PLOS ONE
RESEARCH ARTICLE
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OPEN ACCESS
Citation: Silva Junior EFFd, Campos SL, Leite WS,
Melo PVdS, Lins RAC, Araújo MdGRd, et al. (2023)
Surface electromyography signal processing and
evaluation on respiratory muscles of critically ill
patients: A systematic review. PLoS ONE 18(4):
e0284911. https://doi.org/10.1371/journal.
pone.0284911
Editor: Gustavo Plaza-Manzano, Complutense
University of Madrid: Universidad Complutense de
Madrid, SPAIN
Received: January 20, 2023
Accepted: April 12, 2023
Published: April 27, 2023
Copyright: © 2023 Silva Junior et al. This is an
open access article distributed under the terms of
the Creative Commons Attribution License, which
permits unrestricted use, distribution, and
reproduction in any medium, provided the original
author and source are credited.
Data Availability Statement: All relevant data are
within the manuscript and its Supporting
Information files.
Funding: SLC, 001, The Prorectorate for Graduate
Studies (PROPG) da Federal University of
Pernambuco – UFPE Coordination for the
Improvement of Higher Education Personnel
(CAPES); APQ-0249-4.08/20, Foundation for
Science and Technology Support from
PLOS ONE | https://doi.org/10.1371/journal.pone.0284911 April 27, 2023
Surface electromyography signal processing
and evaluation on respiratory muscles of
critically ill patients: A systematic review
Emanuel Fernandes Ferreira da Silva Junior ID1, Shirley Lima Campos2, Wagner
Souza Leite3, Pedro Vanderlei de Sousa Melo2, Rômulo Aquino Coelho Lins2, Maria das
Graças Rodrigues de Araújo2, Marcelo Renato Guerino ID1,2*
1 Translational Health Graduate Program, Federal University of Pernambuco—UFPE, Recife, Pernambuco,
Brazil, 2 Department of Physiotherapy, Federal University of Pernambuco—UFPE, Recife, Pernambuco,
Brazil, 3 Health-applied Biology Graduate Program, Federal University of Pernambuco—UFPE,
Pernambuco, Brazil
* marcelo.guerino@ufpe.br
Abstract
Background
Surface Electromyography (sEMG) has been used to monitor respiratory muscle function
and contractility in several clinical situations, however there is the lack of standardization for
the analysis and processing of the signals.
Objective
To summarize the respiratory muscles most assessed by sEMG in the critical care setting
and the assessment procedure details employed on those muscles regarding electrode
placement, signal acquisition, and data analysis.
Methods
A systematic review of observational studies was registered on PROSPERO (number
CRD42022354469). The databases included PubMed; SCOPUS; CINAHL, Web of Science
and ScienceDirect. Two independent reviewers ran the quality assessment of the studies
using the Newcastle-Ottawa Scale and Downs & Black checklists.
Results
A total of 311 participants were involved across the 16 studies, from which 62.5% (10)
assessed the diaphragm muscle and 50% (8) assessed the parasternal muscle with similar
electrode placement in both of them. We did not identify common patterns for the location of
the electrodes in the sternocleidomastoid and anterior scalene muscles. 12/16 reported
sample rate, 10/16 reported band-pass and 9/16 reported one method of cardiac-interfer-
ence filtering technique. 15/16 reported Root Mean Square (RMS) or derivatives as sEMG-
obtained variables. The main applicabilities were the description of muscle activation in dif-
ferent settings (6/16), testing of reliability and correlation to other respiratory muscles
1 / 16
PLOS ONE
Pernambuco (FACEPE) and 403341/2020-5,
National Council for Scientific and Technological
Development – CNPq / Ministry of Science,
Technology, Innovation and Communications /
Ministry of Health of Brazil – MoH MRG, 001, The
Prorectorate for Graduate Studies (PROPG) da
Federal University of Pernambuco – UFPE
Coordination for the Improvement of Higher
Education Personnel (CAPES).
Competing interests: The authors have declared
that no competing interests exist.
PLOS ONE | https://doi.org/10.1371/journal.pone.0284911 April 27, 2023
Surface electromyography of respiratory muscles in the critically ill
assessment techniques (7/16), and assessment of therapy response (3/16). They found
sEMG feasible and useful for prognosis purposes (2/16), treatment guidance (6/16), reliable
monitoring under stable conditions (3/16), and as a surrogate measure (5/16) in mechani-
cally ventilated patients in elective or emergency invasive procedures (5/16) or in acute
health conditions (11/16).
Conclusions
The diaphragm and parasternal muscles were the main muscles studied in the critical care set-
ting, and with similar electrodes placement. However, several different methods were observed
for other muscles electrodes placement, sEMG signals acquisition and data analysis.
1. Introduction
Surface Electromyography (sEMG) signals have been recognized as a technological instrument
for capturing respiratory myoelectric signals, and have been highlighted for the evaluation of
respiratory neuromuscular function. In 2002, the American Thoracic Society/European Respi-
ratory Society issued guidelines validating the use of sEMG signals as a method for analyzing
respiratory neural triggering [1].
Respiratory muscle dysfunction is common in critically ill patients, and can lead to acute
respiratory failure, also associated with increased hospital mortality, morbidity and hospital
stay [2]. Therefore, it is crucial to assess respiratory functions, including the activity of the dia-
phragm and other respiratory muscles. Surface electromyography (sEMG) is a useful non-
invasive asset that provides valuable information for monitoring the activity of these muscles
[3] during breathing in critically ill patients.
sEMG signals can be employed to identify patients who are at risk for respiratory failure,
monitoring the response to therapy, and guiding the timing of interventions [4,5]. Further-
more, they can offer insight into the patient’s level of effort during breathing [6], facilitate the
assessment of the effectiveness of various ventilation strategies [6,7] and thus contribute to
improving outcomes by allowing for earlier identification and intervention.
Despite the wide range of functionalities and benefits, the lack of standardization in sEMG
can create issues, such as data inconsistency [8], due to non-standardized procedures for elec-
trode placement, signal acquisition, and data analysis. This can lead to inaccurate diagnoses
and ineffective treatments resulting from potential misinterpretation of data and respective
errors. Moreover, limited comparability and replicability of sEMG protocols [9], which may
hinder evidence-based practices and jeopardize progress in the field.
In 1999, the Surface EMG for Non-Invasive Assessment of Muscle (SENIAM) project
aimed to integrate basic and applied research on sEMG for European cooperation. The project
resulted in recommendations for sensor placement procedures and signal processing for 27
muscle segments, however, respiratory muscles were not included [10]. Thus, bringing the
need for scientific evidence regarding the optimal sEMG procedures and analysis for respira-
tory muscles [11,12].
Based on the considerations presented, we conducted a systematic review of surface electro-
myography to address the following research questions:
1. What were the main respiratory muscles assessed through sEMG in the critical care setting?
2. What sEMG procedure details are described, regarding electrode placement, signal acquisi-
tion, and data analysis?
2 / 16
PLOS ONE Surface electromyography of respiratory muscles in the critically ill

2. Methods
2.1 Design
This study was conducted as a systematic review, adhering to the PRISMA (2020) guidelines
for reporting of systematic reviews and meta-Analysis [13] S4 Table. Details of the protocol for
this review were registered on PROSPERO (number CRD42022354469).

2.2 Data sources and search strategy

Five databases were searched for this review, including Medical Literature Analysis and
Retrieval System Online (Medline) of the United States National Library of Medicine
(PubMed), SCOPUS, Cumulative Index to Nursing and Allied Health Literature (CINAHL),
Web of Science and ScienceDirect. The bibliographic survey was conducted until August 11,
2022 with no restrictions on language or year of publication. The search terms were formu-
lated using adaptation to the PICO framework, and indexed terms from the Medical Subject
Headings (MeSH) metadata system were combined with and keywords, “surface electromyog-
raphy”; “respiratory muscles” and “intensive care unit”, to create a comprehensive search strat-
egy tailored to each database’s particularities, as described in S1 Appendix.

2.3 Eligibility criteria

The inclusion criteria for this study were as follows: (1) study design—observational studies,
including retrospective, prospective cohort, case-control, and cross-sectional; (2) assessment
instrument—respiratory assessment using sEMG; (3) population–adults aged 18 years or
older; (4) Condition: admitted to an intensive care unit. Studies that applied other methods of
muscle electrical activity assessment aside from sEMG, such as needle EMG, were excluded, as
well as those focusing solely on burn patients or patients requiring neuromuscular blockers, or
missing information of sEMG parameter configuration or signal processing.

2.4 Screening and data extraction

First, the eligible studies had their title and abstract screened using the Systematic Review-Ray-
yan [14] synthesis software by two independent reviewers (E. F. F. S. J. and W. S. L.). Secondly,
full-text screening was performed on the selected studies, and in cases of disagreement
between the pair of reviewers, a third assessor was consulted to resolve discrepancies. Finally,
the data extracted comprised: author, year, country, study objectives, study design, sample
characteristics, and sEMG data-related variables, such as respiratory muscles assessed, elec-
trode placement, signal acquisition, and data analysis. The flowchart of included and excluded
localized literature is represented using terms described in (Fig 1).

2.5 Quality assessment

The quality appraisal of observational studies was conducted using two checklists: Newcastle-
Ottawa [15] and Downs & Black scales [16]. The Newcastle-Ottawa scale comprises three
domains: selection, comparability, and exposure receiving scores from zero to nine. The result-
ing interval scores are used to qualify the studies into Good (7–9 points), Satisfactory (5–6
points), or Poor (0–4 points) quality [15]. The scale presents a slight difference in the scoring
system for case-control and cross-sectional studies.
The Downs & Black scale comprises a questionnaire consisting of 27 items categorized into
five domains: reporting (10 items), external validity (3 items), study bias (7 items), confound-
ing factors (6 items), and study power (1 item). The final items are scored as yes or no
responses. The final scores assigned to studies are used to determine their methodological

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PLOS ONE Surface electromyography of respiratory muscles in the critically ill

Fig 1. Identification of studies through databases according to Preferred Reporting Items for Systematic Reviews and Meta-
analyses (PRISMA).
https://doi.org/10.1371/journal.pone.0284911.g001

quality with scores categorized as: Excellent (26–28); Good (20–25); Righteous (15–19); and
Poor (�14) points [16].

3. Results
The total of 36,901 articles were initially screened, then reduced to 36,341 after excluding 560
duplicates. An additional 36,317 articles were excluded based on their failure to meet the inclu-
sion criteria after the title/abstract screening and further 8 articles were excluded due to miss-
ing information of sEMG parameter configuration or signal processing. As a result of this
screening process, 16 articles were included in this review (Fig 1).

3.1 Quality assessment

15 studies (93.75%) were scored as cross-sectional design and one study (6.25%) were scored
as case-control design. By using the Newcastle-Ottawa scale, 11 studies (68.75%) were rated as

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PLOS ONE Surface electromyography of respiratory muscles in the critically ill

Table 1. Quality assessment of the included studies.

Author, year, Country Study design Methodological quality (Score)
Newcastle-Ottawa Scale Downs & black Scale
Pozzi et al. (2022) [17], Cross-sectional 6 15
Italy (Satisfactory) (Fair)
Graßhoff et al. (2021) [18], Germany Cross-sectional 6 15
(Satisfactory) (Fair)
Bureau et al. (2021) [19], France Cross-sectional 7 15
(Good) (Fair)
Lokin et al. (2020) [20], Netherlands Cross-sectional 7 15
(Good) (Fair)
Roesthuis et al. (2020) [21], Netherlands Cross-sectional 7 16
(Good) (Fair)
Souza Costa et al. (2020) [22], Brazil Cross-sectional 7 15
(Good) (Fair)
Bellani et al. (2018) [6], Cross-sectional 5 15
Italy (Satisfactory) (Fair)
Duarte et al. (2017) [23], Cross-sectional 5 15
Brazil (Satisfactory) (Fair)
Sánchez et al. (2017) [24], Colombia Case-control 7 15
(Good) (Fair)
Ortega et al. (2017) [25], Colombia Cross-sectional 6 15
(Satisfactory) (Fair)
Walterspache et al. (2017) [26], Germany Cross-sectional 6 16
(Satisfactory) (Fair)
Cecchini et al. 2014 [27], Cross-sectional 6 15
France (Satisfactory) (Fair)
Schmidt et al. 2013 [28], Cross-sectional 5 17
France (Satisfactory) (Fair)
Tassaux et al. 2005 [29], Switzerland Cross-sectional 5 14
(Satisfactory) (Poor)
Tassaux et al. (2002) [30], Switzerland Cross-sectional 6 14
(Satisfactory) (Poor)
Imsand et al. 1994 [31], Switzerland Cross-sectional 5 12
(Satisfactory) (Poor)
https://doi.org/10.1371/journal.pone.0284911.t001

having “satisfactory” quality, while five studies (31.25%) were classified as “good” Table 1.
None of the studies were considered to be of poor methodological quality, as detailed in S1
and S2 Tables. Meanwhile, using the Downs & Black scale, 13 studies (81.25%) were classified
as having fair methodological quality, while three studies (18.75%) were considered to be of
“poor” quality, as outlined in S3 Table.

3.2 Outcome: sEMG processing variables for respiratory muscles

Table 2 shows the processing data for the sEMG analysis. Sampling rate was mentioned in
twelve studies (75%) obtaining variations between 500 and 10,000 Hz [6,17–19,21,23–
27,29,30], Bandpass filters were reported in 10 studies (62.5%) with variations between
0–1,000 Hz [6,17,19,21,22,24–27,31]. Only one study (6.25%) reported high-pass and low-pass
filters for EMG signal processing details [26].
Regarding cardiac-interference filtering techniques to prevent EMG noise contamination,
nine studies (50%) have reported a number of techniques, including gating [6,17,18,20,31], or
some sort of adaptive filter [21,25,30] or even visual inspection [26]. Amplifier gain is one of
the settings for high quality EMG signals with low noise. This setting is defined as the ratio
between the voltage that enters and exits the amplifier, should suit the characteristics of the

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PLOS ONE Surface electromyography of respiratory muscles in the critically ill

Table 2. Summary of respiratory muscle sEMG processing variables.

Author/Year Respiratory muscle sEMG processing data
Sample rate LPF HPF Band-pass CIF technique Amplifier Data acquisition Unit Measures Software
(Hz) (Hz) (Hz) (Hz) Gain duration
Pozzi et al. (2022) [17] 500 NR NR 0–200 Gating NR 180s μV RMS LabChat
Graßhoff et al. (2021) 1.000 NR NR NR Gating NR NR μV RMS NR
[18]
Bureau et al. (2021) 10.000 NR NR 40–500 NR NR 600s NR EMGMAX/ LabChart
[19] EMGAUC
Lokin et al. (2020) NR NR NR NR Gating NR 900s μV RMS MATLAB
[20] R2016a
Roesthuis et al. (2020) 2.048 NR NR 25–500 Wavelet-based NR 300s % EMGPEAK; MATLAB
[21] adaptive filter EMGAUC/min R2014b
Souza Costa et al. NR NR NR 20–500 NR NR 60s μV RMS NR
(2020) [22]
Bellani et al. (2018) 500 NR NR 0–200 Gating 20 NR μV RMS Dipha Software
[6]
Duarte et al. (2017) 500 NR NR NR NR NR NR NR RMS NR
[23]
Sánchez et al. (2017) 1.024 NR NR 20–500 NR NR 1.200s NR RMS NR
[24]
Ortega et al. (2017) 1.024 NR NR 10–500 RLS adaptive 5th- NR 180s NR NR NR
[25] order filter
Walterspacher et al. 10.000 500 1.000 20–1.000 Visual inspection 1000 120s % RMS LabChat v.7.2
(2017) [26]
Cecchini et al. (2014) 2.000 NR NR 10–1.000 NR 500 180s % RMS NR
[27]
Schmidt et al. (2013) NR NR NR NR NR NR NR NR EMGMAX; NR
[28] EMGAUC
Tassaux et al. (2005) 1.000 NR NR NR NR NR 60s NR EMG signal NR
[29]
Tassaux et al. (2002) 2.000 NR NR NR 50-Hz filter NR 600s NR EMGAUC AcqKnowledge
[30]
Imsand et al. (1994) NR NR NR 15–1.000 Manual gating NR 60s % EMG signals NR
[31]

LPF: Low-pass filter; HPF: High-pass filter; CIF: Cardiac-interference filtering; NR: Not reported; RMS: Root mean square; EMG: Electromyogram; EMGAUC: Area
under the EMG signal curve; EMGmax: The difference between the maximum amplitude of RMS signal and its baseline; EMGpeak: Peak of muscle activity during
inspiration; EMGAUC/min: End of muscle activity per breath.

https://doi.org/10.1371/journal.pone.0284911.t002

experiment, the type of electrodes used, as well as the muscle studied, and not the adjusted to
exceed the voltage expected from the system [32]. Gain was mentioned in three studies
(18.75%) with variations between 20–1,000 times [6,26,27]. EMG data acquisition recording
reported by twelve studies (75%) varied from 60 through 1.200 seconds [17,19–22,24–27,29–
31] Table 2.
Regarding the sEMG signal units, five papers (31.25%) [6,17,18,20,22] presented them in
microvolts (μV), four studies (25%) [21,26,27,31] in percentages, and eight studies (50%) did
not inform any unit [19,23–25,28–31]. The obtained variables were presented as simple mean
RMS/EMG signal usually rectified or normalized [6,17–20,22–24,26,27,29] or integrated RMS/
EMG signals—the difference between the maximum amplitude of RMS signal and its baseline
(EMGMAX), area under the EMG signal curve (EMGAUC), peak of muscle activity during inspi-
ration (EMGPEAK), and end of muscle activity per breath (EMGAUC/min) [19,21,28,30,31]
Table 2.

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PLOS ONE Surface electromyography of respiratory muscles in the critically ill

For software dedicated to sEMG signal offline analysis, only seven (43.75%) reported which
one they used. Labchart was the most reported by three studies (18.75%) [17,19,26], followed
by two reporting Matlab (12.5%) [20,21] and two reporting Dinha (6.25%) [6], and Acqknow-
ledge (6.25%) [30] Table 2.

3.3 Outcomes: Characteristics of the studies, technical parameters of sEMG

of the respiratory muscles and clinical applicability
A total of 311 participants were involved across the 16 studies, with 15 studies (66.2%) report-
ing male participants as the majority. The average age of the participants ranged from
62.1 ± 10.56 years Table 3.
According to the objectives of the included studies, the applicability of sEMG used in
mechanically ventilated patients can be summarized to the following categories, description
muscles activation in different settings [17,21–23,28,31], testing of reliability and correlation
to other respiratory muscles assessment techniques [6,18,20,24–27] and assessment of therapy
response [19,29,30]. These studies have found that sEMG was feasible and resourceful tool for
prognosis purposes [17,22] treatment guidance [19,26,27,29–31], reliable monitoring under
stable conditions [20,23,28] and as surrogate measure [6,18,21,24,25] Table 3.
The mechanically ventilated patients’ scenarios for sEMG assessment employment were
either in the elective or emergency invasive procedures [18,20,23,25,26] or in acute health con-
ditions [6,17,19,21,22,24,27–30] Table 3.
Scalene muscles (ESC) were analyzed in four studies (25%) [21,22,27,28] however, informa-
tion related to electrode placement was described in only three studies (18.75%), guided by
ultrasound positioned in the lower region of the muscle third [21], positioned in the posterior
triangle of the neck, at the level of the cricoid cartilage [27] and in bilateral recordings, posi-
tioned in the posterior triangle of the neck at the level of the cricoid cartilage, between the ster-
nocleidomastoid muscle and the clavicle [28]. Some studies did not provide sufficient
information to determine placement [22] Table 3.
Sternocleidomastoid (SCM) muscle analysis was performed in seven studies (43.7%)
[6,17,21,22,24,30,31], therefore, information related to electrode placement was described in
only six studies (37.5%) rejecting each other, being its placement in the middle third, identified
by palpation on the right or left side, generally opposite to the medications due to the fixation
of the central venous catheter [6,17], guided by ultrasound in the lower third of the muscle
[21], 20% of the distance between the mastoid apophysis and the sternal furcula [39], posi-
tioned over the muscle “palpation” and the mastoid process [30] and fixed on the muscle body
[31]. The other studies did not provide information to determine the placement [22] Table 3.
The terminology referring to the parasternal has been characterized by the intercostal por-
tion parallel to the sternum, however, it may be linked to the intercostal muscles, referring to
the fibers parallel to the sternum [33–35]. The selected papers described and analyzed the para-
sternal muscles in eight studies (50%), under the positioning in the second intercostal space
[6,17–19,21,26,28], and electrodes placed in the fifth intercostal space in the posterior axillary
line2, however only [6,17,18,26] placed the electrodes bilaterally Table 3.
The positioning of the electrodes on the Diaphragm (DIA) was measured in ten studies
(62.5%), attached to the lower intercostal spaces in the midclavicular line
[6,17,18,20,22,24,25,29] that of these only three studies analyzed the right hemibody [22,24,25]
and positioning two electrodes in the paraxiphoid region, 5 cm below the xiphoid process, and
the other 2, in the bilateral costal margin region, with a distance of approximately 16 cm
between them [23,26]. Only one study (6.25%) reported analyzing the Rectus Abdominal mus-
cle with its positioning on the left midclavicular line, at the level of the umbilicus [17] Table 3.

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PLOS ONE Surface electromyography of respiratory muscles in the critically ill

Table 3. Summary of sample characteristics, technical parameters of sEMG of the respiratory muscles, clinical use and respective studies’ findings.
Author, year, Objective
Country
Pozzi et al. To describe respiratory muscle
(2022) [17], Italy activation by sEMG during an
spontaneous breathing trial and to
assess their electrical activity in
successful vs. failing weaning
patients.
Graßhoff et al. To investigate the estimation of the
(2021) [18], pressure-time product of
Germany inspiratory muscle pressure via
sEMG by identifying a patient-
specific conversion factor during
end-expiratory occlusions.
Sample characteristics
N. of participants: 37.
Age: 56 (50–62).
Sex: M: 27/ F: 10.
Condition: COPD, Diabetes,
ARDS, atrial fibrillation,
Septic shock.
Inclusion criteria: Patients
who were on IMV for > 48 h
eligible for spontaneous
breathing trial.
N. of participants: 43.
Age: 64 ± 11.
Sex: M: 34/ F: 9.
Condition: Patients scheduled
for elective bronchoscopy.
Inclusion criteria: Intubated,
moderate/deep sedation level,
on assisted spontaneous
ventilation.
Body position, skin electrode
placement and muscles assessed Main findings
Body position: Not reported. Respiratory muscles’ electrical
Reference electrode: Not reported. activity increased during
Inter electrode distance: Not spontaneous breathing trial.
reported. Recruitment of expiratory muscles
Diaphragm: Lower costal margin, quantified by sEMG is associated
bilaterally on the midclavicular line. with this trial failure.
Parasternals: 2nd intercostal space,
bilaterally in the parasternal line.
Sternocleidomastoid: In the middle
third of the sternocleidomastoid
muscle, on the right or left side
(usually opposite the central venous
line).
Rectus abdominis: On the left
midclavicular line, at the level of the
umbilicus.
Body position: Not reported. sEMG was well correlated with
Reference electrode: Sternum. pressure-time product. sEMG can be
Inter electrode distance: Not used as a non-invasive alternative for
reported. monitoring the patients’ inspiratory
Diaphragm: Bilaterally at the lower effort under assisted mechanical
costal margin on the midclavicular ventilation.
line.
Parasternals: Bilaterally in the 2˚
intercostal space on the parasternal
line.

Bureau et al. To evaluate the respective impact of N. of participants: 34. Body position: Not reported. Parasternal intercostal muscles
(2021) [19], customized PAV and PSV settings Age: 66 (57–77). Reference electrode: Not reported. electrical activity and asynchrony
France on patient-ventilator asynchrony. Sex: M: 25 / F: 9. Inter electrode distance: 2 cm. index were lower with PAV and
Condition: Patients on PSV Parasternals: 2˚ intercostal space other PSV modes. Mechanical
under IMV for > 24 h, for lateral to the estrum. ventilation modes did not decrease
respiratory cause with Alae nasi muscles: Placed on the dyspnea and activity of muscles,
hypoxemia. lateral surfaces of the nose. even though PAV was able to reduce
Inclusion criteria: Sedated in asynchrony more effectively.
IMV.
Lokin et al. To compare the ability of N. of participants: 15. Body position: Not reported. sEMG was not reliable for breathing
(2020) [20], diaphragm activity detection Age: 62 (45–72). Reference electrode: Sternum. effort detection in subjects who were
Netherlands between surface electromyography Sex: M: 9 / F: 6. Inter electrode distance: Not invasively ventilated compared with
of the diaphragm and Condition: Adults with reported. transesophageal electromyography.
transesophageal electromyography clinical complications, Diaphragm: Bilaterally below the In stable recordings, however, both
of the diaphragm. elective and emergency front and lower dorsal ribs. of the methods had excellent
surgery. temporal correlation and good
Inclusion criteria: At least 48 agreement.
h of IMV in PSV.
Roesthuis et al. To investigate the effect of different N. of participants: 17. Body position: Not reported. Extradiaphragmatic inspiratory
(2020) [21], inspiratory support levels on the Age: 64 ± 8.2. Reference electrode Patient’s pulse. muscle activity increases in response
Netherlands recruitment pattern of Sex: M: 12 / F: 5. Inter electrode distance: Not to lower inspiratory support levels.
extradiaphragmatic inspiratory Condition: COPD, reported. However, there is a poor correlation
muscles and to evaluate agreement pneumonia, ARDS, Scalenes/Sternocleidomastoid: Lower and agreement with the change in
between activity of abdominal aortic aneurysm. third of the muscles. diaphragm activity.
extradiaphragmatic inspiratory Inclusion criteria: At least 3 Parasternals: 2nd intercostal space, 3
muscles and the diaphragm. days in IMV, light/some deep cm lateral to the sternum.
sedation. Alae nasi muscles: Placement of an
electrode in each nostril
Genioglossus: Below the chin and
above the hyoid bone.
(Continued )

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Table 3. (Continued)
Author, year, Objective
Country
Souza Costa To analyze the respiratory muscle
et al. (2020) [22], groups involved with the timed
Brazil inspiratory index index utilizing the
sEMG.
Bellani et al. To assess the reliability of sEMG of
(2018) [6], Italy the respiratory muscles for
monitoring diaphragm electrical
activity and subject effort during
assisted ventilation.
Duarte et al. To evaluate the diaphragmatic
(2017) [23], surface electromyography of
Brazil postoperative liver transplantation
subjects.
Sánchez et al. To assess the engagement of the
(2017) [24], respiratory muscles as an index
Colombia during spontaneous breathing trial
and to associate the level of
engagement with the muscular
weakness in poisoned patients.
PLOS ONE | https://doi.org/10.1371/journal.pone.0284911 April 27, 2023
Sample characteristics
N. of participants: 46.
Age: 80 (71–87).
Sex: M: 26 / F: 20.
Condition: Sepsis, acute
respiratory failure, stroke and
heart failure.
Inclusion criteria: Patients
who were on IMV for > 24 h,
clinically ready for the
weaning process.
N. of participants: 14.
Age: 56 ± 12.
Sex: M: 12 / F:2.
Condition: Pneumonia,
ARDS, sepsis, trauma.
Inclusion criteria: Patients
intubated or tracheostomized
in PSV mode.
N. of participants: 14.
Age: 57 ± 7.1.
Sex: M: 10 / F:4.
Condition: Liver
transplantation.
Inclusion criteria: Patients
eligible for extubation in
PSV.
Case group
N. of participants: 23.
Age: 30.3 ± 10.
Sex: M: 14 / F:9.
Condition: Patients poisoned
by organophosphate.
Inclusion criteria: Patients
who were on IMV during
spontaneous breathing trial.
Control group
N. of participants: 28.
Age: 27 ± 6.5.
Sex: M: 21/ F:7.
Condition: Healthy patients.
Inclusion criteria: Received
non-invasive ventilation for
900 second.
Surface electromyography of respiratory muscles in the critically ill
Body position, skin electrode
placement and muscles assessed Main findings
Body position: 45˚. Subjects succeeding in a weaning
Reference electrode: Not reported. trial had higher muscle strength. A
Inter electrode distance: Not vigorous diaphragm with low fatigue
reported. potential seems essential for
Diaphragm: In the lower intercostal successful weaning.
spaces on the right side of the body, in
the midclavicular line.
Scalenes: Not reported.
Sternocleidomastoid: Not reported.
External intercostals: In the 5th
intercostal space on the posterior
axillary line.
Body position: Not reported. Diaphragm activity can be reliably
Reference electrode: Not reported. monitored by both electrical activity
Inter electrode distance: Not measured by nasogastric tube with
reported. electrodes and sEMG.
Sternocleidomastoid: Middle third of
the SCM muscle.
External intercostals: 2th intercostal
space, bilaterally on the parasternal
line, for parasternal external
intercostal muscles.
Diaphragm: Inferior costal margin,
bilaterally in the midclavicular line,
for costal diaphragm.
Body position: 35˚. There were significant differences
Reference electrode: Not reported. between the root mean square of the
Inter electrode distance: 16 cm. diaphragm domes under mechanical
Diaphragm: Two electrodes in the ventilation and after extubation,
paraxiphoid region, 5 cm below the showing lower effectiveness of the
xiphoid process, and the other 2, in diaphragm muscle against
the region of the bilateral costal resistance.
margin, with approximately 16 cm
between them.
Body Position: Not reported. Engagement of respiratory muscles
Reference electrode: Not reported. index is a promising index to assess
Inter electrode distance: Not the level of participation of
reported. respiratory muscle on spontaneous
Diaphragm: Anterolateral portion of breathing test in patients poisoned,
the thorax, between the 6th and 8th which could improve the extubation
intercostal space, between the mid- prognosis for these patients.
axillary line and the external clavicular
line
Sternocleidomastoid: 20% of the
distance between the mastoid
apophysis and the sternal notch.
(Continued )
9 / 16
PLOS ONE
Table 3. (Continued)
Author, year, Objective
Country
Ortega et al. To evaluate the feasibility of sEMG
(2017) [25], derived indexes in predicting
Colombia weaning outcomes among
mechanically ventilated subjects
after cardiac surgery.
Walterspache To assess the acute effects on the
et al. (2017) [26], neural respiratory drive measured
Germany by sEMG and the diaphragm in
different body positions during
mechanical ventilation.
Cecchini et al. To compare electrical activity of
2014 [27], diaphragm, scalene, and alae nasi,
France according to the ventilatory mode
and assist level.
Schmidt et al. To determine if sEMG of
2013 [28], extradiaphragmatic inspiratory
France muscles vary with PSV settings and
relate to the degree of discomfort
and the intensity of dyspnea in
acutely ill patients.
Tassaux et al. To test the hypothesis that
2005 [29], increasing the expiratory trigger set-
Switzerlan point could reduce the magnitude
of intrinsic PEEP, the number of
non triggering breaths, the level of
inspiratory effort and triggering
delay.
PLOS ONE | https://doi.org/10.1371/journal.pone.0284911 April 27, 2023
Sample characteristics
N. of participants: 10.
Age: 63.14 ± 16.9.
Sex: M: 10.
Condition: Postoperative
cardiac surgery.
Inclusion criteria: Clinically
stable ready for IMV
weaning.
N. of participants: 9.
Age: 66 ± 18.
Sex: M: 6 / F: 3.
Condition: Lung
transplantation and stroke.
Inclusion criteria:
Tracheostomized patients
hemodynamically stable in
spontaneous breathing trial.
N. of participants: 12.
Age: 68 ± 8.
Sex: Not reported.
Condition: Patients with
acute respiratory failure,
pneumonia, ARDS,
pulmonary edema, septic and
cardiogenic shock
Inclusion criteria: Adults in
IMV capable of triggering
PSV/NAVA.
N. of participants: 12.
Age: 60 ± 15.
Sex: M: 9 / F: 3.
Condition: Patients with
pneumonia, COPD and
septic shock.
Inclusion criteria: Patients
intubated or tracheostomized
in IMV weaning process.
N. of participants: 10.
Age: 68.7 ± 10.
Sex: M: 7 / F: 3.
Condition: Patients with
acute respiratory failure with
COPD Inclusion criteria:
Intubated patients in IMV
weaning phase.
Surface electromyography of respiratory muscles in the critically ill
Body position, skin electrode
placement and muscles assessed
Body position: Not reported.
Reference electrode: Not reported.
Inter electrode distance: Not
reported.
Diaphragm: Between the 7th and 8th
intercostal spaces between the
midaxillary line and the external
clavicular line.
Body position: Supine (lying down),
semi-sitting at 30˚ and sitting at 80˚ in
bed.
Reference electrode: Not reported.
Inter electrode distance: 2cm.
Diaphragm: Bilaterally on the lower
costal margin, 16 cm lateral to the
common electrode, placed 5 cm
cranial to the xiphoid.
Parasternals: Bilaterally in the 2nd
intercostal space.
Body position: Not reported.
Reference electrode: Not reported.
Inter electrode distance: Not
reported.
Scalenes: In the posterior triangle of
the neck, at the level of the cricoid
cartilage.
Alae nasi muscles: They were
obtained by placing an electrode in
each nostril.
Body position: Not reported.
Reference electrode: Not reported.
Inter electrode distance: Not
reported.
Scalenes: Bilateral registers,
positioned in the posterior triangle of
the neck at the level of the cricoid
cartilage, between the
sternocleidomastoid muscle and the
clavicle.
Parasternals: Bilateral records,
positioned in the 2nd intercostal
space, close to the sternum.
Alae nasi muscles: Placement of an
electrode in each nostril.
Body position: Not reported.
Reference electrode: Sternum.
Inter electrode distance: Not
reported.
Diaphragm: Bilaterally on the costal
margin.
Main findings
The obtained indexes show a
correlation between high
expenditure and weaning test failure.
sEMG is becoming a promising
procedure for assessing the state of
mechanically ventilated patients.
Diaphragm’s electrical activity
changed under spontaneous
breathing from supine to sitting and
between semirecumbent to sitting.
Body positioning influences
respiratory drive to the diaphragm
in tracheotomized patients during
unassisted breathing.
NAVA and PSV both reduced
extradiaphragmatic inspiratory
muscle activity, in proportion to the
level of assistance. NAVA resulted in
a predominant contribution of the
diaphragm to inspiratory effort.
sEMG of extradiaphragmatic
inspiratory muscles provides a
reliable and non-invasive indicator
of respiratory muscle loading/
unloading in mechanically ventilated
patients. It is strongly correlated to
the intensity of dyspnea, and could
be used as a surrogate of respiratory
sensations.
Setting expiratory trigger at a higher
percentage of peak inspiratory flow
in patients with obstructive disease
during pressure support improves
patient–ventilator synchrony and
reduces inspiratory muscle effort.
(Continued )
10 / 16
PLOS ONE Surface electromyography of respiratory muscles in the critically ill

Table 3. (Continued)

Author, year, Objective Sample characteristics Body position, skin electrode

Country
Tassaux et al. To compare the effects of ASV and
(2002) [30], SIMV-PS modes on patient-
Switzerlan ventilator interactions in
mechanical ventilation.
Imsand et al. To assess quantitatively the effect of
1994 [31], varying the level of machine
Switzerland assistance on the electrical activity
amplitude of inspiratory muscles.
N. of participants: 10.
Age: 71 ± 9.6.
Sex: F: 6 / M: 4.
Condition: Patients with
COPD exacerbation, acute
pneumonia, asthma and
sepsis.
Inclusion criteria: Intubated
patients in weaning
procedure by SIMV-PS or
ASV mode.
N. of participants: 5.
Age: 58.6 ± 8.
Sex: M: 1 / F: 4.
Condition: COPD
Inclusion criteria: intubated
patients, hemodinamically
stable, conscious and not
sedated.
placement and muscles assessed
Body position: Not reported.
Reference electrode: Not reported.
Inter electrode distance: Not
reported.
Sternocleidomastoid: Placed over the
muscle (palpation) and the mastoid
process.
Body position: 45˚.
Reference electrode: Not reported.
Inter electrode distance: Not
reported.
Sternocleidomastoid: Muscle body.
Main findings
ASV provided levels of minute
ventilation comparable to those of
SIMV-PS. Central respiratory drive
and sternocleidomastoid activity
were markedly reduced in ASV,
suggesting decreased inspiratory
load and improved patient-ventilator
interactions.
The durations of electrical activation
and the integrated electromyograms
of diaphragm and
sternocleidomastoid were similar in
successive spontaneous and assisted
breaths, neither changed with
increasing level of machine
assistance.

ARDS: Acute respiratory distress syndrome; cm: Centimeters; COPD: Chronic obstructive pulmonary disease; sEMG: Surface electromyography; ICU: Intensive care
unit; IMV: Invasive mechanical ventilation; PEEP: Positive end-expiratory pressure; NAVA: Neurally adjusted ventilatory assist; PAV: Proportional assist ventilation;
PSV: Pressure support ventilation; ASV: Adaptive support ventilation; SIMV-PS: Synchronized intermittent mandatory ventilation plus pressure support, F: Female; M:
Male; mm: Millimeters; RMS: Root mean square.

https://doi.org/10.1371/journal.pone.0284911.t003

The alae nasi muscles were analyzed in only four studies (25%) [19,21,27,28] with its elec-
trodes for electromyographic capture placed in each nostril. The genioglossus muscle was ana-
lyzed in only one study (6.25%), reliably reporting its positioning, characterized below the
chin and above the hyoid bone [21]. In relation to the reference electrode, only four studies
(25%) reported its placement, three studies (18.75%) under the sternum [18,20,29], and one
study (6.25%) attached to the patient’s wrist [21].
The interelectrode distance affects the signal quality and determines the volume of muscle
fibers that will be measured, therefore, affecting the selectivity of recording. This parameter
was reported in three studies (18.75%) which reported its distance of 2 cm [19,26] and 16 cm
[23]. Four studies (25%) reported the angle positioning of patients: 35˚ [19], 45˚ [22,31] and in
three different body positions, supine at 0˚, semirecumbent at 30˚ and sitting at 80˚ on the bed
[26] Table 3.

4. Discussion
This review presents findings indicating that the diaphragm and parasternal muscles were the
most commonly used for assessing respiratory function through sEMG in critically ill patients
admitted to the ICU. To the best of our knowledge, this is the first systematic review to com-
prehensively summarize the methodological aspects of the evaluation protocols and sEMG sig-
nals processing of respiratory muscles in patients admitted to the ICU.
Upon analyzing the respiratory electromyographic data processing and analysis procedures
in the included studies, it was found a lack of standardization in the target respiratory muscles,
electrode placement and data acquisition details. Therefore, the studies could not be subjected
to quantitative analyses or meta-analyses. A wide range of significant variation in the anatomi-
cal sites for skin electrode placement, especially for muscles underlying other larger muscles.

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PLOS ONE Surface electromyography of respiratory muscles in the critically ill

This could be minimized by implementing other resources, such as ultrasound guidance, as

demonstrated by Roesthuis et al. [21], although Imsand et al. [31] presented some respiratory
muscles feasible to be tracked for electrode placement by palpating muscle body.
The diaphragm and parasternal muscles were the most common for sEMG assessment in
critically ill patients in the ICU, likely due to their crucial role in respiratory function. The dia-
phragm electromyogram provides a sensitive measure of neural respiratory drive with each
breath and reflects the imposed load on respiratory muscles [36]. Similarly, the parasternal
intercostal muscles are obligatory during respiration [37] and are the first external respiratory
muscles to respond to an increased demand. Electrodes for diaphragm sEMG are typically
placed in the 7th or 8th intercostal spaces along the midclavicular line, which is the zone of
apposition where the active diaphragm thickens with consequent lung volume increase during
breathing [38,39]. For the parasternal muscles, electrodes are typically placed in the 2nd or 3rd
intercostal spaces along the midclavicular line. However, the historical summary of different
locations has challenged the consistency and reliability of its sEMG signals, particularly with
the interference of the large pectoralis major muscle [38]. This site for sEMG of parasternal
has been studied through ultrasound imaging and it was found to be an area audible and visi-
ble for single motor unit activity with an acceptable signal-to-noise ratio [39].
The use of sEMG in critically ill patients undergoing invasive mechanical ventilation may
provide a reliable assessment tool, however, it must be used with caution as the ventilatory
modes can affect the observed results. For example, Roesthuis et al. [21], reported that the
activity of the extra diaphragmatic inspiratory muscles increases when they remain at lower
levels under support pressure. Furthermore, Cecchini et al. [27] showed that increasing levels
of ventilatory support pressure and Neurally Adjusted Ventilatory Assist (NAVA) reduced the
electrical activity of the diaphragm, scalene and alae nasal muscles. Nevertheless the study con-
ducted by Bellani et al. [6] reported that electrical activity of the diaphragm, evaluated using
sEMG, can be reliably used during ventilation with pressure support as it was analyzed and
correlated with esophageal electrical measures. Additionally, Imsand et al. [31] study demon-
strated that the duration of diaphragm and sternocleidomastoid electrical activities were simi-
lar with successive spontaneous and assisted breaths, except that the use of ventilation with
support pressure has been preventing diaphragmatic fatigue [40].
Regarding patient positions during sEMG analysis, only the study conducted by Walterspa-
cher et al. [26], revealed that the diaphragm muscle is the most active in supine and semi-sit-
ting positions, while having reduced activation in the sitting position. The authors explained
this phenomenon by attributing it to the compensation mechanism for changes in the length-
tension of the diaphragm by the changes of body position, which unloads the diaphragm.
Systematic reviews of sEMG protocols in healthy individuals [11] adults and the elderly
[12], were fundamental to research the evidence for sEMG in the ICU. A similar pattern was
noticed with the immense variability of sEMG protocols and analyzes. In the context of the
ICU, Abunurah et al. [5] performed a systematic review, not including details for processing
sEMG or placing surface electrodes on the respiratory muscles, as described in the present sys-
tematic review.
During breathing in the upright position, other muscles besides the diaphragm are
recruited, such as the scalenes and the parasternal intercostals. According to respiratory physi-
ology, when high requirements for increased lung ventilation are present, recruitment of
accessory respiratory muscles is required, characterized by the sternocleidomastoid and exter-
nal intercostal muscles [11,41,42]. Although sEMG is an easy-to-apply and sensitive tool for
capturing muscle activity, it has some disadvantages, such as susceptibility to interference
from activities in other muscle groups (cross-talk) and limited standardization for analysis and
processing of recorded sEMG signals [43].

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PLOS ONE Surface electromyography of respiratory muscles in the critically ill

This systematic review introduces some limitations that require careful consideration. The
inconsistency of methods and data reports in the included studies restricted the possibility of
conducting meta-analyses. For instance, some studies did not report any effect size measures
with EMG signals, leading to an incomplete data assessment. Another fact is that despite the
joint statement of ATS/ERS in 2002, which one of the goals was to promote standardization of
techniques for assessing respiratory muscle function, including electromyographic methods,
minimal adherence to this guideline was observed in the published studies.
Moreover, there is a lack of comparative evidence for different analysis techniques and
removal strategies of motion artifacts, resulting in uncertainty regarding the best approach for
reliable clinical inferences. Limited number of software is currently available to address the
detection and removal of motion artifacts, and even manual inspection for noises has been
reported. Once adequate signal processing is achieved, further research is needed to study the
incorporation strategies of sEMG into clinical practices, including ICU.

5. Conclusion
The diaphragm and parasternal muscles are the most studied muscles in the cited protocols in
the ICU setting, as well as their electrode placement patterns. There is significant variation in
the methods and tools used for analyzing and processing of respiratory sEMG signals. The use
of RMS appears to be essential in identifying muscle contractility behavior at different settings.
Although clinical studies have provided useful information about the positions and analyses of
respiratory sEMG in the ICU. Further studies are warranted to better explore the muscles
physiological aspects in such a vulnerable population and tailor strategies to increase their
chances of better outcomes.

Supporting information
S1 Appendix. Full search strategy.
(DOCX)
S1 Table. Results of the critical appraisal using the Newcastle-Ottawa scale adapted for
cross-sectional studies.
(DOCX)
S2 Table. Results of the critical appraisal using the The Newcastle-Ottawa scale (NOS) for
case-control study.
(DOCX)
S3 Table. Risk of bias assessment assessed by the Downs and Black.
(DOCX)
S4 Table. PRISMA checklist.
(PDF)

Author Contributions
Conceptualization: Emanuel Fernandes Ferreira da Silva Junior, Shirley Lima Campos, Wag-
ner Souza Leite.
Data curation: Emanuel Fernandes Ferreira da Silva Junior, Wagner Souza Leite.
Formal analysis: Emanuel Fernandes Ferreira da Silva Junior, Wagner Souza Leite, Pedro
Vanderlei de Sousa Melo, Rômulo Aquino Coelho Lins.

PLOS ONE | https://doi.org/10.1371/journal.pone.0284911 April 27, 2023 13 / 16

PLOS ONE Surface electromyography of respiratory muscles in the critically ill

Funding acquisition: Marcelo Renato Guerino.

Investigation: Emanuel Fernandes Ferreira da Silva Junior, Wagner Souza Leite.
Methodology: Emanuel Fernandes Ferreira da Silva Junior, Wagner Souza Leite.
Project administration: Emanuel Fernandes Ferreira da Silva Junior.
Resources: Emanuel Fernandes Ferreira da Silva Junior, Marcelo Renato Guerino.
Software: Emanuel Fernandes Ferreira da Silva Junior.
Supervision: Shirley Lima Campos, Maria das Graças Rodrigues de Araújo, Marcelo Renato
Guerino.
Validation: Emanuel Fernandes Ferreira da Silva Junior, Shirley Lima Campos, Wagner Souza
Leite, Marcelo Renato Guerino.
Visualization: Emanuel Fernandes Ferreira da Silva Junior, Shirley Lima Campos, Wagner
Souza Leite, Marcelo Renato Guerino.
Writing – original draft: Emanuel Fernandes Ferreira da Silva Junior, Shirley Lima Campos,
Wagner Souza Leite, Rômulo Aquino Coelho Lins.
Writing – review & editing: Emanuel Fernandes Ferreira da Silva Junior, Shirley Lima Cam-
pos, Wagner Souza Leite, Maria das Graças Rodrigues de Araújo, Marcelo Renato Guerino.

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