Diaphragmatic electromyography in infants: an overview of possible clinical applications

ABSTRACT Preterm infants often experience breathing instability and a hampered lung function. Therefore, these infants receive cardiorespiratory monitoring and respiratory support. However,

the current respiratory monitoring technique may be unreliable for especially obstructive apnea detection and classification and it does not provide insight in breathing effort. The latter

makes the selection of the adequate mode and level of respiratory support difficult. Electromyography of the diaphragm (dEMG) has the potential of monitoring heart rate (HR) and respiratory

rate (RR), and it provides additional information on breathing effort. This review summarizes the available evidence on the clinical potential of dEMG to provide cardiorespiratory

monitoring, to synchronize patient-ventilator interaction, and to optimize the mode and level of respiratory support in the individual newborn infant. We also try to identify gaps in

knowledge and future developments needed to ensure widespread implementation in clinical practice. IMPACT * Preterm infants require cardiorespiratory monitoring and respiratory support due

to breathing instability and a hampered lung function. * The current respiratory monitoring technique may provide unreliable measurements and does not provide insight in breathing effort,

which makes the selection of the optimal respiratory support settings difficult. * Measuring diaphragm activity could improve cardiorespiratory monitoring by providing insight in breathing

effort and could potentially have an important role in individualizing respiratory support in newborn infants. You have full access to this article via your institution. Download PDF SIMILAR

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POSITIVE AIRWAY PRESSURE TRIAL IN EXTREMELY PRETERM INFANTS Article 17 September 2020 INTRODUCTION Preterm infants often experience difficulties in breathing due to their immature

respiratory system leading to an unstable breathing pattern with frequent apnea and a hampered lung function.1,2 For this reason, most infants need cardiorespiratory monitoring to detect

breathing instability and respiratory support to restore lung function.1,3 The current respiratory monitoring technique used in daily clinical practice, chest impedance (CI), is not always

reliable in detecting and classifying apnea of prematurity.1,2,3,4 Furthermore, CI does not provide insight in breathing effort, which makes selecting the optimal mode and level of

respiratory support difficult in newborn infants.1,2,3,4 Over the last decade, measuring the electrical activity of the diaphragm, the main breathing muscle, with electromyography (dEMG) has

been investigated as an alternative technique for cardiorespiratory monitoring. dEMG has the potential to provide data on heart rate (HR) and respiratory rate (RR), but also breathing

effort.5 This review will summarize the current evidence on the use of dEMG as a cardiorespiratory monitor in newborn infants to highlight its potential for future clinical application, to

identify knowledge gaps, and to direct future research. METHOD This narrative review was written based on a comprehensive literature search in PubMed from 1968 (first dEMG article in PubMed)

up to 2023. Search terms included: ‘diaphragm’, ‘electromyography’, ‘transcutaneous electromyography’, ‘esophageal electromyography’, ‘newborns’, ‘neonates’, ‘preterm infants’, ‘term

infants’. In contrast to a systematic review, we have only included studies within the scope of our narrative review, being potential clinical dEMG applications. As in the past years other

reviews have been published describing the use of esophageal dEMG in newborn infants, we also referred to these reviews instead of redoing their work.6,7 DIAPHRAGMATIC ACTIVITY The diaphragm

is the main breathing muscle and consists of a costal and crural part, which are innervated by the left and right phrenic nerve.8 During normal breathing, the respiratory control center in

the brainstem receives and combines information on the efficacy of gas exchange and lung stretch, which in turn sends an action potential via the phrenic nerves towards the diaphragm.

Consecutively, its muscle fibers are depolarized followed by the formation of action potentials that facilitate diaphragmatic contraction.8,9,10,11 As the diaphragm flattens, the chest

volume increases and the intrapleural pressure decreases, resulting in an influx of air into the lungs.8 With dEMG, a summation of the electrical activity of the innervated muscle fibers

near the measurement electrodes can be measured. Since the electrical activity of the cardiac muscle is detected as well, it can also provide data on cardiac activity.12 In newborn infants,

diaphragm activity is measured using either a transcutaneous or an esophageal route. Transcutaneous dEMG uses adhesive skin electrodes placed bilaterally in the frontal midclavicular line at

the costal margin and one reference electrode on the sternum.5,13 Recently, dry electrodes incorporated in a belt have also been used.14 Transcutaneous dEMG mainly reflects the activity of

the costal diaphragm. The dorsal diaphragm activity can also be measured by placing two additional electrodes on the back, at the same level as the frontal electrodes.13 Changing the lead

configuration, these five electrode positions can also be used to compare the electrical activity of the left and right diaphragmatic hemisphere.15 Esophageal dEMG mainly records the crural

diaphragmatic activity and is measured with a special naso- or orogastric tube containing multiple electrodes and is positioned at the level of the gastroesophageal junction.7,16

Irrespective of the differences between the two measurement methods, a good correlation between both was observed in adults on assisted ventilation and in healthy adults during spontaneous

breathing with a predetermined inspiratory load.17,18 To obtain a respiration waveform, the acquired signal must first be processed to remove the cardiac interference.12 The resulting

waveform can be used to observe the breathing pattern and extract the RR. The waveform can also be used to assess breathing effort, by extracting several dEMG-related parameters, such as the

amplitude, peak activity, tonic (end-expiratory) activity and area under the curve (AUC) (see Fig. 1).12 dEMG is measured in µV and its signal strength depends on technical factors (e.g.,

electrode placement, skin-electrode contact and the used hardware and software) as well as factors determined by the patient (e.g., skin type, subcutaneous tissue and chest wall anatomy).12

This results in the lack of normative dEMG parameter values for transcutaneous dEMG and a wide range in peak activity measured with esophageal dEMG, being generally between 6 and 13 µV.7

Therefore, we recommend comparing the measured dEMG within an infant (e.g., over time, left versus right hemisphere of the diaphragm, pre- versus post-intervention) instead of the absolute

µV values. REPORTED CLINICAL APPLICATIONS OF DEMG CARDIORESPIRATORY MONITORING Several studies have assessed dEMG as a technique for cardiorespiratory monitoring in newborn infants. These

studies mainly examined the agreement of the HR and RR between dEMG and the electrocardiogram (ECG)/CI. Both in the delivery room (DR) and the neonatal intensive care unit (NICU),

transcutaneous dEMG provided a high level of HR-agreement with ECG. However, the agreement in RR between dEMG and CI was less robust in both settings.5,19 It has been suggested that this

suboptimal agreement in RR is caused by the differences in measuring techniques (impedance versus electrical activity) and the impact of patient handling and movement on both signals. The

latter is supported by the observation that RR agreement significantly improved when solely stable dEMG and CI data were used for the analysis.5 Similar results were observed when using

esophageal dEMG for HR and RR monitoring.20,21,22 Next to measuring HR and RR, transcutaneous and esophageal dEMG also enable apnea detection, which is of great importance in the preterm

population. Several studies have shown that both dEMG techniques are able to detect apnea and one study also suggested that transcutaneous dEMG resulted in an improved classification of

central and obstructive apnea compared to CI. In addition, a study using esophageal dEMG showed the ability to detect congenital central hypoventilation syndrome (central apnea during

sleep).6,7,22,23,24 DEMG AS A MONITOR FOR BREATHING EFFORT As previously mentioned, dEMG also has the ability to quantify the amount of electrical activity delivered by the diaphragm.

Studies in adults and children have shown that electrical effort of the diaphragm measured with esophageal dEMG was linearly related to the work of breathing (WOB) based on esophageal

pressure and airway pressure during expiratory occlusion.25,26 More recently, a study in preterm infants showed a modest correlation between peak activity measured with transcutaneous dEMG

and conventional WOB measured with volume and esophageal pressure recordings.27 Other studies provided more indirect evidence that the electrical activity of the diaphragm reflects changes

in WOB, showing that deterioration in the infant’s respiratory status or an increased demand for respiratory support led to an increase in peak diaphragmatic activity measured with

esophageal dEMG.7 However, it should be noted that the relationship between dEMG and breathing effort or WOB depends on the neuro-muscular efficiency (i.e., the measured electrical activity

of the diaphragm in µV and the consecutively generated airway pressure). This efficiency could be lowered due to sedation (iatrogenic) or in patients with neuromuscular disease (e.g., spinal

muscular atrophy).28,29,30 These studies suggest that dEMG provides important insight in breathing effort, which could also be used to optimize respiratory support, as discussed in the

following paragraphs. DEMG FOR PATIENT-VENTILATOR SYNCHRONIZATION During invasive and non-invasive mechanical ventilation, the spontaneous breathing effort of the patient is supported with

mechanical inflations. Ideally, these mechanical inflations are synchronized with the onset and the end of a spontaneous breath. Historically, changes in airway pressure, airway flow and

volume have been used to detect the start of inspiration. However, during invasive mechanical ventilation this requires placement of a pressure or flow sensor in the patient circuit which

can increase physiological dead space which is a potential problem in infants requiring small tidal volumes. Furthermore, leakage around the endotracheal tube compromises the accuracy of

triggering.4 Air leakage is an even bigger problem when trying to synchronize non-invasive mechanical ventilation, with leaks via the mouth and around the nasal interface. This leads to

patient-ventilator asynchrony (PVA) which is associated with less effective support, prolonged mechanical ventilation, increased WOB, dynamic hyperinflation and an increased need for

sedation.4,31 The ability of dEMG to monitor the breathing cycles also provides the opportunity to use its signal to trigger the onset and offset of a mechanical inflation in response to a

spontaneous breath.6,7 The dEMG technique may reduce the delay time between the onset of the spontaneous breath and the start of the mechanical inflation as diaphragm contraction precedes

thoracic expansion and the subsequent change in flow and pressure.32 Furthermore, the dEMG measurement does not necessarily require a flow or pressure sensor in the patient circuit and is

not impacted by leakage at the airway opening. Although, in case of using dEMG to trigger respiratory support, a flow/pressure sensor could be used to enable flow/pressure based triggering

during periods of signal noise in the dEMG recording. If not suitable to have an additional flow/pressure sensor, one could activate back-up ventilation during dEMG signal noise periods.

Studies have shown that esophageal dEMG can be used to initiate and cycle off mechanical inflations during invasive and non-invasive respiratory support6,7, in a wide range of newborns,

including preterm and low birth weight infants, infants with unilateral diaphragmatic paralysis or congenital diaphragmatic hernia.6,33,34,35,36,37 Using esophageal dEMG to synchronize

(non-)invasive support in newborn infants, reduces PVA compared to other triggering modes.6,7,38 Synchronizing inflations with transcutaneous dEMG has not yet been studied. PROPORTIONAL

ASSIST BASED ON DEMG Some experts believe that respiratory support should unload the disease-related increase in WOB, also referred to as proportional assist ventilation. Given the ability

of dEMG to provide insight in breathing effort, diaphragm activity might be used as the input signal to determine the level of pressure needed to unload the inspiratory WOB of an individual

infant.4 Until now, proportional assist ventilation using dEMG is only available on one commercial ventilator, which uses an esophageal catheter to measure diaphragmatic activity. During

this so-called neurally adjusted ventilatory assist (NAVA) ventilation, the peak inflation pressure is proportional to the electrical activity of the diaphragm. The clinician sets the level

of pressure delivered per microvolt of diaphragm activity (“gain” or “NAVA-level”).6,7 Studies have shown that the concept of NAVA is feasible in newborn infants during both invasive and

non-invasive support.6,7 Regarding the long-term effects of NAVA, a retrospective study and a randomized controlled trial in extremely low birth weight preterm infants compared nasal CPAP

(nCPAP) to non-invasive NAVA. These studies observed among others a lower reintubation rate and a shorter duration of mechanical ventilation in the non-invasive NAVA group, and no difference

in the incidence of bronchopulmonary dysplasia and death.39,40 The duration of invasive ventilation did not differ in preterm infants on NAVA compared to conventional mechanical

ventilation.41 WEANING OF RESPIRATORY SUPPORT The ability of dEMG to provide insight in breathing effort can also be used to assess if the level or mode of (non-)invasive respiratory support

is sufficient for the individual patient. Most of the studies on dEMG have looked at its role in weaning patients of respiratory support. WEANING FROM INVASIVE RESPIRATORY SUPPORT Assessing

extubation readiness in newborns is challenging with a reported extubation failure rate varying between 13 and 46%.42,43,44,45,46,47 This may have serious consequences as continuing

invasive mechanical ventilation too long could lead to ventilator-induced lung injury and diaphragm dysfunction. On the other hand extubating too soon with subsequent failure is associated

with increased mortality, health care costs and length of hospital stay.48,49,50,51 Several studies investigated whether diaphragm activity measured before extubation could predict

extubation readiness. One study that measured transcutaneous dEMG showed a higher diaphragm activity (peak and tonic activity) before extubation in the infants that failed compared to the

infants successfully extubated.46 However, three other studies, two using esophageal and one using transcutaneous dEMG, observed no difference in diaphragm activity before extubation in

infants successfully extubated and those failing.47,52,53 Studies also investigated if measuring dEMG during a spontaneous breathing trial (SBT) could improve the prediction of extubation

failure. During a SBT the patient is switched from mechanical ventilation to endotracheal continuous positive airway pressure (CPAP) to challenge the patients’ ability to maintain adequate

gas exchange in absence of mechanical inflations.54 Two studies, one using esophageal and the other using transcutaneous dEMG, reported a significant increase in diaphragm activity in all

newborn infants during the SBT compared to mechanical ventilation.44,55 However, only one study using transcutaneous dEMG observed a significantly higher median increase in diaphragmatic

activity (expressed with the AUC) during the SBT in the group that failed extubation compared to those successfully extubated.55 Some studies assessed the change in diaphragm activity before

and after extubation, aiming to identify patients who are going to fail as soon as possible after extubation, thereby avoiding significant clinical deterioration on non-invasive support.

These studies reported an overall increase in diaphragm activity after extubation, which is probably caused by the reduction in level of support.46,53 When comparing the group of patients

successfully extubated and those failing, a relative increase in diaphragmatic activity was observed in the success cases. However, the group that showed higher absolute values of

diaphragmatic activity after extubation differed between the studies.46,53 Although the abovementioned studies show the potential of dEMG to assess extubation readiness and reduce infants

failing extubation, they also show that the results are inconsistent. Differences in measurement period, sample size, and mode of support after extubation may explain some differences

between the reported studies. Furthermore, an increase in diaphragmatic activity following extubation may be physiological to a certain level and promote successful extubation, while the

inability to do so may lead to extubation failure. On the other hand, requiring supraphysiological levels of diaphragmatic activity for a longer period of time might also be the cause of

extubation failure. Normative data collected in future studies might enable the clinician to differentiate between these two scenarios. The role of dEMG in weaning mechanical ventilation

settings (e.g., tidal volume, airway pressure) was examined in one study which described the effect of weaning positive end-expiratory pressure (PEEP) during mechanical ventilation on

diaphragmatic activity.56 Applying zero PEEP in intubated infants led to a significant increase in tonic activity of the diaphragm measured with esophageal dEMG, which was immediately

reversed after reapplying the PEEP. Although zero PEEP is usually not applied in clinical practice, this study does show the potential of dEMG to guide weaning of mechanical ventilation in

the future as PEEP seems to influence the tonic activity measured with dEMG. WEANING OF NON-INVASIVE RESPIRATORY SUPPORT In most institutions weaning non-invasive respiratory support is not

protocolized and left to the discretion of the attending physician who uses a trial and error approach, based on his/her own experience and clinical condition of the patient. A more

objective measure to wean non-invasive support is urgently needed and several studies investigated the potential role of dEMG for this application. One study, including stable preterm

infants on nCPAP, assessed the effect of changing the nCPAP level between 2, 4, and 6 cmH2O on diaphragmatic activity. They reported no significant changes in most of the dEMG parameters.27

Other studies, applying different high flow nasal cannula (HFNC) levels (4, 6 and 8 L/min) or weaning HFNC flow in steps of 1 L/min, also reported no significant differences in diaphragmatic

activity between different flows.57,58,59 As most of the infants did not show clinical deterioration during the weaning steps, these results could indicate that many infants were probably

overtreated and could be weaned more rapidly. Studies also assessed the effect of switching between different non-invasive support modalities on diaphragmatic activity. A cross-over study

between nCPAP (mean 5 cmH2O) and HFNC (mean 5 L/min) using esophageal dEMG, found no significant differences in diaphragm activity.60 Similarly, switching from nCPAP to HFNC in a 1:1

pressure-to-flow ratio also did not lead to changes in diaphragm activity measured with transcutaneous dEMG.61 As in most of these studies the intent was probably to switch between

modalities and not so much wean the level of support, the dEMG findings confirm that this was successful. Some studies measured changes in diaphragmatic activity when switching to a mode

considered less supportive or even no support at all. Two studies, measuring dEMG via the transesophageal route, reported an increase in peak activity, amplitude and neural RR when

transferring infants from HFNC to room air or low flow nasal cannula (LFNC).57,62 One of these studies also reported a trend towards higher diaphragm activity in the success group compared

to the group of infants that failed the weaning attempt.57 Another study showed that weaning from nCPAP from a median level of 3 cmH2O to a LFNC level of 1 L/min in stable preterm infants

initially increased peak and tonic diaphragmatic activity, measured with transcutaneous dEMG, followed by a gradual decrease over time. Infants failing this weaning attempt tended to have a

higher diaphragm activity than those successfully weaned.63 These studies again suggest that dEMG could potentially contribute to selecting the adequate mode and level of non-invasive

respiratory support. EFFECT OF OTHER RESPIRATORY INTERVENTIONS ON DEMG Studies have also used dEMG to assess the effect of other respiratory interventions on diaphragmatic activity, often to

clarify the working mechanism of these interventions on the respiratory system. One of these interventions is the administration of caffeine, a breathing stimulating drug often given to

preterm infants. Studies using transcutaneous and esophageal dEMG have shown that an intravenous loading dose of caffeine in spontaneously breathing infants or mechanically ventilated

infants results in an increased diaphragm activity.64,65,66 This increase of diaphragmatic activity resulted in an increased tidal volume and minute ventilation.65 In contrast, doxapram,

another breathing stimulant, had no effect on transcutaneous and esophageal measured diaphragm activity, indicating that this drug influences neural drive or breathing pattern rather than

effort.67,68 The effect of minimally invasive surfactant administration on dEMG was also studied. The authors reported a reduction of diaphragm activity in the majority of infants in the

first hour after surfactant treatment, which probably reflects the improved lung compliance resulting in less WOB.69 dEMG has also been used to assess respiratory interventions in the DR. A

study reporting that an initial high fraction of inspired oxygen (FiO2) increased minute volume compared to a low FiO2 in preterm infants, showed that this increased minute volume was

accompanied by a higher diaphragm activity measured with transcutaneous dEMG. This could suggest an oxygen dependent increase in diaphragm activity leading to improved ventilation.70,71 When

measuring dEMG and airway flow simultaneously, the active and passive phase of expiration can be discriminated. The active phase, also called post-inspiratory activity (PIA), describes the

remaining diaphragm activity during expiratory flow, while the passive phase could consist of a plateau in the dEMG waveform whilst expiratory flow remains present (or at least no

inspiratory flow is measured). After the passive expiratory phase, the diaphragm activity increases before inspiratory flow occurs, which is called the ramp inspiratory activity and

represents diaphragmatic contraction.72 A study showed that during hypercapnia the PIA as measured with transcutaneous dEMG was prolonged, suggesting that mechanisms to increase

end-expiratory lung volume via expiratory braking are intensified during hypercapnia in preterm infants. In addition to the PIA, the peak activity during inspiration was also increased

during hypercapnia.73 Another study showed that using a helium-oxygen mixture compared to air-oxygen during invasive ventilation, resulted in a reduction in diaphragm activity measured with

esophageal dEMG.7,74 This reduction was explained by the lower density and increased laminar flow of the helium-oxygen mixture compared to air, both reducing airway resistance and thereby

WOB.75 Lastly, certain sedatives also seem to influence diaphragm activity. For example, children on mechanical ventilation who received a bolus of propofol showed a mean reduction in

diaphragm activity measured with esophageal dEMG of 32%.76 Beck et al. also described that a reduction in sedation in newborn infants resulted in an increase in esophageal dEMG.7

DIAPHRAGMATIC DYSFUNCTION Diaphragm dysfunction caused by abnormal development or phrenic nerve damage can cause serious breathing problems.8 Currently, chest X-ray and ultrasound are used

to, respectively, show diaphragm elevation or reduced or absent diaphragmatic movement. However, these techniques have disadvantages such as exposure to radiation, the occurrence of

false-negative results caused by paradoxical movements of the diaphragm, or not being applicable at the bedside.77 Several case reports have indicated that dEMG can play an important role in

diagnosing diaphragmatic dysfunction in newborn infants. Absent or reduced diaphragmatic activity, measured with transcutaneous dEMG, has been reported in unilateral diaphragmatic

paresis.15 Unlike transcutaneous dEMG, in esophageal dEMG the detection of unilateral diaphragmatic dysfunction may be less clear compared to bilateral dysfunction because this technique is

unable to measure the electrical activity of the left and right hemisphere separately. In addition to the diagnosis of diaphragmatic dysfunction, repeated measurements or continuous

monitoring of transcutaneous or esophageal dEMG may also provide insight in spontaneous recovery over time.78 In case of neuromuscular disorders, the dEMG technique could identify aberrant

respiratory patterns in pediatric intensive care unit (PICU) patients that could not be observed clinically and, as mentioned before, a lowered neuro-muscular efficiency could be observed.29

The neuro-muscular efficiency is also lowered in critically ill PICU patients on mechanical ventilation and further decreases over time during mechanical ventilation, which could be due to

inspiratory muscle atrophy.28 Moreover, dEMG can detect diaphragmatic inactivity during mechanical ventilation, which could be suggestive for a surplus of assistance or sedation.79 KNOWLEDGE

GAPS In this narrative review, the potential of measuring diaphragm activity in preterm and term infants has been described and several knowledge gaps have been identified. First, normative

values of diaphragm activity representing an (in)adequate breathing effort are lacking. Second, the relation between diaphragm activity and WOB requires further research. Third, the ability

to trigger ventilator inflations and to provide proportional assist with transcutaneous dEMG should be studied. Finally, using dEMG to predict weaning readiness, to early detect weaning

failure and to individualize the mode and level of respiratory support require further research. FUTURE DIRECTIONS More information on these knowledge gaps could be obtained when widespread

routine dEMG monitoring is enabled as this would result in big (continuous) data recorded with a standardized measurement set-up. Nowadays, usage of dEMG is limited as only the esophageal

technique is applied in clinical practice. Esophageal dEMG is mainly used to trigger ventilator inflations and to provide proportional assist. When used during non-invasive support, it can

also monitor breathing and detect apnea. However, the esophageal dEMG technique is invasive, expensive and only available on one commercial ventilator. To further increase the accessibility

of dEMG, it would be beneficial if the transcutaneous technique would become available in clinical practice and could be enabled in combination with commercially available ventilators and/or

patient monitors. Before implementation can occur, this technique needs to be optimized. Transcutaneous dEMG should be measured without the need for additional electrodes and hardware. A

study has already shown that diaphragmatic activity can be measured using ECG/CI electrodes and the same hardware.80 The dEMG technique can be further improved by using a wireless and

non-adhesive interface to increase user- and patient-friendliness. For this purpose, a novel wireless and non-adhesive cardiorespiratory monitoring belt based on dEMG has been developed.14

When cardiorespiratory monitoring is performed with this belt, big data on dEMG can be obtained. In general, we do believe that incorporating the dEMG technique in already used hardware

(i.e., no additional electrodes are required and an existing connection to the cardiorespiratory monitor), would be preferable.80 The resulting big data could be used to assess the influence

of technical factors and factors determined by the patient on the variability of the measured signal strength. In addition, this data could contribute to obtaining normative dEMG values

(absolute µV or delta values) in infants or in subgroups of infants (e.g., different age or birth weight groups). When transcutaneous dEMG is introduced on a larger scale for

cardiorespiratory monitoring in clinical practice, data on neural breathing effort can be measured in a larger group of infants. These data could be used to obtain normative values by

grouping infants, to assess the relation with other WOB related measures, and to determine cut-off values that indicate weaning readiness and failure. Routine dEMG monitoring could also

stimulate further research on the role of dEMG in individualizing respiratory support by observing (changes in) diaphragm activity when changing the mode and level of respiratory support.

Moreover, research can be done on the ability to trigger ventilator inflations and to provide proportional assist based on the transcutaneous technique. CONCLUSION This review underlines the

potential of measuring diaphragmatic activity in clinical practice, using either esophageal or transcutaneous electrodes, in newborn infants. Electromyography provides accurate and direct

information on HR, RR, and breathing pattern, including the detection of apnea. In contrast to currently used monitoring techniques (ECG and CI), dEMG also provides information on (neural)

breathing effort. Although more evidence is needed, studies have shown that the characteristics of dEMG provide a great potential to use it for cardiorespiratory monitoring, triggering of

mechanical ventilation and selection of the optimal mode and level of respiratory support. Further development of the interface (non-adhesive and/or wireless), hardware and software will

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monitoring electrodes. _Pediatr. Pulmonol_. 57, 2754–2762 (2022). Download references AUTHOR INFORMATION AUTHORS AND AFFILIATIONS * Department of Neonatology, Amsterdam UMC location

University of Amsterdam, Meibergdreef 9, Amsterdam, the Netherlands Anouk W. J. Scholten, Ruud W. van Leuteren, Cornelia G. de Waal, Juliette V. Kraaijenga, Frans H. de Jongh, Anton H. van

Kaam & Gerard J. Hutten * Amsterdam Reproduction & Development research institute, Amsterdam, the Netherlands Anouk W. J. Scholten, Ruud W. van Leuteren, Cornelia G. de Waal, 

Juliette V. Kraaijenga, Anton H. van Kaam & Gerard J. Hutten * Faculty of Science and Technology, University of Twente, Drienerlolaan 5, Enschede, the Netherlands Frans H. de Jongh

Authors * Anouk W. J. Scholten View author publications You can also search for this author inPubMed Google Scholar * Ruud W. van Leuteren View author publications You can also search for

this author inPubMed Google Scholar * Cornelia G. de Waal View author publications You can also search for this author inPubMed Google Scholar * Juliette V. Kraaijenga View author

publications You can also search for this author inPubMed Google Scholar * Frans H. de Jongh View author publications You can also search for this author inPubMed Google Scholar * Anton H.

van Kaam View author publications You can also search for this author inPubMed Google Scholar * Gerard J. Hutten View author publications You can also search for this author inPubMed Google

Scholar CONTRIBUTIONS A.S. wrote the first version of the manuscript. A.S., R.v.L., F.d.J., C.d.W., J.K., A.v.K., and J.H. modified the manuscript. All authors have read and agreed to the

published version of the manuscript. CORRESPONDING AUTHOR Correspondence to Gerard J. Hutten. ETHICS DECLARATIONS COMPETING INTERESTS The authors declare no competing interests. ADDITIONAL

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Scholten, A.W.J., van Leuteren, R.W., de Waal, C.G. _et al._ Diaphragmatic electromyography in infants: an overview of possible clinical applications. _Pediatr Res_ 95, 52–58 (2024).

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