Journal of the Neurological Sciences 351 (2015) 187–190

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Cauda equina conduction time in Guillain-Barré syndrome Hideyuki Matsumoto a,b,⁎, Ritsuko Hanajima b,c, Yasuo Terao b, Hideji Hashida a, Yoshikazu Ugawa d a

Department of Neurology, Japanese Red Cross Medical Center, Tokyo, Japan Department of Neurology, The University of Tokyo, Tokyo, Japan c Department of Neurology, Kitasato University School of Medicine, Kanagawa, Japan d Department of Neurology, School of Medicine, Fukushima Medical University, Fukushima, Japan b

a r t i c l e

i n f o

Article history: Received 23 December 2014 Received in revised form 4 February 2015 Accepted 27 February 2015 Available online 6 March 2015 Keywords: Acute inflammatory demyelinating neuropathy (AIDP) Acute motor axonal neuropathy (AMAN) Magnetic stimulation Motor-evoked potential Spinal nerve Cauda equina

a b s t r a c t The proximal segment of peripheral nerves is assumed to be involved in both demyelinating and axonal types of Guillain-Barré syndrome (GBS). However, electrophysiological examinations have not yet clarified if this segment is involved. We measured cauda equina conduction time (CECT) in nine demyelinating GBS and seven axonal GBS patients. Compound muscle action potentials (CMAPs) were recorded from the abductor hallucis muscle. Electrical stimulation was given at the ankle and the knee, and magnetic stimulation was given over the first sacral (S1) and first lumbar (L1) spinous processes using a magnetic augmented translumbosacral stimulation (MATS) coil. CECT was obtained by subtracting S1-level latency from L1-level latency. CECT was prolonged in all the patients with demyelinating GBS who had leg symptoms, whereas motor conduction velocity (MCV) at the peripheral nerve trunk was normal in all the patients. In all the patients with axonal GBS having leg symptoms, CECT and MCV were normal and no conduction blocks were detected between the ankle and the neuro-foramina. The cauda equina is much more frequently involved than the peripheral nerve trunk in demyelinating GBS. In axonal GBS, usually, CECT is normal and segmental lesions are absent between the ankle and the neuro-foramina. Therefore, the CECT measurement should be very useful for directly detecting demyelinating lesions in GBS. © 2015 Elsevier B.V. All rights reserved.

1. Introduction Guillain-Barré syndrome (GBS) is an acute peripheral neuropathy that usually follows a respiratory or intestinal infection; it reaches its nadir within 4 weeks and then the patients recover over weeks or months [1,2]. Some immune-mediated pathogenesis such as antiganglioside antibodies or some other circulating factors might be involved in the disease process [3,4]. Based on the electrophysiological and pathological findings, GBS is currently classified into demyelinating and axonal forms: demyelinating GBS (acute inflammatory demyelinating polyneuropathy: AIDP) and axonal GBS (acute motor axonal neuropathy: AMAN) [2,3]. In demyelinating GBS, nerve conduction studies (NCSs) more frequently show a prolonged distal latency of compound muscle action potentials (CMAPs) and a conduction block at the common site for entrapment neuropathy compared to the slowing of motor conduction velocity (MCV). The F-wave technique also often shows prolonged latency or unobtainable F-waves [5,6]. In axonal GBS, on the other hand, NCS does not show any severe conduction delays. A conduction block (reversible conduction failure) at the nerve ⁎ Corresponding author at: Department of Neurology, Japanese Red Cross Medical Center 4-1-22 Hiroo, Shibuya-ku, Tokyo 150-8935, Japan. Tel.: + 81 3 3400 1311; fax: +81 3 3409 1604. E-mail address: [email protected] (H. Matsumoto).

http://dx.doi.org/10.1016/j.jns.2015.02.049 0022-510X/© 2015 Elsevier B.V. All rights reserved.

terminal axon or a common site for entrapment neuropathy is observed [7,8]. As the mechanism of a conduction block in axonal GBS, sodiumchannel dysfunction has been postulated. F-waves are also often unobtainable. On the basis of these electrophysiological findings, it is speculated that the sites vulnerable to the lack, destruction, or malfunction of the blood nerve barrier are preferentially involved rather than the peripheral nerve trunk in both types of GBS. As proximal lesions, the conduction block at the spinal nerve roots, including the cauda equina, prolonged refractoriness of the most proximal axon for backfiring, or decreased excitability of spinal motoneurons are assumed to produce F-wave abnormalities [8,9]. The disappearance of F-waves is frequently the sole abnormal finding in both types of GBS [10]. In such cases, we cannot accurately classify GBS into a demyelinating or axonal form. Even when F-waves are elicited, the F-wave technique does not localize the lesion sites in the peripheral nerves. Therefore, electrophysiological examinations have not yet clarified if the cauda equina is involved. We have recently developed a novel magnetic stimulation method to measure cauda equina conduction time (CECT) using a specially devised powerful coil called a magnetic augmented translumbosacral stimulation (MATS) coil [11,12]. This enables us to activate the spinal nerves at both the proximal and distal sites of the cauda equina and to measure cauda equina conduction time (CECT) [13,14], which reflects the nerve conduction within the cauda equina. Furthermore, using the MATS coil, supramaximal stimulation can be achieved at the neuro-

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foramina (the most distal cauda equina), which provides us with information on the presence of a conduction block between the distal site and the neuro-foramina [11,13]. In this study, to investigate the involvement of the proximal segment of the peripheral nerves in GBS, we measured CECT and tried to detect a conduction block at the proximal parts of peripheral nerves in demyelinating and axonal GBS using MATS coil stimulation.

aid, grade 2 = ambulates independently, grade 1 = minimal signs and symptoms, able to run, and grade 0 = normal) [15]. Informed consent to participate in this study was obtained from all subjects. The procedure was approved by the Ethics Committee of the University of Tokyo and the study was conducted in accordance with the ethical standards of the Declaration of Helsinki. 2.2. Stimulation, recording, and analysis

2. Patients and methods 2.1. Subjects We studied 16 GBS patients (12 men and 4 women) whose diagnosis was made according to the established diagnostic criteria [1]. The mean ± standard deviation (SD) age and body height of the patients were 44.1 ± 15.9 (range 27–65) years and 170.0 ± 7.2 (158–183) cm, respectively. These patients were classified into the two types of GBS according to the electrodiagnostic criteria of Hadden et al. [2]: 9 demyelinating GBS and 7 axonal GBS. The 9 demyelinating GBS and 7 axonal GBS also fulfilled the electrodiagnostic criteria of Ho et al. [3]: 9 AIDP and 7 AMAN. In all demyelinating GBS patients, the CMAP distal latency or F-wave latency was prolonged in at least two peripheral nerves. On the other hand, in all axonal GBS patients, the CMAP amplitude was decreased but all latencies were not severely prolonged. Patients in whom reliable CMAPs were not obtained by electrical stimulation were excluded from this study. If patients were not classified into the two types of GBS (equivocal GBS in the electrodiagnostic criteria of Hadden et al. [2] or unclassified GBS in Ho et al. [3]), NCS was repeatedly performed for the classification. The clinical profile of the studied patients is summarized in Table 1. Their disabilities were assessed using the Hughes functional grading scale (grade 6 = dead, grade 5 = requires assisted respiration, grade 4 = bed bound, grade 3 = able to walk 5 m with

During the examination, patients lay comfortably on a bed in the prone position. CMAPs were recorded from the abductor hallucis muscle (AH) on the more affected side. Disposable silver–silver chloride disc electrodes of 9 mm diameter were placed in a belly-tendon montage over AH. Signals were amplified with filters set at 20 Hz and 3 kHz and recorded by a computer (Neuropack MEB-2306; Nihon Kohden Corporation, Tokyo, Japan). The skin temperature was maintained at around 32 °C to 33 °C. For NCS at a distal segment, the posterior tibial nerve was stimulated at the posterior medial malleolus of the ankle and the popliteal fossa using a conventional electrical stimulator (Neuropack MEB-2306; Nihon Kohden Corporation, Tokyo, Japan). MCV was calculated by dividing the ankle–knee length by the latency difference. To measure CECT, magnetic stimulation was performed with a monophasic stimulator, Magstim 2002 (The Magstim Co. Ltd., Whitland, UK) and a MATS coil (diameter 20 cm, 0.98 T; The Magstim Co. Ltd., Whitland, UK) [11,12]. For the most distal cauda equina stimulation at the neuro-foramina, the edge of the MATS coil was positioned over the first sacral (S1) spinous process, which induces eddy currents to flow along the spinal nerves at their exit site from the spinal canal [11,13,14]. Stimulus intensity was gradually increased, and if possible, supramaximal CMAPs were obtained at the most distal cauda equina (neuro-foramina). For the most proximal cauda equina stimulation, the edge of the MATS coil

Table 1 Clinical profile and results of 16 GBS patients. Case

Age

Gender

Experimental date

Hughes scale

MCV (m/s)

CECT (ms)

F-wave persistence (%)

F-wave latency (ms)

Anti-ganglioside antibodies

Muscular weakness

Demyelinating GBS D1 D2 D3

29 54 49

M F F

2 days 2 days 3 days

4 4 4

42 40 49

7.2 ↑ 5.9 ↑ 3.0

ND 100 100

ND 53.1 ↑ 48.3

Diffuse Diffuse Diffuse

D4 D5 D6

65 58 31

M F M

3 days 8 days 13 days

3 1 3

44 45 42

8.6 ↑ 6.2 ↑ 6.5 ↑

100 100 ND

58.9 ↑ 50.0 ND

D7 D8 D9

56 58 37

M M M

14 days 15 days 1 month

4 1 1

40 39 40

5.8 ↑ 6.2 ↑ 5.7 ↑

100 100 100

54.3 ↑ 50.0 55.3 ↑

GD1b-IgG ND GQ1b-IgG GD1b-IgG GT1a-IgG GT1b-IgG ND ND GM1-IgG GM2-IgG GalNAc-GD1a-IgM GD1a-IgG NE NE

Axonal GBS A1

38

M

5 days

2

45

4.0

93.8

43.0

Distal dominant

A2

40

M

9 days

1

47

5.1

100

53.0 ↑

A3 A4 A5 A6 A7 Normal values (mean ± SD, n = 20 normal subjects) Lower limit or upper limit (mean − or + 2.5 SD)

28 58 27 44 33

M F M M M

12 days 13 days 16 days 3 months 3 months

1 1 3 2 4

42 51 41 52 49 49.3 ± 4.4

2.7 5.3 2.9 4.2 4.1 3.7 ± 0.8

100 100 87.5 100 100

51.3 46.9 52.6 ↑ 47.9 45.4 44.6 ± 3.0

GM1-IgG GM1-IgM GM1-IgG GM1-IgM GA1-IgG NE ND NE NE ND

38.3

5.7

52.1

MCV: motor conduction velocity, CECT: cauda equina conduction time, SD: standard deviation, ↑: abnormal increment. ND: not detected, NE: not examined. Note: CECT and F-waves were measured at the same time (but not always at the time that the types of GBS were classified).

Diffuse Distal dominant Distal dominant

Diffuse Distal dominant Diffuse

Distal dominant

Distal dominant Proximal dominant Distal dominant Distal dominant Diffuse

H. Matsumoto et al. / Journal of the Neurological Sciences 351 (2015) 187–190

was positioned over the first lumbar (L1) spinous process to induce currents to flow upward in the body at around the conus medullaris [12–14]. Stimulus intensity was gradually increased, and reproducible CMAPs were obtained at the proximal cauda equina. CECT was obtained by subtracting the CMAP latency to S1-level stimulation from that to L1level stimulation. We judged whether CECT and MCV were normal or abnormal on the basis of normal values made from 20 age- and body height-matched healthy volunteers (normal subjects). We also evaluated the presence of a conduction block between the ankle and the neuro-foramina. 3. Results The results of MCV and CECT in all patients are summarized in Table 1. Fig. 1 shows CMAPs in a representative patient with demyelinating GBS (case D6) and a representative patient with axonal GBS (case A2). In case D6, F-waves were not evoked. MATS coil stimulation, however, allowed us to measure CECT. MCV was normal (42 m/s), and CECT was abnormally prolonged (6.5 ms; mean ± SD normal values are 3.7 ± 0.8 ms, upper limit of normal values is 5.7 ms). In contrast, in case A2, both MCV and CECT were normal (47 m/s and 5.1 ms). L1level stimulation was not supramaximal stimulation. However, the amplitude reduction of CMAPs between the cauda equina was only approximately 25%. In all nine demyelinating GBS patients, MCV was within the normal range. In contrast, CECT was prolonged in eight patients (88.9%). Only one demyelinating GBS patient (case D3) had normal CECT. She presented with bulbar palsy and muscular weakness in the upper extremities and had no leg symptoms when CECT was measured. Later she presented with diffuse muscular weakness. On the other hand, all other demyelinating GBS patients had leg symptoms when CECT was measured. No conduction blocks were detected between the ankle and the knee in all demyelinating GBS patients. Supramaximal CMAPs at the neuro-foramina were not obtained in any demyelinating GBS patient, which made it impossible to evaluate the conduction block between the knee and the neuro-foramina. Both MCV and CECT were normal in all seven axonal GBS patients. Supramaximal CMAPs were obtained at the neuro-foramina in all axonal GBS patients. All of them had leg symptoms, but no conduction blocks were detected between the ankle and the neuro-foramina in any of them.

Fig. 1. MATS coil stimulation in two types of GBS patients. In a demyelinating GBS patient (case D6), F-waves were not evoked. However, MATS coil stimulation allowed us to measure CECT. Motor conduction velocity (MCV) between the ankle and the knee was normal (42 m/s), whereas CECT was prolonged (6.5 ms, upper limit of normal values is 5.7 ms). In an axonal GBS patient (case A2), in contrast, both MCV and CECT were normal (47 m/s and 5.1 ms). In L1-level stimulation, CMAPs were not supramaximal, although the amplitude reduction of CMAPs between the cauda equina was only approximately 25%. On the other hand, there were no conduction blocks between the ankle and the neuro-foramina.

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4. Discussion We demonstrated that CECT prolongation was observed in almost all demyelinating GBS patients. In particular, in demyelinating GBS patients with positive leg symptoms, CECT was always prolonged. These findings suggest the frequent cauda equina involvement in demyelinating GBS patients. In addition, we for the first time demonstrated normal CECT and no segmental conduction problems between the ankle and the neuro-foramina in axonal GBS patients. Consequently, our results revealed that CECT was prolonged in demyelinating GBS and normal in axonal GBS. Moreover, segmental lesions were absent between the ankle and the neuro-foramina in axonal GBS. MATS coil stimulation allowed us to measure CECT even in GBS patients with unobtainable F-waves. Therefore, even if the sole positive finding is the disappearance of F-waves, CECT measurement could be helpful to detect demyelinating lesions in GBS. In demyelinating GBS patients, prior studies using magnetic resonance imaging have revealed that the spinal nerves in the spinal canal are frequently involved [16–18]. Our electrophysiological results support these imaging findings. Previously, similar electrophysiological comparisons in the upper and lower extremities have been reported [19,20]. Inaba et al. (2002) reported that cervical root conduction time in the spinal canal was prolonged in 6 out of 10 demyelinating GBS patients (60.0%) and MCV between the wrist and the elbow was normal in all patients [19]. Maccabee et al. (2011), using a large 8-shaped coil, reported that CECT was prolonged in 13 out of 14 demyelinating GBS patients (92.9%) and that the ankle–knee conduction was delayed in 1 out of 14 demyelinating GBS patients (7.1%) [20]. The present electrophysiological results are also compatible with these findings. In addition, similar conduction delays at the proximal parts were observed in patients with chronic inflammatory demyelinating polyradiculoneuropathy (CIDP) [20,21]. These results suggest that the most proximal parts of the peripheral nerves are very frequently involved in immune-mediated peripheral neuropathies in both acute and chronic disease progression. In those immune-mediated peripheral neuropathies, the lack, destruction, or malfunction of the blood nerve barrier is considered to play a crucial role in the disease process [22,23]. The spinal nerves in the spinal canal have no blood nerve barriers and are directly exposed to the cerebrospinal fluid [24]. These anatomical characters might enable anti-ganglioside antibodies or some other circulating factors to directly access the spinal nerves, including the cauda equina. This would explain the frequent involvement of the cauda equina in demyelinating GBS. In axonal GBS patients, on the other hand, no similar researches have been reported. Although we showed normal conduction time in the cauda equina, this does not exclude segmental lesions in the cauda equina, because L1-level MATS coil stimulation is usually unable to elicit supramaximal responses and is not able to show a conduction block within the cauda equina, even in normal subjects. If present, however, the conduction block may not be so serious in axonal GBS patients. As shown in Fig. 1 (case A2), despite non-supramaximal stimulation at the proximal cauda equina, the amplitude reduction of CMAPs between the cauda equina does not fulfill the criteria of the conduction block (N 50% amplitude reduction) [25]. Hence, at least, in some axonal GBS patients, the severe conduction block is not present. On the other hand, segmental conduction problems are usually absent between the ankle and the neuro-foramina in axonal GBS patients. CECT is normal in all axonal GBS patients, whereas it is prolonged in all demyelinating GBS patients, if GBS patients have leg symptoms. Therefore, the CECT measurement should be very useful for directly detecting demyelinating lesions in GBS. Even when the disappearance of F-waves is the only abnormal finding in electrophysiological studies, MATS coil stimulation could enable a correct diagnosis of GBS. Additionally, we also expect that CECT measurement contributes to revealing the pathophysiology of equivocal GBS (unclassified GBS) patients.

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The limitation of our study is that the examiner was not blinded for the classification of GBS, demyelinating GBS or axonal GBS. In general, the unblinded investigators often tend to predict the findings based on the knowledge, leading us to the subliminal bias. In the future, our findings should be confirmed by other researchers in the doubleblinded studies. In addition, our study includes GBS patients at the recovery phase (cases D9, A6, and A7). In these GBS patients, the remyelination or axonal regeneration must contribute to the CECT. Sequential studies also may provide us with novel insights. Finally, we did not investigate the relationships between anti-ganglioside antibodies and CECT. Such investigations must be required to uncover the pathophysiology of GBS. In conclusion, we demonstrated that the cauda equina is frequently involved in demyelinating GBS. In axonal GBS, usually, CECT is normal and segmental lesions are absent between the ankle and the neuroforamina. MATS coil stimulation can be considered very useful to directly detect demyelinating lesions in GBS. As a research tool, MATS coil stimulation could contribute to the pathophysiological clarification of GBS. As a clinical tool, it could enable ready access to a correct diagnosis, thus ensuring that appropriate therapy is provided to GBS patients. Conflict of interest statement The authors report no conflict of interest. Acknowledgments Dr. Hanajima was supported by a Research Project Grant-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology of Japan and Dainippon Sumitomo Pharma. Co., Ltd. She has also received a speaker’s honorarium from Kyowa Hakko Kilin Co., Ltd. Dr. Terao was supported by a Research Project Grant-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology of Japan and by grants from GlaxoSmithKline and Boehringer Ingelheim. He has also received a speaker's honorarium from Boehringer Ingelheim. Dr. Ugawa was supported by a Research Project Grant-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology of Japan; by grants for the Research Committee on Degenerative Ataxia from the Ministry of Health and Welfare of Japan; by the Research Committee on Insomnia in Parkinson's Disease from the Ministry of Health and Welfare of Japan; by a grant from the Committee of the Study of Human Exposure to EMF from the Ministry of Public Management, Home Affairs, Post and Telecommunications; and by a grant from the Uehara Memorial Foundation. He has also received speaker's honorariums from the Taiwan Movement Disorders Society, Astellas Pharma Inc., Eisai Co., Ltd., FP Pharmaceutical Corporation, Otsuka Pharmaceutical Co., Ltd., Elsevier Japan K. K., Kissei Pharmaceutical Co. Ltd., Kyorin Pharmaceutical Co., Ltd., Kyowa Hakko Kirin Co., Ltd., GlaxoSmithKline K. K., Sanofi-Aventis K.K., Daiichi Sankyo Co., Ltd., Dainippon Sumitomo Pharma Co., Ltd., Takeda Pharmaceutical Co., Ltd., Mitsubishi Tanabe Pharma Corporation, Teijin Pharmaceutical Ltd., Nippon Chemiphar Co., Ltd., Nihon Pharmaceutical Co., Ltd., Nippon Boehringer Ingelheim Co., Ltd., Novartis Pharma K.K., Bayer Yakuhin,

Ltd., and Mochida Pharmaceutical Co., Ltd. He has received royalties from Chugai-Igakusha, Igaku-Shoin Ltd., Medical View Co. Ltd., and Blackwell Publishing KK.

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Cauda equina conduction time in Guillain-Barré syndrome.

The proximal segment of peripheral nerves is assumed to be involved in both demyelinating and axonal types of Guillain-Barré syndrome (GBS). However, ...
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