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 Table of Contents  
ORIGINAL ARTICLE
Year : 2020  |  Volume : 37  |  Issue : 2  |  Page : 50-56

Electrodiagnostic patterns of demyelination and hughes functional grading in typical chronic inflammatory demyelinating polyneuropathy


1 Neurophysiology Unit, Baghdad Teaching Hospital, Medical City, Baghdad, Iraq
2 Department of Physiology, College of Medicine, Al-Nahrain University, Baghdad, Iraq

Date of Submission20-Jul-2019
Date of Decision20-Feb-2020
Date of Acceptance26-Mar-2020
Date of Web Publication29-Jun-2020

Correspondence Address:
Farqad Bader Hamdan
Department of Physiology, College of Medicine, Al-Nahrain University, Baghdad
Iraq
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/NSN.NSN_8_20

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  Abstract 


Background: Chronic inflammatory demyelinating polyneuropathy (CIDP) is characterized by progressive or relapsing motor or sensory symptoms, with variants differing in the relative distribution of these symptoms and electrophysiologic findings. We aimed to correlate the electrodiagnostic patterns of demyelination using Hughes Functional Grading Scale in patients with CIDP. Methods: A case–control study was conducted at the neurophysiology department of Al-Imamian Al-Kadhymian Medical city and Nursing Home Hospital, Medical City, Baghdad from December 2017 to June 2018. Fifteen patients with CIDP aged 30–60 years with disease duration between 6 months and 2 years and 20 age-matched healthy subjects (control group) were included in the study. The participants were submitted to medical history, clinical neurological examination, and electrophysiologic tests. Results: Patients with CIDP demonstrated prolonged distal sensory and motor latencies, decreased sensory nerve action potential amplitude, slowing of sensory and motor nerve conduction velocity, and prolonged mean F-wave latency. The majority showed absent sural sensory responses. Significant relationships were demonstrated between the Hughes Functional Grading Scale and different neurophysiologic parameters, and no correlation was found with the terminal latency index. Conclusions: Patients with high Hughes functional scoring also have severe abnormalities in motor parameters, usually in the range of demyelination. The involvement of nerve segments was multifocal affecting mostly the proximal and intermediate nerve segments; the terminal segments were involved to a lesser extent.

Keywords: CIDP, Hughes Functional Grading Scale, terminal latency index


How to cite this article:
Towman FH, Hamdan FB. Electrodiagnostic patterns of demyelination and hughes functional grading in typical chronic inflammatory demyelinating polyneuropathy. Neurol Sci Neurophysiol 2020;37:50-6

How to cite this URL:
Towman FH, Hamdan FB. Electrodiagnostic patterns of demyelination and hughes functional grading in typical chronic inflammatory demyelinating polyneuropathy. Neurol Sci Neurophysiol [serial online] 2020 [cited 2020 Sep 25];37:50-6. Available from: http://www.nsnjournal.org/text.asp?2020/37/2/50/288422




  Introduction Top


Chronic inflammatory demyelinating polyneuropathy (CIDP) is an acquired peripheral neuropathy that demonstrates progressive course and evolves slowly with gradual worsening over months (at least >2 months), with relapsing symptoms.[1]

Clinically, CIDP presentation ranges from pure sensory deficits to severe tetraparesis with distal or proximal weakness, autonomic with bilateral symmetrical or multifocal involvement, and autonomic dysfunction.[2]

The typical neurophysiologic hallmark CIDP features are prolonged distal latencies, reduced sensory and motor nerve conduction velocities (CVs), and conduction block (CB).[3] An electrophysiologic examination can provide important information about the distribution of demyelinating lesions. In accordance with the neurophysiologic criteria for demyelination,[4] patients with CIDP were sorted as having “distal,” “intermediate,” or “diffuse” demyelination when conduction abnormalities were present in distal nerve segments (distal to the wrist) or intermediate nerve segments (wrist to elbow) or both.[5]

The patients were classified as having “distal” demyelination when distal latencies were >125% of the upper limit of normal or as having “intermediate” demyelination when CVs were <80% of lower limits of normal [6] or there was CB (and/or) abnormal temporal dispersion.[7]

The extremely prolonged distal latencies are in harmony with the smaller terminal latency index (TLI) and the existence of an abnormal median-normal sural sensory pattern or abnormal radial-normal sural, all of which imply another findings of demyelination, especially in the distal nerve terminals.[8]

The study aims to correlate the electrodiagnostic patterns of demyelination with Hughes Functional Grading Scale in patients with CIDP.


  Methods Top


This was a case–control study conducted at the neurophysiology department of Al-Imamian Al-Kadhymian Medical city and Nursing Home Hospital, Medical City, Baghdad from December 2016 to June 2017. Written informed consent was obtained from all individual participants included in the study.

Subjects

Fifteen patients with CIDP of either sex (11 males and 4 females) who were diagnosed by a senior neurologist when they met the clinical and electrodiagnostic criteria for definite CIDP, as defined by the European Federation of Neurological Societies/Peripheral Nerve Society,[7],[9] were included in the study group.

Their mean age was 48.6 ± 14.99 (range: 30–60) years. The disease duration was between 6 months and 2 years. Another 20 (10 males and 10 females) healthy and symptom-free age-matched (49.5 ± 7.8 years) subjects comprised the control group.

Patients with acute progressive symptoms of <1 month, CIDP variants, and other illnesses that might cause neuropathy such as diabetes mellitus or malignancy and those with evidence of median nerve entrapment or cervical radiculopathy determined in nerve conduction studies or cervical spine imaging were excluded from the study.

Clinical functional grading

The clinical disease course was assessed using the Hughes score (F-score) where upper and lower limbs are evaluated separately [10] in a range from 0 to 6. The scale was scored as follows: 0 – normal; 1 – able to run with minimal symptoms and signs; 2 – able to walk 5 m independently; 3 – able to walk 5 m with aids; 4 – chair or bedbound; 5 – requiring assisted ventilation; and 6 – dead.

The Medical Research Council [11] sum scores for grading muscle strength (power) was assessed for the following muscle pairs: upper arm abductors, elbow flexors, wrist extensors, hip flexors, knee extensors, and foot dorsal flexors. It was measured as follows: 0 = no movement, 1 = flicker, 2 = moves with gravity eliminated, 3 = moves against gravity but not resistance, −4 = slight movement against resistance, 4 = moderate movement against resistance, +4 = submaximal movement against resistance, and 5 = normal power.

Deep tendon reflexes were graded as follows: 0: absent, ±: present only with reinforcement, +1: present but depressed, +2: normal, +3: increase, and +4: clonus.[12]

Electrodiagnostic tests

A KeyPoint (Natus Medical Incorporated, San Carlos, CA, USA) electromyography machine was used to study the nerve conduction studies.

All subjects were checked for skin temperature using a special skin thermometer, which was maintained at around 34°C. Whenever it was needed, an infrared lamp was used to ensure the proper skin temperature.

The same evaluator assessed the peroneal, tibial, ulnar, and median motor nerves and the sural, median, and ulnar sensory nerves, bilaterally. The nerve CVs, compound muscle action potentials (CMAPs), sensory nerve action potentials (SNAPs), distal sensory latency (DSL), and distal motor latencies (DMLs), in addition F-responses were recorded after distal stimulation either in the wrist or ankle by supramaximal stimulation (the shortest F-wave latency of at least ten consecutive F-responses) using conventional procedures.[13]

TLI is an electrophysiologic parameter used to identify abnormalities in the distal segment of the motor nerve [14] by comparing the distal segment (distal to the wrist or distal to the ankle) with the intermediate segment (wrist to the elbow or ankle to the fibular head). It was calculated using the following formula: distal conduction distance (mm)/forearm (leg) CV (m/s)/distal latency (ms).[15] Distal conduction distance was measured from the recording electrode over the muscle to the site of stimulation.

CB was defined as at least a 20% decrement in the amplitude of the proximal negative peak CMAP relative to distal.[9] Temporal dispersion was described as a more than 15% increment in the CMAP duration after proximal stimulation compared with distal stimulation.

The involvement of the proximal nerve segment was represented by F-wave latency, intermediate segment by CV and/or CB, the distal segment by DML, and terminal nerve segment by TLI.

Statistical analysis

Microsoft excel 2016 (Microsoft corporation, USA) and IBM SPSS (statistical package for social sciences) version 23 (IBM incorporation, USA) were used. Continuous data were presented as mean ± standard deviation and comparisons between means of study groups were performed using an unpaired Student's t-test. Non-continuous data were presented as frequency and percentage. A comparison between frequencies of the study groups was made using Fisher's exact test. Spearman correlation analysis was performed between grading and different parameters of each nerve. P value of less than 0.5 was considered statistically significant.


  Results Top


CIDP profile

In [Table 1], 14 (93.3%) of the total 15 patients presented with pain and paresthesia in the lower limbs. Six (42.86%) of the 14 patients also had pain and paresthesia in the upper limbs. Furthermore, only one (6.7%) patient had no symptoms of pain and paresthesia in the upper and lower limbs. Only 2 (13.3%) of the total patient group presented with dysarthria and dysphagia. All patients (100%) presented with sensory deficits in the lower limbs and 14 (93.3%) presented with a sensory deficit in the upper limbs.
Table 1: Profiles of patients with chronic inflammatory demyelinating polyneuropathy

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Considering the examination of tendon reflexes, knee tendon hyporeflexia was presented in 8 (53.3%) patients, whereas areflexia was present in 7 (46.7%) patients. Similarly, 13 (86.3%) patients presented with ankle tendon hyporeflexia versus only 2 (13.7%) with areflexia.

For the upper limb, biceps tendon areflexia was found in 14 (93.3%) patients, whereas only 1 (6.7%) patient presented with hyporeflexia. Thirteen (86.3%) patients presented with wrist tendon hyporeflexia, while the rest 2 patients (13.7%) presented with distal areflexia.

The muscle strength (power) was of grade +3 in 2 (13.3%) versus 13 (86.7%) of the distal and proximal muscles of the lower limb. In the distal muscles of the upper limb, muscle strength grade −4 was noticed in 3 (20%) patients, grade +3 in 2 (13.3%), and +4 in 10 (66.7%) patients. Moreover, in the proximal muscles of the upper limb, muscle strength was grade +3 in 2 (13.3%) and +4 in 13 (86.7%) of the total patient group.

The functional assessment of the patients using the Hughes Functional Grading Scale showed that only one patient (6.7%) presented as Grade 1, eight (53.3%) patients were Grade 2, four patients (26.7%) were Grade 3, and two patients (13.3%) were Grade 4.

Electrophysiologic data

[Table 2] shows prolonged DSL, reduced SNAP amplitude, and slowed sensory conduction velocity (SCV) (P < 0.001) of both the median and ulnar nerves in patients with CIDP as compared with the control group. Likewise, sural DSL was prolonged (P = 0.04), the SCV was slowed (P < 0.001), and SNAP amplitude was insignificantly reduced (P = 0.168) in patients with CIDP as compared with the controls.
Table 2: Electrophysiology in patients with chronic inflammatory demyelinating polyneuropathy and controls (unpaired t-test)

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Concerning the data of motor nerves, the DML of all tested nerves was prolonged (P < 0.001); the motor conduction velocity (MCV) and the distal and proximal CMAP amplitudes of all tested nerves were reduced (P < 0.001) in patients with CIDP in comparison with those of the control group.

The TLI of patients with CIDP was reduced as compared to that of the control group in the median and peroneal nerves (P < 0.001, respectively).

The median, ulnar, and sural sensory responses were absent in 17 (56.7%), 16 (53.3%), and 24 (80%), respectively, out of the total 30 nerves tested for the right and left upper and lower limbs.

Depending on the cutoff values for the abnormality of F-wave latency, which is ≥32 ms for the median nerve and ≥56 ms for the tibial nerve, 30 (100%) F-wave responses of the tibial nerve were abnormal and 26 (92.9%) of the 28 F-wave responses were abnormal for the median nerves.

The percentage of CB “depending on the cutoff value of ≥20%” was 100% (24) common peroneal nerves, 26 (92.9%) of the 28 tibial nerves; 29 (96.7%) of the 30 median nerves, and 25 (89.3%) of the total 28 ulnar nerves [Table 3].
Table 3: Percentage of nerves showing conduction abnormalities indicative of demyelination in chronic inflammatory demyelinating polyneuropathy

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According to the cutoff values for the frequency of involvement of the different segments of nerves tested in the patients with CIDP, the proximal segment was involved in 30 (100%), the intermediate segment in 29 (96.7%), the distal segment in 28 (93.3%), the CV in 26 (86.7%), and the terminal segments in 24 (80%) of the total 30 median nerves tested. Of the 28 tested ulnar nerves, the intermediate segments were involved in 26 (92.7%), the CV in 26 (92.7%), and the distal segment in 24 (85.9%).

Regarding the 24 peroneal nerves tested, the intermediate segments and the CV were involved in 24 (100%, respectively), the distal segment in 23 (95.7%), and the terminal segment in 22 (91.8%). Furthermore, the proximal segment and the CV were involved in 27 (96.9%, respectively), and the intermediate segments and CV in 26 (96.4%, respectively) of the 28 tibial nerves tested [Table 4].
Table 4: Frequency of nerve segment involvement in chronic inflammatory demyelinating polyneuropathy

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[Figure 1] (upper left) illustrates positive relationship between Hughes Functional Grading Scale and the DML of common peroneal (r = 0.814; P < 0.001), tibial nerve (r = 0.709; P < 0.001), ulnar nerve (r = 0.658; P < 0.001), and the median nerve (r = 0.615; P < 0.001).
Figure 1: Hughes Functional Grading Scale in relation to distal motor latency (upper left), motor conduction velocity (upper right), conduction block % (lower left); and an abnormality of F-wave latency (lower right) in patients with CIDP

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On the contrary, a negative correlation was found between Hughes Functional Grading Scale and CV of the tibial (r = −0.805; P < 0.001), common peroneal (r = −0.655; P < 0.001), median nerve (r = −0.561; P < 0.001), and ulnar nerve (r = −0.519; P < 0.005) [Figure 1] upper right].

The Hughes Functional Grading Scale showed a positive correlation with CB in the median nerve (r = 0.506; P = 0.004), ulnar nerve (r = 0.497; P = 0.007), tibial nerve (r = 0.465, P = 0.013), and common peroneal nerve (r = 0.436, P = 0.033) [Figure 1] lower left].

Moreover, [Figure 1] (lower right) demonstrates the positive relationship between Hughes Functional Grading Scale and the abnormality of F-wave latency in the tibial nerve (r = 0.337; P = 0.048) and median nerve (r = 0.376; P = 0.041). Furthermore, no significant relationship was demonstrated between Hughes Functional Grading Scale and the TLI of the median nerve (r = −0.068; P = 0.71) and peroneal nerve (r = −0.200; P = 0.3).


  Discussion Top


The electrodiagnostic abnormalities shown in our study followed the definition of CIDP. We thus featured the electrophysiologic criteria of demyelination:[3],[6],[15],[16],[17] first for motor nerves with prolonged DML, decreased CV and CB, and prolonged F-wave latency, and second for sensory nerves with decreased CV. Our cohort also demonstrated reduced amplitude of the motor and/or sensory responses, which denotes temporal dispersion or axonal degeneration secondary to demyelination.[16],[18]

Our study showed that the sural SNAP amplitude was not significantly different between patients with CIDP and controls. This finding agrees with the 2010 EFNS guidelines, which endorse normal sural with abnormal median or radial SNAP pattern as helpful arguments for the characteristic features of demyelination,[9] and in agreement with study of Kuwabara et al.,[8] which denotes that in sensory nerve conduction studies, the abnormal median-normal sural sensory responses were significantly more frequent in typical CIDP.

The frequency of absent sural responses in patients with CIDP [Table 3] was in harmony with the observation of Rajabally et al.[19] but contrary to the results of Kuwabara et al.[8] which could be due their patients presenting with mild-to-moderate demyelination with a mild degree of secondary axonal degeneration.

In this study, CB was quite common in 89.3%–100% of the patients depending on the nerve studied, though the definition used was a reduction of at least 20% in proximal motor amplitude compared with distal motor amplitude, with a duration increase of no more than 15%.[9] The certainty of the CB normally depends on the extent of temporal dispersion;[6],[7] thus, CB may be overestimated due to the small number size because of the high sensitivity of the CB definition used, necessitating a >20% to 60% decrement in amplitude or area for proximal CMAP relative to distal CMAP.

During the initial phase of the disease, electrodiagnostic demyelinating alterations might primarily involve the distal nerve terminals where the blood–nerve barrier is most vulnerable.[5] Nevertheless, with disease progression in individuals with typical CIDP, a continuing disruption of the blood–nerve barrier in the nerve trunk occurs and the demyelination also affects the intermediate nerve trunk. This event signifies an intense NC slowing and CB and/or abnormal temporal dispersion in the intermediate nerve segments, as detected on motor nerve conduction studies.[7]

In addition to a prolonged DML, we demonstrated shorter TLI,[5],[8] both of which denote motor nerve demyelination [14] and also propose that demyelination affects the distal nerve terminals preferentially.

A prolonged DML to a greater extent than that suggested by the MCV which reflects the most proximal segment of the limb could explain the shorter TLI. Low TLI confirms the presence of a distal and length-dependent demyelinating neuropathy in CIDP.[8] TLI thus could be used to confirm the electrophysiologic classification of demyelination. In our cohort, significantly shorter TLI (0.15 ± 0.005) was demonstrated in CIDP with a distal pattern of demyelination when compared with those with intermediate (0.41 ± 0.07), diffuse pattern (0.27 ± 0.12), and also with normal subjects (0.35 ± 0.05).

The proximal segment (represented by F-wave) of the lower limb was involved in 100% versus 92.9% of the upper limb in this study. Kuwabara et al.[8] also reported such an observation. Owing to the lack of a well-formed perineurium, the permeability of the spinal root blood–nerve barrier increased, making the proximal nerve segments more vulnerable to demyelination.[20],[21]

According to [Table 3], the majority of patients with CIDP tend to show dominant electrophysiologic motor changes. This is because of the lower motor axon excitability than that of sensory axons bringing about ready development of a nerve CB. Further, there is considerable anatomic and physiologic diversity in peripheral motor and sensory axons where motor axons have branching near the neuromuscular junction. This principally makes motor nerve axons more susceptible to CB by the process of demyelination.[5]

Our study showed that Hughes scoring correlated well with the electrophysiologic parameters of demyelination (prolonged DML, MCV slowing, CB%, and F-wave abnormality), which indicates several patterns of distribution of demyelinating lesions. High-scoring patients usually present with severe abnormalities in motor parameters, typically in the range of demyelination. Kuwabara et al. correlated all types of CIDP (typical and atypical form) with the degree of demyelination and demonstrated that there was multifocal demyelination that could involve the distal nerve terminals, intermediate nerve segments, and nerve roots, and there was a significant association between the Hughes clinical grading and the type of demyelination.[8],[22]

Furthermore, the absent correlation of Hughes scoring with TLI could be explained by the fact that thick myelinated fibers are more liable to be affected by CIDP than thinly myelinated fibers.[23] In segmental demyelination, the process of impulse conduction along the nerve is transformed from saltatory conduction to a continuous smooth type of conduction similar to that in type C fibers. Hence, the terminal segment may be particularly less susceptible because of its distance from the cell body.[24]

To the best of our knowledge, no comparable data are present considering the relationship between Hughes Clinical Grading Scale and degree of demyelination depending on individual electrophysiologic parameters in typical CIDP.


  Conclusions Top


The present findings suggest that the degree of demyelination in patients with typical CIDP is highly correlated with Hughes Functional Grading Scale. Our data imply that multifocal distribution of demyelination lesions along nerve segments mostly affects the proximal and intermediate segments. Moreover, Hughes scoring correlated well with the degree of demyelination in the distal segment, followed by the intermediate segment.

Acknowledgment

We thank Professor Dr. Akram Al-Mahdawi (Iraqi Committee of Medical Specialization) for clinically evaluating the patients. Our thanks extend to Dr. Majid Hameed (College of Medicine, Al-Nahrain University) for doing the statistical analysis.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
Dyck PJB, Tracy JA. History, diagnosis, and management of chronic inflammatory demyelinating polyradiculoneuropathy. Mayo Clin Proc 2018;93:777-93.  Back to cited text no. 1
    
2.
Ellrichmann G, Gold R, Ayzenberg I, Yoon MS, Schneider-Gold C. Two years' long-term follow up in chronic inflammatory demyelinating polyradiculoneuropathy: Efficacy of intravenous immunoglobulin treatment. Ther Adv Neurol Disord 2017;10:91-101.  Back to cited text no. 2
    
3.
Dimachkie MM, Barohn RJ. Chronic inflammatory demyelinating polyneuropathy. Curr Treat Options Neurol 2013;15:350-66.  Back to cited text no. 3
    
4.
Bromberg MB. Review of the evolution of electrodiagnostic criteria for chronic inflammatory demyelinating polyradicoloneuropathy. Muscle Nerve 2011;43:780-94.  Back to cited text no. 4
    
5.
Kuwabara S, Misawa S. Chronic inflammatory demyelinating polyneuropathy: Clinical subtypes and their correlation with electrophysiology. Clin Exp Neuroimmunol 2011;2:41-8.  Back to cited text no. 5
    
6.
Fuglsang-Frederiksen A, Pugdahl K. Current status on electrodiagnostic standards and guidelines in neuromuscular disorders. Clin Neurophysiol 2011;122:440-55.  Back to cited text no. 6
    
7.
Joint Task Force of the EFNS and the PNS. European Federation of Neurological Societies/Peripheral Nerve Society guideline on management of multifocal motor neuropathy. Report of a joint task force of the European Federation of Neurological Societies and the Peripheral Nerve Society – First revision. J Peripher Nerv Syst 2010;15:295-301.  Back to cited text no. 7
    
8.
Kuwabara S, Ogawara K, Misawa S, Mori M, Hattori T. Distribution patterns of demyelination correlate with clinical profiles in chronic inflammatory demyelinating polyneuropathy. J Neurol Neurosurg Psychiatry 2002;72:37-42.  Back to cited text no. 8
    
9.
Van den Bergh PY, Hadden RD, Bouche P, Cornblathd DR, Hahne A, Illa I, et al. European Federation of neurological societies/peripheral nerve society guideline on management of chronic inflammatory demyelinating polyradiculoneuropathy: Report of a joint task force of the European Federation of Neurological Societies and the Peripheral Nerve Society – First revision. Eur J Neurol 2010;17:356-63.  Back to cited text no. 9
    
10.
Sung JY, Tani J, Park SB, Kiernan MC, Lin CS. Early identification of 'acute-onset' chronic inflammatory demyelinating polyneuropathy. Brain 2014;137:2155-63.  Back to cited text no. 10
    
11.
Vanhoutte EK, Faber CG, van Nes SI, Jacobs BC, van Doorn PA, van Koningsveld R, et al. Modifying the Medical Research Council grading system through Rasch analyses. Brain 2012;135:1639-49.  Back to cited text no. 11
    
12.
Hadjiu S, Revenco N, Călcîi C, Lupuşor N. Acute inflammatory demyelinating polyneuropathy in children. J Romanian Child Adolesc Neurol Psychiat 2014;17:61-73.  Back to cited text no. 12
    
13.
Preston DC, Shapiro BE. Detailed nerve conduction studies. Routine upper extremity, facial, and phrenic and lower extremity nerve conduction techniques. In: Electromyography and Neuromuscular Disorders: Clinical–Electrophysiologic Correlations. 3rd ed., Ch. 10 and 11. Sec. 4 and 6. Philadelphia: Elsevier Saunders; 2013. p. 97-100, 115,116, 119.  Back to cited text no. 13
    
14.
Vahdatpour B, Khosrawi S, Chatraei M. The role of median nerve terminal latency index in the diagnosis of carpal tunnel syndrome in comparison with other electrodiagnostic parameters. Adv Biomed Res 2016;5:110.  Back to cited text no. 14
    
15.
Kuwabara S, Isose S, Mori M, Mitsuma S, Sawai S, Beppu M, et al. Different electrophysiological profiles and treatment response in 'typical' and 'atypical' chronic inflammatory demyelinating polyneuropathy. J Neurol Neurosurg Psychiatry 2015;86:1054-9.  Back to cited text no. 15
    
16.
Rajabally YA, Samarasekera S. Electrophysiological sensory demyelination in typical chronic inflammatory demyelinating polyneuropathy. Eur J Neurol 2010;17:939-44.  Back to cited text no. 16
    
17.
Taioli F, Cabrini I, Cavallaro T, Acler M, Fabrizi GM. Inherited demyelinating neuropathies with micromutations of peripheral myelin protein 22 gene. Brain 2011;134:608-17.  Back to cited text no. 17
    
18.
Chung T, Prasad K, Lloyd TE. Peripheral neuropathy: Clinical and electrophysiological considerations. Neuroimaging Clin N Am 2014;24:49-65.  Back to cited text no. 18
    
19.
Rajabally YA, Simpson BS, Beri S, Bankart J, Gosalakkal JA. Epidemiologic variability of chronic inflammatory demyelinating polyneuropathy with different diagnostic criteria: Study of a UK population. Muscle Nerve 2009;39:432-8.  Back to cited text no. 19
    
20.
Shimizu F, Sawai S, Sano Y, Beppu M, Misawa S, Nishihara H, et al. Severity and patterns of blood-nerve barrier breakdown in patients with chronic inflammatory demyelinating polyradiculoneuropathy: Correlations with clinical subtypes. PLoS One 2014;9:e104205.  Back to cited text no. 20
    
21.
Shimizu F, Kanda T. Breakdown of blood-nerve barrier in immune-mediated neuropathy. Clin Exp Neuroimmunol 2015;6:139-48.  Back to cited text no. 21
    
22.
Alabdali M, Abraham A, Alsulaiman A, Breiner A, Barnett C, Katzberg HD, et al. Clinical characteristics, and impairment and disability scale scores for different CIDP Disease Activity Status classes. J Neurol Sci 2017;372:223-7.  Back to cited text no. 22
    
23.
Cocito D, Isoardo G, Ciaramitaro P, Migliaretti G, Pipieri A, Barbero P, et al. Terminal latency index in polyneuropathy with IgM paraproteinemia and anti-MAG antibody. Muscle Nerve 2001;24:1278-82.  Back to cited text no. 23
    
24.
Hamada MS, Popovic MA, Kole MH. Loss of saltation and presynaptic action potential failure in demyelinated axons. Front Cell Neurosci 2017;11:45.  Back to cited text no. 24
    


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    Tables

  [Table 1], [Table 2], [Table 3], [Table 4]



 

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