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VOLUME 31 NUMBER 1
JANUARY-DECEMBER 2023
VOLUME 31 NUMBER 1
JANUARY-DECEMBER 2023
E-ISSN 2774-0048E-ISSN 2774-0048
Clinical Critical Care
Volume 31, Article ID e0004, 7 pages
https://doi.org/10.54205/ccc.v31.260228
RESEARCH PROTOCOL
eISSN 2774-0048eISSN 2774-0048
The relationship of lung recruitability assessment by
recruitment to ination ratio, electrical impedance
tomography, and lung ultrasound: The research protocol
Kridsanai Gulapa1, Yuda Sutherasan1, Detajin Junhasavasdikul1, Pongdhep Theerawit2
1Division of pulmonary and pulmonary critical care Medicine, Department of Medicine, Ramathibodi Hospital, Mahidol University, Bangkok, Thailand, 10400
2Division of Critical Care Medicine, Department of Medicine, Ramathibodi Hospital, Mahidol University, Bangkok, Thailand, 10400
ABSTRACT:
Background: Recently, the recruitment-to-ination ratio (R/I ratio) from the sin-
gle-breath technique has been proposed for identifying lung recruitability in
acute respiratory distress syndrome (ARDS). This technique is based on measur-
ing end-expiratory lung volume (EELV). Also, electrical impedance tomography
(EIT) can estimate the EELV, providing the potential role of EIT in measuring the
R/I ratio. In addition, the lung ultrasound was proved to identify lung recruitment.
However, a study validating those techniques has not been conducted.
Methods: We plan to conduct a single-center prospective physiological study on
moderate to severe ARDS patients. The R/I ratio by single-breath technique and
EIT will be collected before the recruitment maneuver. If the patient has no air-
way opening pressure (AOP), PEEP of 8 cmH2O will be set as PEEPlow. The PEEPhigh
denes as initially set at +10 cmH2O from the PEEPlow. However, if the patients
have AOP presence, AOP +10 cmH2O will be set as PEEPhigh. The lung ultrasound
score (LUS) will be performed at PEEPhigh and PEEPlow during the single-breath
technique. Variables that will be used to analyze the relationship are recruited
volume (Vrec), R/I ratio, and LUS.
Hypothesis: We hypothesize that there are associations between the R/I ratio by
both techniques and lung ultrasound score (LUS).
Ethics: The study protocol has been approved by the ethics committee of the fac-
ulty of medicine, Ramathibodi Hospital, Mahidol University (COA.MURA2021/433).
Keywords: Acute respiratory distress syndrome, Recruitment-to-ination ratio,
Lung ultrasonography, Electrical impedance tomography, Recruitability assess-
ment
OPEN ACCESS
Citation:
Gulapa K, Sutherasan Y, Junhasavasdikul
D, Theerawit P. The relationship of lung
recruitability assessment by recruitment
to ination ratio, electrical impedance
tomography, and lung ultrasound: The
research protocol. Clin Crit Care 2022; 31:
e0004.
Received: December 1, 2022
Revised: February 12, 2023
Accepted: February 14, 2023
Copyright:
© 2021 The Thai Society of Critical Care
Medicine. This is an open access article
distributed under the terms of the Cre-
ative Commons Attribution License, which
permits unrestricted use, distribution, and
reproduction in any medium, provided
the original author and source are cred-
ited.
Data Availability Statement:
The data and code were available upon
reasonable request (Pongdhep Theerawit,
email address: kridsanai.gul@mahidol.
ac.th)
Funding:
The authors declare that there is no fund-
ing.
Competing interests:
None to disclose.
Corresponding author:
Pongdhep Theerawit
Division of Critical Care Medicine, Depart-
ment of Medicine, Ramathibodi Hospital,
Mahidol University, Bangkok, Thailand,
10400
Tel: (+66) 95-449-8244
Fex: (+66) 2-201-1619
E-mail: kridsanai.gul@mahidol.ac.th
Clinical Critical Care
2
KEY MESSAGES:
• Lung recruitability assessment by recruitment-
to-ination ratio (by single breath reduction and
electrical impedance tomography) and lung ul-
trasonography
INTRODUCTION
e recruitment maneuver (RM) is one of the life-saving
procedures for moderate to severe acute respiratory dis-
tress syndrome (ARDS) [1]. Several methods have been
applied to assess alveolar recruitment as the volume of gas
reaeration from poorly aerated lungs, dened as the lung
recruitability [2,3]. Unfortunately, no best method can ac-
curately predict high recruiter patients in various features
of ARDS lung.
e gold standard assessment method is the volumet-
ric chest computed tomography (CT) to evaluate the gas
volume and lung tissue changing during RM [3-5]. In cur-
rent practice, imaging studies, namely lung ultrasound,
electrical impedance tomography (EIT), and lung volume
measurements, have become comfortable and well-estab-
lished bedside tools for assessing lung recruitability. How-
ever, chest CT is impractical and potentially increases the
risk of hemodynamic instability during transportation
and radiation exposure.
Chiumello et al. found good correlations between
end-expiratory lung volume (EELV) measurement by the
nitrogen wash-out/wash-in technique and helium dilu-
tion and CT scan in patients ventilated with low levels of
positive end-expiratory pressure (PEEP) [6]. Moreover,
PEEP-induced change in lung volume is another method
for determining lung recruitability by measuring the vol-
ume trapped by PEEP above functional residual capacity
(FRC) by prolonged exhalation to the atmospheric pres-
sure [7,8] at two levels of PEEP. Chen et al. have recently
developed a simplied method using the same principle
of PEEP-induced change in lung volume by single-breath
reduction technique [9]. e single breath reduction tech-
nique provided the recruitment/ination (R/I) ratio de-
rived from the ratio of recruited lung compliance (Crec),
which is calculated from recruited volume (Vrec) over
the respiratory system compliance at low PEEP (Crs at
PEEPlow). e author reported that the Vrec was strongly
correlated with the standard multiple pressure/volume
(P/V) methods. e R/I ratio that discriminates recruiters
from non-recruiters corresponds to the median value of
0.5 [9].
Lung ultrasound score (LUS) as a reaeration score is
the most non-radiated simple imaging tool. Bouhemad
et al. found that PEEP-induced lung recruitment greater
than 600 ml related to detection on lung ultrasound re-
aeration score of more than 18 [10]. Nevertheless, lung
ultrasonography is limited in detecting the overdistension
zone. is problem can be solved with EIT, another bed-
side imaging method that may be similar to a CT scan.
EIT can give real-time regional zone gas distribution and
tidal impedance during PEEP titration [11]. Also, EIT can
estimate the EELV, providing the potential role of EIT in
measuring the R/I ratio. However, a study validating those
techniques has not been conducted.
We aim to analyze the relationship between the R/I ra-
tio by single breath reduction from exhaled tidal volume
measurement, EIT-derived parameters, and LUS.
OBJECTIVES
To analyze the relationship between the R/I ratio by the
single breath method, the R/I ratio by EIT, and the lung
ultrasound score (LUS).
MATERIALS AND METHODS
Study Design
A prospective cohort study had been planned to conduct
in moderate to severe ARDS patients in ICU Ramathibo-
di hospital between December 2020 and February 2023.
erefore, this study protocol was registered retrospec-
tively. e ethics committee of the faculty of medicine,
Ramathibodi Hospital, Mahidol University, approved this
study with an approval number of COA.MURA2021/433.
e written informed consent will be obtained from the
patient's next of kin.
Study population
Patients over 18 years old undergoing mechanical ven-
tilators will be evaluated. e patients will be recruited
in the study if they meet the following inclusion criteria.
Inclusion criteria
- Diagnosed moderate to severe ARDS[1]
- Currently on mandatory mechanical ventilation,
received sedative and neuromuscular blocking agents,
and presence of arterial line and central line.
Exclusion criteria
- e patient who has a history of recent exacerbated
obstructive airway disease within eight weeks according
to the Global Initiative for Chronic Obstructive pulmo-
nary disease criteria [12]
- e presence of pneumothorax or intercostal chest
drainage catheter
- Pregnancy
- e patient who has the contraindications for in-
sertion of the esophageal balloon catheter
- e patient who has the contraindications for RM
(hemodynamic instability, received norepinephrine dos-
ing > 0.5 mcg/kg/min or increased dosage of norepineph-
rine in the past 6 hours of >30% of the previous baseline,
uncorrected acute respiratory acidosis, has the PaCO2 of
>50 mmHg with the pH change, and intracranial hyper-
tension).
Recruitability assessment method by bedside imaging tools
3
Baseline characteristics, including the severity of the
medical comorbidities, causes, and types of ARDS; Acute
Physiology and Chronic Health Evaluation II (APACHE
II) score in the rst 24 hours of admission, the pattern of
ARDS by imaging, and baseline hemodynamic data will
be collected.
Measurements
Every patient is ventilated supine with the ventilator,
which can be performed with the pressure/volume tool
(Hamilton G5 or S1). With the head of the bed raised to
30 degrees, an esophageal balloon catheter (global trade
item no. GTIN: 07630002803755) will be inserted and po-
sitioned in the lower 1/3 of the esophagus at a 35-40 cm
depth from incisor teeth and inated with air volume be-
tween 1-2 ml. e esophageal balloon catheter is normally
connected to an auxiliary ventilator port to measure the
pressure. e proper position of the esophageal balloon
will be tested by the end-expiratory pause technique [13].
e EIT belt from the PulmoVista 500 by Dräger® will
apply to the patient. e respiratory mechanic, esophageal
pressure, and EIT parameters are continuously recorded
and exported from the ventilator for oine interpreta-
tion.
e protocol will be initiated with AOP measurement
by the low ow pressure-volume (P/V) tool. e measur-
ing measuring Vre c by single-breath method performs as
Chen et al. reported [9]. All patients are passively ventilat-
ed without spontaneous eort in a volume control mode.
If the patient has no AOP, PEEP of 8 cmH2O will be set as
PEEPlow in the lung-protective strategy. e PEEPhigh is ini-
tially set at +10 cmH2O from the PEEPlow. However, if the
patients have AOP presence, AOP +10 cmH2O will be set
as PEEPhigh but not exceed 12 cmH2O of transpulmonary
driving pressure [14].
We plan to perform LUS with a Sonosite M-turbo, por-
table ultrasound system, and 10-15 MHz probe. e LUS
protocol involves the examination of eight lung regions,
the upper and lower parts of the anterior and posterior
aspects of the le and right chest walls demarcated by the
4th intercostal space of midclavicular and anterior axillary
lines. A well-trained pulmonologist (K.G.) will perform
transthoracic ultrasonography. According to the R/I ra-
tio measurement method, we have to set 2 levels of PEEP
(PEEPhigh and PEEPlow as previously described). e lung
ultrasound images will be recorded aer 5-10 minutes of
PEEP change during the R/I ratio measurement (LUS at
PEEPhigh and PEEPlow aer PEEP reduction). All photos
will be saved as video records and renamed in codes set by
the operator. A total of video les will be sent to two in-
dependent observers in two separate le sets for scoring.
If two observers' numbers of the score are discordant, the
consensus score will be used.
Aer nishing the single-breath method, the RM and
decremental PEEP titration will nally be performed. e
RM will conduct in pressure-controlled mode with an in-
spiratory plateau pressure of 25 cm of water, a PEEP of 20
cm of water, a respiratory rate of 10 / per minute, and a 1:1
ratio of inspiration to expiration for two minutes. en,
the pressure control ventilation mode will be set with
a xed inspiratory pressure of 15 cmH2O. e decremen-
tal PEEP trial performs from PEEP of 20 cmH2O to 8
cmH2O with a decrease in 2 cmH2O each step every 1
minute [15-18].
e hemodynamic parameters are simultaneously
monitored via arterial line placement and pulse con-
tour analysis equipment (EV 1000® or Vigellio®, Edward®
life science). If the patients have signs and symptoms of
clinical deterioration, for instance, inability to maintain
blood pressure, need the titration of vasopressor greater
than 0.5 mcg/kg/min or >30% of the previous baseline,
presence of pneumothorax, or progressive respiratory
failure acidosis (PaCO2 >50 mmHg) with the pH change.
e patient will be excluded from the study.
Variables dened denition
Lung ultrasound score
Four ultrasound aeration patterns dene according to
the worst observed ultrasound pattern: normal aeration,
A-lines or a few separated B-lines= 0, three or more well-
spaced B-lines = 1, coalescent B-lines = 2, subpleural
consolidation and consolidation = 3 [18]. e LUS score
is the summation of the aeration score of each area of
interest. en, calculating the total LUS dierence of two
PEEP levels interprets between regions into ∆LUS (LUS
of PEEPhigh – LUS PEEPlow).
Recruited volume and recruitment to ination
ratio
Recruited volume (Vrec ) is the mathematical proportion
of volume distributed into the recruited lung from the
baby lung when PEEP is changed [9]. e baby lung vol-
ume terminology is a small, aerated lung tissue at PEEPlow
or FRC. e R/I ratio by single-breath technique refers to
the compliance of recruited lung (Crec) over the baby lung
compliance (compliance at PEEPlow) as presented by this
equation.
e Vrec is the dierence between the measured
ΔEELV and the predicted ΔEELV (i.e., the compliance at
low PEEP multiplied by the change of PEEP).
e measured ΔEELV is the exhaled tidal volume
(VT) aer single-breath reduction minus tidal volume at
PEEPhigh, as follows;
Regarding the R/I ratio by EIT, EELV is calculated
from the end-expiratory lung impedance (EELI) and tidal
impedance formula as below [19].
Clinical Critical Care
4
And the reason for the equal pressure dierence in the
ratio.
Lung recruitability by EIT
e EIT image is demonstrated in four quadrants axial
view with the dynamic aeration reaching a region of in-
terest (ROI), in which ROI 1-2 are the ventral part and
ROI 3-4 are the dorsal part of the lungs. During the re-
cruitment maneuver, If the lungs respond to RM, the
percentage of gas distributive change in dependent lung
regions will be demonstrated as the portion of gas distri-
bution in the ROI 3 and 4 manifested by EIT may interest-
ingly change. We plan to analyze the correlation between
the R/I ratio produced by both EIT-derived and the sin-
gle-breath technique and the average percentage change
of gas distribution of ROI 3,4.
Adverse events
Due to the usual standard of protective open-lung con-
cept ARDS treatment strategy and the using esophageal
pressure-guided treatment, unexpected adverse events
such as pneumothorax, progressive severity of ARDS, and
hemodynamic instability might occur as regular events
during data collection. However, if an adverse event ap-
pears, the investigator will respond and notify the attend-
ing physician team immediately.
Outcome measurement
e primary outcome is the correlation between the R/I
ratio using the single-breath method and the EIT tech-
nique, together with the correlation of LUS.
Timeline
(Figure1) the owchart of data collection
DATA ANALYSIS PLAN
Sample size calculations
We aim to perform a physiologic pilot study. erefore
we do not calculate the sample size. We have estimated a
sample size of 20.
OUTCOME ANALYSIS PLAN
Statistical analyses
Baseline characteristics will be presented as mean (±Stan-
dard Deviation, SD) or median (interquartile range, IQR)
depending on the data distribution. e correlation co-
ecients between LUS, the R/I ratio by single breath re-
duction, and the R/I ratio by EIT will be determined by
Pearson’s or Spearman according to the characteristics of
the data. Statistical analysis will be conducted with the
IBM® SPSS® program version 22.0 soware (IBM SPSS
Statistics, IBM Corporation, New York, USA). A P-value
of less than 0.05 determined statistical signicance.
Figure 1. e owchart of data collection.
Recruitability assessment method by bedside imaging tools
5
DATA MANAGEMENT AND DATA MONITORING
Input data and monitoring method
Table 1. Clinical characteristics with baseline hemodynamic data in ARDS patients
Characteristics Collection method
Sex, female, n (%) Chart review
Age, years Chart review
BMI, kg/m2 Chart review,
manual calculation
Comorbidities, n (%)
• Immunocompromised Chart review
• Hematologic malignancy Chart review
• HT Chart review
• DM type 2 Chart review
• non-RRT CKD Chart review
• Currently on immunosuppressant Chart review
APACHE II at 1st 24hr admission Chart review
Type of ARDS, n (%)
• Intrapulmonary cause Chart review
• Homogenous pattern on chest CT Chart review
Berlin denition of ARDS severity, n (%)
• Moderate Chart review
• Severe Chart review
PaO2/ FiO2 ratio at inclusion Chart review
Baseline Hemodynamic data
• SBP, mmHg Chart review
• DBP, mmHg Chart review
• MAP, mmHg Chart review
• Vasopressor during inclusion, n (%) Chart review
• Dose of norepinephrine, mcg/kg/min Chart review
• Arterial lactate, mmol/l Chart review
• PPV, % Chart review
• SSV, % Chart review
• CO, liters/min Chart review
Denition of abbreviations: ARDS=acute respiratory distress syndrome; APACHE=Acute Physiology and Chronic Health Evaluation; BMI=body mass
index; CO=cardiac output; DBP=diastolic blood pressure; PPV=pulse pressure variation; RRT=renal replacement therapy; SBP=systolic blood pressure;
MAP=mean arterial pressure; SVV=stroke volume variation.
Dichotomous or nominal categorical variables are described as numbers (percentage); continuous variables are expressed as mean + SD or median (in-
terquartile range 25-75), as appropriate.
Table 2. Respiratory mechanic and gas exchange parameter at the time of inclusion.
Respiratory mechanic and gas exchange parameters Collection method
Baseline lung mechanic proles, n (%)
• VCV mode Chart review
• SetVTi/PBW Chart review
• RR, times/min Chart review
• AOP> 5 cmH2O, n (%) Chart review
• Mean AOP, cmH2O Chart review
• SpO2 , % Chart review
• PaO2/ FiO2 ratio at inclusion Chart review
Clinical Critical Care
6
Respiratory mechanic and gas exchange parameters Collection method
• P peak, cmH2O Chart review
• Plateau pressure, cmH2O Chart review
• CRS, ml/cmH2O Chart review
• ElastanceRS, cmH2O/ml Chart review
• Pes end inspiratory, cmH2O Chart review
• Pes end expiratory, cmH2O Chart review
• TP end inspiratory, cmH2O Chart review
• TP end expiratory, cmH2O Chart review
• TP end inspiratory elastance ratio, cmH2O Chart review
Denition of abbreviations: AOP= Airway opening pressure; CRS = respiratory system compliance; ElastanceRS =respiratory system elastance; P peak= Peak
airway pressure; PBW=predicted body weight; Pes end inspiratory= end-inspiratory esophageal pressure; Pes end expiratory= end-expiratory esophageal
pressure; RR=respiratory rate; TP=transpulmonary pressure; VCV= Volume controlled mandatory ventilation; VTi=Inspiratory volume.
Table 3. e correlation between Lung Ultrasound Score and R/I ratio by both techniques.
Lung ultrasound score Vrec by single
breath
Vrec by EIT R/I by single
breath
R/I by EIT
∆LUS at upper anterior axil-
lary chest
Correlation Coecient
P-value
N
∆LUS at upper anterior chest Correlation Coecient
P-value
N
∆LUS at lower anterior axillary
chest
Correlation Coecient
P-value
N
∆LUS at lower anterior chest Correlation Coecient
P-value
N
∆LUS total 4 regions Correlation Coecient
P-value
N
Denition of abbreviations: EIT=electrical impedance tomography; LUS=lung ultrasound score (summation of each area aeration score); N=number of
participants; R/I ratio=recruitment to ination ratio; ∆LUS= LUS dierence between the two PEEP level (LUSPEEPhigh - LUSPEEPlow). e Aeration score of
LUS [19] is dened as scoring 3=consolidated tissue; 2=multiple (≥3) coalescent B-lines; 1= three or more well-demarcated B-lines; 0= A-lines or few
separated B-lines; Vrec=recruited volume.
DISCUSSION
e R/I ratio by the single-breath technique is recently used
in many ICU settings with dierent validation methods. We
are conducting a trial investigating the association of the
R/I ratio by the EIT method and the single breath. Mauri
et al. studied the comparison between lung volume mea-
surement by helium dilution technique and EIT and found
a strong correlation [21]. In the experimental study by Yang
et al., in pig model-induced ARDS, the author reported that
EIT-derived Vrec was signicantly correlated with ow-de-
rived Vrec[22]. EIT yield benets over helium dilution tech-
nique and EELV measurements in continuously tracking
ination, strain, and recruitment at varying PEEP levels,
either regional or global ventilation, while avoiding airway
disconnection.
Bouhemad et al. compare the P/V curve method with
LUS for assessing PEEP-induced lung recruitment in forty
patients with ARDS. ey found that PEEP-induced lung
recruitment measured by P/V curves and ultrasound re-
aeration scores were signicant (10). erefore, LUS may
be another method to validate the R/I ratio by single breath
method and recruited lung.
Strengths:
(1) We will conduct the rst EIT-derived R/I ratio
study to investigate the correlation of lung volume param-
eters with the R/I ratio from the single-breath technique.
(2) Our study uses feasible bedside ultrasonography
for the accessibility of lung recruitment.
(3) Our study promotes a safe recruitability assess-
ment procedure by EIT and lung ultrasound, which can
discriminate recruiters from non-recruiters.
Recruitability assessment method by bedside imaging tools
7
Limitations:
(1) Small sample size over a short period of data collec-
tion.
(2) Lung ultrasound may not be a precise tool to detect
an overdistended part of the lung.
(3) We did not perform a quantitative volumetric CT
scan, the gold standard for assessing recruitability.
CONFIDENTIALITY
Informed consent is obtained within the isolated private room in the ICU by the
researchers only. Patients’ data are encrypted with the hospital-based healthcare
personnel passcode-locking system in the database. Aer the trial, all data will be
eliminated from all computers or physical documents.
ACKNOWLEDGEMENT
We would like to thank all the intensive healthcare personnel, internal medicine
residents, ICU nurse, pulmonary critical care fellows, and sta in Ramathibodi
hospital for their support and cooperation during this study.
AUTHORS’ CONTRIBUTIONS
(I)Conceptualization: Kridsanai Gulapa; (II) Data curation: Kridsanai Gulapa;
(III) Formal analysis: Kridsanai Gulapa, Yuda Sutherasan, Detajin Junhasavasdi-
kul, Pongdhep eerawit ; (IV)Funding acquisition: Kridsanai Gulapa; (V) Meth-
odology: Kridsanai Gulapa, Yuda Sutherasan, Detajin Junhasavasdikul, Pongdhep
eerawit; (VI) Project administration: Kridsanai Gulapa; (VII) Visualization:
Kridsanai Gulapa; (VIII) Writing-original dra: Kridsanai Gulapa; (IX) Writing –
review & editing: Kridsanai Gulapa, Yuda Sutherasan, Pongdhep eerawit.
SUPPLEMENTARY MATERIALS
None
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