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1 Meakins Christie
Laboratories, ABSTRACT Sinderby, Christer A., Jennifer C. Beck, Lars H. Lindström, and Alejandro E. Grassino. Enhancement of signal
quality in esophageal recordings of diaphragm EMG. J. Appl. Physiol. 82(4): 1370-1377, 1997.
electromyography; bipolar electrode filtering; power spectrum; center frequency; root mean square
INTRODUCTION THE ELECTROMYOGRAM (EMG) of the human diaphragm is
preferably recorded by bipolar electrodes mounted on an esophageal
catheter that is positioned at the level of the gastroesophageal
junction (10). Since the introduction of esophageal electrodes in the measurement of the human diaphragm EMG over 30 years ago (1, 9), a
number of investigators have used the method in the experimental setting to evaluate diaphragm function and fatigue in healthy subjects
(e.g., Refs. 6, 8) and in patients with respiratory-related deficiencies (e.g., Refs. 7, 11).
Esophageal recordings of the diaphragm EMG have been criticized because
of the difficulties in obtaining signals that are of significant
strength and sufficiently free of artifacts. Typical disturbances in
esophageal recordings of the diaphragm EMG include noise, electrode
motion artifacts, esophageal peristalsis, the electrocardiogram (ECG),
and other bioelectric sources. These disturbances can be controlled for
today by computer algorithms (12). As well, changes in the distance
between the diaphragm and the esophageal electrode strongly filter the
EMG signal (5), and the bipolar electrode itself imposes a filter on
the signal (4). These filtering effects can be minimized if the bipolar electrode position with respect to the diaphragm is controlled for. By
implementing a cross-correlation technique, we were able to demonstrate
that it is possible to locate the diaphragm's position along a
multiple-electrode array for each selected EMG segment (4).
It has been demonstrated that the crural diaphragm EMG is recorded from
a sheet of muscle, the fiber direction of which is mostly perpendicular
to the bipolar electrodes (4). The diaphragm EMG recorded within this
region represents the temporal and spatial summations of signals from
asynchronously firing crural diaphragm motor units, and, therefore,
during voluntary activity, the crural diaphragm can be considered as an
"electrically active region" of the diaphragm
(EARdi). The area from which
action potentials are elicited may vary within a contraction in terms
of position with respect to the esophageal electrode. It can be assumed
that within the EARdi, the
distribution of the active motor units has an effective center
(EARdi ctr), from which
the majority of the diaphragm EMG signals originate. Depending on the
bipolar electrode's position with respect to the
EARdi ctr, the diaphragm EMG
is filtered to different degrees (4). The influence of bipolar
electrodes oriented perpendicularly to the muscle fiber direction on
the diaphragm EMG power spectrum was described to progressively
increase the frequency and attenuate the power of the diaphragm EMG
signal as the center of an electrode pair moved from 10 mm away from the EARdi ctr toward it (4).
More than 10 mm away from the EARdi ctr, both the
frequency and power decreased progressively because of
muscle-to-electrode distance-filtering effects (5). It was concluded
that EMG signals recorded by electrode pairs centered either 10 mm
caudal or 10 mm cephalad to the
EARdi ctr, with an array of
electrodes with an interelectrode distance of 10 mm, were the least
influenced by bipolar electrode filtering and muscle-to-electrode
distance-filtering effects (4). The bipolar electrode-filtering effects
and the muscle-to-electrode distance-filtering effects can therefore be
reduced by using an array of electrode pairs (10 mm interelectrode
distance) and by selecting signals 10 mm away from the
EARdi ctr. Of particular importance for the present paper is that, for the electrode pair lying
closest to the EARdi ctr,
the actual position of the
EARdi ctr under that
electrode pair can vary during a contraction, and, therefore, will
influence the signals above and below relatively more or less. For
example, in Fig.
1A,
illustrating an array of electrodes with 10-mm interelectrode distance
(center), the distance between the
EARdi ctr (located under
electrode pair 4) and
electrode pair 5 is less than the
distance between EARdi ctr
and electrode pair 3. According to
theory (4), signals from electrode pair 5 should show relatively more attenuation of power and
higher center frequency (CF) values than electrode
pair 3.
Assuming that the influence of the relative movement of the
EARdi ctr with respect to
the electrode array has a reciprocal effect on the signals cephalad and
caudal to the EARdi ctr (as obtained with an electrode configuration described in Fig. 1, center), one possible way to reduce
the influence would be to subtract the diaphragm EMG signals from the
electrode pairs 10 mm cephalad and 10 mm caudal to the
EARdi ctr. These two signals are negatively correlated at 0-ms time delay (4) and, hence, subtraction of the polarity-reversed signals will yield an effective summation. We hypothesized that subtraction of the polarity-reversed diaphragm EMG signals from the electrode pairs located 10 mm cephalad and 10 mm caudal to the
EARdi ctr would provide a
signal that is less influenced by bipolar electrode filtering, and we
refer to this method as the "double-subtraction technique." The
purpose of the present work, therefore, was to evaluate whether the
double-subtraction technique can reduce the effect of movement of the
EARdi ctr relative to the
electrode array on the diaphragm EMG power spectrum.
MATERIALS AND METHODS Subjects
Signal Acquisition
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
ACKNOWLEDGEMENTS
FOOTNOTES
REFERENCES
The crural
diaphragm electromyogram (EMGdi) is recorded from a sheet of muscle,
the fiber direction of which is mostly perpendicular to an esophageal
bipolar electrode. The region from which the action potentials are
elicited, the electrically active region of the diaphragm
(EARdi) and the center of this region (EARdi ctr) may
vary during voluntary contractions in terms of their position with
respect to an esophageal electrode. Depending on the bipolar
electrode's position with respect to the
EARdi ctr, the EMGdi is
filtered to different degrees. The objectives of the present study were
to reduce these filtering effects on the EMGdi by developing an
analysis algorithm referred to as the "double-subtraction technique." The results showed that changes in the position of the
EARdi ctr by ±5 mm with
respect to the electrode pairs located 10 mm caudal and 10 mm cephalad
provided a systematic variation in the EMG power spectrum
center-frequency values by ±10%. The double-subtraction technique
reduced the influence of movement of the
EARdi ctr relative to the
electrode array on EMG power spectrum center frequency and root mean
square values, increased the signal-to-noise ratio by 2 dB, and
increased the number of EMG samples that were accepted by the signal
quality indexes by 50%.
Fig. 1.
A: schematic description of method
used to determine location of center of electrically active region of
diaphragm (EARdi) (EARdi ctr).
Left, raw signals from each electrode
pair (electrode is illustrated in center).
Right,
r values from cross-correlation of
signals from electrode pairs 1 vs. 3,
2 vs.
4, 3 vs. 5,
4 vs. 6, and
5 vs.
7. Dashed line through 3 most negative
r values, square law-based function
used to interpolate position of
EARdi ctr. B: diaphragm EMG signals obtained from
electrode pairs located 10 mm caudal and 10 mm cephalad to
EARdi ctr,
electrode pairs 3 and
5, respectively, in this
example, to
EARdi ctr,
electrode pair 4 in this example
(left). As revealed by
cross-correlation analysis, signals from electrode pairs located
caudally and cephalad to
EARdi ctr were inversely
correlated at 0 time delay. Right, signal obtained after subtraction of signal from
electrode pair 5 from that of
electrode pair 3. Double subtraction
of inversely correlated signals resulted in a clearly visible increase
in signal amplitude, whereas addition of signals (not shown) reduced
amplitude.
[View Larger Version of this Image (33K GIF file)]
Pes). A two-lead differential ECG was obtained from electrodes placed
on the sternum, vertically and 10 cm apart (Graphic Controls, FC24).
Diaphragm EMG electrode positioning was achieved by on-line display of the raw signals, and the correlation coefficients were obtained by successively cross-correlating the diaphragm EMG signals from every second pair of electrodes along the array (see below).
Diaphragm EMG and ECG signals were amplified (INA102, Burr-Brown) and high-pass filtered at 10 Hz (single-pole filter) with an antialiasing filter at 1 kHz (D70L8L-1.00 kHz, 8-pole Bessel filter, Frequency Devices). The diaphragm EMG and ECG signals were acquired (DT 2821, Data Translation) at 2 kHz (12-bit resolution). Pes and Pga were acquired separately (DT 2801A, Data Translation) at a sampling frequency of 100 Hz (12-bit resolution).
On-Line Display and Analysis of Diaphragm EMG Signals
Diaphragm EMG signals were acquired, displayed, and analyzed with computer software that, based on predetermined criteria, make an evaluation of signal contamination by such factors as the ECG, noise, motion artifacts, and esophageal peristalsis (12). The raw diaphragm EMG signals were automatically selected between the ECG QRS complexes (~50-75% of the R-R interval) from all seven electrode pairs. From the seven raw diaphragm EMG signals, the direct current levels and trends were removed by linear regression analysis; the tails of the raw signals were zero padded from the first and last zero crossings of the EMG signal to fit the segments for a fast Fourier transform of 1,024 points. The time domain diaphragm EMG segments were then converted into the frequency domain by fast Fourier transform, and the power spectra were calculated. CF was calculated from the diaphragm EMG power spectrum as the spectral moment of order one (M1) divided by that of order zero (M0)
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In each subject, signal contamination was evaluated for each electrode
pair's power spectrum by contamination-sensitive indexes. The four
indexes used to evaluate signal contamination were the signal-to-noise
(SN) ratio, the signal-to-motion artifact (SM) ratio, the drop in power
density of the spectrum (DP) ratio, and a spectral deformation (
)
index. Below is a brief description of the signal-contamination
indexes. The reader is referred to the recent work by Sinderby et al.
(12) for a more detailed account of the indexes.
Index.
This index is sensitive to changes in the symmetry and peaking of the
power spectrum and is derived mathematically (3) by the following
formula
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5 to +10 Hz: SM 
12 dB, SN 15 dB, DP 30 dB, and 1.4 (12), and they were the acceptance levels used in the present
study.
Determination of Position of EARdi ctr
With a perpendicular electrode arrangement, signals that are obtained either on opposite sides of the EARdi ctr or on the same side of the EARdi ctr correlate with extreme values (i.e., the r value is expected to be close to1 or +1) at a 0-ms time shift. Cross-correlation analysis was
performed between signals obtained from electrode
pairs 1 vs. 3,
2 vs.
4, 3 vs. 5,
4 vs. 6, and
5 vs.
7 (Fig.
1A,
left, shows the raw signals from all electrode pairs). The correlation coefficients obtained for the respective cross-correlations at zero time delay are plotted in Fig.
1A,
right. The most-negative correlation
coefficient between any two pairs of electrodes indicates that the
respective signals are the most reversed in polarity (e.g.,
electrode pairs 3 vs. 5 in this example); the electrode pair
that is between these two most negatively correlated pairs is the
electrode pair closest to the
EARdi ctr
(electrode pair 4 in this example).
Samples were included in the analysis only if the correlation
coefficient (for the two most negatively correlated signals) was less
than or equal to 0.50. After the three most- negative adjacently
located correlation coefficients were determined (marked by an asterisk
in the example), a square law-based curve fit was applied to
interpolate a more accurate location of the
EARdi ctr with respect to
the multiple-array electrode.
Double-Subtraction Technique
We hypothesized that subtraction of the signals from electrode pairs centered 10 mm above and below the EARdi ctr would provide a signal that is less influenced by movement of the bipolar electrodes (the double-subtraction technique). Figure 1 describes how the double-subtraction technique is performed. First, the electrode pair closest to the EARdi ctr is determined, and then the electrode pairs located 10 mm caudal and 10 mm cephalad to the EARdi center are also determined. As depicted in Fig. 1A, left, signals from the electrode pairs located 10 mm caudal and 10 mm cephalad of the EARdi ctr were reversed in polarity (electrode pairs 3 and 5). Figure 1B, right, gives an example of how the new signal is obtained (the "double-subtracted signal") by subtracting the signal from the electrode pair located 10 mm cephalad to the EARdi ctr (electrode pair 5) from the signal 10 mm caudal to the EARdi ctr (electrode pair 3). For every EMG segment selected between the ECG QRS complex, the double-subtraction technique was applied. The double-subtracted signal was Fourier transformed into the frequency domain, and the power spectrum was calculated; CF and RMS values were also calculated for every double-subtracted signal segment (as described above for the individual electrode pairs).Protocol
The esophageal electrode was passed through the nose, swallowed into the stomach, and positioned at the level of the gastroesophageal junction with the aid of on-line feedback from the EMG signals (see above). Subjects were seated upright in an armchair facing a computer monitor that displayed the raw diaphragm EMG signals, the power spectrum CF values, and the RMS values for each electrode pair in real time. Maximal transdiaphragmatic pressure (Pdimax) maneuvers were performed at functional residual capacity (FRC) and at total lung capacity (TLC) (combined Mueller/expulsive maneuver). The highest of three reproducible values was considered to be maximal.Subjects performed a series of five static, near isometric, voluntary diaphragm contractions. Each contraction lasted ~10 s, and a 2-min rest period was allowed between contractions. Contractions were performed at FRC at a Pdi corresponding to 20-30% of the Pdimax value obtained at FRC and at TLC at a Pdi corresponding to 70-80% of the Pdimax value obtained at TLC. The contractions at TLC were introduced in the protocol to evaluate whether the behavior of the diaphragm EMG signals over the span of the electrode array changes with lung volume or diaphragm activity. Signals were also acquired during 5 min of tidal breathing against a very slight inspiratory flow resistance at a target mean Pdi level corresponding to 10% of the maximum Pdi at FRC. The diaphragm EMG and Pdi were recorded during all runs.
Statistics
CF and RMS values from electrode pairs 10 mm caudal and 10 mm cephalad to the EARdi ctr were compared with the signal created by the double-subtracted technique by using a Student's t-test for matched comparisons. The effect of electrode positioning with respect to the EARdi ctr on CF values was evaluated by linear regression analysis. Pearson product-moment correlation was used to analyze relationships.RESULTS
The double-subtraction technique visibly resulted in an increase in signal amplitude, as shown in Fig. 1B, right. The resultant increase in amplitude was associated with an approximately twofold increase in RMS values (Table 1). The RMS values obtained by the double-subtraction technique were closely linearly related to the original signals; the average correlation coefficient (r) for the five subjects was 0.96 ± 0.02.
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As depicted for one subject in Fig. 2, the
CF values (y-axes) obtained from the electrode
pair located 10 mm caudal to the EARdi ctr
(A,
left) and from the electrode pair
located 10 mm cephalad to the
EARdi ctr
(A,
right) were systematically
influenced by the position of the
EARdi ctr
(x-axes). The position of the EARdi ctr is expressed as
the distance (in mm) from the center of the electrode pair covering the
EARdi ctr. With respect to the electrode pair located 10 mm caudal to the
EARdi ctr, CF values increased when the EARdi ctr
moved in a caudal direction, whereas the CF values for the electrode
pair 10 mm cephalad to the
EARdi ctr decreased, and
vice versa. This reciprocal influence of the position of the
EARdi ctr was reduced for
the CF values of the double-subtracted signal, as shown in Fig.
2B. The individual and mean slopes
describing the influence of the position of the
EARdi ctr on the CF values obtained with electrode pairs located 10 mm caudal or cephalad and CF
values obtained with the double-subtraction technique are presented in
Table 2.
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Mean CF values for the signals obtained 10 mm caudal or 10 mm cephalad of the EARdi ctr during the entire run were not different from the CF values obtained from the double-subtracted signals (Table 1).
Because SN levels are not a problem at high-diaphragm-contraction
levels, the effect of the double-subtraction technique on signal
quality was only analyzed for signals recorded at mild contraction
levels (isometric contractions at 20-30% of
Pdimax). The SN ratios for the
double-subtracted signals were, on average, 2 dB higher than the SN
ratios for the electrode pairs located 10 mm caudal or 10 mm cephalad
to the EARdi ctr (Table 1).
Also, the DP and ratios improved somewhat, whereas no consistent
changes were found for the SM ratio when the double-subtraction
technique was applied (Table 1).
To quantify whether the double-subtraction technique increased the
number of samples that were accepted by the signal-quality indexes, the
number of accepted double-subtracted signals were compared with the
number of accepted samples obtained from electrode pairs located 10 mm
caudal and/or 10 mm cephalad to the
EARdi ctr. Signals used in
the analysis were obtained during tidal breathing with a slight
inspiratory resistance (10% of
Pdimax). Relative to the
electrode pairs located 10 mm caudal and/or 10 mm cephalad to
the EARdi ctr, 50% more
signal segments were accepted by the inclusion criteria for the
double-subtracted signals (Fig. 3).
The behavior of the CF and RMS values obtained along the span of the
electrode array were different among subjects, but within a given
subject the behavior of the CF and RMS values along the span of the
electrode array was similar at FRC and TLC and did not change with
increasing contraction levels. Figure 4
shows CF (squares) and RMS (circles) values for each electrode pair along the array in one subject contracting the diaphragm at 30% of
Pdimax obtained at FRC (dashed
line) and at 70% of the Pdimax obtained at TLC (solid line). Note that the Pdi values are normalized to the Pdimax values obtained at
the same lung volume.
It was noticed that the summation of diaphragm EMG signals from all
seven pairs of electrodes, which is equivalent to a bipolar signal
obtained between the most-caudal and -cephalad electrode rings,
provides a large ECG signal. Figure 5
depicts the signals recorded from each of the seven electrode pairs as
well as the summed signal obtained
(top).
DISCUSSION
The present study demonstrates that subtraction of the diaphragm EMG signal 10 mm cephalad to the EARdi ctr from the signal 10 mm caudal to the EARdi ctr, the double-subtraction technique, reduces the influence of bipolar electrode movement relative to the EARdi ctr, improves the SN ratio, and increases the number of diaphragm EMG segments that can be used in the analysis.
Implications of Double-Subtraction Technique
One of the technical problems associated with the use and interpretation of esophageal recordings of the diaphragm EMG has been the low SN ratio. Low SN ratio is especially a problem when the diaphragm EMG is recorded with esophageal electrodes at low levels of diaphragm contraction, e.g., breathing at rest (2). The double-subtraction technique shows itself to be a promising technique to overcome the difficulties associated with obtaining diaphragm EMG recordings of acceptable quality at low levels of diaphragm contraction. In contrast to the diaphragm EMG signals, signals from distant bioelectric sources will have the same polarity for all electrode pairs along the electrode array. The double-subtraction technique, therefore, results in enhancement of the diaphragm EMG signals (that effectively are added) and cancellation of any distant bioelectric sources common to both pairs of electrodes used in the subtraction and, hence, improves the SN ratio. A slight improvement was also seen in the DP and ratios, both being sensitive to
high-frequency noise (3, 12). As a direct consequence of the improved
signal quality, the double-subtraction technique allowed 50% more EMG
signals to be accepted as uncontaminated, according to the
signal-quality indexes. As expected, the SM ratio, being sensitive to
electrode motion artifacts, was not affected by the double-subtraction
technique.
In healthy subjects, diaphragm EMG CF values decrease by ~20-30% when subjects breathe against inspiratory loads until task failure (unpublished observations). Hence, early indications of diaphragmatic fatigue could be uncertain because of the 20% fluctuations in CF for ±5 mm changes in the position of the center of the EARdi, as demonstrated in the present study. The double-subtraction technique will allow for more accurate detection of developing fatigue and may increase the applicability of diaphragm EMG to detect fatigue in clinical settings.
Limitations of Double-Subtraction Technique
In an implementation of the double-subtraction technique, it is important to know the behavior of the diaphragm EMG signals over the span of the electrode array, i.e., the influence of the transfer function for signals measured with bipolar electrodes oriented perpendicularly to the diaphragm. We have previously shown that the diaphragm EMG recorded with an esophageal electrode in healthy subjects was the "least filtered" at a distance of ~10 mm away from the EARdi ctr, with an interelectrode distance of 10 mm (4).In the present study, we demonstrated that the symmetrical behavior of the CF and RMS over the bipolar electrode array remains stable with changes in lung volume and diaphragm-contraction levels (see Fig. 4). However, it should be noted the selection of signals 10 mm away from the EARdi ctr used in the double-subtraction technique has so far only been applied to signals obtained in healthy subjects. In the case of anatomic or neuromuscular abnormalities, or changes in electrode configuration, the distance between electrode pairs used in the double subtraction and the EARdi ctr may alter.
The behavior of the diaphragm EMG signals over the span of the electrode array, i.e., the influence of the transfer function for signals measured with bipolar electrodes oriented perpendicularly to the diaphragm, is dependent on the radial and axial distances between the esophageal electrode pair and the diaphragm, the thickness of the diaphragm, i.e., size of the EARdi, the interelectrode distance, and the dispersion in arrival times of the single-fiber contributions to the motor unit signal (4). The transfer function for human diaphragm EMG signals measured with bipolar electrodes oriented perpendicularly to the diaphragm has been discussed in detail elsewhere (4). The EARdi ctr can move (due to diaphragm excursions) relative to the electrode array within a single breath and within a single EMG signal segment; as well, any change in motor unit recruitment may result in a repositioning of the EARdi ctr relative to the electrode array. Hence, a power spectrum obtained from one single EMG segment will represent the mean position of the EARdi ctr with respect to the electrode array, i.e., the mean filtering of the signal. Because of the reciprocal behavior of the bipolar electrode-filtering effect for electrode pairs 10 mm caudal and 10 mm cephalad to the EARdi ctr, the signals used by the double-subtraction technique should represent the mean (reciprocal) filtering for the two electrode pairs. Hence, their sum should reduce the influence of relative changes in the position of the EARdi ctr with respect to the electrode array that may occur within a given EMG segment.
We chose a square law-based function of the cross-correlation coefficients obtained between electrode pairs to predict a more accurate position of the EARdi ctr with respect to the electrode array. This square law-based function may not have indicated the exact position of the EARdi ctr; however, assuming that the recorded EMG signals shift polarity at or close to the EARdi ctr when obtained with an electrode array of the same configuration as that used in the present study, the square law-based function should adequately indicate the relative changes in position of the EARdi ctr.
Extracting ECG From Esophageal Electrode Array
The setup in the present study included a separate ECG recording (with electrodes on the chest wall), as well as the seven pairs of EMG signals from the esophageal catheter, for a total of eight channels. The ECG is used in the analysis of the diaphragm EMG signals to guide the selection of EMG segments free of ECG (12). The large ECG signal obtained by summation of signals from all seven electrode pairs is useful because it allows the separate ECG recording to be replaced by an additional electrode pair for diaphragm EMG. The additional electrode pair for the diaphragm EMG is advantageous because it extends the span of the electrode array and hence reduces the possibility of the diaphragm moving off the electrode array.Conclusion
The double-subtraction technique reduces the influence of the relative position of the EARdi ctr with respect to the bipolar electrode array on the frequency content of diaphragm EMG segments and improves the SN ratio. The latter increases the number of diaphragm EMG segments accepted by the signal quality indexes as uncontaminated by 50%.ACKNOWLEDGEMENTS
This study was supported by grants from Inspiraplex-Respiratory Health Network of Centres of Excellence, the Medical Research Council of Canada, the King Gustav V Foundation, the Swedish Association for Traffic and Polio Disabled, the Swedish Association for Neurologically Disabled, and the Fonds pour la Formation de Chercheurs et l'Aide à la Recherche, Quebec, Canada.
FOOTNOTES
Address for reprint requests: C. Sinderby, Meakins-Christie Laboratories, McGill Univ., 3626 St Urbain St., Montreal, Québec, Canada H2X 2P2.
Received 12 June 1996; accepted in final form 29 November 1996.
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B. Singh, J. A. Panizza, and K. E. Finucane Diaphragm electromyogram root mean square response to hypercapnia and its intersubject and day-to-day variation J Appl Physiol, January 1, 2005; 98(1): 274 - 281. [Abstract] [Full Text] [PDF]
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J. BECK, S. B. GOTTFRIED, P. NAVALESI, Y. SKROBIK, N. COMTOIS, M. ROSSINI, and C. SINDERBY Electrical Activity of the Diaphragm during Pressure Support Ventilation in Acute Respiratory Failure Am. J. Respir. Crit. Care Med., August 1, 2001; 164(3): 419 - 424. [Abstract] [Full Text] [PDF]
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C. SINDERBY, J. SPAHIJA, J. BECK, D. KAMINSKI, S. YAN, N. COMTOIS, and P. SLIWINSKI Diaphragm Activation during Exercise in Chronic Obstructive Pulmonary Disease Am. J. Respir. Crit. Care Med., June 1, 2001; 163(7): 1637 - 1641. [Abstract] [Full Text] [PDF]
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L. A. van Eykern, E. J. W. Maarsingh, W. M. C. van Aalderen, and S. Corne Two Similar Averages for Respiratory Muscle Activity J Appl Physiol, May 1, 2001; 90(5): 2014 - 2015. [Full Text] [PDF]
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C. SINDERBY, J. SPAHIJA, and J. BECK Changes in Respiratory Effort Sensation Over Time Are Linked to the Frequency Content of Diaphragm Electrical Activity Am. J. Respir. Crit. Care Med., March 15, 2001; 163(4): 905 - 910. [Abstract] [Full Text]
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C. Sinderby, J. Beck, J. Spahija, J. Weinberg, and A. Grassino Voluntary activation of the human diaphragm in health and disease J Appl Physiol, December 1, 1998; 85(6): 2146 - 2158. [Abstract] [Full Text] [PDF]
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J. Beck, C. Sinderby, L. Lindstrom, and A. Grassino Effects of lung volume on diaphragm EMG signal strength during voluntary contractions J Appl Physiol, September 1, 1998; 85(3): 1123 - 1134. [Abstract] [Full Text] [PDF]
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J. Beck, C. Sinderby, L. Lindstrom, and A. Grassino Crural diaphragm activation during dynamic contractions at various inspiratory flow rates J Appl Physiol, August 1, 1998; 85(2): 451 - 458. [Abstract] [Full Text] [PDF]
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