Dynamic change of proximal conduction in demyelinating neuropathies: A cervical magnetic stimulation combined with maximum voluntary contraction

doi:10.1016/j.clinph.2006.11.013

Clinical Neurophysiology

Volume 118, Issue 4, April 2007, Pages 741-750

https://doi.org/10.1016/j.clinph.2006.11.013 Get rights and content

Abstract

Objective

To evaluate conduction abnormalities in the nerves innervating the proximal muscles in demyelinating neuropathies (DN) using cervical magnetic stimulation.

Methods

We applied cervical root magnetic stimulation in the biceps brachii muscles and examined its activity-dependent conduction changes produced by maximal voluntary contraction (MVC) in 12 DN patients (seven chronic inflammatory demyelinating polyradiculoneuropathy and five multifocal motor neuropathy), six motor neuron disease (MND) patients, and 12 healthy volunteers.

Results

Defining the upper normal limit of motor threshold (31%) and latency (6.7 ms) of the compound muscle action potential (CMAP) as mean + 2SD, most DN patients revealed an abnormality in motor threshold (10/12) and latency (11/12) in contrast to MND patients (motor threshold (1/6) and latency (0/6)). These parameters contribute to the differentiation of DN from MND (P < 0.01). Furthermore, the MVC maneuver transiently decreased the CMAP amplitude ratio (after MVC/before MVC × 100) in DN (83 ± 18 %) compared with MND (P < 0.01). Two of three DN patients who showed normal motor threshold or latency as in MND were successfully differentiated from MND by the MVC maneuver.

Conclusions

In DN patients, conduction abnormality in the nerves innervating the proximal muscles was revealed by cervical magnetic stimulation combined with the MVC maneuver.

Significance

Our results suggested that conduction abnormalities in the proximal nerves innervating the proximal muscles could be evaluated by this method.

Introduction

For the diagnosis of acquired demyelinating neuropathies (DN), such as chronic inflammatory demyelinating polyradiculoneuropathy (CIDP) and multifocal motor neuropathy (MMN), motor nerve conduction studies (NCSs) for the distal hand muscles are commonly used to detect the site of conduction block or slowing. When the lesion site is located in the proximal segment, cervical root stimulation with a magnetic coil is also used. It effectively activates the deep structures with little discomfort (Chokroverty et al., 1991, Cros et al., 1990) and can be used to evaluate proximal motor conduction (Bischoff et al., 1993, Boyacıyan et al., 1996, Inaba et al., 2002, Maegaki et al., 1994, Takada and Ravnborg, 2000, Wöhrle et al., 1995).

It would, however, be difficult to test conduction abnormalities in DN patients with severely atrophied hand muscles due to secondary axonal degeneration, because of the low amplitude of compound muscle action potentials (CMAPs). NCSs using less atrophied proximal muscles would, then, be feasible rather than those of distal hand muscles (Cros et al., 1990, Epstein, 1993). NCSs of the musculocutaneous nerve have been investigated by electric stimulation applied at the axilla and Erb’s point (Trojaborg, 1976). However, this can cause severe discomfort in some subjects and will not detect lesion sites more proximal than Erb’s point.

According to previous reports (Cappelen-Smith et al., 2000, Kaji et al., 2000), patients with MMN and CIDP showed a peculiar fatigue phenomenon after sustained muscle contraction. The CMAPs of their distal hand muscles showed significant decreases of amplitude and increases of threshold after a maximum contraction for 60 s (Cappelen-Smith et al., 2000, Kaji et al., 2000). These studies indicate that hyperpolarization of the axonal membrane induced by activity causes a transient and activity-dependent conduction block, resulting in easy fatigability.

In this study, we examined conduction and also investigated the dynamic changes of CMAP parameters before and after sustained voluntary contraction in proximal muscles to detect occult demyelinating lesions in the nerves innervating the proximal muscle. We also compared the findings before and after intravenous immunoglobulin (IVIg) therapy.

Section snippets

Subjects

Seven CIDP patients (Four women and three men, age 35.4 ± 13.2 years (mean ± SD), range 19–60 years) and 5 MMN patients (one woman and four men, age 56.2 ± 7.8 years, range 48–64 years) participated in this study. Six MND patients (one woman and five men, age 60.0 ± 12.8 years, range 43–73 years) served as disease controls, and 12 healthy volunteers (three women and nine men, age 48.5 ± 15.9 years, range 26–72 years) served as normal controls. All patients but one (Patient 12 in Table 1) were recruited

Results

There were no significant differences in any of the CMAP parameters obtained by conventional NCSs (data not shown) and cervical magnetic stimulation, between the patients with CIDP and those with MMN (Table 2). These two groups were thus regarded as a single DN group. The MND patients were significantly older than the CIDP patients (P = 0.01), but the mean age of patients with DN (grouped CIDP and MMN patients together) (44.1 ± 15.2 years, range 19–64 years) was not significantly different from

Discussion

The present study demonstrated that cervical root magnetic stimulation combined with MVC maneuver could differentiate DN from MND and normal subjects. Motor threshold was increased and CMAP latencies were prolonged in most DN patients, and the MVC maneuver decreased CMAP amplitude selectively only in DN patients. Although the number of subjects was small and we tested the already proven patients, our preliminary findings suggested that the dynamic change of CMAP after MVC could predict

Conclusion

The nerves innervating the proximal muscles revealed conduction failure immediately after the MVC maneuver in patients with DN. The techniques used in this study are regarded as a dynamic conduction test in the time domain rather than in the space or nerve length domain, and is a possible method for differentiating treatable conditions from MND. This technique might detect occult lesions in the proximal site, if present, even though distal muscles are not available because of the severe atrophy

Acknowledgements

We thank Dr. Jun Kimura (University of Iowa, Iowa City, IA) for comments on CMAP change. We thank Dr. Nobuyuki Oka (South Kyoto Hospital, Japan) for assessing the antiganglioside antibody titers and sural nerve biopsy. We thank Drs. Akira Kuzuya and Hirofumi Yamashita for their help with some experiments.

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Using the TST, we demonstrated that all 6 had proximal CB situated between the root emergences and the Erb point. It was previously reported that the most frequent sites of CB in inflammatory demyelinating neuropathies are very proximal, between the root emergence and the Erb point (Hitomi et al., 2007; Inaba et al., 2002). The utility of the TST has been reported in other immune neuropathies (Attarian et al., 2005, 2015; Deroide et al., 2007; Taieb et al., 2015).
Current diagnostic electrophysiological criteria can miss the early stages of Guillain–Barré syndrome (GBS). We evaluated the diagnostic efficiency of the triple stimulation technique (TST) in highlighting proximal conduction blocks (CBs) in patients who do not meet the electrophysiological criteria for GBS.
All patients with a diagnosis of clinical GBS referred to our center between September 2014 and January 2016 were included in the study. For patients who did not fulfill the electrophysiological criteria of GBS, we performed the TST examination.
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TST is useful for the diagnosis of GBS in association with NCS, particularly in the early stages of the disease.
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Usefulness of cervical root magnetic stimulation in assessing proximal motor nerve conduction
2015, Journal of Electromyography and Kinesiology
Objectives: To evaluate the reliability and utility of cervical root magnetic stimulation in exploring proximal motor conduction. Methods: In 20 patients with demyelinating polyneuropathy (DPN), 20 patients with amyotrophic lateral sclerosis (ALS) and 25 healthy subjects, evoked compound muscle action potentials (CMAPs) were recorded from abductor digiti minimi muscle in response to electrical stimulation up to Erb’s point and magnetic stimulation up to the cervical roots. Results: In all healthy and ALS subjects, magnetic root stimulation confirmed the absence of conduction abnormalities, including those in whom supramaximal responses at Erb’s point were not achieved. In the DPN group, conduction block and/or temporal dispersion was revealed by magnetic root stimulation in 9 out of 20 patients (45%), 3 more than those detected at Erb’s point. Conclusions: Cervical root stimulation allowed clear distinction between motor neuronopathy and DPN. It is recommended as part of the routine evaluation of patients suspected of having DPN, especially when distal nerve studies are inconclusive.
Magnetic-motor-root stimulation: Review
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Citation Excerpt :
The focal activation site is explained by the concentration of induced currents into a small canal instead of penetrating the bony structures with a high resistance for electrical currents. Many papers have supported this assumption on the activation site and have demonstrated its clinical utility for cervical motor roots using a round coil (Chokroverty et al., 1991; Ugawa et al., 1990; Britton et al., 1990; Cros et al., 1990a; Schmid et al., 1990; Evans et al., 1990; Maegaki et al., 1994; Benecke, 1996; Boyaciyan et al., 1996; Öge et al., 1997; Inaba et al., 2002; Ugawa, 2004; Hitomi et al., 2007; Temuçin and Nurlu, 2011) and a figure-of-eight coil (Epstein et al., 1991; Mills et al., 1993), as well as for lumbosacral motor roots using a round coil (Chokroverty et al., 1989, 1993; Ugawa et al., 1990; Britton et al., 1990; Macdonell et al., 1992; Ertekin et al., 1994a; Benecke, 1996; Maccabee et al., 1996; Troni et al., 1996; Takada and Ravnborg, 2000; Ugawa, 2004; Souayah and Sander, 2006) and a figure-of-eight coil (Maccabee et al., 1996; Maegaki et al., 1997). Maccabee et al. (1991) verified the assumption that the activation site is the neuroforamina in vitro (Maccabee et al., 1991).
Magnetic stimulation can activate the human central and peripheral nervous systems non-invasively and virtually painlessly. Magnetic stimulation over the spinal enlargements can activate spinal nerves at the neuroforamina (magnetic-neuroforamina stimulation). This stimulation method provides us with information related to the latency of compound-muscle action potential (CMAP), which is usually interpreted as peripheral motor-conduction time (PMCT). However, this stimulation method has faced several problems in clinical applications. One is that supramaximal CMAPs were unobtainable. Another is that magnetic stimulation did not usually activate the spinal nerves in the spinal canal, i.e., the cauda equina, which prevented an evaluation of its conduction. For these reasons, magnetic-neuroforamina stimulation was rarely used to evaluate the conduction of peripheral nerves. It was mainly used to evaluate the conduction of the corticospinal tract using the parameter of central motor-conduction time (CMCT), which was calculated by subtracting PMCT from the latency of motor-evoked potentials (MEPs) elicited by transcranial magnetic stimulation (TMS) over the primary motor cortex. Recently, supramaximal stimulation has been achieved in magnetic-neuroforamina stimulation, and this has contributed to the measurement of both CMAP size and latency. The achievement of supramaximal stimulation is ascribed to the increase in magnetic-stimulator output and a novel coil, the magnetic augmented translumbosacral stimulation (MATS) coil. The most proximal part of the cauda equina can be reliably activated using the MATS coil (magnetic-conus stimulation), thus contributing to the measurement of cauda equina conduction time (CECT) and cortico-conus motor-conduction time (CCCT). These recent developments in magnetic-motor-root stimulation enable us to more precisely evaluate the conduction of the proximal part of peripheral nerves and that of the corticospinal tract for lower-limb muscles. In this review article, we summarise the basic mechanisms, recent topics, clinical applications, comparison to electrical stimulation, pitfalls, safety and additional issues in magnetic-motor-root stimulation.
Activity-dependent conduction block in chronic inflammatory demyelinating polyneuropathy
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For several reasons it is not justified to attribute these CMAP changes to activity-dependent CB. First, in some nerves the CMAPs were already severely decreased (less than 1 mV) before MVC, indicating that only a few conducting axons were left [1,6]. Temporal dispersion of nerve action potentials, induced by MVC, may then yield phase cancellation between the few MUPs contributing to the CMAP, resulting in a decreased CMAP without increase in duration, giving the false impression that MVC induced CB [12].
Previous studies suggested that activity-dependent conduction block (CB) contributes to weakness in chronic inflammatory demyelinating polyneuropathy (CIDP). These studies, however, investigated only one nerve segment per patient, employed cervical magnetic stimulation which may be submaximal, included nerves with extremely low compound muscle action potentials (CMAPs) which precludes assessment of CB, and lacked predefined criteria for activity-dependent CB. Obtaining more robust evidence for activity-dependent CB is important because it may be treated pharmacologically. We investigated 22 nerve segments in each of 18 CIDP patients, employed supramaximal electrical stimulation, excluded nerves with markedly reduced CMAPs, and adopted criteria for activity-dependent CB. Each nerve was tested before and immediately after 60 s of maximal voluntary contraction (MVC) of the relevant muscle. Per nerve segment we calculated segmental area ratio: (area proximal CMAP)/(area distal CMAP). Per nerve we calculated total area ratio: (area CMAP evoked at Erb's point)/(area most distally evoked CMAP). MVC induced no change in mean area ratios and no activity-dependent CB according to our criteria, except for one segment. MVC induced increases in distal and proximal CMAP area and duration. In segments with demyelinative slowing, MVC induced an increase in CMAP duration prolongation. Thus, in CIDP, muscle activity induces virtually no CB, but it may increase temporal dispersion of nerve action potentials.
Micro-multi-probe electrode array to measure neural signals
2009, Biosensors and Bioelectronics
A multi-electrode array (MEA) with 16 channels was designed to record simultaneously the velocity of conduction of neurons in a measurement system for bio-medical applications. MEA were fabricated with MEMS technology on a silicon-on-insulator (SOI) wafer, which controls the thickness of the probe effectively. All used probes have length 3 mm and width 100 μm. The thickness of the probe, 25 μm, was defined by the thickness of the device layer on the SOI wafer. The multiple probes with a 16-site recording electrode array have been manufactured; their strength was tested with a force gauge and their electrical performance was tested with an impedance measurement system. The readout circuitry comprises an array of 16-site preamplifiers fully integrated on a chip that is capable of signal processing to improve the signal-noise-ratio (SNR). To demonstrate the capability, multiple neural signals were recorded simultaneously with all electrodes from each separate probe. To verify its capability of measuring neural signals, the MEA was used to measure these signals from the electrophysiology system of crayfish. The velocity of neural conduction recorded with a fabricated MEA is shown, and is comparable with a measurement with a traditional glass pipette. The MEA for recording neural signals would be improved in further development.
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Dynamic change of proximal conduction in demyelinating neuropathies: A cervical magnetic stimulation combined with maximum voluntary contraction

Abstract

Objective

Methods

Results

Conclusions

Significance

Introduction

Section snippets

Subjects

Results

Discussion

Conclusion

Acknowledgements

Electroencephalogr Clin Neurophysiol

J Neurol Sci

Clin Neurophysiol

Electroencephalogr Clin Neurophysiol

Electroencephalogr Clin Neurophysiol

Electroencephalogr Clin Neurophysiol

Clin Neurophysiol

The value of magnetic stimulation in the diagnosis of radiculopathies

Muscle Nerve

Activity-dependent excitability changes in normal and demyelinated rat spinal root axons

J Physiol

Activity-dependent hyperpolarization and conduction block in chronic inflammatory demyelinating polyneuropathy

Ann Neurol

Cervical magnetic stimulation

Neurology

Multifocal motor neuropathy improved by IVIg: randomized, double-blind, placebo-controlled study

Neurology

M wave potentiation during and after muscle activity

J Appl Physiol

Inflammatory Neuropathy Cause and Treatment (INCAT) Group. Randomized controlled trial of intravenous immunoglobulin versus oral prednisolone in chronic inflammatory demyelinating polyradiculoneuropathy

Ann Neurol

Electrophysiological evaluation of conduction in the most proximal motor root segment

Muscle Nerve

The development of conduction block in single human axons following a focal nerve injury

J Physiol

Activity-dependent conduction block in multifocal motor neuropathy

Brain