Electroencephalography and clinical Neurophysiology, 84 (1992) 433-439

433

© 1992 Elsevier Scientific Publishers Ireland, Ltd. 0168-5597/92/$05.00

EVOPOT 91692

Central sensory and motor conduction in vitamin B12 deficiency V. Di Lazzaro, D. Restuccia, D. Fogli, R. Nardone, S. Mazza and P. Tonali Department of Neurology, Catholic University, Rome (Italy) (Accepted for publication: 3 April 1992)

Summary

Four patients with subacute combined degeneration were studied through upper and lower limb SEPs recorded with a non2cephalic reference montage and through cortical and spinal magnetic stimulation. Clinical signs were confined to the lower limbs in 3 patients; the remaining patient presented only paraesthesiae in 4 limbs. Median nerve SEPs showed a normal cervical N13 response with a significant increase of central conduction time concerning exclusively the P9-P14 interpeak interval. Central motor conduction to upper and lower limb muscles was abnormal. Nerve conduction studies provided no evidence of peripheral nerve involvement. These electrophysiological findings suggest that in vitamin B12 deficiency the higher segments of the cervical cord are usually affected first and that central sensory and motor conduction studies are sensitive methods for detecting such damage.

Key words: Somatosensory evoked potentials; Magnetic stimulation; Subacute combined degeneration; Vitamin B12 deficiency

Nervous system involvement occurs in the majority of patients with vitamin B12 deficiency. The clinical picture varies from simple paraesthesiae to objective signs of lateral and posterior column involvement (Adams and Victor 1989). The diagnosis may be difficult, particularly in the early stage of the disease when only paraesthesiae are present and there may be no objective signs. For this reason it is necessary to find additional neurological signs of subacute combined degeneration (SACD). Previous studies of somatosensory evoked potentials (SEPs) in SACD have demonstrated that SEPs are a sensitive method of detecting disturbances of central sensory conduction (Fine and Hallett 1980; Jones et al. 1987; Dick et al. 1988; Tomoda et al. 1988; Zegers de Beyl et al. 1988a; Fine et al. 1990). In spite of the considerable number of reports, only one of them (Zegers de Beyl et al. 1988a) attempts an analysis of the subcortical scalp far-fields after upper limb stimulation. It has been demonstrated that such a method could better localize the somatosensory dysfunction (Maugui~re and Ibafiez 1985). Central motor pathway conduction can be evaluated non-invasively using the technique of magnetic stimulation of the motor cortex (Barker et al. 1985a,b). There have been only anecdotal reports on central motor conduction in SACD (Ciaramia et al. 1988; Murray

Correspondence to: Dr. V. Di Lazzaro, Istituto di Neurologia, Universit~t Cattolica, Policlinico A. Gemelli, L.go A. Gemelli 8, 00168 Rome (Italy).

1990) The aim of our study was to evaluate the sensitivity of non-cephalic SEP recording and magnetic brain stimulation in detecting and localizing the functional involvement of the central nervous system in SACD.

Patients and methods

The patients The patients gave informed consent to the study. Patient 1. A 57-year-old man presented an 8 month history of progressive gait disturbance. At the age of 49 he had undergone partial gastrectomy for gastric ulcer. The neurological examination revealed spastic gait with enhanced tendon reflexes in the lower limbs, bilateral Babinski sign and lower limb ataxia. Vibration and position sense were diminished in the lower extremities. Megaloblastic anaemia and a serum B12 value of 85 pg/ml (normal, 160-970 pg/ml) indicated B12 deftciency. Patient 2. A 65-year-old woman presented a 1 year history of progressive gait disturbance. At the age of 58 she had undergone vagotomy for gastric ulcer. The neurological examination revealed spastic gait with enhanced tendon reflexes in the lower limbs, bilateral Babinski sign and lower limb ataxia. Vibration and position sense were diminished in the lower extremities. Megaloblastic anaemia and a B12 value of 105 p g / m l indicated B12 deficiency. Patient 3. A 52-year-old man presented a 2 month history of upper and lower limb paraesthesiae. At the age of 47 he had undergone partial gastrectomy for

434 gastric ulcer. The neurological examination was normal. Megaloblastic anaemia and a serum B12 value of 98 p g / m l indicated B12 deficiency. Patient 4. A 67-year-old woman presented a 3 year history of progressive gait disturbance. At the age of 55 she had undergone partial gastrectomy for gastric ulcer. The neurological examination revealed spastic gait with enhanced tendon reflexes in the lower limbs, bilateral Babinski sign and lower limb ataxia. The serum B12 level was normal, 380 p g / m l (she had received vitamin B12 injections just prior to the test). However, Schilling's test produced a 1.9% extraction in 24 h; after intrinsic factor this rose to 20.7%. ECG, EEG, chest radiograph, brain and spinal cord MR were normal in all patients. Motor and sensory nerve conduction velocities using conventional techniques and F wave latencies were studied in lower and upper limbs. Nerve conduction studies and F responses were normal in all patients. Sural sensory action potential amplitudes ranged from 8 /xV to 13 /xV (normal values of sural nerve amplitudes > 7/zV at ages 50-70).

The technique For SEP recording, the patient lay on a couch in a warm and semidarkened room. Stimuli (0.3 msec square pulses) were delivered at the rate of 5 Hz at motor threshold intensity. Stimuli were delivered at the wrist for median nerve SEPs and at the ankle for tibial nerve SEPs. The filter bandpass was 10-3000 Hz; the analysis time was 50 msec for median nerve SEPs and 100 msec for tibial nerve SEPs. Two averages of 2048 trials each were obtained and drawn out by the computer on an X-Y plotter. For median nerve SEP recording the electrodes (impedance below 5 kS2) were placed in the supraclavicular fossa (Erb's point), over the spinous process of the 6th cervical vertebra (Cv6) and in the contralateral and ipsilateral parietal scalp regions. The Erb's point electrode was referred to Fz and the parietal scalp electrodes to the shoulder contralateral to the stimulated side. For recording of the cervical N13 potential we connected grid 1 of the amplifier to the Cv6 electrode and grid 2 to an electrode located immediately above the thyroid cartilage. This latter electrode site will be referred to in text and figures as "anterior cervical" (AC). The rationale for this Cv6 to AC montage was discussed in detail in a previous study (Restuccia and Maugui~re 1991); briefly, it permits the recording of the activity generated by the transverse dipolar source of the N13 potential with a maximal amplitude; moreover it does not record potentials generated above the foramen magnum (Desmedt and Cheron 1981). As in a previous study, the amplitude of the N13 response was assessed by calculating the N13/P9 amplitude ratio, using the Cv6-AC traces (Restuccia and Maugui~re 1991). For assessing conduction in the dorsal column system and in the intracranial

v. DI LAZZAROET AL. segments of the somatosensory pathways we measured the P9-P14 and the P14-N20 interpeak latencies. The P14 and N20 potentials, which were measured on the contralateral parietal traces recorded with shoulder reference montage, are presumed to be generated, respectively, in medial lemniscus above the foramen magnum and in parietal cortex (Desmedt and Cheron 1980; Tsuji et al. 1984; Maugui~re and Ibafiez 1985). To assess better the central sensory pathway conduction we also measured the N13-P14 interpeak interval. For tibial nerve SEP recording, the electrodes were placed over the spinous process of the 4th lumbar vertebra (L4) and the 12th thoracic vertebra (Thl2) and 2 cm posterior to the vertex (Cz'). The L4 electrode was referred to the 2nd lumbar vertebra (L2) to record the response generated by the ascending volley of impulses in the cauda equina (Magladery et al. 1951; Cracco et aL 1975). The Cz' electrode was referred to the forehead (Fz) to record the P40 cortical response (Jones and Small 1978; Kakigi et al. 1982). For recording the spinal N24 potential we connected grid 1 of the amplifier to the Thl2 electrode and grid 2 to an electrode located in the anterior region of the abdomen immediately above the umbilicus (Ant). This Thl2 to Ant montage permits recording of the transverse dipolar source of the N24 potential with a maximal amplitude; moreover, it tends to cancel the N21 potential, which reflects the ascending volley in the dorsal columns (Desmedt and Cheron 1983; Jeanmonod et al. 1989) and is picked up by both recording electrodes. Normative data were collected from 46 normal subjects (18 men, mean age 35.4, range 18-62) for median nerve SEPs and from 25 normal subjects (15 men, mean age 30.2, range 18-49) for tibial nerve SEPs. In patients 1 and 2 the central motor conduction was evaluated using magnetic stimulation of the motor cortex and cervical spine. During the magnetic stimulation the subjects were seated in a reclining chair. Transcutaneous magnetic stimulation of the motor cortex was achieved using a Magstim 200 (Novametrix, U.K.). The magnetic pulses were delivered through a 120 mm diameter circular coil. The maximal magnetic field generated was approximately 2 tesla at the centre of the coil. The stimulus intensity was 100% of the maximal output for cortical stimulation. The coil was centred over the vertex. To obtain preferential activation of each hemisphere, a clockwise inducing current flow, as viewed from above, was used for the right motor cortex and an anti-clockwise flow for the left motor cortex (Day et al. 1990). Cortical stimulation was performed first with the target muscle relaxed and then during a slight voluntary contraction to facilitate the responses, since the CMAP size increases and its latency shortens when the muscle is voluntarily contracted (Hess et al. 1986; Mills et al. 1987). CMAPs were recorded from thenar and tibialis anterior mus-

435

CENTRAL CONDUCTION IN SACD cles by s u r f a c e e l e c t r o d e s a n d a m p l i f i e d w i t h filter settings o f 2 H z a n d 5 kHz. T o e v a l u a t e t h e p e r i p h e r a l m o t o r c o n d u c t i o n f r o m t h e spinal c o r d to t h e muscles, m a g n e t i c s t i m u l a t i o n on t h e cervical a n d l u m b a r s p i n e s was p e r f o r m e d . T h i s t e c h n i q u e activates t h e m o t o r axons o f p e r i p h e r a l n e r v e s n e a r t h e i r exits f r o m t h e spinal c o l u m n ( U g a w a et al. 1989). F o r r a d i c u l a r stimulation, t h e lower e d g e o f t h e coil was p l a c e d just l a t e r a l to C7-D1 a n d L4-L5 s p i n o u s p r o c e s s e s for t h e n a r a n d tibialis a n t e r i o r m u s c l e s respectively. A clockwise inducing c u r r e n t , as v i e w e d f r o m b e h i n d , was u s e d for t h e right m u s c l e s a n d vice v e r s a for t h e left muscles. T h e stimulus intensity was 6 0 % o f m a x i m a l o u t p u t . C e n t r a l m o t o r c o n d u c t i o n t i m e ( C M C T ) to u p p e r a n d l o w e r limb m y o t o m e s was e v a l u a t e d by s u b t r a c t i n g t h e l a t e n c y a f t e r cervical o r l u m b a r s t i m u l a t i o n f r o m t h e l a t e n c y a f t e r c o r t i c a l s t i m u l a t i o n d u r i n g v o l u n t a r y cont r a c t i o n o f t h e t a r g e t muscles. C o n t r o l v a l u e s for t h e latency of CMAPs after cortical and radicular stimulation a n d for C M C T w e r e o b t a i n e d a f t e r b i l a t e r a l studies o n 25 h e a l t h y subjects (13 m e n ; m e a n a g e = 43.7,

S.D. = 18). N o r m a l limits for l a t e n c y a n d C M C T w e r e d e f i n e d by t h e m e a n + 3 S.D.s o f t h e c o n t r o l values.

Results S E P d a t a a r e s u m m a r i z e d in T a b l e I. A l l p a t i e n t s s h o w e d a b n o r m a l SEPs. M e d i a n nerve S E P a b n o r m a l i t i e s c o n c e r n e d P14 l a t e n c y a n d t h e P9P14 a n d N13-P14 intervals exclusively, w h e r e a s N9, P9, N20 a n d t h e P14-N20 interval, as well as t h e N13 l a t e n c y a n d a m p l i t u d e , w e r e within n o r m a l limits bilaterally (Fig. 1). T i b i a l n e r v e S E P a b n o r m a l i t i e s w e r e r e p r e s e n t e d exclusively by t h e a b s e n c e of cortical P40, w h e r e a s t h e l a t e n c i e s o f the c a u d a e q u i n a r e s p o n s e a n d t h e spinal N24 p o t e n t i a l w e r e within n o r m a l limits (Fig. 2). R e p e a t a b l e m o t o r r e s p o n s e s to m a g n e t i c cortical s t i m u l a t i o n w e r e easily o b t a i n e d f r o m u p p e r limb muscles b o t h at rest a n d d u r i n g v o l u n t a r y c o n t r a c t i o n a n d f r o m l o w e r limb m u s c l e s d u r i n g v o l u n t a r y c o n t r a c t i o n

TABLE I SEP findings (latency values in msec). N9

P9

N13

P14

N20

P9-P14

P14-N20 N13-P14 N13/P9 amplitude ratio

right left right left right left right left

9.9 9.9 9 8.6 11.8 11.4 11 10.8

9.2 9.2 8 8 11 10.6 9.8 10

13.5 13.5 12.8 12 15.4 15 15.2 14.9

16.5 16.5 15 15.4

21.5 21.5 19.2 20

7.3

5

3

2

7.3 7 7.4

3

19.3 18.9 18.6 18.4

23.8 23 23.6 23.5

8.3 8.3 8.8 8.4

5 4.2 4.6 4.5 4.1

2 1.8 1.9 2.6

mean S.D. range normal limit ( m e a n + / - 3 S.D.)

10.1 0.7 8.6-12.2

13.3 0.9 12 -15.8

14.6 0.9 13 -17.2

19.3 0.9 17.6-22

5.4 4.7 0.4 0.5 4.2-6.4 3.6-5.9

1.2 0.3 0.2-2

1.9 0.6 1 -3.5

16

17.3

22

6.6

2.1

1.01

Median nerve SEPs

Patient 1 Patient 2 Patient 3 Patient 4 Control subjects

12.2

9.2 0.7 8 -11.3 11.3

5

5.1

6.2

Tibial nerve SEPs

Patient 1 Patient 2 Patient 3 Patient 4 Control subjects

Cauda equina

N24

P40

right left right left right left right left

18.8 18.8 17.6 17.8 19.2 18.9 18 18.3

24 24 23.6 23.8 25 24.8 22.6 23

no response no response no response no response no response no response no response no response

mean S.D. range normal limit (mean + 3 S.D.)

17 0.8 16.6-19.3

22 1.4 20.2-26

38.1 1.3 35.2-41.2

19.4

26.2

42

2.2 3.4 3.9 3.9 3.4 3.5

2

2.2 1.9

436

V. DI LAZZARO ET AL. i

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,20 ms Fig. 1. SEPs evoked by right and left median nerve stimulation in patient 1. Erb-Fz = Erb's point referred to a forehead electrode (Fz); the P14 potential picked up from the frontal electrode is injected as an "N14" negativity. Cv6-Ac = spinous process of the sixth cervical vertebra, referred to an anterior cervical electrode (AC). Par c-Sh = parietal electrode contralateral to the stimulus, referred to the shoulder contralateral to the stimulus (non-cephalic reference electrode). N9, P9, N13 and N20 absolute latencies, as well as P14-N20 interpeak interval are within normal limits, while the P14 potential is delayed and desynchronized and the P9-P14 interpeak interval is prolonged.

~40 ms Fig. 2. SEPs evoked by stimulation of right and left tibial nerves in patient 1. L4-L2 = spinous process of the fourth lumbar vertebra referred to the spinous process of the second lumbar vertebra to record the cauda equina response (CE). T12-Ant = spinous process of the twelfth thoracic vertebra referred to an anterior abdomen electrode (AC). Cz'-Fz = 2 cm posterior to vertex electrode (Cz') referred to a forehead electrode (Fz). The absolute latencies of CE and N24 responses are within normal limits, while the P40 potential is absent.

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Fig. 3. Compound motor action potentials evoked by spinal and cortical stimulation in patient 1. Two consecutive records are superimposed for each trace. Central motor conduction time (CMCT) values are indicated. A: in the top traces right thenar records are shown; CMAP latency following spinal stimulation is normal; CMCT is prolonged. In the lower traces right tibialis anterior records are shown; CMAP latency following spinal stimulation is normal; CMCT is very prolonged. B: left thenar and tibialis anterior records.

CENTRAL CONDUCTION IN SACD

437

in all normal subjects while responses were obtained in 20 of the 25 control subjects from lower limb muscles at rest. Electrophysiological findings obtained after magnetic stimulation of motor cortex and spine are summarized in Table II. Cortical stimulation performed with relaxed target muscles did not evoke any repeatable response in patients 1 and 2. Thenar muscle CMAPs recorded after cortical stimulation during voluntary contraction were slightly prolonged in patient 1 (Fig. 3) and considerably delayed in patient 2. CMAPs recorded from the tibialis anterior muscle after cortical stimulation were considerably delayed in patient 1 (Fig. 3) and on the right side of patient 2 while no response after cortical stimulation was obtained on the left side. The latencies of the responses evoked through cervical and lumbar stimulation were within normal limits in both patients, and excluded any peripheral slowing (Fig. 3). The thenar muscle CMCT was slightly prolonged in patient 1 and considerably so in patient 2. Lower limb CMCT was considerably increased in patient 1 and also in patient 2, on one side but not evaluable on the other side, since CMAPs were completely absent after cortical stimulation.

Discussion

In SACD various structures of the nervous system show different degrees of vulnerability; the spinal cord

is usually affected first and often exclusively (Victor 1984). An electrophysiological assessment of dorsal columns by SEPs and of cortico-spinal lateral tracts by CMCT measurement should therefore be of considerable value in the early diagnosis of SACD. The main SEP feature, common to all our patients, was an abnormal median nerve P14 and P9-P14 and N13-P14 interpeak intervals coexisting with preserved N13 and P14-N20 interpeak interval. This suggests that in SACD central somatosensory pathways are involved above the generators of the cervical N13 and below the generators of the P14 far-field. Therefore, this finding can be explained by conduction delay in the higher dorsal column segments. Central sensory pathway involvement was confirmed by lower limb cortical SEP abnormalities. Electrophysiological abnormalities found in our patients may be related to the diffuse degeneration of spinal cord white matter described in pathological studies (Victor 1984). A high incidence of N13 abnormalities has been reported in previous studies (Jones et al. 1987; Dick et al. 1988; Fine et al. 1990). This finding, which suggests an involvement of cervical gray matter, is very difficult to explain when related to pathological changes of diffuse white matter degeneration in SACD (Victor 1984) and is not confirmed in our study. The abnormality of cervical response described in previous studies is more likely to be due to the recording technique which used a frontal reference electrode for the cervical response. When the P14 component is delayed it is injected as negativity by the frontal reference electrode in the cervical-frontal re-

TABLE II CMCT and latencies of CMAPs obtained after cortical and spinal magnetic stimulation (with voluntary contraction during cortical stimulation).

Thenar muscle CMAPs Patient 1 Patient 2 Control subjects

Latency after cortical stimulation

Latency after spinal stimulation

CMCT

right left right left

22.5 22.2 22.4 29.2

14.3 14 12.9 13

8.2 8.2 9.5 16.2

mean S.D. range normal limit (mean + 3 S.D.)

19.3 0.9 17 -20.5

13.2 0.8 11.1-14.7

6.2 0.5 5 -7.1

22

15.6

7.7

44.6 41.3 40.6 no response

14 13.3 13 12.7

30.6 28 27.6 -

26.7 1.5 23 -29.9

12.9 1.1 10.4-15.4

13.8 1.1 11.2-16

31.2

16.2

17.1

Tibialis anterior muscle CMAPs Patient 1 right left Patient 2 right left Control subjects

mean S.D. range normal limit (mean + 3 S.D.)

438

sponse, producing an abnormal "N14" (Maugui~re and Ibafiez 1985); in this case only the use of a non-cephalic reference makes it possible to distinguish between N13 and P14. Therefore, the cervical responses, identified as delayed N13 in previous studies, may correspond to a delayed P14 recorded at a frontal reference and injected as negativity in the resulting cervical response. Moreover, in previous studies, conduction delay was incorrectly localized in the lower cervical cord, since the abnormalities of the central conduction time mainly concerned the interval between the Erb's point potential and the delayed cervical response. In only one of the previous studies (Zegers de Beyl et al. 1988a) was the analysis of the sub-cortical scalp far-field performed using a linked earlobe reference technique, measuring central sensory conduction from the onset of the N l l neck potential to the onset of the N20 potential. This time was further divided into two intervals, N11-P14, reflecting predominantly the transition time of the afferent volley in the posterior columns, and P14-N20, concerning conduction from brain-stem to cortex (Zegers de Beyl et al. 1988b). Using this technique Zegers de Beyl et al. (1988a) obtained a result quite in agreement with ours: decreased conduction velocity in SACD occurred in the posterior columns. However, although the measurement of the intervals between the N l l , P14, and N20 onsets may be a more correct way to assess central conduction from a physiological point of view (Zegers de Beyl et al. 1988b), we think that the measurement of P9-P14 and P14-N20 interpeak intervals is more valid as a clinical tool because P14 onset cannot be ascertained in all normal subjects without ambiguity (Zegers de Beyl et al. 1988b). The ambiguity of the P14 onset may explain the slight but significant prolongation of P14-N20 interval associated with a clear prolongation of N11-P14 interval in one of the patients of Zegers de Beyl et al. (1988a). CMCT measurement in two of our patients suggested that central motor conduction studies may be useful in detecting clinical and subclinical upper motor neurone pathway involvement in SACD. In fact, central motor conduction was abnormal for both tibialis anterior and thenar muscles although upper motor neurone signs were present only in the lower limbs. In conclusion, our data indicate that, although electrophysiological abnormalities found in our patients have no absolute specificity to SACD, central motor and sensory conduction studies may be of considerable value in the functional assessment of the spinal cord in SACD, in the early stage of the disease as well, as demonstrated by SEP abnormalities in the patient with no objective clinical signs (case 3). Abnormal central sensory and motor conduction associated with normal peripheral conduction in all our patients is in agreement with SACD pathological data demonstrating that neurologi-

V. DI LAZZARO ET AL.

cal manifestations of SACD are due primarily to spinal cord lesions and that degenerative changes in the peripheral nerves occur only, in patients with advanced forms of myelopathy (Victor 1984). Moreover, our data suggest that in patients suspected of having SACD or other diseases affecting posterior columns the use of a non-cephalic reference for SEP recording is necessary for making a correct localization of the central sensory disturbance.

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Central sensory and motor conduction in vitamin B12 deficiency.

Four patients with subacute combined degeneration were studied through upper and lower limb SEPs recorded with a non-cephalic reference montage and th...
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