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Abstract

We sought to investigate electromyographic characteristics of Guillain-Barré syndrome (GBS) patients in the recovery phase by using serial electromyography (EMG). We included seven GBS patients and assessed their neurologic function at admission and 2, 3 and 6 months post onset using Hughes Functional Grading Scale scores. All patients underwent serial electromyographic assessment of compound muscle action potentials (CMAPs), mean conduction velocity (MCV), and distal motor latency (DML) of peripheral nerves. F wave was recorded of the median nerve and ulnar nerve. All seven patients had a Hughes Functional Grading Scale score between 3 and 6 at admission, while three patients at 2 months, one patient at 3 months, and no patient at 6 months post GBS onset had a Hughes Functional Grading Scale score between 3 and 6 (P < 0.05). No F wave was elicited in 41.7% (20/48) of the motor nerves examined at admission, which declined to 25% at 6 months post GBS onset. Decreased amplitude in CMAPs was seen in 50% (24/48) of the motor nerves examined at admission, which decreased to 25% at 6 months (P < 0.05). Moreover, 60.4% (29/48) of the motor nerves showed abnormal abduction velocity, which declined to 0% at 3 and 6 months post GBS onset (P < 0.01). In conclusion, GBS patients exhibit a variable course in recovery of electromyographic parameters, and amplitude in CMAPs cannot fully reflect recovery of muscle tone. Conduction block is reversible and in line with rapid muscle tone recovery.

Keywords

compound muscle action potentials conduction velocity electromyography F wave Guillain-Barré syndrome

Introduction

Guillain-Barré syndrome (GBS) is an acute immune mediated inflammatory peripheral neuropathy. The global annual incidence of GBS is reportedly 0.6–2.4 cases per 100,000 per year¹ and the incidence of GBS in China has recently been reported to be 0.59 cases per 100,000 person years.² Acute inflammatory demyelinating polyneuropathy (AIDP) occurs most commonly in Caucasians,³ while in China acute motor axonopathy and acute motor sensory axonopathy are more common.

Clinical manifestations of GBS are consequent of multiple nerve root and peripheral nerve injuries and most patients with GBS present with progressively flaccid, symmetric and ascending weakness of extremities. Pathologically, AIDP is characterized by demyelination of peripheral nerve and nerve roots and infiltration of macrophages. In some patients, apart from segmental demyelination, axonal degeneration is also present.

Electrophysiological examination is of significance for diagnosis, categorization, and prognosis determination of GBS.^4,5 Patients with early GBS often have conduction block or dispersion of the responses at sites of natural nerve compression such as the carpal tunnel. Electrophysiological changes during gradual recovery of muscle tone, however, are seldom known. In this study, we followed up the electrophysiological features of six GBS cases and investigated changes in compound muscle action potential (CMAP) and their relation with muscle tone recovery.

Patients and methods

Patients

We studied seven patients with GBS who were treated at our hospital between January 2008 and October 2015. GBS was diagnosed according to the diagnostic criteria from the National Institute of Neurological Disorders and Stroke (NINDS) from 1990.⁶ The records of the patients were anonymized and deidentified before analysis. The study protocol was approved by the local institutional review board at the authors’ affiliated institution and patient consent was not required because of the retrospective nature of the study.

Evaluation of neurological function

Neurologic function was assessed using Hughes Functional Grading Scale scores at admission and 2, 3, and 6 months post onset. The scale has a score range of 0–6 (0, asymptomatic; 1, mild signs or symptoms but able to run; 2, able to walk unaided for 5 m; 3, able to walk 5 m with support; 4, bed-ridden or wheel-chair bound; 5, requiring ventilatory assistance; and 6, death^7,8). History of antecedent illness in the form of upper respiratory tract infection, diarrhea, and other viral illnesses was documented.

Electromyographic assessment

All patients gave consent to and underwent electromyographic assessment with a Keypoint evoked muscle potential equipment at admission and 2, 3, and 6 months post disease onset. Concentric needle electrodes were used to record abnormally evoked resting potential at the abductor pollicis brevis, abductor digiti minimi, vastus medialis, and tibialis anterior muscle. Motor unit action potential was recorded during mild contraction, and cluster type of motor unit action potential was recorded during intense contraction. Motor nerve conduction study was done by stimulating the median nerve, ulnar nerve, the common peroneal nerve, and the motor branch of the tibial nerve to assess CMAPs including onset latency, amplitude, and conduction velocity. Surface electrodes were used to record the mean conduction velocity (MCV) and distal motor latency (DML) of the median nerve, ulnar nerve, common peroneal nerve, and the motor branch of the tibial nerve. Amplitude was measured in negative peak value. Sensory nerves examined included the median nerve, ulnar nerve, and sural nerve. Sensory conduction velocity was recorded, and sensory nerve action potential (SNAP) amplitude was measured in negative wave value. F wave was recorded of the median nerve and ulnar nerve. Frequency was recorded. Patient’s skin temperature was kept 32°C–35°C with an ambient temperature of 24°C–28°C.

Statistical analysis

Data were analyzed using SPSS18.0 (SPSS Inc., Chicago, IL, USA). Hughes Functional Grading Scale scores were compared using paired Student’s t-test. Motor nerve data were examined by chi-square test. P < 0.05 was considered statistically significant.

Results

Demographic and baseline characteristics of the study subjects

The demographic and baseline characteristics of the study subjects are shown in Table 1. They included three females and four males with a median age of 34 (range 28–65) years. The median duration from onset to initial examination was 18 (range 10–25) days. All patients had preceding respiratory (6/7) or gastrointestinal infections (1/7). Axonal degeneration was seen in six out of seven patients, while demyelinating lesion was observed in one out of seven patients.

Table 1.

Demographic and clinical characteristics of the study subjects.

Characteristics	Values (n = 7)
Age (years), median (range)	34 (28–65)
Onset time (months), median (range)	20 (15–25)
Male, n (%)	4 (57.1)
Upper respiratory tract infection, n (%)	1 (14.3)
Acute gastroenteritis, n (%)	6 (85.7)
Autonomic dysfunction, n (%)	2 (33.3)
Cranial nerve involvement, n (%)	2 (28.6)
Facial palsy, n (%)	1 (14.3)
Bulbar involvement, n (%)	2 (28.6)
Neck flexor weakness, n (%)	5 (71.4)
Ventilatory support, n (%)	0 (0.0)
Electromyography, n (%)
Primary demyelinating	1 (14.3)
Axonal	6 (85.7)
Hughes Functional Grading Scale scores at admission, n (%)
0–2	0 (0.0)
3–4	7 (100.0)
Outcome, n (%)
Complete recovery	3 (42.9)
Incomplete recovery	4 (57.1)

Hughes Functional Grading Scale scores

All seven patients had a Hughes Functional Grading Scale score of 3 (1/7) or 4(6/7) at admission. Changes in Hughes Functional Grading Scale scores are shown in Figure 1 and Table 2. A significant difference was observed in Hughes Functional Grading Scale score at admission and 2, 3 and 6 months post GBS onset (P < 0.05).

Figure 1.

Hughes Functional Grading Scale scores of the study patients.

Table 2.

Hughes Functional Grading Scale scores of the study patients (n = 7).

Hughes scores	Time				P
Hughes scores	At admission	2 months	3 months	6 months
Mean ± SD	3.86 ± 0.35	2.14 ± 0.99^a	1.57 ± 0.90^a	0.57 ± 0.73^a	<0.001
Range	3–4	0–3	0–3	0–2

Compared with time at admission P < 0.05.

Electromyographic characteristics of the study subjects

Electromyographic studies showed that no wave was elicited in 41.7% (20/48) of the motor nerves examined at admission (Table 3). At 6 months post GBS onset, no wave was elicited in a minority of the patients (25%, 12/48). Furthermore, decreased amplitude in CMAPs was seen in half (50%, 24/48) of the motor nerves examined at admission. Marked improvement was seen at 3 and 6 months post GBS onset as decreased amplitude was demonstrated only in 25% of the motor nerves (12/48; P < 0.01). Moreover, 60.4% (29/48) of the motor nerves showed reduced MCV. The proportion of motor nerves with abnormal conduction velocity significantly decreased at 2 months post GBS onset (16.7%, 8/48; P < 0.01). No abnormality in conduction velocity was observed at 3 and 6 months post GBS onset (P < 0.01).

Table 3.

The number of electromyographically abnormal motor nerves (n = 48).

Time	No F wave elicited, n (%)	Decreased amplitude, n (%)	Abnormal conduction velocity, n (%)
At admission	20 (41.7)	24 (50.0)	29 (60.4)
2 months	22 (45.8)	25 (52.1)	8 (16.7)^a
3 months	18 (37.5)	12 (25.0)^a	0 (0.0)^a
6 months	12 (25.0)	12 (25.0)^a	0 (0.0)^a

Compared with time at admission P < 0.05.

Discussion

Our current study demonstrated considerable slowing of impulse conduction in a significant proportion of both motor and sensory nerve fibers at the onset of GBS. The amplitudes of CMAPs were also significantly reduced in approximately half of the motor nerves examined at the onset and in early GBS. F wave is absent in early GBS, indicative of proximal conduction block.⁹ We also failed to elicit F wave in about 40% of the nerves examined at the onset and in early GBS and in 25% of the nerves examined at 6 months post GBS onset. Gordon and Wilbourn¹⁰ found abnormal F wave in 84% of patients within the first week of muscle weakness.

Alberti et al.¹¹ detected abnormality in motor nerve conduction in 15/18 GBS patients within 4 days of clinical onset. Gordon and Wilbourn¹⁰ showed reduction in amplitude in CMAPs in 71% of the patients. These studies, however, did not address electromyographic changes in the recovery phase of GBS. While early GBS is dominated by patchy peripheral nerves demyelination, conduction slowing mainly due to re-myelination is observed in the clinical recovery stage of GBS.¹² Our study found that recovery of conduction velocity appeared early, suggesting that demyelinating changes recover early. Noticeably, recovery in reduction in amplitude in CMAPs and failure to elicit F waves lagged behind recovery in conduction velocity, suggesting that different electromyographic parameters exhibit distinct behaviors at each stage of GBS. We saw clinical improvement in our patients 2–4 weeks post onset. Electromyography (EMG) showed improvement in conduction velocity at 2 months, while reduction in amplitude in CMAPs and failure to elicit F waves showed no improvement until 3 months post GBS onset, suggesting slow axonal regeneration¹³ and that electromyographic recovery lags behind clinical recovery.^14,15

In conclusion, GBS patients exhibit a variable course in recovery of electromyographic parameters, and amplitude in CMAPs cannot fully reflect recovery of muscle tone. Conduction block is reversible and in line with rapid muscle tone recovery. However, our sample size is very small; additional electromyographic studies involving a larger patient population with longer follow-up duration are needed to further delineate electromyographic changes in the onset and recovery of GBS.

Footnotes

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

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Serial electromyographic findings in Guillain-Barré syndrome patients