Clinical Science (2008) 115, 233–244 (Printed in Great Britain) doi:10.1042/CS20070348
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Diaphragm electromyography using an
oesophageal catheter: current concepts
Yuan Ming LUO∗ , John MOXHAM† and Michael I. POLKEY‡
*Guangzhou Medical College, National Key Laboratory of Respiratory Disease, Guangzhou 510210, People’s Republic of China,
†Department of Respiratory Medicine, King’s College Hospital, London SE5 9PJ, U.K., and ‡Respiratory Muscle Laboratory,
Royal Brompton Hospital, London SW3 6NP, U.K.
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The usefulness of diaphragm electromyography recorded from an oesophageal electrode depends
on a reliable signal which is free of artefact. The diaphragm EMG (electromyogram) recorded
from chest wall surface electrodes may be unreliable because of signal contamination from muscle
activity other than the diaphragm. Initially, the oesophageal electrode catheter for human studies
had only one electrode pair, which could be difficult to position accurately and was influenced by
a change in lung volume. Recently, a multipair oesophageal electrode has been developed which
allows a high-quality EMG to be recorded. In the present review, the progress of oesophageal electrode design is outlined. The effects of signal contamination, electrode movement and particularly
the effect of change in lung volume on the diaphragm EMG are discussed. The diaphragm EMG,
recorded from a multipair oesophageal electrode, is useful to assess neural respiratory drive and
diaphragm function in different groups of patients with respiratory disease, including patients with
neuromuscular disease and sleep-disordered breathing, and those in the intensive care unit. When
combined with cervical and cranial magnetic stimulation, an oesophageal electrode can be used
to partition the central respiratory response time and phrenic nerve conduction time.
INTRODUCTION
The diaphragm is the most important respiratory muscle,
accounting for 70 % of respiration in normal humans [1].
Diaphragm weakness is associated with breathlessness
and respiratory failure [2–6]. Electrical assessment of
diaphragm and phrenic nerve function can provide important information on the diagnosis and management of
patients with neuromuscular disease [7–13]. By recording
the diaphragm CMAP (compound muscle action potential) and MEPs (motor-evoked potentials), respiratory
neural pathways can also be assessed [14–19]. The diaphragm EMG (electromyogram) is also useful in detecting diaphragm fatigue [20–25] and assessing neural respiratory drive [26–34], as well as to trigger [33] and adjust
[34] mechanical ventilation. Measurement of the electrical
activity offers different and complimentary information
to that provided by the measurement of oesophageal pressure and Pdi (transdiaphragmatic pressure). However, the
usefulness of the diaphragm EMG is dependent on
the accurate recording of the signal without artefact.
Three methods can be used in humans to record a
diaphragm EMG: needles, surface electrodes and an
oesophageal catheter. Although needle electrodes have
been used in humans in small physiological studies
[35,36], they are impractical for most clinical studies,
particularly if there are factors which increase the risk
of and from a pneumothorax.
Chest wall surface electrodes provide a non-invasive
technique and have been used to record the diaphragm
Key words: diaphragm, diaphragm function, electromyography, neural respiratory drive, oesophageal electrode, respiratory muscle.
Abbreviations: CMAP, compound muscle action potential; COPD, chronic obstructive pulmonary disease; EMG, electromyogram;
Fc, centroid frequencies; H/L ratio, ratio of high-frequency power to low-frequency power; ICU, intensive care unit; MEP, motorevoked potential; OSA, obstructive sleep apnoea; Pdi , transdiaphragmatic pressure; RMS, root mean square.
Correspondence: Professor Michael I. Polkey (email [email protected]).
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Figure 1 CMAP recorded simultaneously from lower chest
wall and oesophageal electrodes during stimulation of the
phrenic nerve only (upper traces) and both the brachial
plexus and the phrenic nerve (lower traces)
In the lower chest wall recording, the latency of CMAP is shorter when stimulation
co-activates the brachial plexus. The amplitude of CMAP is also reduced. In the
oesophageal recordings, the waveforms of CMAP are similar. Four stimulations
are superimposed; results are from one subject. This Figure was reproduced from
Thorax (1999), volume 54, pp. 765–770, with permission from the BMJ Publishing
Group.
EMG, but this approach has disadvantages. First, the
diaphragm EMG recorded from the chest wall surface
electrodes can be unreliable because of signal contamination [37–40]. It has been reported that the diaphragm
CMAP recorded from chest wall surface electrodes is
likely to be contaminated by signals from adjacent
muscles when the brachial plexus is co-activated, particularly likely with magnetic stimulation [37–39] (Figure 1).
Similarly, the power spectrum and RMS (root mean
square) activity derived from the spontaneous diaphragm
EMG recorded from chest wall surface electrodes can be
unreliable because of cross-talk signals from intercostal
and abdominal muscles, which are also active during
loaded breathing [40]. Secondly, the diaphragm EMG
recorded from chest wall surface electrodes can be
affected by subcutaneous fat, which significantly reduces
signal strength due to muscle-to-electrode filtering effects
[41]. Thirdly, it has been reported that the surface
diaphragm CMAP is subject to power line artefacts
[42]. Finally, although several possible sites have been
reported [13,17,18,37–39,43,44], there is no standardized
method for placing the chest wall electrodes, which
makes data comparison between subjects and studies
difficult. In contrast, the diaphragm EMG recorded from
an oesophageal electrode is less affected by obesity, power
line artefact and cross-talk signals [37–41]. Consequently,
oesophageal diaphragm electromyography has become
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an increasingly important clinical and research technique
[7,10,11,18,20–28,30–34,37–41,44]. Because assessment
of diaphragm function, including electromechanical
efficiency, is best done by recording both Pdi (gastric
pressure−oesophageal pressure) and the diaphragm
EMG, a single EMG electrode catheter mounted with
two balloons for measurement of oesophageal and gastric
pressure [45–47] has additional advantages over chest wall
surface electrodes.
Historically, the diaphragm was considered as one
muscle [48]; however, studies have suggested that the
diaphragm consists of two separate muscles, the costal
and crural diaphragm [49]. This distinction is important
because the oesophageal EMG measures signals from the
crural component, whereas surface electrodes measure
signals from the costal component. Some studies have
found a small difference between the crural and costal
diaphragm. An animal study [50] showed that there
was more post-inspiratory activity in the costal than
the crural muscle, but the distinction was most apparent
during anaesthesia. It has also been reported, in cats, that
the crural EMG is more sensitive to CO2 stimulation
and to changes brought about by posture than the costal
EMG [51]. However, the close correlation of the electrical
activity in the crural and the costal parts has been well
documented in humans during respiratory tasks [52,53].
The EMG recorded from the costal diaphragm was
similar to that from the crus in terms of synchronous
activation and time course in both quiet and loaded
breathing [48,51,54]. Lastly, in a series of studies, Sharshar
et al. [18] showed that the effect of various respiratory
tasks on the diaphragm MEP was the same whether
measured from oesophageal or surface electrodes. It
should be noted, however, that other tasks relating to
specific functions (e.g. postural or gastro-oesophageal
sphincter control) may well be associated with differential
activation of different portions of the diaphragm. The
diaphragm EMG recorded by an oesophageal electrode
is mainly from the crural part [55–58].
OESOPHAGEAL ELECTRODE DESIGN
Oesophageal electrodes have been used for more than
40 years since they were introduced for recording human
diaphragm EMGs in the 1960s [55,59]. An oesophageal
electrode consists of an oesophageal catheter with metal
coils at the distal end. Initially, oesophageal electrode
catheters contained only one electrode pair [55,59].
Later, a modified oesophageal electrode with three
pairs of electrodes was used [56]. Multipair electrodes
with more than three pairs have been widely used
[7,10,11,18,27,28,30–34,37–39,45,60,61]. Different metals
have been used to construct oesophageal electrodes,
including stainless steel [60,61], copper [23,25–28], silver
[55,58,62] and platinum [46,63].
Oesophageal diaphragm electromyography
a good quality diaphragm EMG or CMAP can also be
recorded using an interelectrode distance of 3 cm within
a pair [7,10,11,27,28,38].
A power line artefact is one of the most common problems with recording the diaphragm EMG; it originates
from the power line and mains power equipment and
will typically have a 50 or 60 Hz signal depending on
the power source. Proper earth connections and using a
differential amplifier with a high common mode rejection
ratio (e.g. > 100 dB) are useful to reduce the artefact
[7,66]. An isolated pre-amplifier with ‘notch filters’ and
shielded electrode cable can minimize the artefact further.
Another source of artefact is electrode motion, which
usually occurs during voluntary contractions, but it is
relatively easy to deal with by using a high-pass-filter
setting at 20 Hz [25,66]. The diaphragm CMAP produced
by single twitch is usually free of motion artefact, as
electrical activity occurs prior to any mechanical response
[39]. Oesophageal peristalsis produces an additional lowfrequency large amplitude deflection of the baseline, but
does not cause major problems if a high-pass-filter setting
at 10 or 20 Hz is used [27,28,66].
Figure 2 Diaphragm CMAP recorded from an oesophageal
electrode with different configurations
Left-hand panel, oesophageal electrode: pair A (electrodes 6 and 5), pair B
(electrodes 6 and 4), pair C (electrodes 6 and 3), pair D (electrodes 6 and 2)
and pair E (electrodes 6 and 1). Right-hand panel, diaphragm CMAP simultaneously
recorded from the five pairs of electrodes during bilateral magnetic phrenic nerve
stimulation. CMAP recorded from pair A has the smallest amplitude. The amplitude
of CMAP increases with increasing interelectrode distance. The amplitude of CMAP
recorded from pair C is 94 % of the amplitude of pair E. CMAP recorded from
pair C has a more stable baseline than that recorded from pair D and E. Two
signals are superimposed.
Interelectrode distance is important for the accuracy of
recording the diaphragm EMG. Because the amplitude
of the diaphragm CMAP elicited by phrenic nerve stimulation, and the magnitude of the diaphragm EMG during
spontaneous breathing, relates to interelectrode distance
[58] (Figure 2), to ensure data are comparable a constant
interelectrode distance should be used. However,
different interelectrode distances have been used since
oesophageal recording was introduced. Initially, a 1 cm
interelectrode distance was usually used [46,53,55,59,63],
but other electrode configurations have also been
employed; for example Gross et al. [64] used a 1.8 cm
interelectrode distance. Some investigators have used a
< 1 cm interelectrode distance [23,25,60,61]. McKenzie
and Gandevia [58] found that the amplitude of CMAP
increased with increasing interelectrode distance and
they therefore used a 5 cm interelectrode distance [58,65].
There is no universal agreement about the optimal interelectrode distance, although an interelectrode distance
of 1 cm was usually used to record interference pattern
EMGs by Sinderby’s group [32,34]. We have found that
ECG ARTIFACT
The diaphragm CMAP recorded from the oesophageal
electrode can be contaminated by the superimposed
ECG. The diaphragm EMG frequency is from 20–
250 Hz, whereas most of the ECG frequency is 0–
100 Hz [25]. It is therefore difficult to eliminate the
ECG effectively using filters because of the overlap in
the range of the two signals, although the P and T waves
are relatively easy to delete by setting a high-pass filter at
20 Hz [20,25]. Wiener filtering could be useful to reduce
the ECG artefact, but it is usually unable to completely
separate the ECG from the EMG [67]. Many methods
have been used to reduce or eliminate the ECG artefact.
Gating techniques are often used online or offline, which
delete both the EMG and QRS complex simultaneously
for approx. 0.4 s around the QRS complex [25,68]. Some
investigators have attempted to zero the EMG signal
for the duration of QRS complex and to replace it with
adjacent EMG activity [67] (Figure 3). A similar method,
which we have favoured, is to analyse the EMG between
QRS complexes [27,28,64], for example selected data
between 50–75 % of the QRS complex interval [67], or
to trigger sampling of the EMG with the ECG after a
time delay [20]. Because the diaphragm EMG amplitude
can be larger than the ECG during maximal breathing, it
is not always reliable to trigger sampling with the ECG
when using an oesophageal electrode, so surface signals
are preferred for this purpose [20]. An additional channel
for recording the ECG is sometimes necessary to act as
a trigger source [20]. A more complex method is subtraction of the ECG template from the EMG signal in the
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Figure 3 Diaphragm EMG contaminated by an ECG (lefthand panel) and the section with the ECG deleted using a
gate method and replaced with a section from an adjacent
EMG (right-hand panel)
section contaminated by the ECG waveform [68]. Several
procedures are employed, including generating an ECG
template by averaging the number of QRS complexes during expiration, and alignment of an ECG template to the
ECG complexes overlapping the EMG and subtracting
the ECG template from the EMG contaminated by ECG.
These methods are considered to be more complicated
than gating but also more accurate [68]. Fortunately,
the effect of the ECG on the diaphragm CMAP elicited
by phrenic nerve stimulation can be eliminated easily by
simply discarding those CMAPs contaminated by the
ECG, because the baseline and shape of the CMAP
overlapped by the ECG will change [7,37–39,69].
EFFECT OF CHANGES IN LUNG VOLUME ON
THE DIAPHRAGM EMG
Concerns about changes in lung volume on the diaphragm
EMG have hampered the application of the oesophageal
diaphragm EMG in clinical practice. Many studies
[53,60,62,65,70,71] have tried to address the effect of lung
volume on the amplitude of the diaphragm EMG by using
different electrode design. It was hypothesized that a
change in the amplitude of the diaphragm CMAP was
due to alternations in the distance between the electrode
and the diaphragm secondary to the change in lung
volume during respiration [65]. On this basis, a balloonanchored oesophageal electrode catheter was considered,
at this time, to be useful to more reliably record the
diaphragm CMAP. However, Smith and Bellemare [62]
found that diaphragm CMAP changed with the movement of the electrode during respiration, despite using
a balloon-anchored oesophageal catheter. To retain
the anatomical relationship between the electrode and
diaphragm during respiration, Gandevia and McKenzie
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[65] added an additional weight at the proximal part of the
catheter, which itself had a ‘stabilized’ balloon at the distal
end, to let the catheter be slightly pulled out by the weight
during expiration and pulled in by the pushing of the balloon by the diaphragm during inspiration. However, they
found the diaphragm CMAP amplitude (peak to peak) at
TLC (total lung capacity) was 3.4 times larger than at RV
(residual volume), indicating either that their technique
could not effectively maintain electrode position or that
the distance between the electrode and the diaphragm
was not the cause of the variance. They also observed
that during deep breathing the electrode catheter could
move up to 8 cm, which is beyond the maximal movement
of the crus [61,70]. The large movement of the catheter
during respiration suggested that the catheter with both
a balloon and the weight was actually unable to reliably
record the diaphragm EMG because the electrodes failed
to track the movement of the crus of the diaphragm
[70,71]. Previously, we have used a multipair oesophageal
electrode with an interelectrode distance of 3 cm within
a pair and found that changes in lung volume of up to
2 litres had little effect on the amplitude of the diaphragm
CMAP, providing the oesophageal electrode catheter was
optimally positioned and then fixed on the nose [71].
However, Beck et al. [70] reported that the amplitude of
the diaphragm CMAP changes with lung volume when
using an electrode with an interelectrode distance of
1.0 cm within a pair. Nevertheless, it now seems clear that
the oesophageal electrode with a stabilized balloon does
not record the diaphragm EMG reliably [27,28,56,61,70].
To overcome the influence of lung volume on the
diaphragm EMG, multipair oesophageal electrodes have
been used to record the diaphragm EMG. Daubenspeck
et al. [60] found that the diaphragm EMG could be reliably recorded by summation of the EMG recorded from
seven consecutive pairs of electrode in spite of a change in
lung volume. It has been suggested that the orientation of
the crural diaphragm fibres with respect to the axis of the
oesophagus is perpendicular [41]. Therefore the electrode
pairs caudal and cephalad to the central area of the crus
would have a similar amplitude and opposite polarity
if both electrode pairs were the same distance from the
centre [7,38,39,71]. Sinderby and co-workers [67] have
developed a cross-correlation method to determine the
electrode pair closest to the diaphragm. A catheter with
seven [72] or eight [67] consecutive pairs of electrodes
with a 1 cm interelectrode distance within a pair was
used to track the position of the diaphragm’s electrically
active centre. A correlation coefficient was calculated for
every other pair and the difference between the signals
that had the best correlation was obtained (the doublesubtracted signal) [67,72] to enhance the signal-tonoise ratio and to reduce the artefact originating from
diaphragm movement. With this technique, they also
found that the diaphragm EMG was independent of
changes in lung volume; however, it should be pointed out
Oesophageal diaphragm electromyography
that the double-subtracted signal was from the electrode
pairs slightly away from the diaphragm, rather than
the pair at the electrically active centre, although the signal
obtained from the pair exactly at the electrical activity
centre was sometimes included for analysis [45].
POSITIONING OF ELECTRODES
To accurately record the diaphragm EMG, the oesophageal electrode should be positioned as close to the
diaphragm as possible. Unlike chest wall surface electrodes, oesophageal electrodes cannot be positioned
simply using fixed anatomical landmarks. Traditionally,
investigators [23] positioned the oesophageal electrode
by observing the magnitude of the diaphragm EMG
during sniffs or during maximal or quiet breathing efforts
on the assumption that the maximal EMG signal would
be obtained when the catheter was optimally positioned
[23,55,73]. Luo et al. [7,38,71] developed a technique to
accurately position an electrode based on the amplitude
and polarity of the diaphragm CMAP elicited by bilateral
magnetic phrenic nerve stimulation [7,71]. We used a
catheter with seven metal coils (number 1 being proximal
and 7 being distal) created with four electrode pairs
(Figure 4) , the interelectrode distance within a pair being
3 cm. Electrode 3 was positioned close to the diaphragm
based on the amplitude and opposite polarity of the diaphragm CMAP recorded from pairs 1 and 3, since the
CMAP shape is sensitive to electrode position [61,74].
The position was adjusted further by observing the
amplitude and polarity of the CMAP recorded from pair
2, which was characterized by a small or absent CMAP,
since there is a cancellation of the potential when both
recording electrodes are equally close to the source of the
diaphragm potential [65,71,72]. The ideal position of
the electrode was characterized by a large CMAP amplitude from pairs 1 and 3, with opposite polarity, and a small
CMAP was recorded from electrode pair 2 (Figure 4).
This method can position the electrode accurately, but it
requires the use of phrenic nerve stimulation which is a
complex technique. Luo et al. [27,28] have demonstrated
the positioning of a multipair oesophageal electrode
based on a spontaneous EMG recorded simultaneously
from four or five pairs of electrodes. The optimal position
was characterized by a large EMG from two electrode
pairs which shared the middle electrode and a small EMG
from the pair straddling the middle electrode (Figure 5).
Figure 4 Diaphragm CMAP recorded from four pairs of
electrodes
Left-hand panel, an oesophageal electrode catheter consisting of seven coils which
form four recording electrode pairs. Each electrode is 1 cm in length and there
is a 1 cm gap between electrodes. The interelectrode distance within an electrode
pair is 3 cm. Electrode 3 is placed at the centre of the electrically active region
of the diaphragm (EARdi). Right-hand panel, CMAP recorded from four electrode
pairs at functional residual capacity. The signal from pairs one and three are
opposite in polarity. Pair 2 only records a small CMAP since both electrodes are
close to the EARdi centre. Pair 4 records a small CMAP, as the electrode is 3 cm
away from the diaphragm. Reproduced from [71], with permission. Copyright
(2000) European Respiratory Society Journals Ltd.
by the stimulator output. A supramaximal stimulation
of the phrenic nerve is usually desirable, although since
submaximal stimuli recruit large (and therefore faster)
bundles of axons preferentially the measured nerve
conduction time does not greatly depend on the stimulus
intensity whereas the amplitude does (Figure 6). For
the amplitude of the diaphragm CMAP to be useful,
only the signals elicited by demonstrably supramaximal
(conventionally 20 % higher than maximal) stimulation
are usually analysed. To eliminate the influence of the
ECG, CMAPs are usually selected from those with a
constant shape and stable baseline before and after stimulation [7,38,39,69]. Similar principles are used in the analysis of the MEP [14–19] following stimulation of the
diaphragm motor area of the cortex, but it should be
noted that, because the MEP reflects a volley of impulses,
deciding where the signal begins (and hence the latency)
may be more difficult (Figure 7).
TIME AND FREQUENCY DOMAIN ANALYSIS
OF THE DIAPHRAGM [75]
ANALYSIS OF EMG SIGNALS
Time domain EMG analysis
For the diaphragm CMAP, latency and the amplitude are
measured [7,14,37–39,44,58]. The latency is synonymous
with the conduction time, which is measured from stimulation artefact to the onset of CMAP [7,14,37–39,44,58].
The amplitude of the diaphragm CMAP is greatly affected
Time domain EMG analysis is used to describe the
relationship between EMG strength and time so that,
broadly speaking, activity is the product of the amplitude
of the signal and its duration. To facilitate computerized
processing, the signal is usually rectified and integrated
[46,63,76,77]; however, some groups prefer to use a
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Figure 5 Diaphragm EMG recorded from a multipair oesophageal electrode during CO2 rebreathing
The oesophageal electrode configuration is shown in the left-hand panel. The oesophageal electrode catheter consists of ten coils that form five recording electrode
pairs. Each electrode is 1 cm in length, and there is a 0.5 mm gap between electrodes. The interelectrode distance within an electrode pair is 3.2 cm. Electrode 5 is
accurately positioned at the centre of the diaphragm electrically active region on the basis of the amplitude of the diaphragm EMG recorded from the five pairs of
electrodes during resting spontaneous breathing. This is characterized by a large EMG from pairs 1 and 5 and the smallest EMG from pair 3. Pair 2 and pair 4 recorded
a smaller EMG than pairs 1 and 5 because they were slightly further away from the diaphragm electrically active centre. Pair 3 only recorded the smallest EMG
because of signal cancellation. The diaphragm EMG increases during CO2 rebreathing. In spite of the dynamic hyperventilation that occurs in patients with COPD, the
electrode pairs which recorded the maximal EMG at rest (pairs 1 or 5) were the same as that at the end of CO2 rebreathing, indicating that lung volume change did
not significantly affect electrode positions. This Figure was reprinted from Respiratory Physiology & Neurobiology , volume 146, Y.M. Luo and J. Moxham, Measurement of
neural respiratory drive in patients with COPD, pp. 165–174, Copyright (2005), with permission from Elsevier (http://www.sciencedirect.com/science/journal/15699048).
moving average, peak activity or rate of rise of activity
[26]. The RMS of the diaphragm EMG has been used
(Figure 8) to quantify the activity of the diaphragm
[27,28,31,34,78] because it reflects the number and firing
rate of the motor units recruited. It has been demonstrated that the RMS of the diaphragm EMG is independent of a change in lung volume and is a reliable index of
global diaphragm activation [45,67,70].
of high-frequency power to low-frequency power) are
usually measured [25]. Fc reflect the relative contribution
of low- and high-frequency components in a given
bandwidth, and its number represents that frequency at
which the power above and below it is the same [23,25].
The H/L ratio is the ratio of power at high frequencies
(129–246 Hz) to power at low frequencies (31–51 Hz)
[25]. Both Fc and the H/L ratio have been used to
identify diaphragm fatigue [20,21,23,25].
Frequency domain analysis
Power spectral analysis of the EMG has been used to
assess diaphragm fatigue [20,21,24,25,73,79], although
enthusiasm for its use has diminished following the
demonstration that EMG indices of fatigue correlate
poorly with mechanical indices of fatigue [80] (Figure 9).
In brief, this approach seeks to describe the relationship
between the frequency and power of the diaphragm
EMG. Fc (centroid frequencies) and the H/L ratio (ratio
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APPLICATIONS
Testing the integrity of the phrenic
nerve–diaphragm unit
Accurately recording the diaphragm CMAP elicited by
electrical or magnetic stimulation of the phrenic nerve
is very useful for assessing diaphragm function and for
Oesophageal diaphragm electromyography
Figure 6 CMAP recorded from the oesophageal electrode
elicited by electrical stimulation and by unilateral magnetic
stimulation at different stimulator output
The amplitude of CMAP increases with increasing stimulator output, and
becomes the same as with electrical stimulation. Reproduced from [38], with
permission. Copyright (1999) European Respiratory Society Journals Ltd.
Figure 7 Examples of results produced by transcranial
magnetic stimulation during a facilitated inspiration
Left-hand panel, MEP; right-hand panel, P di , oesophageal pressure (P oes) and
gastric pressure (P gas). This Figure was published in Magnetic Stimulation in
Clinical Neurophysiology, 2nd edn (Hallett, M. and Chokroverty, S., eds), Polkey,
M.I. and Moxham, J., Magnetic stimulation in the assessment of the respiratory
muscle pump, pp. 381–392, Copyright (2005), with permission from Elsevier.
selecting patients for diaphragm pacing. Because surface
electrodes may be associated with varying conduction
times [38,39,81] and are not practical in the obese or those
with a chest wall deformity, the oesophageal electrode
often offers a better chance of achieving accurate data.
Measurement of phrenic nerve conduction time with an
oesophageal electrode is useful in differentiating axonal
neuropathies (e.g. motor neuron disease) from neuropathies where damage primarily occurs to the axonal
myelin [7–9,12,13,69]. Patients with Guillain-Barré
syndrome and hereditary motor sensory type 1 usually
have a prolongation of phrenic nerve conduction time
[8,13]. In contrast, conduction times in patients with
motor neuron disease or hereditary motor sensory type 2
are usually normal [13]. The normal range for phrenic
nerve conduction time measured by an oesophageal electrode is 7.6 +
− 0.7 ms on the left and 6.9 +
− 0.9 ms on the
right [7]. This reflects the length of the nerve, with
the phrenic nerve conduction time on the right side being
slightly, but significantly, shorter than that on the left
[58].
Oesophageal electrodes can also be used to assess
patients who have undergone open chest surgery, including cardiac surgery, to determine whether the phrenic
nerve has been injured during the operation [9]. Because the multipair oesophageal electrode can reliably record the diaphragm CMAP elicited by magnetic stimulation, patients with suspected hemi-diaphragm or bilateral
diaphragm paralysis can be accurately diagnosed [7,10],
although the assessment of the magnitude weakness will
usually require the measurement of twitch Pdi [7,82].
Assessment of cortical diaphragmatic
pathways
Oesophageal electrodes can be used to record the
diaphragm EMG response to transcranial electrical [83]
or magnetic [14–19] stimulation to investigate neural
pathways of the diaphragm. Sharshar et al. [18] found
that the diaphragm MEP could be reliably recorded
with an oesophageal electrode (Figure 7). By combining
transcranial and cervical magnetic stimulation, central
conduction time can be estimated by subtraction of the
latency of the CMAP elicited by neck stimulation from
transcranial stimulation [14–19,84]. On the basis of the
MEP, it has been suggested that patients with stroke have
impaired central motor conduction to the diaphragm
[17]. A possible supplementary diaphragm motor area
(3 cm anterior to the vertex) has been identified during
transcranial magnetic stimulation mapping with the
help of an oesophageal electrode [85]. Motor control of
the costal and crural diaphragm can also been assessed
with the help of the oesophageal EMG technique
[18].
Efficiency of diaphragm contraction and
diaphragm fatigue
The EMG recorded from an oesophageal electrode can
be used to establish the relationship between EMG
amplitude and Pdi . Similar to the relationship between
quadriceps force and EMG amplitude [86], a linear
relationship exists between Pdi and the diaphragm EMG
recorded from needle [87] or oesophageal [88] electrodes.
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Figure 8 Recording and analysis of the diaphragm EMG
The diaphragm EMG is recorded with an oesophageal catheter with ten coils. EMG signals are amplified with a gain of 1000 and filtered. RMS of the diaphragm EMG
is generated after eliminating the ECG.
Figure 9 Force response to electrical stimulation at
20 Hz/force at 100 Hz following repeated submaximal
voluntary contractions in the quadriceps
The Figure illustrates substantial low-frequency fatigue, with the EMG H/L ratio
remaining normal. This Figure was reproduced from Moxham, J., Edwards, R.H.T.,
Aubier, M. et al. (1982) Changes in EMG power spectrum (high/low ratio) with
force fatigue in man, Journal of Applied Physiology , 53, 1094–1099, and is
used with permission. Copyright American Physiological Society.
It has also been shown that there is a linear relationship
between twitch Pdi and the amplitude of the diaphragm
CMAP (r = 0.8) [7], which could be clinically important
because the diaphragm EMG could be used to predict
the strength of the diaphragm, assuming neuromuscular
transmission is normal. When Pdi and the diaphragm
EMG are measured simultaneously, contraction effi
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ciency can be assessed and peripheral low-frequency
diaphragm fatigue can be detected based on a decrease in
the Pdi /integrated diaphragm EMG ratio [89].
The power spectrum of the diaphragm EMG can be
recorded from an oesophageal electrode and a shift to
lower frequency has been considered to be an indicator
that fatigue is occurring [20–25,64,73,79,80]. Fc and the
H/L ratio have been used to diagnose diaphragm fatigue
in patients, including those with OSA (obstructive
sleep apnoea) [24,79], patients undergoing weaning
from mechanical ventilation [21] and patients with
COPD (chronic obstructive pulmonary disease) during
exhaustive exercise [23,32]. From power spectral data, it
has been considered that diaphragm fatigue contributes
to weaning failure and respiratory symptoms [3,6,90],
but findings obtained using magnetic nerve stimulation
have established that true low-frequency fatigue is hard
to elicit in clinical practice [91–94]. Because the relationship between the power spectral shift and fatigue remains
controversial and the underlying cellular mechanisms
remain unknown, in particular because power spectral
analysis can be affected by the change in lung volume and
the distance between the electrode and the diaphragm
[70,72], the shift of the power spectrum to lower
frequency is of uncertain clinical significance.
Assessment of neural respiratory drive
It is increasingly useful to assess neural respiratory
drive, as the product of EMG amplitude against time, in
normal subjects and patients with respiratory disease.
The diaphragm EMG has long been considered to be
a powerful physiological tool to assess neural respiratory
drive [26–34,52,56,71]. The diaphragm EMG increases
Oesophageal diaphragm electromyography
Figure 10 Peak of RMS increases during CO2 rebreathing
There is a good relationship between end-tidal CO2 and the amplitude of
the RMS. No plateau of EMG is observed. Results are from a patient with
COPD. This Figure was reprinted from Respiratory Physiology & Neurobiology ,
volume 146, Y.M. Luo and J. Moxham, Measurement of neural respiratory drive
in patients with COPD, pp. 165–174, Copyright (2005), with permission from
Elsevier (http://www.sciencedirect.com/science/journal/15699048).
gradually during CO2 rebreathing [26–28,46,76], and
there is a linear relationship between the RMS of the
diaphragm EMG and ventilation in normal subjects [28]
and patients with COPD [27] (Figure 10). The observation that pressure support reduces both Pdi and diaphragm EMG equally in normal subjects [34] suggests
that two measures reflect neural respiratory drive.
However, inspiratory pressure underestimates neural
respiratory drive in patients with COPD because of
hyperinflation. For example, Sinderby et al. [32] have
shown that diaphragm electrical activity increased progressively during incremental exercise in COPD, whereas
Pdi reached a plateau, indicating that the diaphragm EMG
is a better index of neural respiratory drive. Luo and
Moxham [27] found neural drive, as assessed by RMS of
the diaphragm EMG, increased linearly with an increase
in end-tidal CO2 in patients with COPD. Furthermore,
they found that the diaphragm EMG in patients with
COPD increased initially but eventually reached a plateau
during constant rate treadmill exercise, indicating the
importance of the exercise protocol.
Application in the ICU (intensive care
unit)
An important application of the oesophageal diaphragm
EMG is in the assessment of diaphragm function in
patients in the ICU [11]. Because patients in the ICU frequently develop a neuromuscular abnormality [12,95,96],
including dysfunction of the diaphragm [97], which
contribute to weaning failure, measurement of the
diaphragm CMAP with an oesophageal electrode can
provide useful information about phrenic nerve and dia-
Figure 11 Diaphragm EMG recorded from five pairs of
oesophageal electrodes during polysomnography
Signals from top to bottom are two-channel EEGs, two-channel EOGs (electrooculograms), airflow recorded from pneumotachometer, EMGs (1–5) recorded from
a multipair oesophageal electrode, chest and abdominal movement and S aO2 %
(percentage arterial O2 saturation). During cessation of airflow, there is barely
any chest and abdominal movement, therefore, the event appears to be central
sleep apnoea. However, there is obvious EMG during cessation of the airflow, and
the event should therefore be defined as OSA. The inconsistent changes between
chest/abdominal movement and the diaphragm EMG suggests that the diaphragm
EMG recorded from oesophageal electrode can more accurately identify the type of
respiratory events. Results are from a patient with OSA.
phragm function [7,8]. Luo et al. [11] measured CMAP
with a multipair oesophageal electrode in the ICU and
found that the amplitude of the diaphragm CMAP in
patients was half that of normal subjects. An attractive
potential application of the oesophageal electrode is
triggering and adjusting ventilation from the diaphragm
EMG [30–34]. Conventionally, ventilators are triggered
by flow or pressure, but these methods could fail to detect
the onset of breathing causing asynchrony between the
patient and the ventilator [33]. Because the diaphragm
EMG appears ahead of airflow or a change of pressure,
particularly so when there is intrinsic or applied positive
end-expiratory pressure, the diaphragm EMG recorded
from a multipair oesophageal electrode could be used
to trigger the ventilator and improve patient–ventilator
synchrony [33]. The diaphragm EMG can also be used to
automatically adjust a ventilator in response to varying
patient effort [30,33,34]. With this model, ventilatory
assistance is given in proportion to the neural drive.
Spahija et al. [30] reported that, during loaded breathing
in healthy subjects, it was possible to automatically
adjust the level of ventilatory assistance from one breath
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241
242
Y. M. Luo, J. Moxham and M. I. Polkey
to the next and to maintain diaphragm activation within
a predetermined target range. Ventilator adjustment
using the diaphragm EMG can efficiently unload the
respiratory muscles during maximal inspiration [34].
Applications in sleep medicine
Vincken et al. [98] used an oesophageal electrode to
investigate the mechanism of airway opening in OSA and
concluded that reopening of the airway is not related to
respiratory muscle fatigue. Some studies have investigated
diaphragm activity during obstructive events in an
attempt to determine whether OSA is associated with
diaphragm derecruitment [24,79]. Conventionally, distinguishing obstructive from central apnoea/hypopnoea
depends on detection of respiratory effort measured from
chest and abdominal movement or oesophageal pressure.
The diaphragm EMG can accurately assess neural respiratory drive [27,28,31–33,99], therefore, it could be
a useful technique to differentiate types of respiratory
events [100,101] (Figure 11); this distinction may be of
importance in conditions such as heart failure, where
nocturnal ventilatory support is indicated for patients
with OSA but not central sleep apnoea.
CONCLUSIONS
In conclusion, measuring the diaphragm EMG may be
useful for the diagnosis and treatment of respiratory
disease. Recent technical advances mean that an oesophageal electrode is simpler to use and, therefore,
should now, in most cases, be the technique of choice in
preference to surface electrodes.
ACKNOWLEDGMENTS
Y. M. L. is supported by a grant from the Natural Science
Foundation of Guangdong, People’s Republic of China
(No. 6113858) and holds British Council researcher
exchange programmes awards.
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Published on the Internet 12 September 2008, doi:10.1042/CS20070348
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The Authors Journal compilation
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2008 Biochemical Society