A literature review of the methodology of EMG recordings of the diaphragm

Journal of Electromyography and Kinesiology 20 (2010) 185–190

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Review

A literature review of the methodology of EMG recordings of the diaphragm G.J. Hutten *, H.F. van Thuijl, A.C.M. van Bellegem, L.A. van Eykern, W.M.C. van Aalderen Department of Paediatric Pulmonology, Academic Medical Centre (G8-211), Emma Children’s Hospital, University of Amsterdam, Meibergdreef 9, 1105 AZ Amsterdam, The Netherlands

a r t i c l e

i n f o

Article history: Received 28 July 2008 Received in revised form 24 February 2009 Accepted 26 February 2009

Keywords: Electromyography Diaphragm

a b s t r a c t Introduction: EMG measurements of the diaphragm (rEMG) provide insight in to ventilatory muscle activity. Applicability of these measurements has improved, but literature of the different rEMG measurement techniques is inconsistent. This makes it difficult to compare studies of rEMG technique. This study summarizes the current available literature on rEMG and focuses on the validation of the techniques. Furthermore, we propose to use validation criteria to improve the quality, for further research. Methods: Pubmed, Ovid Medline and EMBASE were searched for studies describing rEMG experiments with transcutaneous (tc-rEMG) and/or transesophageal (te-rEMG) methods.Validation criteria included feasibility, repeatability, signal disturbance and ECG gating. Results: 650 studies were eligible for reviewing; 211 were excluded, and 39 articles described the measurement technique and were analyzed according to the criteria. 194 studies referred to another paper with a description of the technique and 206 failed to describe the technique nor had references to it. Conclusions: Many studies showed neither a description of the technique used, nor a validation of this technique. Others referred to studies that described the measurement technique. We propose that future studies on rEMG measurements at least meet the above mentioned criteria, in order to be able to compare study results. Ó 2009 Elsevier Ltd. All rights reserved.

Contents 1. 2.

3. 4. 5.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1. Types of studies. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2. Type of participants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3. Types of outcome measures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.4. Search methods for identifying studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Methods of review . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Results. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.1. Quality of rEMG measurements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2. Limits of method . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.3. Conclusions and proposals for future rEMG studies in clinical settings . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1. Introduction Over the last decades electromyography (EMG) has progressed to become a useful clinical test. It records electrical activity of the muscle. This information is used to determine muscle capacity

* Corresponding author. Tel.: +31 20 5662851; fax: +31 20 6917735. E-mail address: [email protected] (G.J. Hutten). 1050-6411/$ - see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.jelekin.2009.02.008

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in terms of contractile functions and changes in various conditions (Stegeman et al., 2000). In addition to its diagnostic use in neuromuscular disorders, EMG has also been used to measure electrical activity of the diaphragm (rEMG). Using rEMG may help to provide a more comprehensive picture of the control of breathing, since the diaphragm is only one of the components in the generation of the tidal flow wave form. A comprehensive picture of the changes in lung mechanics in disease or exposure to environmental toxins or drugs

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can only be achieved when lung mechanics are measured in relation to changes in respiratory muscle activity. In clinical settings rEMG is frequently used in sleep studies (Stoohs et al., 2005) and in the field of intensive care (Sinderby et al., 1999; Beck et al., 2001; Emeriaud et al., 2006). In research, rEMG has proven helpful in providing better insight into breathing patterns in neonates (Prechtl et al., 1977), the control of breathing, and in the mechanism underlying tidal breathing (Lopes et al., 1981; Mortola et al., 1982; Kosch and Stark, 1984; Saboisky et al., 2007). Moreover, it has been used as a non-invasive tool in estimating lung function in children with asthma (Maarsingh et al., 2000), and in adults with COPD (Duiverman et al., 2004). Three methods are currently used to detect the electrical signal, and each type is useful in specific situations; the transcutaneous method (tc-rEMG) in which sensors are placed on the skin, the transesophageal method (te-rEMG) in which sensors are mounted on a catheter, which is positioned in the oesophagus and the intramuscular method (im-rEMG), in which needle or wire sensors are introduced in the muscle tissue. Standards concerning practical aspects of rEMG in general have been published (2002), that needs in mind when reading a rEMG study. The electrical signal of the diaphragm, when measured as tc-rEMG or te-rEMG, is considerably affected by interference of the electrical activity of the heart during contraction (Schweitzer et al., 1979; O’Brien et al., 1983; Sinderby et al., 1997). So, each method has pitfalls and results that have been published have led to question the value of such studies. Diaphragm activity monitoring techniques continue to develop and expand. Future studies will be compelled to compare results between different measurement systems. We hypothesise that most of the studies that have been performed up to now do not adhere to earlier defined standards. We aimed to address the available literature to the following issues: Which methods of rEMG measurement have been used, to what extent adhere the measurement techniques to the earlier defined standards concerning practical aspects of measurement (2002). In addition, we aimed to rate the available literature by category of evidence. Finally, based on these observations, we propose recommendations for future studies. 2. Methods 2.1. Types of studies All studies describing experiments with tc-rEMG and/or terEMG methods were included. Im-rEMG studies were excluded because of discomfort and invasiveness for individuals undergoing these measurements, making the test unsuitable for regular use in clinical settings. 2.2. Type of participants Individuals of all ages, with and without disease, were considered for this study. 2.3. Types of outcome measures Experiments describing both the tc-rEMG as well as the terEMG method were graded separately. The outcomes were the type of method of rEMG measurement, the description of the technique that was being used, and the quality of evidence. Papers with a description of the technique were subjected to different criteria which can be divided into general and validation criteria. General criteria were description of the population that was used in the study, and feasibility and reproducibility of the mea-

surements. Feasibility is defined as the percentage of subjects involved in the research on which the method was applied successfully. Short-term reproducibility was scored when recording instruments were kept in position and experiments were repeated, and when measurements of consecutive breaths were included in the original analysis. Long-term reproducibility was defined as the repetition of the experiment on different occasions. The validation criteria are based on earlier defined standards and apply to the technique of measurement (2002).With respect to the quality of the EMG signal these include a description of ECG interference with the EMG signal, e.g., ECG/QRS gating of the EMG signal, and minimization of the amount of interfering side noise, e.g., movement artefacts (Schweitzer et al., 1979; Zipp and Ahrens, 1979; O’Brien et al., 1983). When case authors referred to third papers containing information about validation of the technique, the reference was accessed and used in the analysis. The category of evidence was graded according Centre for Evidence Based Medicine, Oxford, scale () (Table 1). 2.4. Search methods for identifying studies Pubmed, MEDLINE (1950 – January 2007) and EMBASE (1980 – January 2007) were searched using the search terms ‘electromyography’ and ‘diaphragm’. The search was limited to English papers and human studies. 3. Methods of review Each study was independently reviewed by two reviewers. Reviewers were not blinded to authorship, journal or results at the time of review. Evaluation of the papers was performed by GJH an HFvT. Studies which met the inclusion criteria for the review were evaluated on the presence of a description of the EMG method. Furthermore, we evaluated whether the paper described the quality of the technique that was used. When authors referred to a third paper for technique validation, the referenced paper was used. (Fig. 1) shows the scoring algorithm used. When a paper was not lucid on one or more of our score criteria or the reviewers had different opinions on a paper, the reviewers reviewed the paper together and reached consensus as to whether or not to include the paper in the study. 4. Results We identified 493, 628 and 398 studies in Pubmed, MEDLINE, and EMBASE, respectively. All hits in Pubmed where also identified in MEDLINE. The search in EMBASE resulted in 25 other studies that were not found in Pubmed. Three studies from MEDLINE were excluded due to duplicate reporting, leaving 650 papers eligible for reviewing and inclusion in the analysis. Of these 650 studies 211 were excluded because they were inconsistent with the above mentioned inclusion criteria (79 studies described the im-rEMG technique and 132 did not concern rEMG experiments). Of the remaining 439 papers, the level of evidence was scored as follows: 39 studies at level IIb, 194 studies at level III, and 206 at level IV. 238 described the tc-rEMG technique and 176 the te-rEMG technique. In 25 papers both techniques were described. The 39 papers with a level IIb (the highest scoring level) described the measurement technique and are summarized in Table 2 (Guttmann and Silver, 1965; Lourenco and Mueller, 1967; Hixon et al., 1969; Lopata et al., 1976, 1977; Tusiewicz et al., 1977; Prechtl et al., 1977; Grassino et al., 1978; Schweitzer et al., 1979; Onal

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Table 1 Classification of recommendations and evidence. Level of evidence Ia Ib IIa IIb III IV

Evidence Evidence Evidence Evidence Evidence Evidence

Strength of recommendation A B C D

Directly Directly Directly Directly

from from from from from from

based based based based

meta-analysis of randomized controlled trials at least one randomized controlled trial at least one controlled study without randomization at least one other type of quasiexperimental study nonexperimental descriptive studies, such as comparative studies expert committee reports, or opinion, or clinical experience of respected authorities, or both on on on on

category category category category

I evidence II evidence or extrapolated recommendation from category I evidence III evidence or extrapolated recommendation from category I and II evidence IV evidence or extrapolated recommendation from category I, II or III evidence

Fig. 1. Flow charts for the analysis of the studies resulting in the level of evidence. For explanation of the level of evidence see (Table 1).

et al., 1979; Gross et al., 1979; Singhal et al., 1981; Bellemare and Grassino, 1982; Bruce and Goldman, 1983; O’Brien, 1985; McKenzie and Gandevia, 1985; Sieck et al., 1985; O’Brien et al., 1987; Worth et al., 1988; Chambille et al., 1989; Daubenspeck et al., 1989; Lansing and Savelle, 1989; Sharp et al., 1993; Sinderby et al., 1995; Beck et al., 1995, 1996; Weinberg et al., 1997; Beck et al., 1997; Sinderby et al., 1997; Luo et al., 1998, 1999a,b; Maarsingh et al., 2000; Hemmerling et al., 2000; Hemmerling et al., 2001; Duiverman et al., 2004; Luo and Moxham, 2005; Stoohs et al., 2005; Glerant et al., 2006). Of these 39 studies, 14 described the tc-rEMG technique, 18 the te-rEMG technique, and in 7 papers both techniques were described. The percentages of the papers that contained the different validation criteria are shown in Fig. 2. Signal disturbances and ECG gating were described in 17 (43.6%) and 30 (68.9%), respectively. In 27 papers (69.2%) reproducibility was investigated, in 24 (55.6%) of the papers feasibility was described. The quantity and description of the participants were reported in 38 (97.4%) and 30 (68.9%), respectively. The 194 papers with level III evidence failed to describe the technique that was used, but referred to third papers. The 206 papers with level IV evidence both failed to describe the technique that was used and did not refer to a third article. 5. Discussion We aimed to summarize the available literature of the different applications of rEMG and investigated whether the used methodology of the rEMG measurements was sufficiently described and validated. Only 39 of the 439 (8.9%) papers that were eligible for reviewing were rated in category IIb ‘‘Evidence from at least one

other type of quasiexperimental study”. No papers had a higher rating, and the rest of the papers had a lower rating. Signal disturbances and ECG gating was described in 17 (43.6%) and 30 (68.9%) papers, respectively. In 27 papers (69.2%) reproducibility was investigated, in 24 (55.6%) of the papers feasibility was described. We found that many studies lack a description of the population that was used, and miss general criteria such as feasibility and reproducibility of the technique that was used. Despite earlier validation criteria were defined by the ATS/ERS (2002), such as description of interference of the EMG signal by movements of the subjects, cross-talk between the QRS complex with the EMG, and description of ECG gating, a substantial amount of the reviewed studies failed to adhere to these standard. 5.1. Quality of rEMG measurements To our knowledge this is the first study that summarizes the available literature of the different applications of electromyography of the diaphragm, and investigates whether the methodology of the rEMG measurement was described and validated. Initially, rEMG was used in research settings (Strohl et al., 1980; Onal and Lopata, 1982), but it has progressed into a diagnostic tool in clinical settings (Hemmerling et al., 2001). Because of its invasiveness and inconvenience for subjects undergoing the measurements, this study does not include im-rEMG, despite that this method being reported to be safe, feasible and reliable (Chen et al., 1996). A considerable number (194) of papers referred to studies describing technical aspects of EMG measurements. However, none of the papers contains a complete description of all the crite-

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Table 2 Studies describing the measurement technique. Authors

Method

Beck et al. (1995) Beck et al. (1996) Beck et al. (1997) Bellemare and Grassino (1982) Bruce and Goldman (1983) Chambille et al. (1989) Daubenspeck et al. (1989) Duiverman et al. (2004) Glerant et al. (2006) Grassino et al. (1978) Gross et al. (1979) Guttmann and Silver (1965) Hemmerling et al. (2000) Hemmerling et al. (2001) Hixon et al. (1969) Lansing and Savelle (1989) Lopata et al. (1976) Lopata et al. (1977) Lourenco and Mueller (1967) Luo et al. (1998) Luo et al. (1999a) Luo et al. (1999b) Luo and Moxham (2005) Maarsingh et al. (2000) McKenzie and Gandevia (1985) O’Brien (1985) O’Brien et al. (1987) Onal et al. (1979) Prechtl et al. (1977) Schweitzer et al. (1979) Sharp et al. (1993) Sieck et al. (1985) Sinderby et al. (1995) Sinderby et al. (1999) Singhal et al. (1981) Stoohs et al. (2005) Tusiewicz et al. (1977) Weinberg et al. (1997) Worth et al. (1988)

te-rEMG te-rEMG te-rEMG te-rEMG tc-rEMG /te-rEMG tc-rEMG te-rEMG tc-rEMG tc-rEMG te-rEMG tc-rEMG/te-rEMG tc-rEMG tc-rEMG tc-rEMG te-rEMG tc-rEMG te-rEMG te-rEMG te-rEMG tc-rEMG/te-rEMG tc-rEMG/te-rEMG te-rEMG te-rEMG tc-rEMG tc-rEMG/te-rEMG tc-rEMG tc-rEMG te-rEMG tc-rEMG te-rEMG tc-rEMG/te-rEMG tc-rEMG/te-rEMG te-rEMG te-rEMG te-rEMG tc-rEMG tc-rEMG te-rEMG tc-rEMG

Signal disturbances p p p

p

ECG gating p p p p p p p p

p p p

p p p

p

p

p p p p

p p p p p p p p p p p p p p

p p

p p p p

Repeatability p p p p p p p p p p

Feasibility p p p

p

p p p

p

p

p p p p p p

p p p p p p

p p p p p p p

p p

p

p p

ria we have used for this study, such as description of the population, feasibility and reproducibility of the method, and technical information about the measurement technique.

Fig. 2. The different general and validation criteria expressed as a percentage of the total number of studies with description of the technique. Signal disturbance: Minimization of the amount of interfering side noise, e.g., movement artefacts. ECG gating: Description of ECG interference with the EMG signal, e.g., ECG/QRS gating of the EMG signal. Repeatability: The recording instruments were kept in position and experiments were repeated, and when measurements of consecutive breaths were included in the original analysis. Feasibility: the percentage of subjects involved in the research on which the method was applied successfully. Participant’s quantity: The total amount of participants. Participant’s description: Description of the participants (e.g., healthy participants).

p

p p

p p p p p p p

Participants quantity p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p

Participants description p p p p p p p p p p p p

p p p p p p p p p p p p p p p p p p

Description of the feasibility of a technique is an important step in the ongoing process, from the use in research settings, towards use in a more clinical setting. Information about reasons for exclusion of subjects or measurements is important for the validation process of a technique, and may be of importance when deciding on whether or not to implement the technique. The closeness of agreement between the results of the successive measurements obtained under the same conditions, i.e., repeatability, is an important criterion to describe. For rEMG measurements this requires a stable electrical signal, expressed in stable frequency and amplitudes values. Line frequency and movement artefacts greatly diminish the signal quality (O’Brien et al., 1983). Line frequency is caused by capacitive coupling of the subject’s body, as well as of the electrode cables, to surrounding power lines and mainspowered equipment. Motion artifact voltages result from mechanical disturbances of electrodes, which will result in change in electrode impedances and therefore will cause change in output signal during movements (Zipp and Ahrens, 1979). Thus, the recognition of possible artifacts is important in analyzing the signal. Ignoring these criteria will affect the rEMG signal results and makes therefore the interpretation of these results less reliable. The electrical signal of the EMG when measured as tc-rEMG or te-rEMG, is considerably affected by interference of the electrical activity of the heart during contraction (Schweitzer et al., 1979; O’Brien et al., 1983; Sinderby et al., 1997). This interference is intense, because the intensity of the cardiac pulse is much stronger than that of the electrical signal of the respiratory muscles, and influences amplitude and frequency parameters of the EMG. Up to now, there is no ideal manner of separating the ECG and

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EMG components from the signal have been found. The two methods currently employed for the reduction of the ECG contamination are the gating technique (Schweitzer et al., 1979; van Eykern et al., 2001) and the (double-)subtraction technique(Lopata et al., 1976; Levine et al., 1986; Sinderby et al., 1997). The former technique involves the removal of a section of the EMG signal centered on the QRS complex. The created gate is filled with a running average (Schweitzer et al., 1979; Sprikkelman et al., 1998; Maarsingh et al., 2000). Two limitations have been recognized with this technique: First, greater proportions of the rEMG signal must be gated with an increasing of the heart rate, and secondly, segments of rEMG activity of particular interest must be discarded if they are contaminated by ECG activity (Levine et al., 1986). The subtraction technique implies the subtraction of an ECG template from the EMG signal of the diaphragm at each occurrence of the ECG waveform (Bartolo et al., 1996). This technique may not work if the ECG signal is fluctuating (Fox et al., 1988). Until now we have found no consensus on which technique is preferred, and for which purpose. 5.2. Limits of method The validation criteria of the ATS/ERS were defined in 2002 (2002), so the question arises whether it is possible to evaluate studies before 2002 with these criteria. This study strives to provide insight in the quality of the tc-rEMG or te-rEMG applications. With this insight it may be possible to increase the quality of the rEMG technique in future research. The rEMG appears to be a promising technique to provide a more comprehensive picture of the control of breathing. 5.3. Conclusions and proposals for future rEMG studies in clinical settings We summarized the literature on tc-rEMG and te-rEMG measurements and investigated whether the used methodology of these rEMG measurements was described and validated. Furthermore we tried to estimate the level of evidence for each of these applications. We found that most studies lack one or more of the general and/ or validation criteria. Only a minority of the studies (8.9%) scored an evidence level IIb, all other studies had a lower rating. Our observations indicate that there is a need for further validation of the EMG of the respiratory muscles. For this validation process it is important to start with level 1 diagnostics (randomized controlled trials) or validating cohort studies with homogeneity. The clinical usefulness of the different techniques depends not only on its ability to measure parameters to discriminate between health and disease and to clarify the underlying pathophysiology. Also within-subject reproducibility both within and between test occasions is important. For example, ability to assess repeatability of rEMG measurements in intubated patients is influenced by factors as clinical instability, or the challenge of maintaining stable measurements conditions in the face of changing clinical status. So there is a need for studies which describe parameters to distinguish what constitutes a clinically significant change as a result of disease progression or response to treatment in individual patients or as part of a clinical trial. This leads to a prognostic estimation or a diagnostic category. Furthermore, it seems necessary to achieve to a consensus on how to reduce the contamination of the rEMG signal by the ECG signal. Acknowledgement The authors are grateful to Gavin ten Tusscher for editorial advice.

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References ATS/ERS Statement on respiratory muscle testing. Am J Respir Crit Care Med 2002;166:518–624. Bartolo A, Roberts C, Dzwonczyk RR, Goldman E. Analysis of diaphragm EMG signals: comparison of gating vs. subtraction for removal of ECG contamination. J Appl Physiol 1996;80:1898–902. Beck J, Sinderby C, Weinberg J, Grassino A. Effects of muscle-to-electrode distance on the human diaphragm electromyogram. J Appl Physiol 1995;79:975–85. Beck J, Sinderby C, Lindstrom L, Grassino A. Influence of bipolar esophageal electrode positioning on measurements of human crural diaphragm electromyogram. J Appl Physiol 1996;81:1434–49. Beck J, Sinderby C, Lindstrom L, Grassino A. Diaphragm interference pattern EMG and compound muscle action potentials: effects of chest wall configuration. J Appl Physiol 1997;82:520–30. Beck J, Gottfried SB, Navalesi P, Skrobik Y, Comtois N, Rossini M, et al. Electrical activity of the diaphragm during pressure support ventilation in acute respiratory failure. Am J Respir Crit Care Med 2001;164:419–24. Bellemare F, Grassino A. Evaluation of human diaphragm fatigue. J Appl Physiol 1982;53:1196–206. Bruce EN, Goldman MD. High-frequency oscillations in human respiratory electromyograms during voluntary breathing. Brain Res 1983;269:259–65. Chambille B, Vardon G, Monrigal JP, Dehan M, Gaultier C. Technique of on-line analysis of diaphragmatic electromyogram activity in the newborn. Eur Respir J 1989;2:883–6. Chen R, Collins SJ, Remtulla H, Parkes A, Bolton CF. Needle EMG of the human diaphragm: power spectral analysis in normal subjects. Muscle Nerve 1996;19:324–30. Daubenspeck JA, Leiter JC, McGovern JF, Knuth SL, Kobylarz EJ. Diaphragmatic electromyography using a multiple electrode array. J Appl Physiol 1989;67:1525–34. Duiverman ML, van Eykern LA, Vennik PW, Koeter GH, Maarsingh EJ, Wijkstra PJ. Reproducibility and responsiveness of a noninvasive EMG technique of the respiratory muscles in COPD patients and in healthy subjects. J Appl Physiol 2004;96:1723–9. Emeriaud G, Beck J, Tucci M, Lacroix J, Sinderby C. Diaphragm electrical activity during expiration in mechanically ventilated infants. Pediatr Res 2006;59:705–10. Fox RE, Kosch PC, Feldman HA, Stark AR. Control of inspiratory duration in premature infants. J Appl Physiol 1988;64:2597–604. Glerant JC, Mustfa N, Man WD, Luo YM, Rafferty G, Polkey MI, Moxham J. Diaphragm electromyograms recorded from multiple surface electrodes following magnetic stimulation. Eur Respir J 2006;27:334–42. Grassino A, Goldman MD, Mead J, Sears TA. Mechanics of the human diaphragm during voluntary contraction: statics. J Appl Physiol 1978;44:829–39. Gross D, Grassino A, Ross WR, Macklem PT. Electromyogram pattern of diaphragmatic fatigue. J Appl Physiol 1979;46:1–7. Guttmann L, Silver JR. Electromyographic studies on reflex activity of the intercostal and abdominal muscles in cervical cord lesions. Paraplegia 1965;3:1–22. Hemmerling TM, Schmidt J, Hanusa C, Wolf T, Schmitt H. Simultaneous determination of neuromuscular block at the larynx, diaphragm, adductor pollicis, orbicularis oculi and corrugator supercilii muscles. Br J Anaesth 2000;85:856–60. Hemmerling TM, Schmidt J, Wolf T, Hanusa C, Siebzehnruebl E, Schmitt H. Intramuscular versus surface electromyography of the diaphragm for determining neuromuscular blockade. Anesth Analg 2001;92:106–11. Hixon TJ, Siebens AA, Minifie FD. An EMG electrode for the diaphragm. J Acoust Soc Am 1969;46:1588–90. Kosch PC, Stark AR. Dynamic maintenance of end-expiratory lung volume in fullterm infants. J Appl Physiol 1984;57:1126–33. Lansing R, Savelle J. Chest surface recording of diaphragm potentials in man. Electroencephalogr Clin Neurophysiol 1989;72:59–68. Levine S, Gillen J, Weiser P, Gillen M, Kwatny E. Description and validation of an ECG removal procedure for EMGdi power spectrum analysis. J Appl Physiol 1986;60:1073–81. Lopata M, Evanich MJ, Lourenco RV. The electromyogram of the diaphragm in the investigation of human regulation of ventilation. Chest 1976;70:162–5. Lopata M, Evanich MJ, Lourenco RV. Quantification of diaphragmatic EMG response to CO2 rebreathing in humans. J Appl Physiol 1977;43:262–70. Lopes J, Muller NL, Bryan MH, Bryan AC. Importance of inspiratory muscle tone in maintenance of FRC in the newborn. J Appl Physiol 1981;51:830–4. Lourenco RV, Mueller EP. Quantification of electrical activity in the human diaphragm. J Appl Physiol 1967;22:598–600. Luo YM, Moxham J. Measurement of neural respiratory drive in patients with COPD. Respir Physiol Neurobiol 2005;146:165–74. Luo YM, Polkey MI, Johnson LC, Lyall RA, Harris ML, Green M, et al. Diaphragm EMG measured by cervical magnetic and electrical phrenic nerve stimulation. J Appl Physiol 1998;85:2089–99. Luo YM, Lyall RA, Lou HM, Rafferty GF, Polkey MI, Moxham J. Quantification of the esophageal diaphragm electromyogram with magnetic phrenic nerve stimulation. Am J Respir Crit Care Med 1999a;160:1629–34. Luo YM, Johnson LC, Polkey MI, Harris ML, Lyall RA, Green M, et al. Diaphragm electromyogram measured with unilateral magnetic stimulation. Eur Respir J 1999b;13:385–90.

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G.J. Hutten et al. / Journal of Electromyography and Kinesiology 20 (2010) 185–190

Maarsingh EJ, van Eykern LA, Sprikkelman AB, Hoekstra MO, van Aalderen WM. Respiratory muscle activity measured with a noninvasive EMG technique: technical aspects and reproducibility. J Appl Physiol 2000;88:1955–61. McKenzie DK, Gandevia SC. Phrenic nerve conduction times and twitch pressures of the human diaphragm. J Appl Physiol 1985;58:1496–504. Mortola JP, Fisher JT, Smith B, Fox G, Weeks S. Dynamics of breathing in infants. J Appl Physiol 1982;52:1209–15. O’Brien MJ. Respiratory EMG findings in relation to periodic breathing in infants. Early Hum Dev 1985;11:43–60. O’Brien MJ, van Eykern LA, Prechtl HF. Monitoring respiratory activity in infants: a non-intrusive diaphragm EMG technique. In: Rolfe Peter, editor. Non-invasive physiological measurements 1983;2. London: Academic Press; 1983. p. 131–77. O’Brien MJ, van Eykern LA, Oetomo SB, Van Vught HA. Transcutaneous respiratory electromyographic monitoring. Crit Care Med 1987;15:294–9. Onal E, Lopata M. Periodic breathing and the pathogenesis of occlusive sleep apneas. Am Rev Respir Dis 1982;126:676–80. Onal E, Lopata M, Evanich MJ. Effects of electrode position on esophageal diaphragmatic EMG in humans. J Appl Physiol 1979;47:1234–8. Prechtl HF, van Eykern LA, O’Brien MJ. Respiratory muscle EMG in newborns: a nonintrusive method. Early Hum Dev 1977;1:265–83. Saboisky JP, Gorman RB, De TA, Gandevia SC, Butler JE. Differential activation among five human inspiratory motoneuron pools during tidal breathing. J Appl Physiol 2007;102:772–80. Schweitzer TW, Fitzgerald JW, Bowden JA, Lynne-Davies P. Spectral analysis of human inspiratory diaphragmatic electromyograms. J Appl Physiol 1979;46:152–65. Sharp JT, Hammond MD, Aranda AU, Rocha RD. Comparison of diaphragm EMG centroid frequencies: esophageal versus chest surface leads. Am Rev Respir Dis 1993;147:764–7. Sieck GC, Mazar A, Belman MJ. Changes in diaphragmatic EMG spectra during hyperpneic loads. Respir Physiol 1985;61:137–52. Sinderby C, Lindstrom L, Grassino AE. Automatic assessment of electromyogram quality. J Appl Physiol 1995;79:1803–15. Sinderby CA, Beck JC, Lindstrom LH, Grassino AE. Enhancement of signal quality in esophageal recordings of diaphragm EMG. J Appl Physiol 1997;82:1370–7. Sinderby C, Navalesi P, Beck J, Skrobik Y, Comtois N, Friberg S, et al. Neural control of mechanical ventilation in respiratory failure. Nat Med 1999;5:1433–6. Singhal SS, Jain VK, Jain VK, Bhatia VK, Dwivedi RN, Nath K. Integrated electric activity of the diaphragm in health and cardiopulmonary diseases. J Assoc Physicians India 1981;29:89–93. Sprikkelman AB, van Eykern LA, Lourens MS, Heymans HS, van Aalderen WM. Respiratory muscle activity in the assessment of bronchial responsiveness in asthmatic children. J Appl Physiol 1998;84:897–901. Stegeman DF, Blok JH, Hermens HJ, Roeleveld K. Surface EMG models: properties and applications. J Electromyogr Kinesiol 2000;10:313–26. Stoohs RA, Blum HC, Knaack L, Butsch-von-der-Heydt B, Guilleminault C. Comparison of pleural pressure and transcutaneous diaphragmatic electromyogram in obstructive sleep apnea syndrome. Sleep 2005;28:321–9. Strohl KP, Hensley MJ, Hallett M, Saunders NA, Ingram Jr RH. Activation of upper airway muscles before onset of inspiration in normal humans. J Appl Physiol 1980;49:638–42. Tusiewicz K, Moldofsky H, Bryan AC, Bryan MH. Mechanics of the rib cage and diaphragm during sleep. J Appl Physiol 1977;43:600–2. van Eykern LA, Maarsingh EJ, van Aalderen WM. Two similar averages for respiratory muscle activity. J Appl Physiol 2001;90:2014–5. Weinberg J, Sinderby C, Sullivan L, Grassino A, Lindstrom L. Evaluation of diaphragm electromyogram contamination during progressive inspiratory maneuvers in humans. Electromyogr Clin Neurophysiol 1997;37:143–53. Worth H, Grahn S, Lakomek HJ, Bremer G, Goeckenjan G. Lung function disturbances versus respiratory muscle fatigue in patients with systemic lupus erythematosus. Respiration 1988;53:81–90. Zipp P, Ahrens H. A model of bioelectrode motion artefact and reduction of artefact by amplifier input stage design. J Biomed Eng 1979;1:273–6.

Jeroen Hutten worked at the frontier between biomedical engineering and lung physiology. He implemented a new technology of measuring EMG of the respiratory muscles in infants and compared this technique with standard infant lung function in spontaneously breathing unsedated infants.

Hinke van Thuijl, medical student.

Annemarie van Bellegem, Paediatrician.

Leo van Eykern is autodidacted in the fields of medical electronics, electrophysiology, neurophysiology and movement sciences. Worked at the Medical Faculty of the University of Groningen for the departments of Developmental Neurology, Medical Physiology, Movement Sciences and Neurology. Research topics: developing electronic measurement systems, signal analysis methods and software packages for building virtual physiological instruments. Holds several patents on these topics. Teaches in Biomedical Technologies (BMT) the subject Physiological Instruments. Consultancies in research and industrial projects.

Wim van Aalderen is professor in Paediatric Respiratory Medicine and Vice Chairman of the Emma Childrens Hospital AMC. The scope of his research focusses on the development of paediatric asthma early in life.