Clinical Neurophysiology 124 (2013) 197–203

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Clinical Neurophysiology

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Diagnostic value of lumbar root stimulation at the early stageof Guillain–Barré syndrome

Tulay Kurt Incesu a,⇑, Yaprak Secil a, Figen Tokucoglu a, Nevin Gurgor a,Tolga Özdemirkiran a, Galip Akhan a, Cumhur Ertekin b

a Atatürk Education and Research Hospital, Department of Neurology, Izmir, Turkeyb Aegean University, Medical School Hospital, Bornova, Izmir, Turkey

a r t i c l e i n f o

Article history:Accepted 5 July 2012Available online 25 August 2012

Keywords:Guillain–Barré syndromeLumbar root stimulationEMGEarly diagnosisNeurophysiologyProximal conduction block

1388-2457/$36.00 � 2012 International Federation ohttp://dx.doi.org/10.1016/j.clinph.2012.07.004

⇑ Corresponding author. Address: 169 Sok, No. 3 D35000 Izmir, Turkey. Tel.: +90 232 2435760; fax: +90

E-mail address: tkurt2@hotmail.com (T.K. Incesu).

h i g h l i g h t s

� Lumbar root stimulation at the laminar level is a useful method to diagnose the Guillain–Barrésyndrome in the first week.� M-responses obtained by lumbar root stimulation denote the first electrophysiological abnormality.� This method enables demonstration of attenuated M-responses motor conduction block at the root/proximal nerve significantly as early as possible.

a b s t r a c t

Objective: The aim of this study is to investigate diagnostic value of electrical lumbar root stimulation(RS) at the laminar level in the early stage of Guillain–Barré syndrome (GBS).Methods: Fifteen patients (30 sides) and nine controls (17 sides) were included in the study. Conventionalnerve conduction studies, needle electromyography, F responses and electrical lumbar RS were obtainedfrom both groups. The needle electrical stimulation was performed at the L2–3 intervertebral level. Vas-tus lateralis, tibialis anterior and soleus muscles were investigated bilaterally and simultaneously in thefirst and fourth weeks.Results: In all patients, the amplitudes elicited by lumbar RS were significantly attenuated while the con-ventional electrophysiological findings were normal and/or not diagnostic in 6 of 15 patients (40%)within the first week. Motor latencies by the lumbar RS were prolonged in the patients, compared tothe controls, but the results were not statistically significant.Conclusions: M-responses elicited by lumbar RS appear to be helpful in disclosing proximal conductionabnormalities of GBS early in the course.Significance: Lumbar RS seems to be a useful method in making the diagnosis of GBS early and there is noconsiderable side effect of this particular method.� 2012 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights

reserved.

1. Introduction

The well-known typical Guillain–Barré syndrome (GBS) can beeasily diagnosed by clinical, electrophysiological and cerebrospinalfluid (CSF) findings within the first weeks of acute demyelinatedpolyneuropathy. In addition, some acute motor axonal neuropathy(AMAN) patients show transient conduction block/slowing in inter-mediate and distal nerve segments, mimicking demyelination butwithout the development of abnormal temporal dispersion, namedreversible conduction failure, which can be recognised only by seri-

f Clinical Neurophysiology. Publish

.10 Basin Sitesi, Karabaglar,232 2434848.

al recordings (Uncini and Kuwabara, 2012). However, the diagnosismay be delayed 2–3 weeks after the onset of first motor symptoms.The motor and sensory conduction studies’ results can be foundwithin normal limits in upper and lower extremity nerves, whetherthe M-responses induced distally by the electrical stimulation ofthe accessible sites of the peripheral nerves during the acute stageof the GBS are normal or low. It has been reported that the electro-diagnosis of GBS could not be sufficient in 15–30% of overall pa-tients with GBS (Albers and Donofrio, 1985; Ropper et al., 1990;Gordon and Wilbourn, 2001; Vucic et al., 2004). On the other hand,establishing the diagnosis early is very important for immediatetreatment of GBS (Van der Meché and Schmitz, 1992).

However, focal demyelination and the conduction block at themotor roots cannot easily be evaluated by electrophysiological

ed by Elsevier Ireland Ltd. All rights reserved.

198 T.K. Incesu et al. / Clinical Neurophysiology 124 (2013) 197–203

methods because this area is not easily accessible (Ad Hoc Subcom-mitee of the American Academy of Neurology AIDS Task Force,1991; Hughes et al., 2001; Saperstein et al., 2001; Nicolas et al.,2002; Alfonsi et al., 2003). As the demyelination process or acuteimmune attacks are often directed to the proximal part of motornerves or motor roots, there is no electrophysiological finding sug-gesting that there may be demyelinating polyneuropathy. This per-iod can last up to 7–10 days despite the motor paresis of limbs(King and Ashby, 1976; Menkes et al., 1998; Vucic et al., 2004;Temucin and Nurlu, 2011).

Obviously, detecting a proximal conduction block is the mostimportant point in such early GBS patients. Previously, there wereattempts to resolve the early electrodiagnostic problem of the GBSby different electromyographic (EMG) methods. Among them aresoleus H-reflex, F-waves, multiple A-waves, prolonged distal motorlatency, distal motor conduction time, size of M-responses, blinkreflexes and others (Mills and Murray, 1985; Fross and Daube,1987; Ropper et al., 1990; Brown et al., 1993; Kiers et al., 1994;Kornhuber et al., 1999; Kuwabara et al., 1999, 2002; Albertíet al., 2011). These are mainly indirect techniques suggesting thatthere may be proximal conduction block. Abnormal results may bepresent not only in GBS but also in other types of polyneuropathiesand radiculopathies. Their sensitivity can be significantly high butnot specific in patients with GBS (Olney and Aminoff, 1990; Gordonand Wilbourn, 2001; Alfonsi et al., 2003).

However, M-responses, distal motor conduction time and distalmotor latencies should be separately evaluated at the time of theearly diagnosis of GBS. Reduced M-response amplitudes and de-layed distal latencies in peripheral nerves are well-known earlyEMG findings. These two abnormal EMG findings or one of themcould be encountered in about 60% or more patients with GBS inthe first week of disease. In some patients, EMG findings couldnot be found in any of the above-mentioned nerves (Menkeset al., 1998; Gordon and Wilbourn, 2001; Vucic et al., 2004,2009; Cleland et al., 2006; Temucin and Nurlu, 2011). Thus, theyare not sufficient diagnostic marks for GBS in the first week ofthe disease.

Alternative diagnostic methods of early GBS depend on theassumption that the demyelination process and the motor conduc-tion block could only be found in the proximal spinal nerves and/ormotor roots in GBS (Menkes et al., 1998; Inaba et al., 2002; Alfonsiet al., 2003; Vucic et al., 2006; Maccabee et al., 2011; Temucin andNurlu, 2011). The motor roots can be stimulated by either mag-netic coil or high-voltage surface electrical stimulation (Chokrover-ty, 1989; Cros et al., 1990; Evans et al., 1990; Ertekin et al., 1994b;Inaba et al., 2002; Alfonsi et al., 2003; Gardill, 2005; Matsumotoet al., 2010; Akaza et al., 2011; Maccabee et al., 2011). Magneticstimulation may not stimulate the motor roots and spinal nervessupramaximally after leaving the neural foramina, which may bemisinterpreted as proximal conduction block (Ertekin et al.,1994b; Menkes et al., 1998; Vucic et al., 2006). However, somenew approaches with magnetic stimulation have shown that mo-tor roots could be stimulated supramaximally from the lumbarsurface skin (Maccabee et al., 1996; Gardill, 2005; Senocak et al.,2009). The high-voltage electrical stimulation was used in particu-lar to stimulate lumbar roots in radiculopathies and demyelinatingpolyneuropathies (Alfonsi et al., 2003; Gardill, 2005). This methodis painful and unpleasant and cannot be easily used even thoughsome useful and positive results have been reported (Gardill,2005).

Some newer studies have shown the advantage of single-needleelectrical stimulation of cervical spinal roots to evaluate early find-ings for the diagnosis of GBS in early periods (Menkes et al., 1998;Vucic et al., 2006). However, GBS usually begins from the lowerlimbs and these methods should be applied to lumbosacral nerveroots.

The single-needle electrical stimulation of the lumbar roots atthe laminar level without entering the spinal theca has been previ-ously described, especially for radiculopathies (Ertekin et al.,1994a; Zileli et al., 2002). In addition, Vucic et al. described a meth-od using needle electrical stimulation of cervical nerves for thediagnosis of primary demyelinating neuropathies (Vucic et al.,2006). A monopolar needle electrode was introduced into theintervertebral space (i.e., L2–3) where the all cauda equina motorroot fibres were lying. The tip of the needle electrode is very closeto the motor roots that descend to the lower limbs. Therefore, itcan provide easy access to the stimulation of the motor roots.The advantages of this method are that it better stimulates the mo-tor roots and it has little or no major risks or complications. Then,we can conclude that electrical stimulation of lumbar motor rootscan demonstrate the proximal conduction block in GBS in the firstweek, compared to the M-responses of lower limb nerves obtainedfrom peripheral nerve stimulation.

2. Methods

Fifteen patients, 30 sides with clinically diagnosed GBS usingthe Asbury and Cornblath criteria (mean age: 52.26 ± 16.15 years,range: 20–76) (Cosi and Versino, 2006) and nine normal controls(mean age: 39.1 + 14.5 years, range: 25–68), 17 sides were in-cluded the study. Diagnostic criteria were used for the secondexamination in the fourth week (Albers and Donofrio, 1985; Alamet al., 1998). Patients who did not meet the same criteria were ex-cluded from the study after second examination in the fourthweek. During the hospitalisation, all patients were monitored forcardiac rhythm and blood pressure changes. For safety, the pa-tients who had autonomic instability and respiratory failure wereexcluded as well as those with other metabolic and/or neuromus-cular diseases (such as diabetes mellitus, renal failure, chronicperipheral neuropathy, connective tissue diseases, hereditaryneuropathies and porphiric neuropathy). Members of the normalcontrol group had no history of neurologic disease and had a nor-mal neurologic examination. The local ethical committee approvedthe study protocol and informed consent was obtained from eachparticipant.

The patients’ first electrophysiological examination was per-formed within the first week and the second examination was inthe fourth week. A two-channelled Medtronic Keypoint EMG(Skovlunde, Denmark) was used for all electrophysiologicalexaminations.

2.1. Conventional nerve conduction studies

Conventional nerve conduction studies (NCSs) of peroneal, pos-terior tibial, median, ulnar and sural nerves were performed. Inaddition, needle EMG and F responses of median and posterior tib-ial nerves were obtained.

2.2. Distal nerve stimulation

Before the lumbar root stimulation (RS), M-responses to distalstimulation were recorded from vastus lateralis (VL), tibialis ante-rior (TA) and soleus (SOL) muscles bilaterally. Using the belly ten-don method, recording Ag–AgCl surface electrodes were placedover the muscles. The femoral nerve was stimulated over the ingui-nal ligament site and the responses were obtained from the VLmuscle. The peroneal nerve was stimulated at the poplitea andthe responses were obtained from the TA muscle. The posteriortibial nerve was stimulated at the poplitea and the responseswere obtained from the SOL muscle. Maximal stimulation wasused to produce the highest response twice to ensure waveform

Fig. 1. (A) Schematic representation of the lumbar root stimulation technique (modified from Ertekin et al., 1994a). (B) Schematic drawing showing needle position inrelation to vertebra.

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reproducibility. After the highest responses were obtained, therecording surface electrodes were fixed and used as recordingelectrodes during RS.

2.3. Lumbar RS

Afterwards, the laminar stimulation of lumbar roots was ap-plied according to the method of Ertekin et al. (1994) (Ertekinet al., 1994a). The subjects were brought to a prone position onthe examination bed. The needle electrical stimulation was per-formed at the L2–3 intervertebral level. Teflon-coated monopolarneedles (Ambu, 50 mm, 38 mm) were used for stimulation. Thecathode (50 mm) electrode was inserted between the spinal pro-cesses of the L2 and the L3 vertebrae at the midline until the exam-iner had felt the long needle touch the bone structure (laminae)after the cleaning of the lumbar skin. The tip of the cathode elec-trode was placed at the dorsal part of the laminae of the lumbarspine. The anode (38 mm) was inserted subcutaneously two orthree levels above the cathode (Fig. 1).

Rectangular electrical pulses of 1.0-ms duration were used forthe RS procedure and the stimulus intensity gradually increasedduring the examination. The lowest intensity that produced anM-response and a muscle twitch was accepted as the threshold le-vel. The stimulus intensity increased step by step until the highestresponse amplitude was obtained, which was also accompanied bya stronger muscle contraction called the maximal stimulus level.During the stimulation, Ag–AgCl surface electrodes were placed

Table 1Summary of the electrophysiological findings in patient and control groups (VL: Vastus la

Muscles Patients first examination(n = 15, side = 30) (mean ± SD)

Patients second e(n = 15, side = 30)

Distalstimulation

Rootstimulation

Amplitudedecrease (%)

Distalstimulation

Rs

VLAmp. (mV) 5.6 ± 2.9 1.3 ± 1.3 76.3 ± 16.7 7.8 ± 4.2Lat. (ms) 4.6 ± 1.3 9.0 ± 4.0 3.9 ± 1.5

TAAmp. (mV) 4.9 ± 3.0 1.5 ± 2.3 68.7 ± 26.2 6.6 ± 2.7Lat. (ms) 6.1 ± 1.0 17.2 ± 7.7 5.4 ± 1.0 1

SOLAmp. (mV) 6.2 ± 4.5 1.6 ± 2.0 73.6 ± 18.5 7.5 ± 3.9Lat. (ms) 5.6 ± 0.9 14.6 ± 8.3 6.0 ± 1.6 1

p < 0.05 Values printed in bold characters.

over VL, TA and SOL muscles. As a two-channelled EMG was used,it was possible to record responses from homologue muscles withsingle stimulation at the same time. After optimum responses wereobtained, three consecutive responses were recorded. The latencyand amplitudes of the muscle responses obtained by distal andlumbar stimulation were measured. The amplitude decrease ratios(%) were calculated by using the amplitudes of M-responses elic-ited by lumbar RS, which were compared to responses elicited bydistal stimulation for each muscle. This was calculated by

"M"ADS � "M"ARS="M"ADSð Þ � 100

where ‘‘M’’ ADS = maximum peak to peak amplitude produced bydistal stimulation, ‘‘M’’ ARS = maximum peak to peak amplitude pro-duced by RS. A reduction more than 50% was accepted as a proximalconduction block (Rhee et al., 1990).

This procedure was performed on both patients and normalcontrols. There were localised pain complaints by some subjectsduring lumbar RS, but this was not more than the pain caused byneedle EMG. None of the subjects reported severe discomfort andthere were no other side effects.

GBS diagnosis was confirmed in all patients by clinical and elec-trophysiological examination according to established criteria,after the second examination (Albers and Donofrio, 1985; Alamet al., 1998). There was no significant age difference between pa-tient and control groups (p > 0.05). Fifteen patients were examinedwithin the first week and the fourth week.

teralis, TA: Tibialis anterior, SOL: Soleus, Amp: amplitude, Lat: Latency).

xamination(mean ± SD)

Normal controls(n = 9, side = 17) (mean ± SD)

oottimulation

Amplitudedecrease (%)

Distalstimulation

Rootstimulation

Amplitudedecrease (%)

2.8 ± 1.7 61.0 ± 18.8 13.9 ± 5.1 8.7 ± 3.9 41.6 ± 13.59.7 ± 3.6 3.2 ± 0.9 7.5 + 1.4

2.3 ± 2.1 71.6 ± 21.17 11.5 ± 4.2 7.3 ± 3.0 34.4 ± 23.089.1 ± 4.2 4.4 ± 0.4 14.4 ± 2.5

2.1 ± 2.1 72.4 ± 17.0 17.7 ± 9.5 9.1 ± 3.0 48.3 ± 19.19.2 ± 3.6 4.6 ± 1.0 15.7 ± 3.4

Fig. 2. The distal and root stimulation responses of a control and a patient at the first week examination (A: control B: patient.). Note calibration difference of amplitudes onthe left (A) and right (B) sides.

200 T.K. Incesu et al. / Clinical Neurophysiology 124 (2013) 197–203

All statistical analyses were performed with Statistical Packagefor Social Sciences (SPSS) 15.0 for Windows. Descriptive analysesfor all parameters were done and Mann–Whitney U and indepen-dent-samples t tests were used for evaluating differences betweengroups. A probability value of p < 0.05 was considered significant.

3. Results

The conventional NCSs were diagnostic in nine patients (60%)and not diagnostic in six patients (40%) within the first week.The second examination within the fourth week showed demyelin-ating neuropathy in all patients. A lumbar tap was performed in 10patients within the first week, and in four patients within the sec-ond week. One patient refused the lumbar tap. In the cerebrospinalfluid (CSF), an increase of protein content (more than 50 mg dl�1)without cell was defined as albuminocytologic dissociation (Victorand Ropper, 2001). According to this, while five patients (50%) hadalbuminocytologic dissociation, CSF analyses of other five patients(50%) were in normal limits within the first week. Four patientswho had a lumbar tap within the second week also had albumino-cytologic dissociation.

3.1. Distal stimulation

There was no significant difference between right- and left-sideexamination in both groups. The amplitudes elicited by distal stim-ulation were significantly lower than in the control group in thefirst week and fourth week in all patients (p < 0.05). There was also

a latency difference between the two groups with distal stimula-tion, but the results were not statistically significant except forthe TA muscle (Table 1). However, the distal stimulation valuesof six patients who had non-diagnostic conventional NCSs werein normal limits and there was no significant difference betweenthese patients and controls.

3.2. Lumbar RS

There was no significant difference between right- and left-sideexaminations in both groups. The amplitudes elicited by lumbar RSin all patients were significantly lower than controls in the first andthe fourth week (p < 0.05) (Figs. 2 and 3). The amplitude decreaseratios (%) of each muscle were well above the normal controls.Even though results were not statistically significant, there was alatency difference between the two groups with lumbar RS(p > 0.05) (Table 1).

In one of the patients M-responses were recorded with distalstimulation, but there was no response to lumbar RS from VL, TAand SOL muscles (Fig. 4A). Likewise one patient had no responsefrom TA, another from SOL with lumbar RS. However, in the secondexamination lumbar RS produced disperse M-responses with lowamplitude in all of these patients suggesting some recovery of con-duction block (Fig. 4B).

Clinical improvement was observed in all patients during thesecond examination. Although the amplitudes elicited by lumbarRS were increased and the amplitude decrease ratio (%) was re-duced at the second examination compared to the first, the differ-ence did not reach a statistically significant level (Table 1, Fig. 5).

Fig. 3. M-response amplitudes produced by RS in control and patient groups at thefirst week.

T.K. Incesu et al. / Clinical Neurophysiology 124 (2013) 197–203 201

4. Discussion

We performed electrophysiological examination twice in thisstudy. The second examination in the fourth week showed demye-linating neuropathy in all patients. Thus, we could exclude AMANpatients with reversible conduction failure, which can be recogni-sed only by serial recordings (Uncini and Kuwabara, 2012). In ourstudy, no characteristic electrophysiological findings of acutedemyelinating polyneuropathy including conduction block, slowedmotor conduction velocities and delayed distal latencies (Albersand Kelly, 1989) could be found in peripheral examination of legand arm nerves in the first week of the disease in six of the patients(40%). These findings in peripheral EMG examination seem to behigher than in previously reported series (Gordon and Wilbourn,2001; Albertí et al., 2011). This may be due to patient group charac-teristics. Because even though all patients were quadriparetic, theirsymptoms could be considered relatively mild. None of themneeded respiratory support and had autonomic disorder. However,when we evaluated the results of lumbar RS, electrophysiologicalfindings were in favour of GBS, because the amplitudes of the M-re-sponses produced by lumbar RS were decreased more than 50%(Fig. 2). In some cases, the absence of M-response by lumbar RSwas found in the first week. Thus, it should be said that the use oflumbar RS is very sensitive when combined with peripheral nervestimulation of one particular muscle. The attenuation of the M-re-sponse tends to improve but it was not well correlated with clinicalrecovery in the fourth week. It is well known that there is no closecorrelation between the degree of conduction abnormalities and

the severity of clinical symptoms, and that clinical improvementprecedes electrophysiological improvement (McLeod et al., 1976;Miyoshi and Oh, 1977; McLeod, 1981; Oh, 1993).

There are several factors that may lead to misinterpretation ofthe focal demyelination during the stimulation of the nerve atthe proximal sites, especially at spinal motor root levels.

(1) When the proximal stimulation is not supramaximal, theattenuation of the M-response might be misinterpreted asa proximal conduction block. For example, magnetic RSexcites fewer axons than the electrical stimulation at thespinal root levels. The attenuated M-response amplitude ismistakenly considered a proximal conduction block due toinsufficient stimulation (Cros et al., 1990; Menkes et al.,1998). However, Maccabee et al. have recently investigatedacute inflammatory demyelinated polyneuropathy by lum-bar magnetic stimulation using different coils and found sig-nificant motor conduction abnormalities in the proximalroot-nerve segment. However, their cases seem to be alreadyclinically and electrophysiologically diagnosed as GBS andthe duration of investigation has not been reported (Macca-bee et al., 2011).

(2) When demyelinating polyneuropathy is present, the excit-ability threshold of the proximal/distal motor nervesbecomes higher (Ertekin, 2006). Therefore, the strength ofstimulation should be carefully checked and must besupramaximal.

(3) In spite of every preventive measure, to overcome the issuesrelated with proximal stimulation problems, sometimes it isnecessary to use a needle stimulation electrode to be closerto investigated nerves or motor roots. Therefore, we usedTeflon-coated needle electrodes to produce sufficient stimu-lation of cauda equina fibres at the laminar level of the L2–3to evaluate lumbar radiculopathies (Ertekin et al., 1994a; Zil-eli et al., 2002).

(4) Interphase cancellation among the muscle fibres may be theresult of the attenuation of the M-response due to abnormaldesynchronisation in the nerve fibres within the area of thefocal demyelination. Besides the M-response reduction, thetemporal dispersion is also increased (Rhee et al., 1990).According to the interphase cancellation, the negative andpositive phases of different motor units can overlap and theycan cancel out each other due to temporal dispersion in thenerve fibres, in which case, the proximal nerve stimulationmay be erroneously defined as a conduction block (Kimura,1984; Rhee et al., 1990). The maximum interphase cancella-tion between the positive and negative components cannotproduce more than 50% decrease of the negative area ofthe M-response (Kimura, 1984). The conduction block canbe found even though nerve conduction velocity is normal.We have observed normal peripheral EMG in some of ourpatients, who had conduction block at the root level severeenough to cause amplitude decrease more than 50% ofperipheral M-response; furthermore, in some patients RSproduced no response (Fig. 4).

In some previous studies, the cervical RS was used to evaluatedemyelinating polyneuropathies including GBS but it may have arisk for developing pneumothorax (Sander et al., 1997, 1999; Vucicet al., 2006). GBS has usually an ascending course and lowerextremities are first affected at the beginning of the illness. There-fore, using the lumbar RS seems to be more important for makingthe diagnosis of GBS early. In addition, lumbar RS studies relatedwith radiculopathy have not reported any side effects. Consistentwith previous studies, neither considerable discomfort nor riskwas observed in the present study.

Fig. 4. The distal and RS responses of a patient at the first and fourth weeks. There is a total block shown by RS at the first week (A) but the all M-responses appeared at thefourth week (B).

Fig. 5. The comparison of M-response amplitudes of patient group produced by RSat the first and fourth week.

202 T.K. Incesu et al. / Clinical Neurophysiology 124 (2013) 197–203

It is concluded that lumbar RS may not be the required methodfor all GBS patients. However, if the examiner and electromyogra-pher could not reach any satisfactory result by conventional elec-trophysiological methods, lumbar RS should be applied as asupplementary method to reach an accurate diagnosis.

Acknowledgements

This work was presented as a poster announcement in the 29thInternational Congress of Clinical Neurophysiology, 2010, Kobe,Japan.

We are very grateful to Erdem Özkan and Malcolm Brook forEnglish revision of the manuscript.

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