Received: 14 April 2017 | Revised: 27 June 2017 | Accepted: 11 July 2017

DOI: 10.1002/jcu.22526

RESEARCH ARTICLE

Pulmonary ultrasound scoring system for intubated

critically ill patients and its association with clinical
metrics and mortality: A prospective cohort study

David M. Tierney MD1 | Lori L. Boland MPH2 | Josh D. Overgaard MD1 |

Joshua S. Huelster MD3 | Ann Jorgenson RN2 | James P. Normington MS2 |
Roman R. Melamed MD3

1
Department of Graduate Medical
Education, Abbott Northwestern Hospital,
Abstract
Minneapolis, Minnesota
Purpose: Pulmonary ultrasound (PU) examination at the point-of-care can rapidly identify the eti-
2
Division of Applied Research, Allina Health,
ology of acute respiratory failure (ARF) and assess treatment response. The often-subjective
Minneapolis, Minnesota
3
classification of PU abnormalities makes it difficult to document change over time and communi-
Department of Critical Care, Abbott
Northwestern Hospital, Minneapolis, cate findings across providers. The study goal was to develop a simple, PU scoring system that
Minnesota would allow for standardized documentation, have high interprovider agreement, and correlate
with clinical metrics.
Correspondence
David Tierney, Department of Medical Methods: In this prospective study of 250 adults intubated for ARF, a PU examination was per-
Education, Abbott Northwestern Hospital, formed at intubation, 48-hours later, and at extubation. A total lung score (TLS) was calculated.
800 East 28th Street, Minneapolis, MN
Clinical metrics and final diagnosis were extracted from the medical record.
55407.
Email: david.tierney@allina.com Results: TLS correlated positively with mortality (P 5 .03), ventilator hours (P 5 .003), intensive
care unit, and hospital length of stay (P 5 .003, P 5 .008), and decreasing PaO2/FiO2 (P < .001).
Agreement of PU findings was very good (kappa 5 0.83). Baseline TLS and subscores differed sig-
nificantly between ARF categories (nonpulmonary, obstructive, and parenchymal disease).

Conclusions: A quick, scored, PU examination was associated with clinical metrics, including mor-
tality among a diverse population of patients intubated for ARF. In addition to diagnostic and
prognostic information at the bedside, a standardized and quantifiable approach to PU provides
objectivity in serial assessment and may enhance communication of findings between providers.

KEYWORDS
intubation, point-of-care ultrasound, pulmonary ultrasonography, respiratory insufficiency

1 | INTRODUCTION Acquisition, interpretation, and integration of PU findings at an iso-

lated point in time are essential to prompt and accurate diagnosis.
Pulmonary ultrasound (PU) has become an essential tool for rapidly Tracking PU changes over time is equally important in confirming a
identifying the etiology of acute respiratory failure (ARF), following diagnosis and adjusting treatment. To do so requires a standardized
treatment progress, and clarifying nonspecific chest radiograph (CXR) approach to PU such that providers can document and agree not only
1–5
abnormalities among critically ill patients, and with test characteris- with themselves but also with each other over time.11–14
6,7
tics better than the clinical examination and CXR. When used in PU scoring models have been developed to meet the need for
combination with cardiac and vascular ultrasound, it can enhance the standardization and have been shown to correlate with various metrics
understanding of etiology3 and may reduce the need for CXR or chest in specific patient populations.5,11,15–17 Scoring systems correlate with
8–10
CT. mortality in patients with acute respiratory distress syndrome

14 | V
C 2017 Wiley Periodicals, Inc. wileyonlinelibrary.com/journal/jcu J Clin Ultrasound. 2018;46:14–22.
TIERNEY ET AL.
(ARDS),17,18 on hemodialysis,19 with dyspnea and/or chest pain,15 and
with congestive heart failure (CHF),20 and PU can be used to quantify
extravascular lung water,16,21–24 which predicts outcomes in critically ill
patients.4,15,16,25–35
An ideal examination and scoring model would (1) have good intra-
rater and interrater agreement, (2) be rooted in a routine clinical PU
workflow, (3) be technically feasible, (4) be quick to perform and docu-
ment, but (5) be sensitive enough to detect significant but subtle
pathology, and (6) yield a score that has clinical predictive value.
The primary objective of this study was to establish a PU workflow
and scoring system in a large, diagnostically diverse group of intubated
patients that met the above criteria and was associated with clinical
outcomes.
2 | MATERIALS AND METHODS
2.1 | Setting and study design
This prospective cohort study took place at a 640-bed (62 intensive
care unit [ICU] beds) quaternary care center and enrolled 250 adult
inpatients between December 2013 and March 2015. All intubated
ICU patients who had provided consent for use of their electronic
health record data for research purposes were screened for eligibility
by a research nurse. Patients were excluded if they were intubated
solely for airway protection, had a history of pleurodesis, pneumonec-
tomy, or video-assisted thoracoscopic surgery, had been extubated or
had been intubated for >24 hours before a first PU examination, had
been transitioned to comfort care, or were imminently dying (Figure 1).
Because of physician availability, daily enrollment was limited to the 3
most recently intubated patients each morning. The protocol was
approved by an institutional review board (Schulman Associates IRB,
Inc, Approval No. 4080-2E).
2.2 | Ultrasound examination protocol
PU examinations were performed at 3 time points during a patient’s
ICU stay: (1) as soon after intubation as possible, (2) 48 hours after the
initial examination, and (3) at extubation if the patient’s previous exami-
nations did not already coincide with extubation. The patient was posi-
tioned supine with the head of the bed elevated 208 to 408. All
examinations were performed with a SonoSite EDGE portable ultra-
sound system equipped with a P21 (1–5 MHz) phased-array transducer
(FUJIFILM SonoSite Inc, Bothell, Washington).
Four physicians with greater than 3 years of PU experience per-
formed all examinations. They participated in a prestudy 1-hour train-
ing session to ensure uniformity of the pulmonary classifications and
then independently scored 64 virtual patients with videoclips. Overall
and entity-specific interrater agreements were calculated.
Physicians performing the PU examinations were not involved in
the patient’s care and were blinded to history, laboratory data, imaging,
treatments, and diagnosis. They were instructed not to examine medi-
cation drips or ventilator settings during the ultrasound examination.
| 15
2.3 | Lung zone classification criteria
The chest was divided into 9 zones (Figure 2), based on a modification
of previously established protocols,5,36 to approximate lobar anatomy
of the lung and reflect our clinical workflow in intubated patients. Each
zone was classified based on an overall impression from an area no
larger than 7.5 3 5 cm. Classification of findings (Figure 3) could be
accomplished without advanced computer technology37 or the need to
freeze an image and count abnormalities.
Similar to a previous study,15 each zone was classified as follows:
 A 5 lung sliding, presence of A-lines, and lack of B-lines or
consolidation
 B1 5 1 to 3 B-lines present per intercostal space
 B2 5 quantity of B-lines between B1 and B3
 B3 5 confluent B-lines occupying >50% of an intercostal space
Areas of nonaerated lung >3 cm in its axis perpendicular to pleura with
dynamic air bronchograms and lack of compressive reason for aeration
loss (eg, pleural effusion, elevated diaphragm) were classified as nona-
telectatic consolidation. Areas of nonaerated lung >3 cm in its axis per-
pendicular to pleura with distinct features suggesting volume loss
atelectasis, such as a pleural effusion size consistent with volume of
tissue-like lung, lack of dynamic air bronchograms, typical atelectatic
distribution in the inferior, lateral tip of lung with a smooth re-aeration
line, were classified as atelectasis. A combined classification of atelecta-
sis/consolidation was assigned when the area examined consisted of
tissue-like density and the physician was unable to see discriminating
features indicative of either specific entity. Zones with small, focal, <3-
cm areas of peripheral consolidation were classified as small consolida-
tions. The pleural effusion classification was added to each zone when
present.
2.4 | Scoring system
An individual lung zone received 0 points for an A classification, 1 point
for a B1, 2 points for a B2, and 3 points for any of the following: B3,
consolidation, atelectasis, or small consolidations. Each zone received
an additional point if effusion was present. The maximum score per
zone was 4 points. Isolated atelectasis without other parenchymal
abnormalities existing in zone 3 or 8 only received 1 point (Figure 3).
Total lung score (TLS) was the summation of all points across the 9
lung zones (possible range 5 0–36). Total B score represented the sum
of only the B-line points (B1, B2, B3) (range 5 0–27), and total atelecta-
sis/consolidation score was the sum of points assigned for atelectasis
and consolidation classifications across zones. Total anterior score
included points from zones 1, 2, 6, 7 and total posterior score from
zones 3, 5, 8, 9.
2.5 | Data collection
Independent of previous examinations, the physician performing the
PU examination entered findings into an electronic data collection tool
after leaving the patient’s room. Relevant clinical data were abstracted
16 | TIERNEY ET AL.

FIGURE 1 Study patient flow. Abbreviations: ALI, acute lung injury; ARDS, acute respiratory distress syndrome; CHF, congestive heart
failure; COPD, chronic obstructive pulmonary disease; PU, pulmonary ultrasound; VATS, video-assisted thoracoscopic surgery

from the electronic health record by a research nurse. A final diagnosis 2.6 | Statistical analysis
for each patient’s ARF was determined via review of clinical notes, for-
Patient and event characteristics were described using means or
mal imaging, laboratory values, and the care team’s final diagnosis after
medians, and proportions. Subscores of TLS were expressed as mean
discharge, which was conducted by study physicians who did not per-
values and as the mean percentage of TLS and were examined overall
form the ultrasound examinations and were blinded to examination
results. and by etiology of ARF.
TIERNEY ET AL.
FIGURE 2 Locations and numbering of the examination zones. Abbreviations: AAx, anterior axillary line; MC, midclavicular line; PAx,
posterior axillary line
Mortality, ICU, and hospital length of stay (LOS), PaO2/FiO2 ratio,
and ventilator hours were examined across tertiles of TLS, with
Cuzick’s trend test used to assess trends across tertiles.
Lung scores were also examined by the common clinical respira-
tory disease categories of no pulmonary disease (eg, altered level of
consciousness, upper airway obstruction, and neuromuscular weak-
ness), obstructive disease (eg, asthma and chronic obstructive
FIGURE 3 Lung zone classification and associated point assignment
| 17
pulmonary disease [COPD]), and parenchymal disease (eg, pneumonia,
ARDS, aspiration, and CHF), with one-way analysis of variance used to
assess whether disease category explained a significant amount of the
variation in scores.
Fleiss’s kappa coefficient was used to assess interrater agreement
in the prestudy training set. All analyses were conducted using Stata
14.1 (StataCorp, LP, College Station, Texas).
18 | TIERNEY ET AL.

T AB LE 1 Patient characteristics overall and by etiology of acute respiratory failure

% In-hospital
Variable N Age % Male Ventilator days P/F ratio at intubation ICU LOS Hospital LOS mortality

All patients 250 65 (23–93) 48 4.1 (0.1–34.4) 222.5 (63–584) 7.8 (1.0–40.8) 13 (2–58) 24

Diagnosis
Pneumonia 76 66 (28–93) 45 5.0 (0.5–15.8) 184 (88–494) 9.9 (1.7–38.6) 14 (3–41) 18
Aspiration 34 72 (49–91) 47 4.3 (0.1–34.4) 232 (86–483) 8.0 (1.3–30.8) 15 (2–39) 24
Sepsis 29 67 (30–87) 59 3.7 (0.5–13.2) 233 (158–530) 8.3 (1.4–25.4) 15 (2–58) 21
CHF 27 71 (50–89) 44 2.3 (0.8–15.0) 218 (68–417) 5.8 (1.7–21.8) 10 (2–25) 30
Cardiac arrest 22 67 (31–79) 45 4.6 (0.3–13.8) 254 (64–584) 7.0 (1.5–20.5) 12 (2–48) 45
ALI/ARDS 18 61 (30–78) 39 7.2 (0.6–13.5) 161 (63–336) 11.3 (3.1–36.9) 15 (7–37) 33
COPD/asthma 17 64 (55–87) 59 2.3 (1.3–11.6) 234 (120–348) 4.3 (1.9–12.1) 9 (2–12) 24
Othera 27 65 (23–88) 52 3.9 (0.9–10.8) 248 (75–474) 7.6 (1.0–40.8) 15 (2–51) 19

Abbreviations: ARF, acute respiratory failure; CHF, congestive heart failure; COPD, chronic obstructive pulmonary disease; ICU, intensive care unit;
LOS, length of stay; P/F, PaO2/FiO2.
Results are expressed as median (range) or % as appropriate.
a
Other: acute myocardial infarction (1.6%), altered level of consciousness (2.0%), atelectasis (0.8%), neuromuscular weakness (0.8%), pulmonary embo-
lism (0.8%), pulmonary fibrosis (0.8%), blastomycosis (0.4%), cryptogenic organizing pneumonia (0.4%), Kaposi sarcoma (0.4%), obstructive sleep apnea
(0.4%), pleural effusion (0.4%), pneumothorax (0.4%), pulmonary aspergillosis (0.4%), upper airway obstruction (0.4%), and pulmonary vasculitis (0.4%).

3 | RESULTS
A total of 1308 patients were screened for enrollment, of which 1014
(77%) did not meet inclusion criteria (Figure 1). The most common diag-
nosis for ARF was pneumonia (Table 1).
TLS for baseline examinations ranged from 0 to 31 points (mean 5
12), with the highest mean observed in those with ARDS and the low-
est in patients with COPD/asthma (Table 2). Posterior lung scores con-
tributed a greater proportion to the TLS than anterior lung scores in all
diagnostic groups except ARDS. The contribution of B score to TLS
was greater than atelectasis/consolidation across all diagnostic catego-
ries, especially in CHF, ARDS, and aspiration (Table 2).
Tertiles of baseline TLS (0–9, 9.5–18, 18.5–36) were positively
associated with mortality (P 5 .03), median ICU (P 5 .003), and hospital
LOS (P 5 .008), and ICU ventilator hours (P 5 .003), and inversely asso-
ciated with baseline PaO2/FiO2 ratio (P < .001) (Figure 4).
Patients in the 3 clinical groupings had significantly different total
lung, B, anterior, and posterior scores (P < .001, .005, <.001, .002,
respectively) with the highest scores in the parenchymal group (Table
3). The 8 patients in the no pulmonary disease group had a nonpulmo-
nary etiology for intubation on final chart review not apparent at the
time of initial inclusion.
Average time to perform the PU examination on 10 randomly
selected days (n 5 28 examinations) was 135 seconds (range 5 88–
205). Among the 64 virtual patients scored by the 4 participating
physicians during prestudy training, interrater agreement was very
good for TLS (kappa 5 0.83), almost perfect for assignment of the A
classification (kappa 5 0.96), very good for atelectasis/consolidation
(kappa 5 0.84), and substantial for the B1, B2, and B3 classifications
(kappa 5 0.77, 0.61, 0.74, respectively).
4 | DISCUSSION
Respiratory failure is one of the most common conditions in the ICU
and often requires chest imaging for accurate diagnosis.38,39 Physicians
need to make an accurate diagnosis, define disease severity, assess

T AB LE 2 Mean total and sub lung scores at baseline, overall, and by etiology of acute respiratory failure

Variable N Total lung score B score Atl/Consol score Anterior score Posterior score

All patients 250 12.0 8.6 (70) 2.5 (22) 5.8 (42) 6.1 (58)

Diagnosis
ARDS 18 20.3 16.1 (79) 3.2 (16) 12.1 (59) 8.2 (41)
CHF 27 14.0 10.5 (72) 2.1 (16) 6.3 (39) 7.6 (61)
Pneumonia 76 12.9 8.7 (66) 3.3 (27) 6.5 (47) 6.4 (53)
Cardiac arrest 22 11.2 7.5 (67) 3.0 (26) 5.6 (42) 5.5 (58)
Other 27 10.6 8.0 (71) 1.8 (21) 5.0 (35) 5.5 (65)
Aspiration 34 9.6 7.4 (78) 1.5 (14) 4.4 (40) 5.3 (60)
Sepsis 29 9.4 5.5 (54) 3.1 (37) 4.2 (34) 5.2 (66)
COPD/asthma 17 8.1 7.6 (96) 0.2 (2) 2.9 (33) 5.1 (67)

Abbreviations: ARDS, acute respiratory distress syndrome; Atl/Consol, atelectasis/consolidation; CHF, congestive heart failure; COPD, chronic obstruc-
tive pulmonary disease.
Results are expressed as mean or mean (% total lung score).
 TIERNEY
ET AL.

FIGURE 4 Clinical metrics by total lung score tertile. Abbreviations: Hosp, hospital; ICU, intensive care unit; LOS, length of stay; P/F, PaO2/FiO2; Vent, ventilator
|
19
20 | TIERNEY
response to treatment, and prognosticate, and PU represents an
emerging technique for accomplishing these in a safe, timely, and cost-
efficient manner. Portable chest radiograph has significant limitations7
and potential risks (eg, accidental removal of lines/tubes), whereas
chest CT has notable drawbacks, such as increased radiation, cost, and
the need to transport the patient from the ICU.9,10,40
Small studies of PU scoring systems in disease-specific patient
populations and their association to various clinical metrics
exist,5,11,15–20 as does a large (260 patients) study proposing a standar-
dized diagnostic system based on lung ultrasound profiles.1 However,
to our knowledge, a large prospective study of a simple lung ultrasound
scoring system and its association to clinical outcomes including mor-
tality across a wide spectrum of clinical disease has not been previously
reported. The current approach was studied in 250 patients from medi-
cal/surgical, neurological, and cardiovascular ICUs, and thus the results
are highly applicable to a diverse ICU population. Furthermore, this 9-
point examination, taking on average 2 to 3 minutes to perform, can be
feasibly integrated into the daily physical examination of patients in
their typical positioning.
The 9 lung zones included in this algorithm reflect a clinical examina-
tion in an applied setting, rather than a workflow designed for a research
protocol. There are no formally endorsed approaches to a clinical PU
examination, although both an 8- and 28-point examination have been
5
described. A clinical PU examination sequence often involves concep-
tual lobar anatomy, and thus the right lateral caudal area was divided into
both an anterior and a posterior zone over the right middle and lower
lobes, respectively. Designation of an “extra” zone in the right lung, in
addition to being clinically relevant, can be physiologically rationalized
based on the greater total lung capacity of the right lung.41 Of interest,
3.9% of our patients with aspiration and pneumonia had findings present
only in the right lateral caudal zone on the anterior axillary line that
would have been missed if that zone was not included in the examina-
tion. A sensitivity analysis was conducted both with and without this
additional zone included, and similar associations between lung scores
and outcomes were observed with both methods.
Many previous studies have examined the association of the pres-
ence of B-lines to various outcomes. However, in this study, ascending
points (0 to 3) were assigned to the continuum of lung abnormality clas-
sifications from the normal, fully aerated A classification (0 points) to
the least aerated consolidation and atelectasis (3 points). Of note, there
T AB LE 3 Various lung scores by clinical groupings
Clinical grouping (n) Total lung score
No pulmonary disease (8) 4.3
Obstructive disease (17) 8.1
Parenchymal disease (155) 13.2
P value a
<.001
“No pulmonary disease” 5 altered level of consciousness, neuromuscular weakness, and upper airway obstruction. “Obstructive disease” 5 COPD and
asthma. “Parenchymal disease” 5 pneumonia, CHF, aspiration, ALI/ARDS.
a
One-way analysis of variance.
ET AL.
was no significant difference in the predictive power of our score when
atelectasis, consolidation, or small consolidations resulted in an extra
point beyond the B3 classification (ie, the zone was given a total of 4
points rather than 3) versus if each of these entities received 3 points
for simplicity. By assigning 1 point for each zone with effusion (with
patients positioned semi-upright), a feasible and semi-quantitative
assessment of pleural effusion was incorporated into the TLS. The mod-
ification of isolated atelectasis in the lateral caudal lung zone on the
posterior axillary line receiving 1 point instead of 3 resulted in improved
predictive power across metrics and is consistent with the limited sig-
nificance this isolated finding has in the clinical environment.
The association of this PU scoring system to mortality in a large
population of intubated ICU patients with ARF is important from a clin-
ical standpoint, because various small studies have only demonstrated
associations of specific PU findings with outcomes in specific disease
states.15,17–20 Non–ultrasound-based models predict mortality among
ICU patients; however, they typically rely on a combination of physio-
logic variables and comorbid conditions, and few exist specifically for
intubated patients.42,43 Beyond the observed association with mortal-
ity, potential use of the TLS in predicting ventilator hours and LOS may
be useful in guiding family expectations, patient flow, and quality meas-
ures tied to LOS, but this requires further study.
Some limitations to our study exist. To preserve efficiency, we exam-
ined a limited surface area of the lung, and this may have led to overesti-
mation of a process that only existed under the transducer, or the
inability to visualize a pulmonary process present just outside the area of
examination. Our interobserver agreement was calculated based solely
on image review, thus dismissing the variability that can exist in image
acquisition. Physicians performing the examination were blinded to
patient data, but there were opportunities for this blinding to have been
incomplete and possibly influence their assessment (eg, medication infu-
sions visible at the bedside, other provider discussions in/around the
patient room). Having a single provider perform the repeat examinations
on an individual patient, although meant to ensure consistency, may
have introduced bias with the examiner knowing the previous location of
findings. Despite these instances of potential “unblinding,” they all do
reflect the reality of PU in the clinical setting. Retrospective chart review
was used to determine a final diagnosis, but, as can be the case in ARF
patients, more than 1 etiology may have been contributing, or the diag-
nosis was not definitive. The number of extubation examinations more
B score Anterior score Posterior score
2.5 0.9 3.4
7.6 2.9 5.1
9.6 6.6 6.7
.005 <.001 .002
TIERNEY ET AL.
than 48 hours after the initial examination was small (n 5 30) because of
ICU workflow and difficulty coordinating a blinded US examination with
the treatment team. This prevented us from adequately assessing TLS
change from baseline to extubation.
The differential diagnosis for ARF is often difficult to narrow
based on history, physical examination, and laboratory data alone. PU
is immediately available at the bedside and can provide helpful diag-
nostic information in these patients, especially when combined with
cardiac and vascular US. This simple PU scoring system, which pro-
vides for standardized quantification and communication of PU find-
ings between examinations and providers, had good agreement
among providers, was quick to perform, and correlated well with
important clinical outcomes.
AC KNOW LE DGME NT
Thanks to Anne Uttermark, RRT for coordination of the respiratory
therapy’s involvement in the study.
C ONFLICT OF INT E RE ST
This manuscript has not been previously published and is not under
consideration in the same or substantially similar form in any other
peer-reviewed media. All authors listed have contributed sufficiently
to the project to be included as authors. No conflict of interest,
financial or otherwise, exists for any of the authors.
OR CID
David M. Tierney MD http://orcid.org/0000-0003-4202-1101
R E FER E NCE S

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How to cite this article: Tierney DM, Boland LL, Overgaard JD,
et al. Pulmonary ultrasound scoring system for intubated crit-
ically ill patients and its association with clinical metrics and
mortality: A prospective cohort study. J Clin Ultrasound.
2018;46:14–22. https://doi.org/10.1002/jcu.22526