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1 UPRES EA 2397, Université Pierre et Marie Curie Paris VI, 75013 Paris; 2 Service de Physiologie Respiratoire et Sportive, Hôpital Charles Nicolle, Centre Hospitalier Universitaire, Rouen 76000; 3 Service d'Explorations Fonctionnelles Respiratoires, and 4 Laboratoire de Physiopathologie Respiratoire, Service de Pneumologie, Groupe Hospitalier Pitié-Salpêtrière, Assistance Publique-Hôpitaux de Paris, 75013 Paris; and 5 Laboratoire d'Explorations Fonctionnelles Respiratoires, Centre Hospitalier Universitaire La Cavale Blanche, 29200 Brest, France
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Phrenic nerve stimulation, electrical (ES) or from cervical magnetic stimulation (CMS), allows one to assess the diaphragm contractile properties and the conduction time of the phrenic nerve (PNCT) through recording of an electromyographic response, traditionally by using surface electrodes. Because of the coactivation of extradiaphragmatic muscles, signal contamination can jeopardize the determination of surface PNCTs. To address this, we compared PNCTs with ES and CMS from surface and needle diaphragm electrodes in five subjects (10 phrenic nerves). At a modified recording site, lower and more anterior than usual (lowest accessible intercostal space, costochondral junction) with electrodes 2 cm apart, surface and needle PNCTs were similar (CMS: 6.0 ± 0.25 ms surface vs. 6.2 ± 0.13 ms needle, not significant). Electrodes recording the activity of the most likely sources of signal contamination, i.e., the serratus anterior and pectoralis major, showed distinct responses from that of the diaphragm, their earlier occurrence strongly arguing against contamination. With ES and CMS, apparently uncontaminated signals could be consistently recorded from surface electrodes.
phrenic nerve; accessory phrenic nerve; cervical magnetic stimulation; electromyography
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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MAGNETIC STIMULATION of the phrenic nerves, first introduced in 1988-1989 under the form of cervical magnetic stimulation (CMS) (34), has become an established tool to study diaphragm function in health and disease. CMS is painless and easy to perform, thus alleviating some of the pitfalls of electrical phrenic stimulation (ES), although the two techniques bring complementary information. Of note, several techniques are now available, including unilateral magnetic stimulation (UMS) (24), bilateral anterior magnetic phrenic stimulation (23), and anterior magnetic stimulation (27, 28, 35). The mechanical response of the diaphragm to those stimulations is well described (15, 27, 36), and there have been various pathophysiological and clinical applications.
Besides giving access to a nonvolitional measure of the diaphragm contractile efficiency, phrenic nerve stimulation is also a unique tool to assess the function of the phrenic nerve itself. This is achieved by measuring the latency of the diaphragmatic motor response after stimulation, or phrenic nerve conduction time (PNCT), and in fact has been the primary application of the technique (8, 25). The PNCT derived from electrical stimulation in the neck (ES-PNCT) is known from numerous studies (see Table 1 in Ref. 35) and revolves around a 7-ms figure. Measuring ES-PNCT is necessary to make the diagnosis of many types of phrenic nerve damage and is instrumental to their follow-up. The absence of diaphragm response to ES of the phrenic nerve should be the only rigorous criterion to attribute diaphragm abnormalities to phrenic nerve paralysis, strictly speaking (10). However, ES can be painful and difficult to achieve because of the morphology of the subject or for anatomic reasons. Indeed, the phrenic nerve is small and not always fully constituted at the base of the neck (14) and hence can be difficult to locate. Therefore, ES carries a risk of falsely negative results. In addition, ES cannot stimulate the share of motor fibers destined to the diaphragm that constitute the accessory phrenic nerve (29).
Because magnetic stimulation gives easier access to the nerve,
it should have become popular for phrenic nerve conduction studies.
This has not been the case, and several teams using magnetic stimulation mentioned difficulties in collecting the related diaphragm electromyogram (EMG) signals. Our finding of CMS-PNCTs shorter by an
average of 1 ms than ES-PNCTs (35), which we
attributed to a more distal depolarization of the nerve with CMS, has
been ascribed by others to a contamination of the EMG signal by the unavoidable contraction of coactivated extradiaphragmatic muscles (17). This phenomenon has also been reported for UMS
(16) and has led some to deem unreliable the measurement
of PNCTs using surface recordings in response to magnetic stimulation.
Of note, contamination of the signal picked up by surface electrodes
aimed at recording diaphragm activity has also been reported in
response to ES of the phrenic nerve (18). We had reasons
to believe that, in our setting, surface electrodes could provide an
uncontaminated diaphragm signal with CMS as well as with ES. Among the
strongest of these reasons was the fact that surface electrodes could
be silent in response to CMS in patients with phrenic paralysis
(1, 6, 35). In our view, the most likely explanation
for the difference between our findings and those of others is our use of a variant placement of the electrodes over the chest wall. Indeed,
compared with classical descriptions and other studies, we place the
electrodes closer together and at a lower and more medial site (Fig.
1). We assume that this should reduce the
likelihood of signal contamination by moving the electrodes away from
the main sources of stimulation related electrical activity, namely the
muscle masses of the pectoralis major and of the serratus anterior.
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Because intramuscular electrodes have a very limited sampling volume and hence carry a low risk of signal contamination through volume conduction, we designed this study to test the above hypothesis. We compared surface recordings of diaphragm contractions induced by CMS and ES with concomitant recordings obtained from needles inserted in the diaphragm, considering contamination present if a surface PNCT was markedly shorter than the corresponding needle one.
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MATERIALS AND METHODS |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Subjects
Five healthy volunteers participated in the study (Table 1), after completion of the French legal procedure for studies in human volunteers. The study was approved by the Comité Consultatif de Protection des Personnes se prêtant à des Recherches Biomédicales, Pitié-Salpêtrière. All subjects were informed in detail of the purpose of the study and methods used and gave written consent. They were studied sitting on a chair equipped with headrests, abdomen unbound. In each subject, the right and the left phrenic nerves were studied sequentially, providing 10 sets of data for analysis.
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Methods
Abdominal displacements. Changes in abdominal circumference were monitored with a strain gauge consisting of a piezoelectric sensor encased in a molded box 3 cm × 3 cm (Nihon Kohden, Tokyo, Japan) and attached to an elastic belt placed at the level of the umbilicus.
EMGs. Surface recordings were obtained by using pairs of skin-taped silver cup electrodes filled with conductive paste. The distance between the two electrodes of a given pair was kept to a minimum, never exceeding 2 cm. The positioning of the two electrodes respective to one another was adjusted (stepwise displacement of one of the electrodes around the other on a circle passing by each electrode center) until the obtainment of a clear return of the signal to its baseline after the stimulation artifact and the elimination of any short-latency small wave such as those described by Luo et al. (17). In our experience, these criteria are quasi-always possible to achieve, which was the case in this study. Four pairs of electrodes were used (Fig. 1A): 1) lower chest, anterior (Sant): active electrode in the eighth intercostal space, between the costochondral junction and the midclavicular line, reference electrode on the relief of the above rib, with a slight lateral displacement; 2) lower chest, axillary (Sax): active electrode in the sixth or seventh intercostal space just before the anterior axillary line, reference electrode on the relief of the above rib; 3) posterior (Spost): active electrode in the sixth intercostal space on the posterior axillary line (aimed at recording EMG activity arising from the latissimus dorsi and the serratus anterior), reference electrode on the relief of the above rib; and 4) upper chest, anterior (Sup): two electrodes on the muscle mass of the pectoralis major, on the midclavicular line, over the third or fourth intercostal space.
Intradiaphragmatic recordings were obtained with the use of bipolar concentric needle electrodes (diameter 0.3 mm, length 25 mm, sampling surface 0.03 mm2; Medelec, Old Woking, UK). In all subjects, two needle electrodes were inserted in each hemidiaphragm (Fig. 1A), one adjacent to Sant (Nant), the other (Nax) adjacent to Sax. Electrode insertion and positioning were performed after the technique described by Bolton et al. (3), modified regarding the site of insertion. In brief, the needle was inserted in the intercostal space at the upper border of the lower rib and slowly advanced at an upward angle of 45° with continuous auditory and visual monitoring of the EMG signal, until the activity from motor units discharging rhythmically with inspiration could be heard and seen. Then the subjects were asked to breathe in slowly but strongly while protruding the abdominal wall, as shown by the abdominal strain gauge. If necessary, the electrode was further advanced so as to record an optimal burst of EMG activity during this predominantly diaphragmatic inspiration. In most cases, the optimal site of recording was attained immediately after the operator had had to overcome a slight elastic resistance, which was at times reported as triflingly painful. All signals were fed to a Nihon Kohden Neuropack Sigma electromyograph (Nihon Kohden, Tokyo, Japan) with a 10-kHz sampling rate and a 20-Hz to 5-kHz bandwidth. They were stored on an Apple McIntosh computer for analysis (PowerLab, AD Instruments, Hastings, UK).Stimulations. All stimuli were delivered with the glottis closed, at relaxed end expiration and with the same abdominal configuration as judged from the continuous monitoring of the abdominal circumference trace. Lung volume and abdominal configuration were thus kept roughly constant (5, 11). Various stimulation techniques were used, as follows.
ES of the phrenic nerve (ESphren) was performed by using a bipolar electrode (anode and cathode 2 cm apart) delivering square-wave pulses of 0.1-ms duration. The phrenic nerve was stimulated at the posterior border of the sternocleidomastoid muscle, at the level of the cricoid cartilage or slightly lower. Once an EMG response was observed on Sant and Nant, maximal recruitment of the stimulated phrenic fibers was obtained by progressively augmenting the intensity of the stimulating current until the amplitude of the action potentials stabilized. Intensity was then increased by a further 20%. The operator took maximal care to isolate the diaphragm response from clinically visible responses of other muscles. ES of the brachial plexus (ESbrach) was achieved by displacing the electrode backward and upward from the ESphren spot until 1) phrenic nerve stimulation was lost (disappearance of clinically perceptible diaphragm contractions) and 2) characteristic arm movements were produced in addition to a visible Spost response. The purpose of this was to examine whether Sant and Sax could pick up a signal arising from brachial plexus innervated muscles in the absence of diaphragm contractions. ESbrach intensity was set to be at least equal to that of supramaximal ESphren. CMS was performed by using a Magstim 200 stimulator equipped with a circular doughnut-shaped 90-mm coil producing a maximum output of 2.5 T (Magstim, Whitland, Dyfed, UK). As in a previous study (35), the technique was slightly modified compared with its initial description (33, 34) in that the subjects kept the neck in a neutral position instead of bending it forward. The handle of the coil was directed caudally and held either parallel to the vertebral column or at a 45° angle. Two different coil positions were used, centered over the spinous process of the seventh cervical vertebra (C7-CMS) ("traditional" technique) or lower, over the spinous process of the second thoracic vertebra (T2-CMS). Stimulations were delivered by using the maximal output of the stimulator, after building simplified recruitment curves (stimulations at 60, 85, 90, and 95% of maximal output).Conventions for data analysis. The term "M-wave," abbreviated as "M-w," will henceforth be used to designate motor responses to phrenic stimulation. M-w latencies were measured as the time elapsed between the stimulus and the onset of the action potential, namely, the first departure of the signal from baseline. Data were rejected if the return of the signal to baseline after the stimulation was ambiguous or if there was evidence of contamination by an electrocardiogram complex. M-w latencies provided thereafter correspond to the average of five accepted stimulations. M-w amplitudes were measured from peak to trough. For Sant and Sax, signal contamination was deemed present when, in two or more of the five stimulations analyzed, the surface M-w latency was shorter than the corresponding needle M-w latency by more than 0.75 ms or closer to the latency measured in Spost or Sup than to the latency measures at the relevant needle electrode. The first of these criteria stemmed from the fact that needle electrodes are known to possibly provide longer latencies than surface electrodes for a given muscle (13, 22) with a difference of up to 2 ms, the 0.75-ms figure arbitrarily chosen here thus being conservative. The second criterion stemmed from the experience and common practice in routine clinical neurophysiology at our institution.
Statistical analysis. Analysis was performed by using the SuperAnova software (Abacus Concept, Berkeley, CA) on an Apple Macintosh computer. Differences between M-w latencies were assessed by using an analysis of variance for repeated measures followed by a Fisher's protected least-square difference test. Differences were considered significant when the probability P of a type I error was 0.05 or less. Mean ± SE values correspond to the results from 10 phrenic nerves.
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RESULTS |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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The M-w latencies measured at different sites with different
stimulation techniques are depicted by Fig.
2. No right-to-left difference could be
detected.
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Surface Latencies
The latencies measured at Sant and Sax with ESphren were in the normal range, not significantly different from one another (6.8 ± 0.25 vs. 6.7 ± 0.35 ms, respectively; P = 0.678) and similar to data obtained in our laboratory with the same technique (35). Analogous observations were made for C7-CMS (6.0 ± 0.25 ms vs. 5.7 ± 0.35 ms, P = 0.201). Moving the coil down (T2-CMS) did not significantly modify the latencies measured at Sant and Sax.At both Sant and Sax, the
C7-CMS-related latencies were significantly shorter than
the ES-related ones (Sant: 6.8 ± 0.25 vs. 6.0 ± 0.25 ms, respectively, P < 10
4;
Sax: 6.7 ± 0.35 vs. 5.7 ± 0.35 ms,
P < 104). Again, this finding is usual
in our hands, and the values are similar to previous ones
(35).
The responses at Sup and Spost were always of shorter latencies than at other sites (Fig. 2).
Needle Latencies
At Nant, the M-w latency of the response to ESphren averaged 7.8 ± 0.7 ms vs. 6.2 ± 0.13 ms in response to CMS (P < 104). At
Nax, those figures were 7.2 ± 0.35 and 6.2 ± 0.16, respectively (P < 104). Again,
there was no difference between C7-CMS and
T2-CMS.
Contamination
According to our convention (see MATERIALS AND METHODS), contamination of the signal picked up by Sax occurred in 1 of 10 phrenic nerves with ESphren, 5 with ESbrach, 2 with C7-CMS, and 1 with T2-CMS. At Sant, contamination was never observed with ESphren, C7-CMS, or T2-CMS and was clearly present in two cases with ESbrach. Figure 3 gives examples of uncontaminated recordings obtained with Sant in response to ESphren, ESbrach, and CMS.
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With CMS, the average latency at Sant was not significantly
different from the one at Nant (P = 0.19).
This was also the case for the difference between Sax and
Nax (P = 0.20). With
ESphren, the average latency at Sant
was significantly shorter than that at Nant
(P = 0.04), with a similar finding for Sax
and Nax (P < 104) (Fig. 2).
The latencies measured at Spost and Sup were
always significantly shorter than those measured at all the other sites
with C7-CMS, T2-CMS, and ESphren
(P < 104). With ESbrach, the
M-w latency measured at Sax when present was significantly
shorter than that measured at Nax (P < 102) and not significantly different from that measured
at Sup (P = 0.14) and Spost
(P = 0.48), illustrating contamination of the axillary
electrode by signals arising from extradiaphragmatic muscles.
Conversely, the latency measured with ESbrach at
Sant was, on average, longer than at Sup and
Spost (P < 104 in both
cases, Fig. 2). Only in two phrenic nerves was the latency at
Sant clearly shorter than at Nant and close to
the latency at Spost or Sup, showing that
contamination is possible but not systematic.
In cases in which contamination was considered likely with a given stimulation technique at maximal intensity, decreasing stimulation intensity did not modify the observed pattern.
Supramaximality
Expectedly according to the chosen experimental design, ESphren provoked supramaximal responses at Nax and Nant in all subjects. This was also the case at Sax and Sant when only uncontaminated data were considered. Simplified recruitment curves showed that this was also the case for C7-CMS and T2-CMS, again when only those Sant and Sax responses that were deemed uncontaminated were taken into account.| |
DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Our results show that it is possible to record an uncontaminated diaphragm response to electrical and magnetic phrenic nerve stimulation with the use of surface electrodes, which should make CMS a reasonable means of determining PNCTs in the clinical setting. In addition, the comparison of needle ES-PNCTs and needle CMS-PNCts supports the notion that ES and CMS depolarize the phrenic nerve in a different manner or at a different site.
Comparison With Previous Data From Our Laboratory
The PNCTs obtained in the present study are comparable to those reported by our laboratory several years back with the same techniques (35). As noted by Luo et al. (17), the PNCT values reported in earlier studies from our laboratory were longer (32, 33). This is likely accounted for by the lower power of the stimulator used in these studies. Indeed, increasing the power of a magnetic pulse applied to a peripheral nerve results in a distal shift of the site of depolarization and hence in a shortening of the latency of the evoked motor potential (19, 30), independently of the supramaximal nature of the stimulus.Signal Contamination
Relevance. With CMS and UMS, the coactivation of extradiaphragmatic muscles is unavoidable (15, 17, 33). With ES, it can be difficult to dissociate the stimulation of the phrenic nerve from that of the brachial plexus (2, 18). If this coactivation perturbs the signal picked up by "diaphragm" electrodes, then this signal cannot be used as an index of the function of the phrenic nerve. Reviewing the literature, Luo et al. (18) remarked several studies possibly affected by this problem. The issue is thus worth clarifying.
Reality of the risk of signal contamination. In response to nerve stimulation, a pair of surface electrodes principally records the activity of the muscle that lies underneath it. It can also record activity arising from distant, coactivated muscles, because of volume conduction of the signal through the adjacent tissues. This can occur for the diaphragm, as shown by several elegant studies by Luo et al. (16-18). In a first paper, they compared CMS and ES in terms of M-w recorded by a pair of surface electrodes placed in the sixth to eighth intercostal space on the anterior axillary line and by a special esophageal electrode (17). They noted shorter latencies in response to CMS than to ES at both sites. With CMS, the surface tracings consistently showed small short-latency waves preceding the main action potential, which were attributed to contamination from extradiaphragmatic activity (the exact source of contamination was not looked for). In addition, the amplitudes of the CMS-related M-w at the esophageal site were never bigger than their ES-related counterparts, whereas this was common at the surface site, which was also considered as a sign of contamination. In a study focused on ES, stimulating the brachial plexus purposely instead of the phrenic nerve shortened the M-w latency and changed its shape (18). This was also interpreted as a sign of signal contamination. Luo et al. quoted a study (2) mentioning that surface electrodes could pick up a small amount of diaphragm activity during contralateral phrenic stimulation and another one reporting signal contamination arising from the serratus anterior in response to ES (21).
Possibility to record an uncontaminated diaphragm signal. Before the present study, several arguments already supported this possibility. With ES, this is not disputable, and although the possibility to pick up a contralateral diaphragm activity during unilateral phrenic stimulation has been mentioned, seemingly in a single study (2), this is very rare. Over many years and among several hundreds of subjects and patients, we encountered it only twice, in extremely thin subjects with small thoraxes. Laghi et al. (15) mentioned that electrodes placed over the sternocleidomastoid, trapezius, parasternal, and pectoralis muscles did not always pick up activity in response to CMS. Because slight changes in stimulation technique over time can influence the degree of activation of contaminant muscles and because this is generally not controlled for, signal contamination is likely a source of a low reproducibility. We recently reported a case of demyelinating phrenic neuropathy (12) in which CMS and ES latencies varied together over 2 yr, which seems to us an argument against contamination. Another argument is the observation of an abolished response to CMS in patients with phrenic nerve palsy (6). We used this argument in a previous study [complete absence of response from surface electrodes in six patients with amyotrophic lateral sclerosis and complete diaphragm paralysis diagnosed on mechanical grounds (1, 35)]. Luo et al. (17) rebutted this position by postulating that, in our patients, the disease could have affected extradiaphragmatic muscles as well as the diaphragm. This is not likely to have been the case. Indeed, in this particular set of patients, the muscles of the upper rib cage did not appear atrophied, as illustrated by their ability to expand the rib cage in response to CMS (1). In a subsequent study, we described amyotrophic lateral sclerosis patients with diaphragm dysfunction and attenuated but persistent M-w in response to CMS (31). The latencies of these M-w could exceed 10 ms, probably in line with denervation atrophy (9). It is difficult to imagine which upper rib cage muscle activated from CMS could respond with such a delay.
The present study brings several additional arguments. First, the latencies determined from Sant and Sax were in the vast majority of cases clearly longer than the latencies measured at Sup and Spost (Fig. 3). This observation means that the amplitude of the corresponding signal did not incorporate a contaminant component, all the more so that, second, the M-w recorded at Spost and Sup tended to have higher amplitudes than that recorded at Nant and Nax. Third, and principally, the latencies measured by intramuscular diaphragmatic electrodes were, as a rule, closer to the latencies measured by their surface counterparts than to the latencies measured at Spost and Sup. These criteria (see MATERIALS AND METHODS) were not met in only a limited number of cases with CMS (see RESULTS) at Sax and never at the Sant site. By contrast, an important difference between surface and needle latencies was noted with ESbrach in the cases in which the Sax or, less frequently, Sant signals had latencies close or equal to the Sup or Spost ones. This substantiates the fact that needle diaphragm electrodes are hardly sensitive, if at all, to contamination. Of note, Zifko et al. (37), using CMS and needle electrodes, already reached conclusions similar to ours.Mechanisms of the discrepancies between studies. The reasons why our conclusions differ from that of Luo et al. (17, 18) probably lie in the recording techniques. In our setup, the electrodes are set <2 cm apart, compared with the 3- to 5-cm figure mentioned by Luo et al. in one of their studies (18) and the average 5-cm figure generally encountered in the literature. Moving the electrodes closer to one another should make them much more likely to record near-field potentials than far-field ones (4), as observed, for the diaphragm, by Markand et al. (21). The second major difference between our setup and commonly used ones is the location of the electrodes. The most classical placement is the anterior axillary line, used in all the studies by Luo and co-workers (16-18). The intercostal space over which the electrodes are placed varies from the sixth to the eighth one. It is clear from anatomy (Fig. 1) that this implies a high probability for the electrodes to directly overlay muscle fibers from the serratus anterior, particularly so when the electrodes are wide apart (21). The higher the electrodes sit on the thorax, the closer they will be to the muscle mass of the pectoralis major. This is well described in the ES study by Markand et al. (21), in which contamination was frequent when the electrodes were either high or posterior. For instance, contamination was apparent in a derivation comprising an active electrode in the eighth intercostal space 5 cm behind the axillary line but was absent when the active electrode was in the same intercostal space, close to the costochondral junction. Low and median recording sites were free of contamination. Our results with CMS fit the observations of Markand et al. (21). In the way our electrodes are positioned at Sant, the diaphragm should be closer to them than the most anterior insertions of the serratus anterior and latissimus dorsi and than the lowest insertions of the pectoralis major. The only remaining source of cross talk should be insertions of abdominal muscles intermingled with the diaphragm at the inner face of the lower ribs, but these cannot be activated by CMS.
Differences Between Surface and Intramuscular Recordings
The PNCTs from needle electrodes tended to be longer than their surface counterparts (Fig. 2). Similar observations are traditional in other muscles (13), although not constant (22). A needle electrode can provide falsely long latencies if it samples slow motor units (the risk being greater with muscles comprising many slow fibers, such as the diaphragm) or if its tip is distant from the motor plate of the sampled units (13). By contrast, surface electrodes give a more global idea of the muscle response (compound action potential) and should not miss the fastest motor units. It is interesting to note that the smallest needle-surface difference was observed with CMS (Nant vs. Sant 0.2 ms, not significant; Nax vs. Sax 0.5 ms, not significant). This supports the notion that CMS activates fast myelinated fibers more easily than does ES (6, 7).Differences Between ES and CMS
In a previous study (35), our laboratory reported that CMS provided PNCTs shorter than ES and attributed this finding to either the preferential activation of fast fibers by magnetic stimulation or a more distal nerve depolarization site. Signal contamination would invalidate these interpretations. A major argument for the reality of the ES-CMS difference comes from the results obtained here with the needle electrodes. Indeed, both at Nant and Nax, the CMS-PNCTs were shorter than the ES-PNCTs by 1-1.5 ms, which exactly fits the difference between surface CMS and ES PNCTs found in this study and the previous one. It also fits the latency difference reported for other nerves [1.4 ms for Ono et al. (26); 1.2 ms for Schmid et al. (30)]. The underlying mechanism is considered to be a more distal site of depolarization with magnetic stimulation that creates a virtual cathode more distant from the virtual anode than the cathode is from the anode during electrical stimulation. Therefore, the present study consolidates our conviction that CMS activates the phrenic nerve more distally than ES. Although artifacts of electronic source cannot be ruled out to explain the differences in shape that can at times be observed between M-w obtained with ES and CMS (Fig. 3), alternative mechanisms and site of depolarization probably account for most of these differences, which have been reported for other muscles as well.From the results of the present study, which was designed specifically in "latency" terms, going further carries the risk of data overinterpretation. Nevertheless, we have noted that the amplitude of uncontaminated CMS diaphragm M-w tended to be greater than that of ES M-w. This was also true for needle electrodes, ruling out signal contamination as an explanation. The number of phrenic fibers depolarized by ES could thus have been inferior to that depolarized by CMS. If our contention of a more distal depolarization by CMS is true, the stimulation of an accessory phrenic nerve would explain the higher M-w amplitude, because ES cannot reach this contingent of fibers. An accessory phrenic nerve is common (29) in humans and can be sufficient to sustain ventilation, as illustrated by the recovery of a diaphragmatic respiration described after phrenic nerve crushing in the neck for the treatment of tuberculosis (see Ref. 14). Such a hypothesis would imply that combining ES and CMS could allow one to study, in humans, the function of the accessory phrenic nerve, otherwise not accessible.
Practical Consequences
From their conclusion that surface electrodes are unreliable in response to magnetic phrenic nerve stimulation, Luo et al. (16) have advocated the use of esophageal recordings to measure PNCTs. Such recordings are not, however, without inconveniences, beyond their practical limitations. An esophageal recording cannot separate the responses of the two hemidiaphragms during bilateral stimulation. Signal contamination is not impossible (16, 17). The crural diaphragm is preferentially sampled, as opposed to the costal diaphragm with surface electrodes. Given that the crural diaphragm is predominantly innervated by the upper contingent of the cervical phrenic motoneurons (C3-C4) (20) whereas the costal diaphragm is innervated by the lower contingent, CMS coupled with surface recordings could be the safest way to activate and record the greatest possible number of phrenic fibers, which is important for strength and activation studies.We wish to emphasize that our current technique for electrode positioning is the result of a slow evolution over years. From this trial and error process, we propose that, in routine clinical practice, a safe procedure to verify that signal contamination is not a factor in a given patient could include 1) the placement of the electrodes in the lowest accessible intercostal space, close to the chondrocostal junction; 2) keeping the two electrodes as close as possible to one another, as many electrodes repositioning relative to each other as needed to obtain a clear and steady return of the signal to baseline after the stimulation artifact; and 3) simultaneous recordings from electrodes placed on the muscle mass of the pectoralis major or of the latissimus dorsi. An EMG response providing a PNCT shorter than 5 ms and not clearly longer than the concomitant latency of the response of the pectoralis major or of the latissimus dorsi to stimulation should be strongly suspected to be troubled by signal contamination.
In conclusion, our study shows that it is possible to study the EMG of the diaphragm in response to CMS and ES with surface electrodes, hence to diagnose and follow up phrenic nerve conduction abnormalities. In this regard, the study, small in size, must be taken as preliminary: the frequency of signal contamination in the relevant population, which is patients with suspected phrenic nerve problems, remains to be determined. Our results also indicate that CMS-PNCTs cannot be interpreted by using normal values derived from ES studies (we consider 6.5 ms as the upper limit of normal for CMS-PNCT). In this view also, large-scale studies of CMS-PNCTs with comparisons with ES are required to better determine normal values. Meanwhile, every laboratory wishing to implement the technique should perform exploratory studies to optimize its setup.
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ACKNOWLEDGEMENTS |
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This study was funded by the Association pour le Développement et l'Organisation de la Recherche en Pneumologie (ADOREP), Paris, France.
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FOOTNOTES |
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Address for reprint requests and other correspondence: T. Similowski, Laboratoire de Physiopathologie Respiratoire, Service de Pneumologie et de Réanimation, Groupe Hospitalier Pitié-Salpêtrière, 47-83, Bd de l'Hôpital, 75651 Paris Cedex 13, France (E-mail: thomas.similowski{at}psl.ap-hop-paris.fr).
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
10.1152/japplphysiol.00652.2001
Received 25 June 2001; accepted in final form 8 November 2001.
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REFERENCES |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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