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 Table of Contents  
ORIGINAL ARTICLE
Year : 2022  |  Volume : 39  |  Issue : 1  |  Page : 14-20

Tremor and myoclonus is common in immune-mediated and hereditary polyneuropathies


Department of Neurology, Cerrahpasa Faculty of Medicine, Istanbul University-Cerrahpasa, Istanbul, Turkey

Date of Submission11-May-2021
Date of Decision18-Oct-2021
Date of Acceptance04-Nov-2021
Date of Web Publication31-Mar-2022

Correspondence Address:
Damla Cetinkaya Tezer
Department of Neurology, Cerrahpasa Faculty of Medicine, Istanbul University-Cerrahpasa, Istanbul
Turkey
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/nsn.nsn_99_21

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  Abstract 


Objective: Our goal was to identify the frequency and types of involuntary movements in immune mediated and hereditary polyneuropathies. Methods: In this prospective study, we included all consecutive patients with immune mediated or hereditary polyneuropathy between January 2017 and November 2019. The presence and type of the involuntary movements were determined by the clinical examination and multichannel surface electromyography. Results: We identified 23 (48.9%) patients with involuntary movements among 47 patients with immune mediated or hereditary polyneuropathy in the study period. All patients with an involuntary movement had postural tremor with accompanying action and/or rest tremor. Short duration and high-amplitude myoclonus was accompanying in 18 (38.3%) patients. The demographic and clinical characteristics and features of nerve conduction studies were similar between patients with and without involuntary movements. Discussion: Tremor and myoclonus were frequent in our cohort. Postural tremor was the most frequent subtype. There was no significant relationship between myoclonus or tremor and clinical/electrophysiological features. Conclusion: For assessing movement disorders in polyneuropathies not only clinical examination, but also electrophysiological studies such as multichannel surface electromyography should be used.

Keywords: Chronic inflammatory demyelinating polyneuropathy, hereditary neuropathy, myoclonus, polyneuropathy, tremor


How to cite this article:
Tezer DC, Gündüz A, Tütüncü M, Akalın MA, Adatepe NU, Savrun FK, Kızıltan ME. Tremor and myoclonus is common in immune-mediated and hereditary polyneuropathies. Neurol Sci Neurophysiol 2022;39:14-20

How to cite this URL:
Tezer DC, Gündüz A, Tütüncü M, Akalın MA, Adatepe NU, Savrun FK, Kızıltan ME. Tremor and myoclonus is common in immune-mediated and hereditary polyneuropathies. Neurol Sci Neurophysiol [serial online] 2022 [cited 2022 May 16];39:14-20. Available from: http://www.nsnjournal.org/text.asp?2022/39/1/14/342367




  Introduction Top


Tremor is an oscillatory and rhythmic involuntary movement, which is generated by the synergistic or alternating contractions of agonist and antagonist muscles.[1] It is observed in various systemic diseases and neurological disorders with central or peripheral origin. The underlying mechanism is the abnormal peripheral or central input leading to the oscillatory activity.[2] Tremor in polyneuropathies was first reported in hereditary neuropathies and neuropathic tremor was described as early as 1900s.[3],[4],[5] Thereafter, it has been reported in the various kinds of hereditary and immune-mediated polyneuropathies such as Guillain − Barré syndrome (GBS) and multifocal motor neuropathy.[4] The frequency of tremor reaches up to 80%, especially in neuropathies associated with Ig M paraproteinemia.[3],[6],[7] Although there was a small evidence of association between tremor and motor conduction velocities[8] or tremor and upper extremity F-wave latency,[9] no connection has been established with clinical and electrophysiological features.[10]

We observed that involuntary movements such as tremor in polyneuropathy are frequently observed in both hereditary and immune-mediated neuropathies. Based on this, we aimed to evaluate patients with immune-mediated or hereditary polyneuropathy using neurological examination and multichannel surface electromyography (EMG) features to reveal the frequency of involuntary movements and the characteristics of involuntary movements. In a secondary analysis, we compared the demographic, clinical, and electrophysiological features in patients with and without involuntary movements to disclose the associated features.


  Methods Top


Patients

The records of all patients who were admitted to Cerrahpaşa Medical Faculty, Neurology Department, Neuromuscular Disorders outpatient clinic between January 2017 and November 2019 were evaluated. Among these patients, patients with immune-mediated and hereditary polyneuropathies were identified and included in the study. Hereditary polyneuropathy was defined as patients who had genetically validated diagnosis or had the diagnosis clinically and electrophysiologically compatible with hereditary polyneuropathy with a family history. Immune-mediated neuropathies were classified according to the previous reports and consensus guidelines.

Patients with a central or peripheral disease that may cause an involuntary movement (such as epilepsy, essential tremor, and Parkinson's disease), patients who cannot tolerate electrophysiological examinations due to difficulty in cooperation were excluded from the study.

Eligible patients were invited for detailed electrophysiological examinations and clinical evaluation. According to the clinical and electrophysiological evaluation, patients were grouped into two groups: Patients with involuntary movements and patients without involuntary movements.

Documents including the project form of the study and the informed patient consent form were submitted to the clinical research ethics committee of Istanbul University – Cerrahpaşa, Cerrahpaşa Medical Faculty and ethics committee approval was obtained. Each subject gave informed consent.


  Clinical evaluation Top


Demographic characteristics, type of immunosuppressive or immunomodulatory treatments, genetic and laboratory tests, if any, were extracted from the medical records of the patients included in the study.

All patients were examined in detail. The clinical features of involuntary movements (rhythmicity, amplitude, frequency, localization, change during rest, posture or features during performing a specific voluntary movement, and whether they disappeared with distraction) were noted. Spiral drawing and straight-line drawing tests were recorded.

Electrophysiological tests

All recordings were done with Neuropack Sigma MEB-5504k (Nihon Kohden Medical, Tokyo, Japan) device. Silver-silver chloride surface recording electrodes were used. All electrophysiological examinations were performed in a comfortable and convenient position in a quiet room after proper skin temperature was achieved (mean 32°C). A single electrophysiologist (M. E. K.) performed all multichannel surface examinations and long latency reflex studies. The following tests were done.

Peripheral nerve conduction and needle electromyography

We recorded bilateral median, ulnar and sural nerve sensory action potentials, median, ulnar, peroneal and tibial nerve motor conduction velocities, distal latencies and combined muscle action potentials and F-wave responses by applying standard techniques. We measured peak latencies and peak-to-peak amplitudes for sensory responses and onset latencies, onset-to-peak amplitudes and conduction velocities for motor responses. Minimum F-wave response latency was measured and persistence of F response was calculated. The presence of reduction in amplitudes, slowing of conduction velocity, conduction block, and temporal dispersion were noted. We also performed needle EMG examination of the first dorsal interosseous (FDIO) and extensor digitorum communis muscles. Spontaneous activity and characteristics of motor unit potentials (MUPs) were evaluated. According to the electrophysiological characteristics, subtype polyneuropathy was established as axonal, demyelinating, and mixed subtypes.[11]

Multichannel surface electromyography

Surface recording electrodes were placed on the proximal and distal muscle groups of the upper extremities (biceps brachii, wrist flexor muscles, wrist extensor muscles, abductor pollicis brevis (APB), and FDIO in some patients) and involuntary movements were recorded. Sensitivity and analysis time was 200–500 μV/div and 0.1 s/div, respectively. Then, we changed the analysis time to 10 ms/div to examine the discharge properties. The frequency range was 20 Hz–5 kHz.

We examined the involuntary movements during rest, in which full relaxation of involuntary movement was achieved, during maintaining a certain posture and during performing simple voluntary movements. If the involuntary movement occurs when performing a certain movement, recordings were made during that specific movement. The type, frequency, rhythmicity, amplitude, and duration of involuntary movements were evaluated. Tremor was classified as postural, action, or rest tremor according to its properties by multichannel surface EMG.[12]

Myoclonus was evaluated as positive and negative myoclonus according to previously defined criteria.[13],[14] Polyminimyoclonus was evaluated according to the features described by Salazar et al.[15]

Long-latency reflexes

Long-latency reflexes were recorded on APB muscle after electrical stimulation of median nerve at wrist. The duration and intensity of stimulus were 0.2 ms and 20–30 mA, respectively. The recordings were done at rest and during mild contraction. High and low frequency filters were set to 2–2000 Hz. Sensitivity was set at 200 μV/div, and analysis time was 20 ms/div.

Statistical analysis

First, we determined the presence, types, and characteristics of involuntary movements.

According to the presence of involuntary groups, two groups were constituted: Groups with and without involuntary movements. In patient groups with and without involuntary movements, demographic features (age, sex, and duration of neuropathy), clinical features (treatments they received and etiologies) and electrophysiological features (subtype of polyneuropathy, reduction in amplitude, slowing of conduction velocity, conduction block, temporal dispersion, presence of C reflex, spontaneous activity, and MUP changes) were compared. The subtypes of polyneuropathy were classified as predominantly axon loss, predominantly demyelinating, mixed according to previous reports.

Numerical data were presented as mean ± standard deviation (minimum-maximum) and categorical variables in n (%).

The Chi-square test was used to compare the categorical data. We determined whether the numerical data complied with the rules of normal distribution. t-test was used for independent groups when there was a homogenous distribution, and Mann–Whitney U-test was used for nonhomogeneous data. When the number of groups was more than two, Kruskal − Wallis test was preferred.

Statistical analysis was performed using IBM SPSS (version 20.0) (SPSS, Chicago, IL). P value was deemed <0.05.


  Results Top


We determined 59 patients with immune-mediated polyneuropathy or hereditary polyneuropathy during the study period. Nine patients were excluded according to the exclusion criteria. Three patients were excluded from the study because they did not agree when they were invited for the examination.

In total, 47 patients were included in the study, 23 (48.9%) of whom had involuntary movements. All patients with involuntary movements had tremor according to the clinical and multichannel surface EMG examination. Among them, multichannel surface EMG examination revealed that 18 (38.3%) patients also had myoclonus.

We determined that there were patients with chronic inflammatory demyelinating polyneuropathy (CIDP) (n = 22), GBS (n = 11), and hereditary polyneuropathy (n = 14). Among them, the frequency of tremor was higher in GBS (63.6%) followed by CIDP (50.0%) and hereditary polyneuropathy (35.7%).

All patients with involuntary movements had postural tremor. However, in some patients, action and rest tremor was also observed. Postural tremor was not isolated in any patient. The frequency of postural tremor ranged between 3.5 and 12–13 Hz. The frequency of the action tremor was between 4 and 11 Hz. The frequency of rest tremor ranged from 6 to 9 Hz. None of these cases had bradykinesia or rigidity. [Figure 1]a and [Figure 1]b shows the examples of postural tremor with different frequencies in patients with CIDP.
Figure 1: (a) 8 Hz postural tremor in a 36-year-old male chronic inflammatory demyelinating polyneuropathy patient (b) 6–7 Hz postural tremor in proximal muscles in a 56-year-old female chronic inflammatory demyelinating polyneuropathy patient (c) Positive and negative myoclonus in 32-year-old male chronic inflammatory demyelinating polyneuropathy patient (d) Polyminimyoclonus in a 57-year-old male patient with hereditary polyneuropathy

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Myoclonus was detected in 18 of 23 patients who had involuntary movements. All patients had positive myoclonus. Patients with myoclonus also had rest tremor. Ten patients also had negative myoclonus. In 15 of these patients, myoclonic discharges repeated in certain series creating polyminimyoclonus. The duration of one myoclonic discharge ranged between 30 and 110 ms and each one was high in amplitude. C reflex was not detected in any patient with myoclonus. Seven of eighteen patients (38%) were diagnosed with CIDP, 6 (33%) had GBS, and 5 (27%) had hereditary polyneuropathy. [Figure 1]c shows the examples of positive and negative myoclonus in a patient with CIDP, whereas [Figure 1]d shows a representative example of polyminimyoclonus in a patient with hereditary polyneuropathy.

Comparisons of patients with and without tremor

In patients without tremor, eleven (45%) were diagnosed with CIDP, four (16%) with GBS, and nine with hereditary polyneuropathy (37%), whereas there were 11 (45%) patients with CIDP, seven (30%) with GBS, and five (21%) with hereditary polyneuropathy in the group with tremor (P = 0.397).

Among patients with and without tremor, there were three (13.0%) and seven (29.2%) women, respectively (P = 0.160). The mean age was 46.3 ± 19.3 (17–82) years and 47.0 ± 13.1 (15–70) years, respectively (P = 0.950). The disease duration was 8.0 ± 7.9 and 8.6 ± 11.4 years, respectively (P = 0.859). The subtypes of polyneuropathy were similar in the comparison of patients with and without tremor.

All patients with GBS had used intravenous immunoglobulin (IVIg). The medications used by patients with CIDP were IVIg, corticosteroids, or rituximab. The number of patients receiving each treatment among patients with CIDP was similar when groups with and without tremor were compared. Patients with hereditary polyneuropathy did not receive a specific treatment.

[Table 1] shows the comparison of demographic and clinical features as well as findings in nerve conduction studies and needle EMG between patients with and without tremor. [Table 2] shows the subtypes of tremor and myoclonus according to the different etiologies.
Table 1: The comparison of demographic, clinical and electrophysiological features between patients with and without tremor

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Table 2: The comparison of multichannel surface electromyography features according to diagnoses

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  Discussion Top


The most important findings of the study are as follows: (i) There were involuntary movements in almost half of the patients with immune-mediated or hereditary polyneuropathy, (ii) the prevalence was the most common in GBS (63.6%) group followed by CIDP (50.0%) and hereditary polyneuropathy (35.7%), and (iii) tremor was the most common involuntary movement; however, myoclonus accompanied in most (78%) of them in patients with polyneuropathy included in this cohort.

The characteristics of involuntary movements did not differ significantly in patients with different diagnoses. There was no significant difference between patients with and without tremor or among tremor subgroups in terms of demographic characteristics, duration of disease, diagnosis, and electrophysiological parameters. These characteristics were also similar between patients with and without myoclonus.

Interestingly, in our study, the frequency of tremor was higher in the GBS group as compared to the reports in the literature.[16] One of the main reasons why frequency is so variable is the methodological factors regarding the evaluation of tremor. As seen in our study, when detailed examination and electrophysiological findings are combined, tremor is quite common in all types of neuropathy cases. In the study of Wasielewska et al. using the electrophysiological methods (accelerometer and surface EMG), 60% of 89 patients with different types of polyneuropathy or 83% of the CIDP and 73% of Charcot-Marie-Tooth disease (CMT) patients had tremor.[10] Therefore, we suggest that tremor is probably underrated in the various types of polyneuropathy. Although we did not quantify, the amplitude of the involuntary movements was high. Thus, the involuntary movements may be a cause of disability in patients with polyneuropathy and should be evaluated in details. Tremor evaluation is generally not included in clinical scales, and it is clear that electrophysiological analysis has an important role in determining involuntary movement.

The tremor observed in peripheral neuropathies is prominent in the distal muscle groups of bilateral upper extremities.[3],[4],[6] Considering previous studies, it has been reported that rest tremor was accompanied by postural and action tremor in some cases in inflammatory neuropathies, and postural and action tremor was observed in CMT cases similar to essential tremor.[4],[7],[10] In our study, similar to that found in the literature, postural tremor (100%) was the most common, followed by action tremor (91%) and then rest tremor (43%). We found that subtype of tremor was not able to differentiate GBS, CIDP, or hereditary polyneuropathy.

Similar to that, we found no significant association between presence or characteristics of the tremor and the duration of disease, the subtypes of polyneuropathy, the treatments they received, motor conduction slowing, motor conduction block, abnormal F-wave responses latency and persistence, MUP findings. However, previously, the median and ulnar nerve F response latency was found to be significantly correlated with the spiral scores, whereas there was no significant association between other electrophysiological and clinical parameters and tremor association similar to our study.[9]

Neurofascin-155 (NF-155) antibodies were first identified in patients with multiple sclerosis and then shown in GBS and CIDP.[17],[18] The common features of patients with NF-155 antibodies were high-amplitude postural and action tremor leading to disability. It has been speculated that the presence of tremor in CIDP may be a marker in the examination for this group of antibodies, so it may have a prognostic significance in predicting the response to IVIg therapy.[19] In our study, the absence of NF-155 antibodies investigation was a major limitation. However, tremor was not specifically associated with one of the clinical or electrophysiological findings that we have studied. There were IVIg resistant cases that would require the use of rituximab in the nontremor group. Nevertheless, regarding our study group, tremor did not always mean IVIg unresponsiveness. In addition, tremor in CMT had characteristics similar to those seen in CIDP.

Almost all patients in this study had both sensory and motor involvement. However, inability to reveal any relationship between one of the electrophysiological findings and tremor disenabled us to comment on the type of effective peripheral input. An interesting point is that among our GBS cases, although the clinical and electrophysiological findings were completely normal, there were cases, in which tremor continued. This finding suggested that the short-term deterioration in peripheral inputs was sufficient for the formation of tremor after polyneuropathy. The cause did not have to be permanent and was not related to the severity of the findings.

With this study, myoclonus with configuration similar to the cortico-subcortical origin was shown for the first time in the polyneuropathies. There is no significant correlation between the demographic characteristics, duration of disease, diagnosis, polyneuropathy subtype, and electrophysiological features of patients with myoclonus. In the literature, myoclonus originating from peripheral nerves has been reported, but its mechanism is not as clear as those of central origin. Savrun et al. reported a case who developed spinal myoclonus after peripheral nerve injury.[20] After GBS, propriospinal myoclonus has been reported and has been linked to peripheral changes affecting the central generator.[21] Myoclonus, accompanying polyneuropathy, has been reported in two patients diagnosed with CIDP in 63 series of diseases with myoclonus over 60 years of age.[22] A CIDP patient with NF-155 antibody has also been reported to have 5 Hz action and rest tremor with myoclonic discharges that are thought to have subcortical origin confirmed by polymyography.[19] However, myoclonus in this report could not be directly attributed to polyneuropathy because this case also used sodium valproate and venlafaxine due to bipolar disorder.

Morphologically, the myoclonus in our cohort was similar to cortical/cortico-subcortical myoclonus that has been defined by Caviness.[23] The duration of myoclonus was short, and its amplitude was high. There was no C reflex. We did not consider somatosensory-evoked potentials because of the involvement of the sensory nerve action potentials. Electroencephalography and backward averaging was not performed in patients, but central pathologies suggesting cortical hyperexcitability were excluded in patients with myoclonus in the clinical evaluation. Myoclonus was closely associated with rest tremor suggesting a common mechanism with rest tremor. Most patients had poliminimyoclonus, which has been previously described in Hirayama disease.[24] In this report, no evidence of the origin of the poliminimyoclonus was presented, only the relationship with fasciculations was given. In a recent study, fasciculations affecting large muscle fibers have been shown to mimic myoclonus in four cases with amyotrophic lateral sclerosis.[25] Thus, myoclonus in our cohort may be attributed to the spontaneous discharges. However, we observed patients with myoclonus with otherwise completely normal neurological examination, conduction studies and MUP findings. Thus, we suggest that myoclonus may be another unique feature in polyneuropathies.

Besides the above-mentioned limitations, one last limitation was the lack of genetic analysis in some patients with a family history of polyneuropathy. We included these patients in the study because the personal history, family history, and electrophysiological findings were compatible with the hereditary neuropathies.


  Conclusion Top


Tremor and myoclonus in polyneuropathies are quite common. The fact that myoclonus was detected in the majority of patients only by multichannel surface EMG who were clinically evaluated as pure tremor suggests that a more detailed electrophysiological evaluation is required. The characteristics of tremor and myoclonus are similar in hereditary and immune-mediated neuropathies.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

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Shibasaki H, Hallett M. Electrophysiological studies of myoclonus. Muscle Nerve 2005;31:157-74.  Back to cited text no. 13
    
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Salazar G, Valls-Solé J, Martí MJ, Chang H, Tolosa ES. Postural and action myoclonus in patients with parkinsonian type multiple system atrophy. Mov Disord 2000;15:77-83.  Back to cited text no. 15
    
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Querol L, Nogales-Gadea G, Rojas-Garcia R, Diaz-Manera J, Pardo J, Ortega-Moreno A, et al. Neurofascin IgG4 antibodies in CIDP associate with disabling tremor and poor response to IVIg. Neurology 2014;82:879-86.  Back to cited text no. 16
    
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Mathey EK, Derfuss T, Storch MK, Williams KR, Hales K, Woolley DR, et al. Neurofascin as a novel target for autoantibody-mediated axonal injury. J Exp Med 2007;204:2363-72.  Back to cited text no. 17
    
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Bailly L, Mongin M, Delorme C, Apartis E, Saheb S, Viala K, et al. Tremor associated with chronic inflammatory demyelinating polyneuropathy and anti-neurofascin-155 antibodies. Tremor Other Hyperkinet Mov (N Y) 2018;8:606.  Back to cited text no. 19
    
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