporting diagnostic accuracy of 7.5 × 5 cm (the size of our hospital ID badge). A comparison of
PU has defined agreement as compatible ultrasound findings this 9-point examination protocol to other frequently used PU
anywhere within the correct lung as identified by CT. However, protocols (11, 21, 22) can be found in Supplemental Content
two small studies (n = 32 and 20) conducted in patients with 1 (http://links.lww.com/CCM/F166).
ARDS have demonstrated a refined ability of PU to accurately All PU examinations were performed by one of four study
localize findings beyond the correct lung to distinct lung zones physicians with 3+ years of PU experience who participated
on CT defined not by anatomic lung lobe (i.e., right lower lobe, in a 1-hour pre-study teaching session to ensure uniformity
right middle lobe), but by zones corresponding to contempo- of PU classification. They independently scored archived
rary protocolized ultrasound examination regions (18, 19). video clips representing the spectrum of classifications from
The goal of this study was to concurrently evaluate the ac- 64 patients, and inter-rater agreement for pulmonary classifi-
curacy of both PU and pCXR with CT not only for agreement cation was calculated. All examinations were performed with
of findings within the ipsilateral lung or a correlating CT zone, SonoSite EDGE portable ultrasound systems and a P21 (1–5
but within the specific anatomic lobe using a previously pub- MHz) phased-array transducer (FUJIFILM SonoSite, Bothell,
lished, quick, pragmatic, 9-zone PU protocol (20) among di- WA) (see additional methods, Pulmonary Ultrasound Exam
verse medical/surgical, cardiac, and neurologic ICU patient Detail, Supplemental Content 2, http://links.lww.com/CCM/
populations with a wide array of ARF diagnoses. F167).
Ultrasound zones were classified as normal when the region
contained A-lines and lung sliding in the absence of B-lines or
MATERIALS AND METHODS
consolidation/atelectasis. Presence of B-lines was subclassified by
Setting and Study Design B1, B2, or B3 based on quantity (B1 = 1–3 discrete B-lines present
This prospective cohort study took place in a 670-bed, 62 ICU per intercostal space; B3 = confluent B-lines occupying > 50%
bed, quaternary care, teaching hospital. Patients included in of an intercostal space; or B2 = quantity of B-lines between B1
Figure 1. Ultrasound and chest radiograph zone location. AAx = anterior axillary line, LL = left lower, LU = left upper, MC = mid-clavicular line, PAx =
posterior axillary line, RL = right lower, RU = right upper.
Copyright © 2019 by the Society of Critical Care Medicine and Wolters Kluwer Health, Inc. All Rights Reserved.
Clinical Investigation
and B3). An isolated B1 area in the postero-caudal tip of the lung in the ipsilateral lung on CT (not restricted to the specific
was classified as normal. Areas of nonaerated lung greater than anatomic lobe mapping in Table 1) (see additional methods,
3 cm in its axis perpendicular to pleura with dynamic air bron- Pulmonary Ultrasound Agreement Details and Rationale,
chograms and lack of compressive reason for aeration loss (e.g., Supplemental Content 2, http://links.lww.com/CCM/F167).
pleural effusion, elevated diaphragm) were classified as non- Final clinical diagnoses for ARF were adjudicated by two
atelectatic consolidation. Zones with small, focal, less than 3 cm study physicians blinded to, and not having performed, the PU
areas, of peripheral consolidation were subclassified as “small” examination (see additional methods, Final Clinical Diagnosis
consolidations. Areas of nonaerated lung greater than 3 cm in Assignment, Supplemental Content 2, http://links.lww.com/
its axis perpendicular to pleura with distinct features suggest- CCM/F167). They then reviewed the PU examination collec-
ing volume loss atelectasis such as presence of a pleural effusion tively and determined whether it was consistent with the clin-
size consistent with volume of nonaerated lung, lack of dynamic ical diagnosis.
air bronchograms, typical atelectatic distribution in the inferior
or lateral tip of lung with a smooth re-aeration interface, were Data Analysis
classified as atelectasis. A combined classification of atelectasis/ Descriptive statistics were used to describe study sample charac-
consolidation was assigned when the area examined consisted of teristics. With CT findings considered gold standard, the propor-
tissue-like density and the physician was unable to see discrim- tion of patients with agreement between PU and CT, and pCXR
inating features indicative of either specific entity. Pleural effu- and CT was compared using two-sample tests of proportions.
sion was classified as fluid in the pleural space whether simple or Level of agreement was examined for both the combination
complicated with a minimum visceral-parietal pleural dimen- of correct finding in the correct lobar correlate (lobe-specific
sion greater than or equal to 0.5 cm at any location. Individual agreement) and for the correct finding anywhere in the ipsilat-
classifications were also grouped into the categories of paren- eral lung (lung-specific agreement). The sensitivity of PU and
chymal abnormality (normal, interstitial, ground glass, atelec- pCXR to detect CT findings was evaluated overall, by body mass
tasis/consolidation) or pleural effusion for subanalyses. index (BMI), and duration of time between CT and PU/pCXR
A single, expert chest radiologist without PU training, (dichotomized at sample medians) using z tests for difference in
blinded to PU results and clinical information, reviewed all proportions. Fleiss’s kappa coefficient was used to assess inter-
pCXR and chest CT studies to classify each anatomical zone rater agreement in the pre-study training set. A sample size of 67
(pCXR) and lobe (CT) as normal, interstitial, ground glass (CT patients achieved 83% power to detect an overall difference of
only), atelectasis, consolidation, or pleural effusion. CXR zones
22% between the agreement of ultrasound and pCXR, using the
were defined as shown in Figure 1. CT regions were defined by
two-sided z test with pooled variance. Statistical analyses were
anatomical lobe.
conducted at 5% significance level. Analyses were conducted
Agreement for lung findings and zones/lobes across modal-
using Stata 14.1 (StataCorp, LP, College Station, TX).
ities are presented in Table 1. “Lobe-specific” agreement was
defined as identification of an agreeing PU/pCXR finding in an
agreeing PU/pCXR zone with the CT finding and specific ana- RESULTS
tomic lobe. “Lung-specific” agreement was defined as identifi- From the broader 250 patient cohort (20), 67 patients (Table 2)
cation of a PU/pCXR finding to an agreeing finding anywhere met inclusion criteria. The most common ARF diagnosis was
Clinical diagnosis, n (%) Left upper lobe 91.0 59.7 < 0.001
Congestive heart failure 5 (8) Ground glass 89.9 72.5 < 0.001
Chronic obstructive pulmonary disease 4 (6) Atelectasis/ 95.6 72.5 < 0.001
exacerbation consolidation
Acute lung injury/acute respiratory 4 (6) Effusion 100.0 74.5 < 0.001
distress syndrome Overall 88.9 66.3 < 0.001
Acute myocardial infarction 3 (5) Lung-specific agreement by category
Neuromuscular weakness 2 (3) Right lung parenchymalc 92.5 65.7 < 0.001
Pulmonary embolism 1 (2) Right pleural effusion 98.5 86.6 0.009
Pneumothorax 1 (2) Left lung parenchymalc 83.6 71.6 0.097
Cryptogenic organizing pneumonia 1 (2) Left pleural effusion 98.5 85.1 0.005
Allergic bronchopulmonary 1 (2) Two-sample proportion z test.
a
aspergillosis b
Agreement for the right lower zone on single-view portable chest radiograph
was with findings in either the right lower or middle lobe on CT.
Left ventricular systolic function, n (%) Normal, interstitial, ground glass, atelectasis/consolidation classifications
c
Copyright © 2019 by the Society of Critical Care Medicine and Wolters Kluwer Health, Inc. All Rights Reserved.
Clinical Investigation
Figure 2. Discrepant case images. A and B, Case 1 chest CT; arrows = pleural-based nodules. C, Case 2 chest CT; arrows = bullae. D, Case 3 chest
CT; arrow = right upper lobe mass. E, Case 3 portable chest radiograph without visible right upper lobe mass. F, Case 4 chest CT; arrow = posterior left
lower lobe consolidation missed by ultrasound; *stomach. L = left, R = right. See high resolution image versions of the figures (Supplemental Content
3, http://links.lww.com/CCM/F168).
to a lobe with presumed airway obstruction for suctioning or than with normal lung using this 9-point protocol among this
to a lobar parenchymal consolidation for culture. Evaluation patient population.
of lobe-specific agreement also allows for examination of dif- Our study has limitations, some inherent to clinical POCUS
ferences in PU agreement within specific lobes such as the LLL workflow. First, study physicians did not discuss patients with
which can be difficult to visualize due to recumbent patient caregivers prior to or during the examination. However, clin-
positioning and positioning of the heart in the left hemithorax. ical clues in the room, such as antibiotic or diuretic infusions,
Lower agreement of PU in the LLL (82.1%) reveals a poten- may have influenced zone interpretation. Second, the inclu-
tial pitfall of PU in mechanically ventilated patients that would sion requirement of CT and pCXR within 24 hours of PU ex-
likely improve with examination of posterior zones. Basal re- amination may have introduced a bias for more severe illness
gions, especially the left retrocardiac region can also be difficult in this subgroup. Although not detracting from the findings,
to evaluate with pCXR and is a potential shortcoming of both this may impact generalizability. However, comparison of the
modalities (24). original 250 patient cohort (20) and the 67 patient subgroup
The PU lobe-specific agreement in our study (87%) is sim- showed strong similarities in clinical markers (mortality: 24%
ilar to that reported by Lichtenstein et al (19) where overall vs 28%, median ventilator days: 4.1 vs 4.1, mean P/F ratio: 223
concordance of PU with CT regions (not anatomic lobes) vs 234, respectively) and diagnoses (pneumonia: 30% vs 30%,
among a cohort of 32 ARDS patients was 83%. Both studies aspiration: 14% vs 15%, sepsis: 12% vs 9%, CHF 11% vs 8%,
report very good inter-rater agreement across categories and ARDS and chronic obstructive pulmonary disease/asthma: 7%
show significantly greater accuracy of PU compared with CXR. vs 6%, respectively), thus supporting greater generalizability
The main differences between our study and the study by of our subgroup results. Third, to preserve PU protocol effi-
Lichtenstein et al (19) include as follows: 1) size of study (67 vs ciency, each zone’s examination area was restricted to the size
32 patients, respectively), 2) a wide spectrum of ARF diagnoses of our hospital ID badge potentially resulting in a lower sen-
versus ARDS alone, 3) a 9-point examination protocol limited sitivity for processes just outside the scanned area. In clinical
to a 7.5 × 5 cm area at each point versus a 12 zone examina- use when suspicion is high and a limited PU examination is
tion with full exploration of each zone, and 4) PU examina- normal, a more detailed examination would occur and likely
tion point agreement with CT anatomic lobes versus CT zones improve sensitivity. Fourth, duration of time between imaging
chosen to approximate the PU examination areas. modalities may have positively or negatively impacted agree-
PU had better agreement with CT than pCXR across a va- ment, but we did not observe any meaningful impact on agree-
riety of findings but outperformed pCXR most strongly for in- ment with increasing elapsed time. This may be in part due
terstitial process identification (Table 3). The lower agreement to the severity of illness and predominance of slowly resolving
of PU for the normal CT classification (78.8%) may in fact re- radiographic processes (pneumonia and aspiration) compris-
flect superior sensitivity of PU compared with CT for subtle ing 45% of diagnoses. We conjecture that in healthier patients
interstitial processes seen as 1–3 B-lines in an interspace. One with more rapidly changing ARF etiologies, time between im-
might argue 1–3 B-lines (B1 classification) is a normal find- aging studies may have greater impact on agreement. Finally,
ing, especially in dependent lung locations. However, in our examination of whether PU examination summaries matched
protocol, the B1 classification was assigned to agree with the adjudicated clinical diagnoses had the potential for significant
“interstitial” rather than “normal” (except when isolated to the bias. Therefore, these data are included only to illustrate po-
postero-caudal tip of the lung). Our decision to map the B1 tential pitfalls of the PU examination, and to use available, cor-
PU classification in this manner reflects the clinical experience related CT data to better understand the limitations of our PU
that occasional B-lines in a nondependent location often rep- protocol in certain scenarios.
resents pulmonary pathology but when isolated to the postero-
caudal lung tip are often insignificant. Prior studies evaluating CONCLUSIONS
a greater surface area of the chest have used similar approaches The results of this study, conducted within a clinical ICU
to grouping B-line quantity but have categorized 1–2 B-lines workflow and in a population with diverse ARF diagnoses and
or an “isolated B-line” as “normal” (25, 26). A comparatively severity, demonstrate strong support for the role of PU in not
smaller chest surface area was examined in our study, increas- only pulmonary pathology identification but also its lobar lo-
ing the chance that 1–3 B-lines in the examined area represent calization; in this regard, PU significantly outperformed pCXR.
the penumbra of a more significant process and was a factor in The study also illustrates potential scenarios where PU has
our decision to not map the B1 classification to normal lung on limitations as compared with CT. In the hands of well-trained
CT. Due to the divergence from previous classification schemes, providers with an appreciation for its limitations, PU can be an
a sensitivity analysis was performed evaluating agreement if invaluable, cost-saving, risk-reducing imaging modality as an
all B1 zones were reclassified as normal and showed a 5–10% adjunct or replacement for pCXR and CT in patients with ARF.
reduction in lobe-specific and overall agreement between PU
and CT (Supplemental Table 1, Supplemental Digital Content
4, http://links.lww.com/CCM/F169). This supports that the B1 REFERENCES
1. Barrett ML, Smith MW, Elixhauser A et al: Utilization of Intensive Care
classification (except when isolated to the postero-caudal tip Services, 2011: Statistical Brief #185. Rockville, MD, Healthcare
of the lung) correlates better with an interstitial process on CT Cost and Utilization Project, 2014
Copyright © 2019 by the Society of Critical Care Medicine and Wolters Kluwer Health, Inc. All Rights Reserved.
Clinical Investigation
2. Stefan MS, Shieh MS, Pekow PS, et al: Epidemiology and outcomes 15. Copetti R, Soldati G, Copetti P: Chest sonography: A useful tool to
of acute respiratory failure in the United States, 2001 to 2009: A na- differentiate acute cardiogenic pulmonary edema from acute respira-
tional survey. J Hosp Med 2013; 8:76–82 tory distress syndrome. Cardiovasc Ultrasound 2008; 6:16
3. Ray P, Birolleau S, Lefort Y, et al: Acute respiratory failure in the eld- 16. Frankel HL, Kirkpatrick AW, Elbarbary M, et al: Guidelines for the ap-
erly: Etiology, emergency diagnosis and prognosis. Crit Care 2006; propriate use of bedside general and cardiac ultrasonography in the
10:R82 evaluation of critically ill patients-part I: General ultrasonography. Crit
4. Self WH, Courtney DM, McNaughton CD, et al: High discordance Care Med 2015; 43:2479–2502
of chest x-ray and computed tomography for detection of pulmonary 17. Volpicelli G, Elbarbary M, Blaivas M, et al; International Liaison
opacities in ED patients: Implications for diagnosing pneumonia. Am Committee on Lung Ultrasound (ILC-LUS) for International Con-
J Emerg Med 2013; 31:401–405 sensus Conference on Lung Ultrasound (ICC-LUS): International
5. Syrjälä H, Broas M, Suramo I, et al: High-resolution computed tomog- evidence-based recommendations for point-of-care lung ultrasound.
raphy for the diagnosis of community-acquired pneumonia. Clin Infect Intensive Care Med 2012; 38:577–591
Dis 1998; 27:358–363 18. Chiumello D, Mongodi S, Algieri I, et al: Assessment of lung aeration
6. Claessens YE, Debray MP, Tubach F, et al: Early chest computed to- and recruitment by CT scan and ultrasound in acute respiratory dis-
mography scan to assist diagnosis and guide treatment decision for tress syndrome patients. Crit Care Med 2018; 46:1761–1768
suspected community-acquired pneumonia. Am J Respir Crit Care 19. Lichtenstein D, Goldstein I, Mourgeon E, et al: Comparative diag-
Med 2015; 192:974–982 nostic performances of auscultation, chest radiography, and lung
7. Brenner DJ, Hall EJ: Computed tomography–an increasing source of ultrasonography in acute respiratory distress syndrome. Anesthesi-
radiation exposure. N Engl J Med 2007; 357:2277–2284 ology 2004; 100:9–15
8. Beckmann U, Gillies DM, Berenholtz SM, et al: Incidents relating to 20. Tierney DM, Boland LL, Overgaard JD, et al: Pulmonary ultrasound
the intra-hospital transfer of critically ill patients. An analysis of the scoring system for intubated critically ill patients and its association
reports submitted to the Australian Incident Monitoring Study in Inten- with clinical metrics and mortality: A prospective cohort study. J Clin
sive Care. Intensive Care Med 2004; 30:1579–1585 Ultrasound 2018; 46:14–22
9. Hew M, Corcoran JP, Harriss EK, et al: The diagnostic accuracy of 21. Volpicelli G, Mussa A, Garofalo G, et al: Bedside lung ultrasound in
chest ultrasound for CT-detected radiographic consolidation in hospi- the assessment of alveolar-interstitial syndrome. Am J Emerg Med
talised adults with acute respiratory failure: A systematic review. BMJ 2006; 24:689–696
Open 2015; 5:e007838 22. Baldi G, Gargani L, Abramo A, et al: Lung water assessment by lung
10. Llamas-Álvarez AM, Tenza-Lozano EM, Latour-Pérez J: Accuracy of ultrasonography in intensive care: A pilot study. Intensive Care Med
lung ultrasonography in the diagnosis of pneumonia in adults: Sys- 2013; 39:74–84
tematic review and meta-analysis. Chest 2017; 151:374–382 23. Kim M, Lee KY, Lee KW, et al: MDCT evaluation of foreign bodies and
11. Lichtenstein DA, Mezière GA: Relevance of lung ultrasound in the di- liquid aspiration pneumonia in adults. AJR Am J Roentgenol 2008;
agnosis of acute respiratory failure: The BLUE protocol. Chest 2008; 190:907–915
134:117–125 24. Beydon L, Saada M, Liu N, et al: Can portable chest x-ray examination
12. Lichtenstein D, Mezière G, Biderman P, et al: The “lung point”: An accurately diagnose lung consolidation after major abdominal sur-
ultrasound sign specific to pneumothorax. Intensive Care Med 2000; gery? A comparison with computed tomography scan. Chest 1992;
26:1434–1440 102:1697–1703
13. Volpicelli G, Boero E, Sverzellati N, et al: Semi-quantification of pneu- 25. Mongodi S, Bouhemad B, Orlando A, et al: Modified lung ultrasound
mothorax volume by lung ultrasound. Intensive Care Med 2014; score for assessing and monitoring pulmonary aeration. Ultraschall
40:1460–1467 Med 2017; 38:530–537
14. Lichtenstein D, Mezière G: A lung ultrasound sign allowing bedside 26. Bouhemad B, Liu ZH, Arbelot C, et al: Ultrasound assessment of anti-
distinction between pulmonary edema and COPD: The comet-tail ar- biotic-induced pulmonary reaeration in ventilator-associated pneu-
tifact. Intensive Care Med 1998; 24:1331–1334 monia. Crit Care Med 2010; 38:84–92