Accepted Manuscript

Surface electromyography (sEMG) of extradiaphragm respiratory muscles in

healthy subjects: a systematic review

Elis E.A. Cabral, Guilherme A.F. Fregonezi, Luana Melo, Nada Basoudan,
Sunita Mathur, W Darlene Reid

PII: S1050-6411(17)30459-5
DOI: https://doi.org/10.1016/j.jelekin.2018.07.004
Reference: JJEK 2223

To appear in: Journal of Electromyography and Kinesiology

Received Date: 28 November 2017

Revised Date: 4 July 2018
Accepted Date: 17 July 2018

Please cite this article as: E.E.A. Cabral, G.A.F. Fregonezi, L. Melo, N. Basoudan, S. Mathur, W. Darlene Reid,
Surface electromyography (sEMG) of extradiaphragm respiratory muscles in healthy subjects: a systematic review,
Journal of Electromyography and Kinesiology (2018), doi: https://doi.org/10.1016/j.jelekin.2018.07.004

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 JEK 2017 380

Surface electromyography (sEMG) of extradiaphragm respiratory muscles in healthy subjects: a

systematic review.

Elis E.A. Cabrala, Guilherme A.F. Fregonezia,b, Luana Melod,

Nada Basoudanc, Sunita Mathurd,e, W Darlene Reid d,e, f,*

a
Laboratório de Desempenho PneumoCardioVascular e Músculos Respiratórios, Departamento de Fisioterapia,
Universidade Federal do Rio Grande do Norte (UFRN), Natal, RN, Brazil
b
PneumoCardioVascular Lab, Hospital Universitário Onofre Lopes, Empresa Brasileira de Serviços
Hospitalares (EBSERH), UFRN, Natal, RN, Brazil
c
Princess Nourah bint Abdulrahman University, Riyadh, Kingdom of Saudi Arabia
d
Department of Physical Therapy, University of Toronto, Toronto, ON, Canada
e
Toronto Rehabilitation Institute, Toronto, ON, Canada
f
Interdepartmental Division of Critical Care Medicine, University of Toronto, Toronto, ON, Canada

Keywords: Electromyography; Respiratory Muscles; Healthy Volunteers; Breathing Exercises

*
Corresponding author
W Darlene Reid
Department of Physical Therapy,
University of Toronto,
Toronto, ON, Canada

Email address: darlene.reid@utoronto.ca

Phone +1 416 946-3941

Conflicts of interest
The authors declare that there are no conflicts of interest.

Acknowledgements
Nada Basoudan was supported by a fellowship from the Royal Embassy of Saudi Arabia.

Page 1 of 44
Abstract

The aim of this systematic review was to examine procedures used and outcome measures reported

from surface EMG (sEMG) of extradiaphragm inspiratory muscles in healthy people. Relevant

articles were searched using the concepts “electromyography (EMG)”, “respiratory muscles”

(sternocleidomastoid [SM], scalene, intercostal [IC] and parasternal) and “healthy” in the electronic

databases: MEDLINE, PubMed, EMBASE, Cochrane CENTRAL and Database of Systematic

Reviews, CINAHL, SPORTDiscus, LILACS, and PEDro. Twenty-five papers were included and

quality assessment was performed using an adapted Downs and Black checklist. Twenty-eight

percent of included papers were classified as moderate quality and the rest were low quality. The SM

was the muscle most often investigated. Description of EMG techniques were often incomplete for

features such as the procedure before electrode placement, description of the surface electrodes, the

EMG detection mode and amplification. Of note, descriptions of the IC muscle electrode positioning

varied widely. Comparison of outcomes among studies was challenging because of the very diverse

EMG outcomes reported. There are many controversies regarding methods and technique used to

assess sEMG of extradiaphragm inspiratory muscles. Therefore, studies with higher methodological

quality utilizing standardized EMG procedures including electrode positioning will enable accurate

and reliable comparison among studies of the extradiaphragm inspiratory muscles.

Page 2 of 44
 Contents

1. Introduction…………………………………………………………………………………... 4
2. Methods………………………………………………………………………………………. 6
2.1. Search strategy................................................................................................................ 6
2.2. Study criteria and data abstraction……………………………………………………. 7
2.3. Quality assessment……………………………………………………………………. 8
3. Results....................................................................................................................................... 8
3.1. Study selection………………………………………………………………………… 8
3.2. Quality assessment…………………………………………………………………….. 9
3.3. Characteristics of participants…………………………………………………………. 9
3.4. Characteristics of protocols of MIP and/or acute bout of respiratory muscles loading 9
3.5. sEMG of extradiaphragm respiratory muscles and electrode position .....……….. 10
3.6. sEMG procedures and outcomes……………………………………………….…….. 11
4. Discussion................................................................................................................................. 15
Limitations section................................................................................................................. 21
5. Conclusion…………………………………………………………………………………… 22
Conflicts of Interest………………………………………………………………………… 22
References……………………………………………………………………………...…… 22
Appendix A………………………………………………………………………………….
Appendix B………………………………………………………………………………….

Page 3 of 44
1. Introduction

The respiratory muscles are vital for life to produce adequate ventilation and gas exchange.

Contraction of respiratory muscles creates a negative pressure gradient that results in an inflow of air

into the lungs (Green and Moxham, 1985). The diaphragm performs the largest portion of

inspiratory work in healthy people although several muscles contribute to inspiration and

expiration (Reid and Dechman, 1995). Other primary muscles of inspiration recruited during tidal

breathing in upright persons are the scalenes (SC) and the parasternal intercostals (PI). Inspiratory

muscles recruited at higher levels of ventilation are defined as accessory. Accessory muscles that

provide a considerable contribution to the respiratory pump are the sternocleidomastoid (SM) and

external intercostal (IC) muscles (DeTroyer and Estenne, 1984; 1988). In contrast to other skeletal

muscles, the respiratory muscles are recruited every minute throughout life. Thus, fundamental to

understanding their function is to discern how respiratory muscle fatigue affects healthy

individuals and how it might contribute to respiratory compromise and ventilatory failure in

several patient populations (Ratnovsky et al., 2008).

Many structural and functional attributes of inspiratory muscles are similar to the other limb

muscles (Palla, 2004) and comparable assessment tools can be utilized to evaluate their tolerance to

loading. Electromyography (EMG) is a technology that captures the electrical activity of

muscles, which can be analyzed to determine normal and abnormal function of the neuromuscular

system, including the respiratory muscles (American Thoracic Society/European Respiratory

Society, 2002; Soderberg and Knutson, 2000). Commonly used EMG measures are the level of

activation, the timing of activation, the force/EMG signal relationship and indirect myoelectric

manifestations of muscle fatigue (American Thoracic Society/European Respiratory Society, 2002;

Paterno et al., 2004; Vollestad, 1997). EMG monitoring of the respiratory muscles has been

Page 4 of 44
evaluated in a variety of evaluated in a variety of clinical and experimental scenarios. Examples

include: EMG assessment of respiratory muscles in patients during mechanical ventilation (Cecchini

et al., 2014; Dres et al., 2012; Muttini et al., 2015); during an acute exacerbation of chronic

obstructive pulmonary disease (COPD) patients (Jolley et al., 2015; McKenzie et al., 2009; Suh et

al., 2015); for prognosis and exercise capacity of neuromuscular diseases (Mohammadi et al.,

2014; Stewart et al., 2001); to investigate respiratory muscle function and fatigue during loaded

breathing in healthy people (Chiti et al., 2008; Segizbaeva and Aleksandrova, 2014) and to assist

with biofeedback during breathing exercises (Gallego et al., 1991; Parket al., 2015).

EMG of the respiratory muscle can be performed invasively through oesophageal or

intramuscular electrodes, however surface EMG (sEMG) is more commonly used (Caruso et al.,

2015). sEMG is advantageous because it is easy to apply, sensitive to detect myoelectric activity,

more tolerable by the subject, and can provide continuous monitoring. Major disadvantages are

the interference from the activity of other muscle groups (cross-talk) and the limited

standardization for analysis of the signal (Caruso et al., 2015). In 1999, the European concerted

action SENIAM (surface EMG for non-invasive assessment of muscle) developed a

recommendation on the use of sensors, sensor placement, signal processing and modelling in detail

for 27 skeletal muscles but the respiratory muscles were not included in these standards (Hermens

et al., 1999).

The ATS/ERS statement on respiratory muscle testing describes EMG monitoring of the

diaphragm at length. Yet this statement provides few recommendations about EMG methods to be

applied to extradiaphragm inspiratory muscles, as defined by the primary or accessory muscles that

contribute to inspiration besides the diaphragm. The reproducibility of sEMG of primary and

accessory muscles of inspiration has been demonstrated (Duiverman et al., 2004; Maarsingh et

Page 5 of 44
al.,2000). However, there are considerable differences and controversies related to sEMG methods

for the extradiaphragm inspiratory muscles including the SM, SC, IC and PI. Many of these

disparities appear to be related to fundamental technique such as sEMG acquisition and data

processing that hinder standardization and comparison between studies. Therefore, we undertook a

systematic review of sEMG of extradiaphragm inspiratory muscles to address the following

research questions:

1. What sEMG procedures were applied to extradiaphragm inspiratory muscles (specifically SM,

SC, IC and PI) regarding electrode position, data processing and outcome measures in healthy

adults?

2. Did the consistency or inconsistency among sEMG procedures, at least in part, explain

differing outcomes in studies examining extradiaphragm inspiratory muscle activity?

3. Did different inspiratory loading protocols (e.g. incremental versus constant; resistive,

threshold or hyperpnoea) result in different magnitudes or directional changes of sEMG

parameters in the extradiaphragm inspiratory muscles?

2. Methods

2.1. Search strategy

The Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines

(PRISMA) guided this review (Moher et al., 2009). Electronic searches were performed on the

following databases from their inception to March 6, 2018: MEDLINE, PubMed, EMBASE,

Cochrane CENTRAL and Database of Systematic Reviews, CINAHL, SPORTDiscus, Latin

American and Caribbean health (LILACS) and Physiotherapy Evidence Database (PEDro). Three

concepts were combined for the search strategy by using the operator “and”; these were

“electromyography (EMG)”, “respiratory muscles (e.g. scalene, sternocleidomastoid, intercostal,

Page 6 of 44
and parasternal)” and “healthy”. Other terms within these concepts were combined with the

Boolean operator “or”. A complete search strategy for MEDLINE is provided in Appendix A.

2.2. Study criteria and data abstraction

The inclusion criteria for studies were: (1) healthy adult subjects aged >18 years; (2) sEMG

performed on at least one of the extradiaphragm inspiratory muscles- SM, SC, PI, and IC; in

sitting position and during respiratory muscle loading or maximal inspiratory pressure

(MIP) measurements; (3) randomized controlled trials (RCT), prospective cohort, retrospective

cohort; and cross-sectional studies; (4) published in English or Portuguese. The studies were

excluded if: (1) sEMG was only performed on the diaphragm and/or abdominal muscles; (2)

participants had associated procedures i.e. drug or oxygen administration that could modify the

sEMG outcomes; or (3) data were only reported as abstracts, review articles, short reports, case

reports, editorials, letters, book chapters, thesis or dissertation.

The first author (EC) paired with one of the other coauthors (NB, LM, SM, WR) reviewed

all the titles, abstracts and full texts to screen for inclusion based on a consensus process.

Reviewers were not blinded to authors, journals and institutions. When there were disagreements

between the reviewers, another reviewer was consulted. Data abstraction was performed

using standardized forms by two independent reviewers that used a consensus process to

come to agreement and if not resolved, a third author was consulted. The following data were

extracted: author(s), year of publication; primary study objective; inclusion and exclusion

criteria; description of participants (sample size, age, anthropometric data [height, weight

and body mass index]); details of the respiratory loading (resistive or threshold loaded

breathing or isocapnic/normocapnic hyperpnoea or MIP); sEMG procedure; posture during

sEMG acquisition; muscle(s) examined; electrode position, electrode material, procedure set

Page 7 of 44
up and outcomes.

2.3. Quality Assessment

Quality assessment was performed by pairs of reviewers (EC, NB, LM, WR) who

independently used a modified checklist for non-randomized studies (Downs and Black, 1998;

Munn et al., 2010). In the event of disagreement, another reviewer was consulted. The modified

checklist has 16 questions that are subdivided into four categories: reporting, external validity,

internal validity (bias), and internal validity (confounding - selection bias) (Appendix B). Study

quality was ranked based on the number of criteria reported in the study as follows: high if >75%,

moderate if 60 to 74% and low if <60% (Munn et al., 2010). The quality assessment is reported in

Table 1. Studies were assessed further for internal validity by evaluating the reporting of sEMG

procedure; posture during sEMG acquisition; muscle(s) examined; electrode position, and details of

signal acquisition and processing (see Table 3).

3. Results

3.1. Study Selection

Fig. 1 depicts the search strategy and selection process from databases, of which 7048 titles

were identified and retrieved into reference management software (Endnote X7, Thomson Reuter

USA). After duplicates were removed, a total of 5170 titles and abstracts were screened. From this

pool, 46 papers were selected for full text screening. An additional paper for inclusion was

identified through hand searching. After full-text article review, 22 papers were excluded resulting

in 25 papers that were included in the systematic review (Fig. 1 outlines reasons for exclusion). It

should be noted that papers published before SENIAM (Hermens et al., 1999) and

ATS/ERS (2002) guidelines were included for historical completeness. However, a

number of confounding factors may have been present in these papers.

Page 8 of 44
3.2. Quality assessment

Table 1 provides a summary of the quality assessments with subtotals for each category of

quality and for each paper. According to the ranking of quality by Munn et al. (2010) (Appendix A),

seven papers reported items consistent with moderate quality (60-74%) (Da Gama et al., 2013; de

Andrade et al., 2005; de Bisschop et al., 2017; Hawkes et al., 2007; Reilly et al., 2013; Trevisan et al.,

2015; Walterspacher et al., 2018) and the remaining were rated as low quality. The most

commonly reported items were “Outcomes clearly described” in the Reporting category and

“Accurate outcome measure” in the Internal validity category, both of which were described in

100% of studies. In contrast, the items that were reported least were those that related to whether

the sample was representative of the general population, and consideration of confounding

variables.

3.3. Characteristics of participants

Characteristics of participants are reported in Table 2. The twenty-five articles reported on 362

participants, of which 61.2% were male. Eleven papers only included male subjects, eleven studies

included both sexes and three articles did not state the sex of participants. The mean age of the

participants ranged between 18 to 68 years, with average age of 30.7 ± 7.6 years old and one paper

did not provide the age of the sample.

3.4. Characteristics of protocols of MIP and/or an acute bout of respiratory muscle loading

The respiratory muscle loading protocols used during sEMG monitoring were diverse among

the 25 papers (Table 2): six studies (24%) performed EMG only during MIP (Brancatisano et al.,

1993; Nava et al., 1993; Ratnovsky et al., 2006; Segizbaeva et al., 2015; Trevisan et al., 2015;

Zakynthinos et al., 1999); ten studies (40%) during inspiratory threshold loading (ITL), of which

seven (28%) performed constant load ITL (Breslin et al., 1990; Citterio and Agostoni, 1981; de

Page 9 of 44
Andrade et al., 2005; Hawkes et al., 2007; Jung and Kim, 2016; Ramsook et al., 2016; Scharf et

al., 1984) whereas three (12%) performed incremental ITL (Da Gama et al., 2013; Reilly et al.,

2013; Shadgan et al., 2011); four studies (16%) during resistive loaded breathing (Butler et al.,

1996; de Bisschop et al., 2017; Jardim et al., 1981; Ringel et al., 1985), four studies (16%) during

hyperpnoea (Gonzalez et al., 1999; Guenette et al., 2011; Katayama et al., 2015; Vilozni et al.,

1987) and one study performed sEMG during several types of loading - MIP, constant load ITL,

resistive loaded breathing and hyperpnoea (Walterspacher et al., 2018).

3.5. sEMG of extradiaphragm inspiratory muscles and electrode position

Table 3 describes EMG procedures and outcomes for the SM, SC, IC and PI. The IC muscle

was studied in 12 papers of which six articles use the term “IC muscles” (de Bisschop et al., 2017;

Guenette et al., 2011; Jardim et al., 1981; Katayama et al., 2015; Ramsook et al., 2016; Shadgan et

al., 2011) and the others use the term “external IC muscles” (Brancatisano et al., 1993; Gonzalez et

al., 1999; Hawkes et al., 2007; Jung and Kim, 2016; Ratnovsky et al., 2006; Scharf et al., 1984). The

SM was evaluated in fifteen (Breslin et al., 1990; Da Gama et al., 2013; de Andrade et al., 2005;

Guenette et al., 2011; Jung and Kim, 2016; Katayama et al., 2015; Nava et al., 1993; Ramsook

et al., 2016; Ratnovsky et al., 2006; Ringel et al., 1985; Segizbaeva et al., 2015; Shadgan et al., 2011;

Trevisan et al., 2015; Vilozni et al., 1987; Walterspacher et al., 2018), the PI muscle was evaluated

in ten studies (Brancatisano et al., 1993; Butler et al., 1996; Citterio and Agostoni, 1981; Nava et al.,

1993; Ramsook et al., 2016; Reilly et al., 2013; Segizbaeva et al., 2015; Shadgan et al., 2011;

Walterspacher et al., 2018; Zakynthinos et al., 1999) and SC in three papers (Butler et al., 1996;

Ramsook et al., 2016; Segizbaeva et al., 2015).

Fifteen papers (60%) assessed sEMG on the right side (Butler et al., 1996; Citterio and

Agostoni, 1981; Gonzalez et al., 1999; Guenette et al., 2011; Hawkes et al., 2007; Jardim et al.,

Page 10 of 44
1981; Jung and Kim, 2016; Katayama et al., 2015; Nava et al., 1993; Ramsook et al., 2016; Scharf et

al., 1984; Segizbaeva et al., 2015; Shadgan et al., 2011; Vilozni et al., 1987; Zakynthinos et al.,

1999), six papers (24%) assessed on both sides (left and right) (Da Gama et al., 2013; de Bisschop et

al., 2017; Ratnovsky et al., 2006; Reilly et al., 2013; Trevisan et al., 2015), three papers (12%) did

not report the side of body assessed (Brancatisano et al., 1993; Breslin et al., 1990; de Andrade et al.,

2005) and only one paper (4%) assessed EMG on the left side (Ringel et al., 1985).

Positioning of the surface electrodes for the same muscles differed among studies. For the

external IC, the electrodes were positioned on the 3rd intercostal space along the midaxillary line,

(Brancatisano et al., 1993; Gonzalez et al., 1999; Scharf et al., 1984) and only Hawkes et al. (2007)

used the 5th intercostal space (at the posterior axillary line). Electrodes were most often positioned

along the anterior axillary line for the intercostal space but varied along the height of the ribcage

from the 2nd to 8th intercostal space (Table 3). Only one study placed the electrode for the IC along the

“posterior mid-axillary line” at the 8th intercostal space (de Bisschop et al., 2017).

In contrast to the IC, the positioning of the electrode for the PI, SM and SC was fairly

consistent. The placement of the electrodes for the PI was reported to be in the 2nd or 3rd intercostal

space. The placement of the electrodes for the SM was described somewhat similarly, being

positioned over the middle third of the muscle or midpoint of the muscle belly (Table 3). The

placement of the electrodes for the SC was on the posterior triangle of the neck at the level of the

cricoid cartilage (Butler et al., 1996; Ramsook et al., 2016; Segizbaeva et al., 2015) (Table 3).

3.6. sEMG procedures and outcomes

The sEMG procedures and outcomes can be expressed in different ways according to EMG

acquisition, amplification and processing, and these parameters were often closely related to the

study objectives. Nineteen papers (76%) used band pass filters ranging from 0-10000Hz

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(Brancatisano et al., 1993; Breslin et al., 1990; Butler et al., 1996; de Andrade et al., 2005; de Bisschop et

al., 2017; Gonzalez et al., 1999; Hawkes et al., 2007; Jardim et al., 1981; Jung and Kim, 2016; Katayama

et al., 2015; Nava et al., 1993; Ramsook et al., 2016; Reilly et al., 2013; Scharf et al., 1984; Segizbaeva

et al., 2015; Trevisan et al., 2015; Vilozni" et al., 1987; Walterspacher et al., 2018; Zakynthinos et al.,

1999) to process EMG signals (Table 3). Six studies (24%) used both band-pass and low pass filter to

process the data (Jardim et al., 1981; Katayama et al., 2015; Nava et al., 1993; Ramsook et al., 2016;

Trevisan et al., 2015; Walterspacher et al., 2018) and three studies (12%) also used high pass filters,

together with band-pass and low pass filters to process the data (Jardim et al., 1981; Ramsook et al., 2016;

Walterspacher et al., 2018). The sampling rate was reported in 15 papers (60%) (Table 3) (Butler et al.,

1996; de Andrade et al., 2005; de Bisschop et al., 2017; Gonzalez et al., 1999; Guenette et al., 2011;

Hawkes et al., 2007; Jung and Kim, 2016; Katayama et al., 2015; Ramsook et al., 2016; Ratnovsky et al.,

2006; Reilly et al., 2013; Shadgan et al., 2011; Trevisan et al., 2015; Vilozni et al., 1987; Walterspacher et

al., 2018) and ranged from 1000 to 10000Hz and the resolution of the system used to acquire the data was

only mentioned in eight studies (32%), in which five (20%) of them used 16-bit systems (Table 3) (de

Bisschop et al., 2017; Katayama et al., 2015; Reilly et al., 2013; Shadgan et al., 2011; Walterspacher et

al., 2018).

The gain was reported in seven studies (28%) and ranged from 1000 to 3000 times (Da Gama et al.,

2013; de Andrade et al., 2005; Hawkes et al., 2007; Jardim et al., 1981; Jung and Kim, 2016; Katayama et

al., 2015; Walterspacher et al., 2018). The units reported varied widely, which took into account the

objective of the study; percentage of EMG was most commonly reported in seven studies (28%) (Butler et

al., 1996; de Andrade et al., 2005; Guenette et al., 2011; Jung and Kim, 2016; Nava et al., 1993; Reilly et

al., 2013; Shadgan et al., 2011), of which five (20%) used the percentage change

Page 12 of 44
of EMG signal obtained during a maximum voluntary contraction of the muscle (de Andrade et al., 2005;

Guenette et al., 2011; Nava et al., 1993; Reilly et al., 2013; Shadgan et al., 2011).

For EMG signal processing, 12 studies (48%) reported rectifying the EMG signal (Brancatisano

et al., 1993; Butler et al., 1996; Citterio and Agostoni, 1981; de Andrade et al., 2005; de Bisschop et al.,

2017; Gonzalez et al., 1999; Guenette et al., 2011; Jardim et al., 1981; Nava et al., 1993; Ratnovsky et

al., 2006; Shadgan et al., 2011; Vilozni et al., 1987; Zakynthinos et al., 1999), seven studies (28%)

integrated the EMG signal (de Bisschop et al., 2017; Guenette et al., 2011; Jardim et al., 1981; Nava

et al., 1993; Ratnovsky et al., 2006; Segizbaeva et al., 2015; Zakynthinos et al., 1999) and 10 studies

(40%) smoothed and/or averaged the EMG data (Brancatisano et al., 1993; Breslin et al., 1990; Butler et

al., 1996; Citterio and Agostoni, 1981; de Bisschop et al., 2017; Gonzalez et al., 1999; Guenette et al.,

2011; Ringel et al., 1985; Shadgan et al., 2011) (Table 3).

The time constant/window used to assess the EMG signal was reported in 12 studies (48%)

(Brancatisano et al., 1993; Citterio and Agostoni, 1981; Hawkes et al., 2007; Nava et al., 1993;

Ramsook et al., 2016; Reilly et al., 2013; Segizbaeva et al., 2015; Shadgan et al., 2011; Trevisan et al.,

2015; Vilozni et al., 1987; Walterspacher et al., 2018; Zakynthinos et al., 1999) and ranged from 25 to

300ms and two studies did not report the type of signal processing (Jung and Kim, 2016; Scharf et

al., 1984). One study used wavelet analysis and continuous wavelet transform to process and analyze

the EMG signals (Da Gama et al., 2013) and another study used fast Fourier transform (Vilozni et al.,

1987).

Nine papers (36%) reported the sEMG signal as the integrated EMG (iEMG) (Brancatisano et al.,

1993; de Bisschop et al., 2017; Gonzalez et al., 1999; Guenette et al., 2011; Nava et al., 1993;

Page 13 of 44
Ratnovsky et al., 2006; Segizbaeva et al., 2015; Shadgan et al., 2011; Zakynthinos et al., 1999). Ten

articles (40%) reported root mean square (RMS) (Citterio and Agostoni, 1981; de Andrade et al., 2005;

Hawkes et al., 2007; Jung and Kim, 2016; Katayama et al., 2015; Ramsook et al., 2016; Reilly et al.,

2013; Scharf et al., 1984; Trevisan et al., 2015; Walterspacher et al., 2018). Peak amplitude was

reported in one paper (Breslin et al., 1990) and peak of onset time was report in one study (Butler et al.,

1996). Frequency spectrum, power spectrum and centroid frequency were reported in three papers,

respectively (Da Gama et al., 2013; Jardim et al., 1981; Vilozni et al., 1987) that aimed to assess

fatigue of the muscles. Only Ringel et al.(1985) did not use specific terminology for the sEMG variables

but simply stated that “EMG activity” increased or decreased (Table 3).

Quantitative synthesis of data in this review was not possible because of the diversity of EMG signal

processing; presentation of directional rather than numerical changes; the different muscles that were

assessed; and the variety of interventions used. Therefore, a summary of EMG during exercise was

limited to those studies that compared baseline to loaded conditions among the muscles (Table 4).

The iEMG or RMS of the respiratory muscles consistently increased during different types of loading

when compared to baseline (rest) as reported in ten studies (40%) (Breslin et al., 1990; de Andrade et al.,

2005; de Bisschop et al., 2017; Gonzalez et al., 1999; Hawkes et al., 2007; Jung and Kim, 2016;

Katayama et al., 2015; Reilly et al., 2013; Shadgan et al., 2011; Walterspacher et al., 2018) (Table 4).

Two studies did not report an increase in RMS when comparing baseline to loading (Scarf et al., 1984;

Walterspacher et al., 2018). The report by Walterspacher et al. (2018), showed that resistive

loading induced a trend towards an increase of RMS in the SM and PI of about 20 to 25%

but no significant changes were reported.

Page 14 of 44
 Two studies that investigated respiratory muscle fatigue evaluated frequency spectrum/centroid

frequency of the EMG (Da Gama et al., 2013; Vilozni et al., 1987) and found a significant decrease of

these parameters during incremental ITL or hyperpnoea, respectively, when compared to baseline values

(Table 4). As summarized in Table 4, the extradiaphragm inspiratory muscles (SM, IC, PI and SC)

demonstrated similar patterns of activation; sEMG activity (iEMG or RMS) increased and the changes

were independent of the type of the loading (ITL, resistive or hyperpnoea). Comparison of sEMG across

different extradiaphragm muscles during different types of loading was limited to one study.

Walterspacher et al. (2018) monitored PI and SM sEMG during MIP, constant ITL, resistive loading and

hyperpnoea. Activation (shown by the RMS) of SM and PI was highest during constant ITL and

hyperpnoea and lowest during flow resistive loading. Worthy of note, SM activation as indicated by the

% of RMS was higher than PI during constant ITL (p=0.035) and tended to be higher during hyperpnoea.

Some authors did not compare sEMG baseline values to those obtained during loading.

Guenette et al. (2011) showed positive correlations between blood flow indices versus iEMG of IC and

SM during hyperpnoea. Ramsook et al. (2016) investigated EMG during constant inspiratory load with

and without specific diaphragmatic breathing instructions and detected that RMS was higher in SM, SC

and PI without instruction and in IC when the instruction was given.

4. Discussion

To our knowledge, this is the first systematic review that synthesized sEMG procedures and

outcomes measures of extradiaphragm inspiratory muscles reported during a maximal strength

manoeuvre (MIP) and/or an acute bout of respiratory muscle loading in healthy people. The diverse

methods used to analyse and present sEMG outcomes, different normalization of the signal, as

Page 15 of 44
well as missing information about EMG preparation, detection and type of data acquisition have limited

the comparisons of sEMG in extradiaphragm inspiratory muscles among studies. Thus, examination of

how sEMG procedures affected outcomes and comparisons of inspiratory loading protocols were

limited by these differences. Although there are standards for reporting EMG data (Merletti, 1996),

most of the studies did not describe EMG detection procedures such as reference electrodes, skin

preparation, gain and impedance. Further, many did not report the resolution of the system acquiring

the EMG signal, which makes it difficult to evaluate the studies regarding quality of the EMG signals.

The iEMG or RMS of the respiratory muscles consistently increased during

different types of loading when compared to baseline (rest) (Table 4). However, comparisons

regarding the magnitude among studies were limited due to a lack of detail and/or differences

in methodology except for one report. Walterspacher et al. (2018) found that activation

(shown by the RMS) of SM and PI was highest during constant ITL and hyperpnoea, and

lowest during flow resistive loading. These data illustrate how target intensity of loading is

not the only factor that determines the magnitude of activation of extradiaphragm

inspiratory muscles. Possible explanations for the lower activation of the SM and PI

during flow resistive loading versus ITL may have been due to greater activation of other

extradiaphragm inspiratory muscles and the differing activation patterns required to

achieve the target mouth pressure for the more gradual increase of a flow resistive

inspiratory load versus the abrupt increase of a threshold load.

Of interest, two studies did not report an increase in RMS when comparing baseline

to constant ITL or resistive loading (Scarf et al., 1984; Walterspacher et al., 2018). The

study by Walterspacher et al. (2018), showed a trend towards an increase of RMS in the

SM and PI of about 20 to 25% but no significant changes were reported,

which may have been related to the selected analyses and multiple comparisons. In the

investigation by Scarf et al. (1984), the moderate ITL imposed appeared to be a within a range

Page 16 of 44
that induced an increase in RMS of respiratory muscles in two studies (de Andrade et al,

2005; Hawkes et al., 2007) but there were two major differences. Scarf et al. (1984)

monitored over a primary muscle of inspiration (PI), whereas the other two reports

monitored accessory muscles - the SM (de Andrade et al, 2005) and lateral IC (Hawkes et

al., 2007). A second difference was that the study by Scarf et al., (1984) was

underpowered; only 2 of 5 participants had sEMG monitored over the Pl

Quality assessment of studies included in the systematic review was either moderate (28% of

articles) or low quality (72% of articles). Most articles scored fair to good results for reporting items

related to bias whereas the descriptions of external validity and confounders were not often included.

Only two studies (Da Gama et al., 2013; Walterspacher et al., 2018) included a sample size calculation.

Most reports (21 of 25) examined small sample sizes of less than 14 subjects, and as mentioned above,

44% of the studies only investigated men. In spite of statistical significance, generalizability could be

limited beyond age and sex. Because most papers (22 of 25) did not stipulate inclusion and exclusion

criteria for recruitment, additional confounding biases could be present such as fitness i.e. participation in

high level, competitive sports and attributes contributing to body stature such as race. Of interest, 6 of

the 7 reports that scored moderate quality in terms of the Downs and Black quality of

assessment, also reported sufficient quantitative data to enable comparisons from baseline to

loaded breathing (Da Gama et al., 2013; de Andrade et al., 2005; de Bisschop et al., 2017;

Hawkes et al., 2007; Reilly et al., 2013; Walterspacher et al., 2018).

Page 17 of 44
 Aspects of EMG monitoring outlined previously (Merletti, 1996) and in a more recent

publication of standards (Hermens et al., 2000) can have profound effects on EMG outcomes and

their description is required to enable the reader to make accurate comparisons among studies. In

spite of published standards for EMG procedures, many included studies published after the standards

for EMG data reporting did not provide comprehensive descriptions of EMG settings. Eight papers were

published before the first statement, which may explain the limited description of EMG procedures,

signal processing and outcomes. Among those papers, only Jardim et al., (1981) detailed detection

mode, signal amplification and filtering (Table 3). Seven of 17 papers published after the first

statement (Da Gama et al., 2013; de Andrade et al., 2005; de Bisschop et al., 2017; Hawkes et al., 2007;

Katayama et al., 2015; Trevisan et al., 2015; Walterspacher et al., 2018) presented more than 50% of the

recommend EMG settings suggested by Merletti et. al. (1996) and SENIAM (Hermens et al., 1999).

Lack of descriptions regarding interelectrode position and distance, electrode position relative to the

innervation zone, the type of acquisition system used and about processing of EMG signals, can prevent

the potential reproducibility of the study by other authors, and compromise the data interpretation and

determination of the quality of the results obtained in these studies (Chowdhury et al., 2013;

Phinyomark et al., 2012; Zipp, 1982).

The lack of published standards that specify electrode position over each of the respiratory

muscles likely contributed to the variable methods used. This was exemplified by four reports that

described similar locations for electrode positions but used different terms for the type of intercostal

muscle. All four reports described the electrode placement being over the second intercostal space 3

cm lateral to the sternum; however, one study termed this location as detecting the IC muscles (Jardim et

al., 1981) whereas three studies (Butler et al., 1996; Citterio and

Page 18 of 44
Agostoni, 1981; Reilly et al., 2013) used the term, PI muscle. According to De Troyer et al., (2005), the

internal IC muscles situated between the sternum and the costochondral junctions are called PI muscles.

Consistency in labelling muscles and in electrodes placement are important to allow reliable data

interpretation, comparisons among studies, and reproducibility of protocols in different healthy and

disease populations.

The importance of proper electrode placement over muscles for an optimal recording of sEMG signals

have been addressed in previous papers (Hermens et al., 1999; Hermens et al., 2000; Mesin et al., 2009;

Rainoldi et al., 2004; Rodriguez-Falces, 2017). In brief, electrode placement over the innervation zone

results in lower EMG amplitude (RMS) due to signal cancellation and a higher frequency (mean power

frequency) because of recording of non-propagating motor unit action potentials (Boccia and Rainoldi,

2014; Smith et al., 2015; Rainoldi et al., 2004). However, a recent study showed that although sEMG

data during a maximal contraction was consistent with this premise, submaximal contractions were

less sensitive to signal cancellation. Further, the rates of fatigue induced changes in the sEMG RMS and

mean power frequency were similar regardless of whether electrode placement was over the innervation

zone or proximal or distal to it (Smith et al., 2015). The use of multichannel or linear array electrodes is

one approach to identify the innervation zone and to optimize signal analysis (Mesin et al., 2009).

Regardless, awareness of how the electrode placement relative to the innervation zone sEMG is critical

depending on the study design and subsequent comparisons.

Whether proper electrode placement on extradiaphragm inspiratory muscles affected

RMS outcomes is difficult to discern in the included studies due to a lack of reported details.

Moreover, variation of electrode placement might be limited due to the anatomy of some

extradiaphragm inspiratory muscles. Electrode positioning for the IC and PI is limited by

the proximity of adjacent ribs and to a lesser extent for the SC by adjacent muscles. In

contrast, the length and surface of the SM provides ample exposure for sEMG electrodes

except in those that have substantial adipose in the anterior neck region. Given that the

Page 19 of 44
innervation zone varies along the length of the SM (Falla et al., 2002), electrode position

could have affected RMS magnitude. Although the SM was the most commonly examined

extradiaphragm inspiratory muscle (Table 4), only two reports described the percentage

magnitude of the increased RMS in response to constant ITL loading at a percentage of MIP

(de Andrade et al., 2005; Walterspacher et al., 2018). However, neither reports described

the electrode position according to the innervation zone but rather as being 5 cm from the

mastoid or 7 cm from the suprasternal notch, respectively (de Andrade et al., 2005;

Walterspacher et al., 2018). The use of linear array electrodes could optimize signal

acquisition and subsequent analysis for derivation of RMS in future studies that examine the response

of the extradiaphragm inspiratory muscles to loaded breathing.

Due to the complexity of muscle fibres direction, shape and action, as well as the possible cross-

talking and signal contamination, the sEMG has limitations to acquire a clean signal while also

capturing the real force-generating capacity of the muscles (De Luca et al., 2010; Sousa et al., 2016).

Other methods to evaluate muscle activation, recruitment, fatigue and neural drive are intramuscular

or multichannel EMG. Intramuscular EMG, which requires insertion of needle electrodes, is reliable,

safe and minimizes signal contamination from cross talking. Disadvantages of this technique are: it’s

invasive, unpleasant for the participants, requires high skills for ideal needle placement and yields

limited information from few motor units. All in all, these factors limit intramuscular EMG in clinical

settings (American Thoracic Society/European Respiratory Society, 2002; Chiti et al., 2008).

Multichannel or linear array sEMG is a well validated, noninvasive and a reliable technique to detect

and to improve the quality of myoelectrical activity recordings from skeletal muscles (Farina et al., 2000;

Farina and Merlettie, 2003; Merletti et al., 2003). It can overcome some of the limitations of the

standard two-channels technique by providing reliable estimates of conduction velocity (Farina et al.,

2004), quantifying spatial changes in muscle activation (Kleine et al., 2000), minimizing cross-talk (De

Luca et al., 2012), and accurately detecting of fatigue-related protocols by analyzing shifts in median

frequency (Gallina et al., 2011). Linear array sEMG of SM and SC has been described regarding

Page 20 of 44
the innervation zone for electrode placement (Falla et al., 2002) and has been utilized for studies of

neck pain (Falla et al., 2004a, 2004b). However, the authors are unaware of the use of linear array sEMG

of inspiratory muscles during studies of inspiratory muscle strength, endurance, and/or loaded

breathing protocols.

The generalizability of results to older individuals should be approached with caution. Aging

results in many alterations of muscle function and structure. Some of the major changes are

decreased muscle strength (Coscrato et al., 2013), decreased voluntary activation and

modifications in the rate of agonist/antagonist co-activation (Hakkinen et al., 1998). Previous studies

have provided evidence that there are gender/sex differences for many of the major determinants

of exercise capacity of skeletal muscle such as substrate metabolism (Horton et al., 1998), muscle

activation patterns (Szucs and Borstad, 2013), exercise performance (Sheel et al., 2004) and fatigability

(Gonzales and Scheuermann, 2006). Therefore, the predominance of young participants that were 61%

male in these studies limits generalizability of the EMG findings to middle-aged and elderly adults and

to a lesser extent to females, dependent on the particular study.

This systematic review presents a couple of limitations that require consideration. The

inconsistency of methods and data reported limited the ability to perform meta-analyses. For

example, some studies did not report the EMG signals obtained during baseline and loading, which

limited comparisons. Further, standards for EMG monitoring of the respiratory muscles were

published only in 2002 (ATS/ERS); although, some reports after that date did not describe the

recommended details. A third limitation is cross talk, a common problem related to sEMG, which is

the contamination of sEMG of the target muscle by the electrical activity of adjacent muscles. For

example, monitoring of the ICs could be very vulnerable to this crosstalk where the external IC

overlap the internal IC and appositional area of the diaphragm.

In conclusion, sEMG monitoring of extradiaphragm inspiratory muscles reveals essential data

to assess muscle activities and identify the outcomes in physiological protocols and in the clinical

setting regarding. sEMG has been demonstrated to be feasible and reliable but there is a need for

Page 21 of 44
studies with high quality methodology to standardize the electrodes position, accurately label

the intercostal muscles as well as to include more complete description of the signal processing

procedures. Adhering to standardized methods and comprehensive reporting of these methods will

enable acquisition of reliable and valid data that will in turn facilitate interpretation and accurate

comparisons among reports. Further, use of multichannel and needle EMG of a given muscle could

provide a more complete description of regional variation within a particular extradiaphragm

inspiratory muscle. Efforts should be made to record sEMG from several primary and accessory

muscles of inspiration during loaded breathing to provide a more comprehensive pattern of

recruitment and whether that recruitment varies throughout the duration of a particular type of

loading to task failure.

Conflict of interest

The authors declare that there is no conflict of interest.

Appendix A Medline Search Strategy

Appendix B Criteria checklist adapted from Downs and Black (Munn et al., 2010).

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Muscles. Phys. Ther. 75, 971–982. doi:10.1093/ptj/75.11.971

Reilly, C.C., Jolley, C.J., Ward, K., MacBean, V., Moxham, J., Rafferty, G.F., 2013. Neural

respiratory drive measured during inspiratory threshold loading and acute hypercapnia in

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inspiratory loading. J. Appl. Physiol. 58, 1646–1653. doi:10.1152/jappl.1985.58.5.1646

Rodriguez-Falces, J., 2017. A new method for the localization of the innervation zone based on

monopolar surface-detected potentials. J. Electromyogr. Kinesiol. 35, 47–60.

doi:10.1016/j.jelekin.2017.05.004

Scharf, S.M., Bark, H., Heimer, D., Cohen, A., Macklem, P.T., 1984. “Second wind” during

inspiratory loading. Med. Sci. Sports Exerc. 16, 87–91.

Segizbaeva, M.O., Aleksandrova, N.P., 2014. Inspiratory muscle resistance to fatigue during

exercise and simulated airway obstruction. Hum. Physiol. 40, 683–689.

doi:10.1134/S0362119714050120

Segizbaeva, M.O., Timofeev, N.N., Donina, Z.A., Kur’yanovich, E.N., Aleksandrova, N.P.,

2015. Effects of inspiratory muscle training on resistance to fatigue of respiratory muscles

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doi:10.1016/j.jelekin.2015.04.014

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Page 33 of 44
 Total Records identified through search
(n=7610) Medline (n=2681)
Identification

Embase (n=2855)
Cochrane Cental (n=627)
Cochrane DSR (n=78)
CINAHL (n=547)
SportDiscus (n=562)
PubMed (n=142)
LILACS (n=59)
PEDro (n=59)

Duplicates removed (n=2440)

Screening

Records screened
(n=5170) Records excluded (n=5126)

Full-text articles assessed

(n=46)
Full-text articles excluded
(n=22)

EMG was not in sitting position (n=8)

Eligibility

Did not specify respiratory muscle (n=3)

Full-text articles included EMG measured during other
(n=24) procedure or type of exercise (n=5)
No details of EMG provided (n=1)
No loaded breathing or MIP (n=4)
Book chapter (n=1)

Retrieved from hand

searching (n=1)
Included

Articles included
(n=25)

Figure 1 – Flowchart of search strategy. Cochrane DSR = Database of Systematic Reviews

Page 34 of 44
Table 1
Quality assessment using modified Downs and Black (Munn et al., 2010). The subtotals of items within
each of 4 categories total scores are provided. Further description of these items are available in
Appendix B.

Author (year) External Internal Internal validity Score

Reporting
validity validity (Bias) (Confounding) (%)
(7 items)
(2 items) (4 items) (3 items)
Brancatisano et al. (1993) 3 0 3 0 37.5
Breslin et al. (1990) 5 1 3 0 56.3
Butler et al. (1996) 4 1 3 0 50.0
Citterio and Agostoni (1981) 4 0 1 0 31.3
Da Gama et al. (2013) 6 2 3 0 68.8
De Andrade et al. (2005) 7 0 3 0 62.5
De Bisschop et al. (2015) 6 1 3 1 68.7
Gonzalez et al. (1999) 6 0 3 0 56.3
Guenette et al. (2011) 6 0 3 0 56.3
Hawkes et al. (2007) 6 1 3 0 68.7
Jardim et al. (1981) 4 0 2 0 37.5
Jung and Kim (2016) 5 0 2 0 43.8
Katayama et al. (2015) 5 0 3 0 50.0
Nava et al. (1993) 5 0 3 0 50.0
Ramsook et al. (2016) 6 0 3 0 56.3
Ratnovsky et al. (2006) 5 0 3 0 50.0
Reilly et al. (2013) 5 1 3 1 62.5
Ringel et al. (1985) 1 0 2 1 25.0
Scharf et al. (1984) 5 0 3 0 50.0
Segizbaeva et al. (2015) 5 0 3 0 50.0
Shadgan et al. (2011) 5 0 3 0 50.0
Trevisan et al. (2015) 6 2 3 0 68.8
Vilozni et al. (1987) 5 1 3 0 56.3
Walterspacher et al (2018) 6 2 3 0 68.8
Zakynthinos et al. (1999) 4 0 3 0 43.8
Total 125 12 70 4 -
Average Score 5 0.48 2.8 0.12 53.0
Average % per category 71.4 25 70 4

Page 35 of 44
 Table 2
Characteristic of participants and interventions.
n Age (years)
Author Height (cm)/ Weight (kg)
INT (M/F) mean + SE Intervention protocol/ load intensity
(year) mean + SE
A/O range
Nava et al. n=9
37.6 ± 4.5 NR MIP
(1993) (NR)
Brancatisano et al. n=5
NR NR MIP
(1993) (NR)
Zakynthinos et al. n=12
35 ± 6 NR MIP
(1999) (12M)
Ratnovsky et al. n=10
32 ± 2 172 ± 6 / 67 ± 4 MIP
MIP

(2006) (4M/6F)
Trevisan et al. n=77
22 ± 0.5 NR MIP
(2015) (24M/53F)
n=10 20 ± 0.6
Segizbaeva et al. 176 ± 2/ 75 ± 2
(10M) (18-23) MIP
(2015)
Walterspacher et n=41 24.0 182±7.5(M) - 170±5.2 (F)
MIP
al. (2018) (25M/19F) (23-25) 74±7.1(M) - 58±7.3(F)
Citterio and n=4 1 subject: 23 1 subject: 188 / 76
Constant ITL at 30 cmH2O
Agostoni (1981) (4M) 3 subject: NR 3 subject: NR / NR
Scharf et al. n=5
36 (25-50) NR Constant ITL at 42 to 45% MIP
(1984) (5M)
Breslin et al. n=18 38 ± 2
NR Constant ITL at 60% MIP
(1990) (4M/14F) (33-47)
n=7
Constant ITL

De Andrade et al.
(NR) 68 ± 1.5 158 ± 4 / 59.7 ± 4 Constant ITL at 30% MIP
(2005)
Hawkes et al. n=12 Constant ITL at 40% MIP
25 ± 2 177 ± 2 / 74 ± 3.5
(2007) (6M/6F)
Jung and Kim n=13
25 ± 0.8 173 ± 2 / 72 ±4 Constant ITL at 0, 40, 60 and 80% MIP
(2016) (13M)
Ramsook et al. n=10
26 ± 1.6 173 ± 3 / 70 ± 3 Constant ITL at 40% MIP
(2016) (10M)
Walterspacher et n=41 24.0 182±7.5(M) - 170±5.2 (F)
Constant ITL at 80% MIP
al (2018) (25M/19F) (23-25) 74±7.1(M) - 58±7.3(F)
Shadgan et al. n=10 Incremental ITL at initial load of 100g and
27.5 ± 0.7 NR
(2011) (10M) add 50g every 2’ interval until task failure
Incremental

Da Gama et al. n=39 M:25 ± 0.9 M: 176 ± 0.02 / 68 ± 4

ITL

Incremental ITL at 10% to 40% MIP

(2013) (19M/20F) F:23 ± 0.4 F:162 ± 0.01 / 54 ± 3
Reilly et al. n=12 Incremental ITL at 10%; 20%; 30%; 40%
30 ± 2 NR
(2013) (8M/4F) and 50% MIP
Jardim et al. n=4 Constant alinear resistance / Decrease
31 ± 2 NR
(1981) (4M) inspiratory flow 0.7 to 0.9 L/s at MIP 80%
n=5 Resistive loaded breathing (pressure drop
Ringel et al.
loaded breathing

(5M) (28-61) NR across 4cmH2O at 0.3 l/s to 38cmH2O at 0.6

(1985)
l/s)
Resistive

Butler et al. n=12 Constant resistive loaded breathing

33 ± 2 66 ± 2 / 68 ± 3
(1996) (7M/5F) inspiratory phase at 250ms
De Bisschop et al. n=11 Constant resistive loaded breathing through
42 ± 4.2 167 ± 3 / 58 ± 3.6
(2015) (6M/5F) 70mm tubing with ID=3 mm
Walterspacher et n=41 24.0 182±7.5(M) - 170±5.2 (F) Constant resistive loaded breathing at 80%
al. (2018) (25M/19F) (23-25) 74±7.1(M) - 58±7.3(F) MIP
Vilozni et al. n=11 32 ± 1.5 Incremental isocapnic hyperpnoea at 20%,
174 ± 2.4 / 71 ± 3
(1987) (9M/2F) (25-40) 40% 60% & 80% MVV
n=10 Constant hyperpnoea at VT 2 L/breaths &
Gonzalez et al.
(10M) 25 ± 1.2 175 ± 2.5 / 74 ± 2.2 RR 15, 30 and 45 f; Different CW restriction
(1999)
0, 25, 50 and 75 mmHg
Hyperpnoea

Guenette et al. n=7 28 ± 2.3 Constant isocapnic hyperpnoea at 25, 40, 55,
176 ± 4 / 69 ± 4
(2011) (6M/1F) (22–40) and 70% of MVV
n=8 Constant isocapnic hyperpnoea (f 60; TI and
Katayama et al.
(8M) 23 ± 1 173 ± 2 / 67 ± 3 TE of one breath cycle 0.5s; VT 30–40% of
(2015)
forced vital capacity)
Walterspacher et n=41 24.0 182±7.5(M) - 170±5.2 (F) Constant isocapnic hyperpnoea at 60%
al. (2018) (25M/19F) (23-25) 74±7.1(M) - 58±7.3(F) MVV, RR = MVol x Target TV

Page 36 of 44
A/O = and/or, cm = centimetres, cmH2O = centimetres of water, CW = chest wall, EMG = electromyography, f = frequency, F = female, g = grams, ID = inner
diameter, ITL = inspiratory threshold load, INT = Intervention, Kg = kilograms, L/min = litres per minute, M = males, MIP = maximal inspiratory pressure, mm
= millimetres, ms = meters per second, MVol = minute volume, MVV = maximal voluntary ventilatory, n = sample, NR = not report ed, Pm = mouth pressure,
RR = respiratory rate, s = seconds, SE = standard error, T E = expiratory time, T I = inspiratory time, VT= Tidal volume, WK = weeks.

Page 37 of 44
Table 3
EMG procedures and outcomes. The papers were categorized according to loading - MIP and type of inspiratory muscle loading.
INT Author Muscle & IED Bit HPF LPF Band- Sample Gain Unit Outcome Processing
(year) Electrode position (cm) (Hz) (Hz) Pass Rate (x) Average/ Tc
Rectify Integrate
(Hz) (Hz) smooth (ms)
Nava et al. PI - 2nd ICS close to the sternum NR NR - Paynter 20- NR NR % iEMG  
(1993) SM- Midpoint of the muscle belly 10000 MVC 300
Brancatisano et EIC- 3rd ICS along the mid- NR NR - - 100- NR NR a.u iEMG   200
al. (1993) axillary line 2000
PI- 2nd ICS
Zakynthinos et PI- Over the 2nd or 3rd ICS near NR NR - - 20 -1000 NR NR a.u iEMG   200
al. (1999) sternum
Ratnovsky et al. EIC – position NR NR NR - Butterworth - 2 1000 NR µV iEMG   NR
(2006) SM– position NR 0
Trevisan et al. SM- Midpoint of the muscle belly NR 14 Butterworth 20–500 2000 NR µV RMS (%) 25
(2015)
Segizbaeva et PI - 2nd ICS close to the sternum; <2 NR - 10– NR NR a.u Peak iEMG  150
al. (2015) SC- posterior triangle of the neck 10000 (% MVC)
at the level of the cricoid cartilage
SM- Midpoint of the muscle belly
Walterspacher PI - 2nd ICS 2 16 0.5 10000 20 - 10000 1000 mV RMS NR NR NR 200
et al (2018) SM – bilaterally at 7 cm 10000 (%MVC)
cranially of the suprasternal
notch
Citterio & PI -2nd ICS, 3-4 cm apart 3 NR 90 630 - NR NR mV RMS (%)   100
Agostoni
(1981)
Scharf et al. EIC-2nd & 3rd ICS NR NR - - 30-500 NR NR NR RMS (%) NR NR NR NR
(1984)
Breslin et al. SM- Over the muscle 2 cm apart 2 NR 20 - 10- NR NR mV Peak  NR
(1990) 10000 amplitude
Constant ITL

De Andrade et SM- 5 cm from the mastoid 1 12 5 - 20–500 2000 1000 % RMS (%)  NR
al. (2005) process MVC
Hawkes et al. EIC- 5th ICS at the posterior 2 NR - - 20-5000 4000 3000 µV RMS (%) 25
(2007) axillary line baseline
Jung and Kim EIC- position NR NR NR - - 5-500 1000 1000 % RMS % NR NR NR NR
(2016) SM- position NR baseline
Ramsook et al. IC- 7th ICS anterior axillary line NR 16 60 500 20-1000 1000 NR mV RMS (%) NR NR NR 100
(2016) PI- 2nd rib 3cm lateral to sternum maximal
SC- posterior triangle of the neck EMG
at the level of the cricoid process
SM- Midpoint of the muscle belly
Shadgan et al. IC- 8th ICS at the anterior axillary 1 16 - 10-100 - 1000 NR % iEMG   50
Incremental ITL

(2011) line MVC

PI- 2nd ICS (lateral at sternum)
SM- Midpoint of the muscle belly
Da Gama et al. SM- 5 cm from the mastoid 2 NR 30 20–500 - NR 1000 Hz Frequency NR NR NR NR
(2013) process, 20 mm apart Spectrum
Reilly et al. PI- 2nd ICS 3 cm from the mid- NR 16 - - 10 - 10000 NR % RMS (%) NR NR NR 50
(2013) point of the sternum 3000 MVC

Page 38 of 44
 Jardim et al. IC- 2 nd- 3rd ICS 1cm from 2 NR 150 - 20 - 46 0 - 3000 NR 1000 High/ Power   NR
(1981) sternum 350 low spectrum
ratio

loaded breathing
Ringel et al. SM- Midpoint of the muscle belly 5-7 NR 1000 10 - NR NR NR Descriptive NR
(1985)
Resistive

Butler et al. SC- Posterior triangle at the 4 NR - - 53 -1000 2000 NR % Peak Peak   NR
(1996) cricoid cartilage ms Onset time
PI- Over 2nd or 3rd ICS 2-3 cm
from the sternum
De Bisschop et IC- 8th ICS in posterior mid- 2 16 - - 20-250 1000 NR mV iEMG    NR
al. (2017) axillary line below the angle of
the scapulae
Vilozni et al. SM- Midpoint of the muscle belly NR NR 20 - 20 - 250 1000 NR Hz Centroid 80-
(1987) frequency 105
Gonzalez et al. EIC- 3rd ICS 2 mm apart along 0.2 - - - 20-500 2056 - mV.s iEMG   NR
Hyperpnoea

(1999) fiber orientation of the muscle

Guenette et al. IC- 7th ICS along the anterior 16 - 30–50 - 1000 - % iEMG    NR
(2011) axillary line MVC
SM- Midpoint of the muscle belly
Katayama et al. IC- 6th ICS anterior axillar line 1 NR - 30 5–500 1000 1000 ∆ of RMS  NR
(2015) SM- Midpoint of the muscle belly 1st min
ACJ = Acromioclavicular joint, a.u = arbitrary unit, Descript = Description of settings, EIC = external intercostal muscle, f = frequency of breathing, HPF = high pass filter, IC = intercostal muscle, ICS
= intercostal space, IED = inter electrode distance, iEMG = integrated EMG, INT = Intervention, ITL = inspiratory threshold load, L = left, LPF = low pass filter, max = maximum, min = minute, mv =
millivolts, MVC = maximum voluntary contraction, ms = millisecond, NR = not reported, PI = parasternal intercostal muscle, R = right, RMS = root mean square, s = seconds, SC = scalene muscle, SM
= sternocleidomastoid muscle, Tc = time constant, X = multiply, μv = microvolts

Page 39 of 44
Table 4
Description of EMG outcomes.

INT Author Change from Baseline During Loaded Breathing

Scharf et al. (1984) no change (n.s) in RMS of PI at 40% of Pdimax.

Breslin et al. (1990) ↑ SM iEMG (p<0.01).

Constant ITL

De Andrade et al. (2005) ↑ SM RMS by 7% (n.s. p=0.09) with load at 30% of MIP.

Hawkes et al. (2007) ↑ IC RMS during ITL at 40% of MIP (P = 0.003).

Jung and Kim (2016) ↑ SM RMS at 60% to 80% of MIP (p<0.05).

Walterspacher et al
↑SM (58%max RMS), compared to PI (45%max RMS) at 80% of MIP (p =0.035).
(2018)

↑ SM iEMG at 70% of ITL until task failure (p<0.05).

Shadgan et al. (2011)
Incremental ITL

↑ PI iEMG at 30% of ITL until task failure (p<0.05).

Da Gama et al. (2013) ↓ SM mean frequency at 30 and 40 cmH2O loads (p<0.05).

↑ PI RMS from 5.3±3.1% during QB to 40+28% of maximum at the end of the ITL
Reilly et al. (2013)
(p<0.001).

↑ IC (8th intercostal space) iEMG during constant alinear inspiratory and expiratory
De Bisschop et al. (2017)
Resistive

resistance (p<0.02).

Walterspacher et al
no change in RMS of SM and PI during constant resistive flow at 80% of MIP
(2018)

Vilozni et al. (1987) ↓ SM Fc to 83.7% (of baseline values) at 80% of MVV (p<0.004)
Hyperpnoea

Gonzalez et al. (1999) ↑ EIC iEMG activity at 90 L/min compared to 30 and 60 L/min (p<0.05).

↑ in ∆RMS of SM and IC during constant hyperpnoea (30-40% of FVC; f=60/min)

Katayama et al. (2015)
(p<0.05).

Walterspacher et al
↑ SM (53% max of RMS) when compared to PI (45% max of RMS) at 60% MVV
(2018)
↑ = increased, ↓ = decreased, Pdimax = maximum transdiaphragmatic pressure, EIC = external intercostal muscle,
EMG = electromyography, Fc = centroid frequency, FVC = forced vital capacity, IC = intercostal muscle, iEMG =
integrated EMG, INT = Intervention, ITL = inspiratory threshold load, n.s. = nonsignificant difference, PI =
parasternal intercostal muscle, QB = quiet breathing, RMS = root mean square, SC = scalene muscle, SM =
sternocleidomastoid muscle, MIP = maximal inspiratory pressure.

Page 40 of 44
Appendix A: Search Strategy
Database: Ovid MEDLINE(R) Epub Ahead of Print, In-Process & Other Non-Indexed Citations, Ovid
MEDLINE(R) Daily and Ovid MEDLINE(R) <1946 to Present>
--------------------------------------------------------------------------------
1 Electromyography/ (74044)
2 Electrodiagnosis/ (6178)
3 (EMG or sEMG or rEMG).mp,kw. (30321)
4 electromyograph*.mp,kw. (85500)
5 electromyogram*.mp,kw. (7744)
6 electroneurograph*.mp,kw. (736)
7 ((electro or electric or electrical) adj2 myograph*).mp,kw. (218)
8 ((esophag* or oesophag*) adj2 (recording* or electrode*)).mp,kw. (529)
9 1 or 2 or 3 or 4 or 5 or 6 or 7 or 8 (98014)
10 exp Respiratory Muscles/ (25209)
11 exp Respiration/ (110264)
12 exp Respiratory Function Tests/ (219358)
13 Breathing Exercises/ (3083)
14 ((respirat* or ventilat* or inspirat* or expirat* or breath*) adj3 muscle*).mp,kw. (12725)
15 diaphragm*.mp,kw. (52410)
16 scalene*.mp,kw. (894)
17 sternocleidomastoid*.mp,kw. (2608)
18 parasternal*.mp,kw. (2495)
19 intercostal*.mp,kw. (10011)
20 serratus anterior.mp,kw. (1107)
21 Neck muscle/ (5486)
22 (neck adj3 muscle*).mp,kw. (7471)
23 sternomastoid*.mp,kw. (518)
24 exp Abdominal Muscles/ (17132)
25 (abdominis or abdominus or abdominal*).mp,kw. (321273)
26 Pectoralis Muscles/ (3481)
27 (pectoral* adj3 muscle*).mp,kw. (6216)
28 or/10-27 (681435)
29 9 and 28 (11951)
30 Healthy Volunteers/ (10224)
31 ((healthy or normal or control*) adj6 (subject* or human* or participant* or volunteer* or adult* or
men* or women* or male* or female*)).mp,kw. (983799)
32 ((healthy or normal*) adj6 control*).mp,kw. (276158)
33 30 or 31 or 32 (1151561)
34 29 and 33 (2921)
35 (exp child/ or exp infant/ or exp adolescent/) not ((exp child/ or exp infant/ or exp adolescent/)
and (exp aged/ or exp adult/)) (1729206)
36 34 not 35 (2863)
37 exp animals/ not (exp animals/ and exp humans/) (4430952)
38 36 not 37 (2807)
39 (eng or por).lg. (23637880)
40 38 and 39 (2695)
41 limit 40 to ed=20170508-20180305 (110)

***************************

Page 41 of 44
Appendix B

Criteria check list adapted from Downs and Black (Munn et al., 2010)

Reporting
1 Is the hypothesis/aim/objective of the study clearly described? Yes-1 No-0
2 Are the main outcomes to be measured clearly described in the introduction or methods section?
Yes-1 No-0
3 Are the characteristics of the subjects included in the study clearly described? Yes-1 No-0
5 Are the distributions of principal confounders in each group of subjects to be compared clearly
described? Yes- 2 Partially-1 No-0
6 Are the main findings of the study clearly described? Yes- 1 No-0
7 Does the study provide estimates of the random variability in the data for the main outcomes? Yes-1
No-0
10 Have actual probability values been reported (e.g., 0.035 rather than <0.05) for the main outcomes
except where the probability value is <0.001? Yes-1 No-0

External validity
11 Were the subjects asked to participate in the study representative of the entire population from
which they were recruited? Yes-1 No-0 Unable to determine-0
12 Were those subjects who were prepared to participate representative of the entire population from
which they were recruited? Yes-1 No-0 Unable to determine-0

Internal validity – bias

15 Was an attempt made to blind those measuring the main outcomes of the intervention? Yes-1 No-0
Unable to determine-0
16 If any of the results of the study were based on “data dredging”, was this made clear? Yes-1 No-0
Unable to determine-0
18 Were the statistical tests used to assess the main outcomes appropriate? Yes-1 No-0 Unable to
determine-0
20 Were the main outcome measures used accurate (valid and reliable)? Yes-1 No-0 Unable to
determine-0

Internal validity – confounding (section bias)

21 Were the patients in different intervention groups (trials and cohort studies) or were the cases and
controls (case‑ control studies) recruited from the same population? Yes-1 No-0 Unable to
determine-0
22 Were study subjects in different intervention groups (trials and cohort studies) or were the cases
and controls (case‑ control studies) recruited over the same period of time? Yes-1 No-0 Unable to
determine-0
25 Was there adequate adjustment for confounding in the analyses from which the main findings were
drawn? Yes-1 No-0 Unable to determine-0

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 Elis E.A. Cabral is physiotherapist and received her MSc in
physiotherapy at the Federal University of Rio Grande do Norte in
2012. Currently, she is working in her PhD at PneumoCardioVascular
Lab at University Federal do Rio Grande do Norte. In 2015/2016 she
was in a collaborative program between the Federal University of Rio
Grande do Norte and University of Toronto. Her research focuses at
the respiratory muscles, pulmonary function and respiratory muscle
training.

Guilherme A F Fregonezi obtained his Bachelor in Physical Therapy

(PT) from the University of Londrina in 1999 and his PhD in
Neuroscience from Universidad Autonoma de Barcelona. Guilherme is
an Associate Professor of Physical Therapy since 2006 and the
coordinator of PneumoCardioVascular Lab at Universidade Federal do
Rio Grande do Norte. He is a fellow of the Brazilian National Research
Council - CNPq since 2010. His research interests are in the fields of
Respiratory Assessment and Rehabilitation; Respiratory Physiology and
Healthy Technology Assessment - HTA. His current hypotheses and
projects are designed to produce evidences in rehabilitation techniques especially in the fields
of respiratory and cardiovascular diseases; describing physiological phenomena of
respiratory system in response to rehabilitation techniques and producing evidences through
the development of systematic reviews.

Luana Melo got her bachelor in physiotherapy and completed her training
in Intensive Care in Fortaleza, Brazil. She finished her PhD in
biotechnology in 2015, in a collaborative program between the State
University of Ceara and University of Toronto. She has a strong
background in rehabilitation, respiratory muscle training, critical care
assistance and mechanical ventilation. She is finishing her postdoctoral
training in a collaborative project between St Michaels Hospital and the
University of Toronto, conducting studies to assess respiratory muscle function and
oxygenation in healthy individuals and critically ill patients. Her main areas of interest
comprise physical rehabilitation, skeletal muscles training, muscle ultrasound in critical
illness, mechanical ventilation and innovation in acute and critical care settings.

Nada Basoudan obtained her bachelor of Physical Therapy (PT) from

king Saud University in 2008 and her MSc of Rehabilitation Sciences
from the University of British Columbia in 2016. She is currently a
lecturer and program coordinator of the Physical Therapy Program in the
Rehabilitation Sciences Department at Princess Nourah Bint
Abdulrahman University. Her research interest is in the area of
cardiopulmonary rehabilitation, exercise physiology and rehabilitation of
chronic illness.

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 Sunita Mathur completed her PhD from the University of British
Columbia in 2006. She is currently an Associate Professor in the
Department of Physical Therapy at the University of Toronto, where she
directs the Muscle Function & Performance Research Lab. Her research
focuses on evaluating skelelal muscle dysfunction and sarcopenia in
individuals with chronic lung disease, lung transplantation and critical
illness.

Darlene Reid obtained her Bachelor of Medical Rehabilitation (PT) from

the University of Manitoba in 1979 and her PhD from the University of
British Columbia in 1988. Darlene was a Professor in the Department of
Physical Therapy at the University of British Columbia and chaired in the
Research Graduate Programs in Rehabilitation Sciences. In the fall of
2014, she moved to the University of Toronto and is a Professor and
Chair of the Department of Physical Therapy. Darlene Reid is a clinical
scientist whose investigations have spanned basic sciences, clinical, and
translational research. Research themes have focused on dysfunction of
the inspiratory and limb muscles in chronic and acute disease that
involves quantification of muscle structure and function at the cellular and macroscopic
level. Her current research is directed towards using non-invasive tools that can be taken to
the bedside including magnetic stimulation, ultrasound, wireless near infrared spectroscopy,
dynamometry, and inclinometry. She has forged research collaborations nationally and
internationally including Europe, Japan, and Brazil.

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