PREFACE ORIGINAL CONTRIBUTION TO KNOIVLEDGE: CONTRIBUTION OF CO-AUTHORS: ACKNOWLEDGMENTS
iv v vii viii
ABSTRACT
x
RESU~I~
xii
NEURAL CONDUCTION AND EVOKED POTENTIALS:
MAGNETICSTlhIULATlON OF THE NERVOUS SYSTEM: BACKGROUND
Principles of magnetic induction ELEC~OPHYSIOUX~Y OFEXCITA~ON CENIRALAND 7HE PERIPHERALMOTOR PATHWAYS
Measuring the peripheral motor conduction time THEEFFECTS O F COMPRESSION AND ISCHEMIA ON NEURAL CONDUCTION IN THE LUMBAR SPINE NEURALANATOMY OFTHE LUMBAR SPINE NELIROPA?HOPHYSIOLOGY OFLUMBAR COMPRESSION CLINICALCORRELATlON TESTING SETUP
CHAPTER 2
2
6 6 7 10 26 27
31 32 37 42 45
51
PREFACE ABSTRACT
OBJEC~VES: MEMODS: RESULTS:
CONCLUSIONS: INTRODUCTION: MATERIAL & METHOD: CLINICAL EVALUAllON:
E~EC~ROPHYSIOLOGICALEVALUATION: DATAANALYSIS: RESULTS: DISCUSSION:
CHAPTER 3
71
ABSTRACT
OBJEC~~: MEIHODS:
RESLZTS: CONCLUSIONS: INTRODUCTION: hfATERL4L.S & bIETHOD: DATAANALYSIS:
RESULTS: CLIMCALDATA: ELEClROPHYSIOLOGICALDATA DATA ANAL.YSES DISCUSSlON ANNEX 3.1 ANNEX 3 . 2
99
CHAPTER 4 SUMMARY AND
CONCLUSIONS
100
BIBLIOGRAPHY
103
iii
Preface The present thesis consists of four chapters.
In Chapter 1, I describe the
methods available to produce motor evoked potentials and detail the neurophysiologicalmechanisms involved. I then review the current knowledge about the electrophysiology phenomena associated with lumbar nerve root compression and ischemia. Finally I will demonstrate how nerve conduction and motor evoked potentials complement each other when evaluating root compression in the lumbar spine. Chapters 2 and 3 are comprised of scientific papers to be submitted in the very near future. Chapter 4 contains a detailed discussion on the importance of motor evoked potentials as a diagnostic and prognostic clinical tool. The limitations of the technique will also be discussed.
In compliance with the guidelines for thesis preparation and submission, the text of section 3 is cited below:
Candidates have the option of including, as part of the thesis, the text of one or more papers submitted or to be submitted for publication, or the clearly duplicated text of one or more published papers. These texts must be bound as an integral part of the thesis. If this option is chosen, connecting texts that provide logical bridges between the different papers are mandatory. The thesis must be written in such a way that it is more than a mere
collection of manuscripts; in other words. results of a series of papers must be integrated. The thesis must still conform to all other requirements of the "Guidelines for Thesis Preparation". The thesis must include: A Table of Contents, an abstract in English and French, an introduction which clearly states the rationale and objectives of the study, a review of the literature, a final conclusion and summary, and a thorough bibliography or reference list. Additional material must be provided where appropriate (e.g.
in
appendices) and in sufficient detail to allow a clear and precise judgment to be made of the importance and originality of the research reported in the thesis. In the case of manuscripts authored by the candidate and others, t h e candidate is required to make an explicit statement i n t h e thesis as t o who contributed to such work and t o what extent. Supervisors must attest to the accuracy of such statements at the doctoral oral defense. Since the task of the examiners is made more difficult in these cases, it is in the candidate's interest to make perfectly clear the responsibilities of all the authors of the co-authored papers.
Original contribution to knowledge: Neurogenic claudication is often seen in patients with lumbar spinal stenosis. The pathogenesis of neurogenic claudication is thought to be due to relative ischemia of cauda equina roots during exercise. It is important to distinguish between neurogenic claudication and vascular claudication
because of the different treatment modality of each condition. We studied the effect of transient ischemia brought on by exercise on motor conduction in patients suffering from lumbar spinal stenosis. We show that there is a statistically significant difference between the motor evoked potential latency time and the peripheral motor conduction time measured before and after the exercise in the patients with signs of neurological deficit (t-test pc0.0001). This difference was not found to be statistically significant in patients without neurological deficits (t-test p>0.05).
We also evaluated the sensitivity of motor evoked potentials in detecting motor conduction abnormalities before and after the onset of neurogenic claudication. We found that 65% of the patients with lumbar spinal stenosis had abnormal evoked potentials. This value increased to 76% after the onset of claudication.
Motor evoked potentials to the lower extremities have been shown to be altered in lumbar spinal compression. Animal experiments have studied the effect of acute compression on motor conduction along the cauda equina. They demonstrated the presence of a direct relationship between the removal of compression and the normalization of the motor conduction time. We studied the relationship between spinal decompression and motor conduction in humans. There was a gradual decrease in MEP latency time
over the six month period and at the end of the study only 14% of the patients had abnormal latency times.
We also evaluated the power of motor evoked potentials to predict clinical outcome in an attempt to develop a new follow-up protocol. We found that MEP at one month was able to predict clinical outcome at six months. Using the MEP data at one week and preoperatively increased the predictive power considerably. Motor evoked potentials have shown to be excellent outcome predictors following decompressive surgery.
They are more
sensitive than the clinical examination and their objective results are both reproducible and reliable.
Contribution of co-authors: The two manuscripts (chapters 2 and 3) are co-authored by Dr. Max Aebi, my supervisor.
He provided expert knowledge on the clinical aspects and
manifestations of lumbar spinal stenosis.
Being a spine surgeon, he also
helped me isolate research questions that had both clinical and surgical importance.
vii
Acknowledgments
I would like to express my thanks to my supervisor, Dr. Max Aebi, for his support
and guidance throughout my studies. I would like to thank Dr. Thomas Steffen for being such a challenging discussion partner.
I would like to thank past and present members of the laboratory for their friendship and help. I would like to thank Rick Rubin and Robert Cox for the LabView programs they created. My thanks also to Helen Athanassiadis for her managerial talents that helped me keep track of sll the patients.
Anthony
Tsantrizos provided excellent advice on statistical methods as well as editorial help with the manuscript, thank-you. Thanks go to Dr. Ronald Schondorf for his enthusiasm with establishing the MEP testing at the JGH. I would also like to thank Micheline Gagnon and Marie-Claude Lupien for all the help with the evoked potentials. My thanks also go to Danny Rizkallah for his help with the "tricky" graph.
I would like to thank all my friends for their moral support. Finally I would like to thank my family who has made this possible: my parents Gabi and Haifa' for all their unrelenting support and e-mails, my sister Hania and my brother Sami for their continuos encouragement.
viii
To my parents, Gabi and Haifa' thank-you
Abstract
Neurogenic claudication is often seen in patients with lumbar spinal stenosis. The pathogenesis of neurogenic claudication is thought to be due to relative ischemia of cauda equina roots during exercise.
We studied the effect of
transient ischemia brought on by exercise on motor conduction in patients suffering from lumbar spinal stenosis.
We found that there is a statistically
significant difference in the motor evoked potential latency time and in tho peripheral motor conduction time measured before and after exercise in the patients with signs of neurological deficit (t-test pc0.0001). This difference was not found to be statistically significant in patients without neurological deficits (ttest p>0.05). We also evaluated the sensitivity of motor evoked potentials in detecting motor conduction abnormalities before and after the onset of neurogenlc claudication. We found that 65% of the patients with lumbar spinal stenosis had abnormal evoked potentials. This value increased to 76% after the onset of claudication.
Motor evoked potentials to the lower extremities have been shown to be altered in lumbar spinal compression. Animal experiments have studied the effect of acute compression on motor conduction along the cauda equina.
They
demonstrated the presence of a direct relationship between the removal of compression and the normalization of the motor conduction time. In our study,
patients with lumbar spinal compression awaiting surgery were recruited and MEPs were performed pre-operatively and up to six months post-operatively. There was a gradual decrease in ME? latency time over the six month period and at the end of the study only 14% of the patients had abnormal latency times. We also evaluated the power of motor evoked potentials to predict clinical outcome in an attempt to develop a new follow-up protocol. We found that the motor evoked potentials measured at one month were able to predict clinical outcome at six months.
Resume
La claudication neurogene est souvent o b s e ~ e echez les patients souffrant de stenose lombaire. La pathogenese de cette claudication est due a I'ischemie relative presente au niveau des racines lombaires durant I'exercice.
Nous
avons etudie I'effet de cette ischemie transitoire sur la conduction nerveuse. Nous avons demontre I'existence d'une difference significative eatre le temps de latence du potentiel evoque moteur (TLPEM) et le temps de latence de la conduction nerveuse peripherique avant et apres I'exercice chez les patients ayant des signes de deficit neurologique.
Cette difference n'a pas ete
demontree chez les patients sans signes de souffrance neurologique. Nous avons egalement evalue la sensibilite des potentiels evoques a detecer des anomalies de conduction avant et apres la claudication. Nous avons trouve que 65 % des patients avec stenose lombaire avaient des potentiels evoqubs anormaux. Cette valeur est montee a 76 % apres claudication.
Les potentiels evoques moteurs aux membres inferieurs sont alteres en cas de compression lombaire. Des etudes sur des animaux ont montre la presence d'une relation directe entre la levee de la compression et la normalisation des potentiels evoques. Nous avons examine les potentiels evoques chez des patients avec
compression
lombaire
avant
et
apres
decompression
chirurgicale. Nous avons trouve qu'il y a une amelioration progressive des
xii
potentiels evoques rnoteurs au cours des premiers six mois postoperatoires. A la fin de ces six rnois, seulernent 14 % des patients presentaient des potentiels alteres. Nous avons egalernent evalue la capacite des potentiels evoques a predire I'etat clinique a six rnois. Nous avons trouve que les potentiels evoques rnesures a un rnois ont une excellente valeur predictive de IUtat clinique a six rnois.
xiii
Motor conduction alterations in lumbar spinal stenosis
Chapter 1
Motor conductionalterations in lumbar spinal stenosis
Neural conduction and evoked potentials: Neural conduction along the peripheral pathways has been studied in great detail. The bulk of our current knowledge of the electrophysiological processes involved in neural conduction stems from animal studies on the peripheral nervous system. The first clues about how action potentials are generated came from the work of Cole and Curtis (Cole & Curtis. 1939) on the squid giant axon. A decade later, Hodgkin and Katz found that the amplitude of the action potential is reduced when the external Na+concentration is lowered (Hodgkin & Katz, 1949). They also found that the rate of repolarization during the falling phase of the action potential is reduced if the external K+ concentration is increased. Based on these experiments we now know that the action potential is initiated by depolarization of the membrane which opens voltage-sensitive sodium channels and the influx of sodium produces the rising phase of the action potential. The nervous system conveys information by means of action potentials which originate in the cell body and travel along the nerve fibers. To assess motor conduction, the muscle action potentials are recorded after stimulation of the mixed nerve supplying the target muscle. Sensory conduction studies orl the other hand depend on recording neural impulses after stimulation of the nerve through surface or needle electrodes. Normal neural conduction is needed in order to obtain a normal evoked response.
In the case of motor evoked
potentials, a normal neuromuscular junction is also needed.
Motor conduction alterations in lumbar suinal stenosis
The earliest forms of muscle response recordings were done by H,=rmann von Helmholtz in 1850 (Helmholtz, 1850).
He stimulated the median nerve
electrically and recorded the mechanical response of the muscle twitch in the thumb. The shape of the response and the conduction velocity he measured are amazingly close to currently accepted normal values (median nerve conduction velocity of 61 +I-5,l mls). Later, Hermann stimulated the brachial plexus and recorded an electric wave-like response from the surface of the forearm, which he called action potential (Hermann, 1878a; Hermann, 1878b). In 1895, Burdon Sanderson showed that this wave of excitation preceded the mechanical response (Burdon Sanderson, 1895).
The study of muscle action potentials did not take off until the development of sensitive recording equipment. Using technology developed by Braun (Braun, 1897) and Einthoven (Einthoven, 1903), Forbes and Thacher used an electron tube to amplify the action potential and a string galvanometer to record it (Forbes & Thacher, 1920). Two years later, Gasser and Erlanger introduced the cathode-ray oscilloscope, which eliminated the mechanical limitation of galvanometers (Gasser & Erlanger, 1922). Piper in 1909 recorded compound muscle action potentials (CMAP) instead of muscle twitch for the determination of motor nerve conduction (Piper, 1909).
Hodes, Larrabee, and German
(Hodes, Larrabee, & German, 1948) calculated the nerve conduction velocity at different levels in normal and neurologic patients.
Around the same time,
Kugelberg used nerve stimulation to study the effect of ischemia on nerve
Motor conduction alterationsin lumbar spinal stenosis
excitability (Kugelberg, 1944). Cobb extended this work by demonstrating slowed action potential propagation in the ischemic nerve (Cobb & Marshall, 1954). The development of these conventional methods of nerve conduction studies mainly dealt with diseases affecting the distal por!ion of the peripheral nerve system. They seldom contributed to the investigation of the remainder of the nervous system. It was only later that new neurophysiological techniques emerged that helped evaluate the function of these less accessible anatomic regions.
Of these, the most extensively used have been the H reflex of
Hoffmann (Hoffmann, 1918; Hoffmann, 1922), the F wave of Magladery (Magladery & McDougal, 1950), and the blink reflex of Kugelberg (Kugelberg, 1952).
The study of the central nervous system function only started much later because of the technical difficulty involved. The technique of signal averaging developed by Dawson and Scott (Dawson & Scott, 1949) helped lay the basis for peripheral sensory conduction studies initially and for sornatosensory evoked potentials (SSEP) later on. The use of SSEP has expanded after the development of computer averaging and the subsequent correlation with laboratory and clinical data (Perot, 1973). It has now become standard followup procedure for various conditions (Albanese, Spadaro, Lubicky, & Henderson, 1991; Aminoff, 1984; Aminoff, 1988; Ducati & Schieppati, 1980; Eisen & Odusote, 1980; Ganes, 1980; Jones, Parry, & Landi, 1981; Machida, Asai, Sato, Toriyama, & Yamada, 1986; Mandell, De, Johnson, & Bennett, 1988;
Motor conductionalterations in lumbar spinal stenosis
Seyal, Sandhu, & Mack, 1989; Siivola, Sulg, & Heiskari, 1981; Small, Matthews, & Small. 1978; Yiannikas & Walsh, 1983). In addition to clinical evaluations, SSEPs are being used intra-operatively to monitor spinal cord function during surgical procedures on the spine (Apel, Marrero, King, Tolo, & Bassett, 1991; Bieber, Tolo, & Uematsu, 1988; Dawson, Sherman, Kanim, & Nuwer, 1991; Heiskari, Siivola, & Heikkinen, 1986; Loder, Thomson, & LaMont, 1991; York, Chabot, & Gaines, 1987).
Despite the wide use of SSEPs and their general consideration as a proxy for the entire spinal cord, they do not provide any direct measure of motor function. There have been reports of paraplegic patients with normal SSEP (Ben-David, Haller, & Taylor, 1987; Ginsburg, Shetter, & Raudzens, 1985; Lesser et at., 1986; Letts & Hollenberg, 1977). This outcome is not altogether surprising when one considers the anatomic separation of the sensory columns from the corticospinal motor pathways by a distance of a few millimeters. The posterior and anterior portions of the spinal cord also have separate blood supplies. The posterior columns are supplied by the posterior longitudinal spinal arteries while the corticospinal tracts are supplied
by the anterior spinal artery
(Williams, Warwick, Dyson, & Bannister, 1989). For this reason, it became evident that there was a need to evaluate motor conduction as well as sensory conduction.
Motor conductionalterations in lumbar spinal stenosis
Central motor conduction evaluation was only made possible with the development of transcranial electrical stimulation by Merton and Morton in 1980 (Merton & Morton. 1980). They applied two electrodes to the scalp using a bipo!ar technique. The anode, which is the stimulating electrode, is positioned over the appropriate region, while the cathode is applied frontally or on the vertex. This type of montage requires currents between 350 and 1000 mA discharged by special stimulators utilizing a brief capacitor discharge (Merton & Morton, 1980). Rossini developed another technique for transcranial electric stimulation (Rossini, 3, & Stanzione, 1985a) which requires a lower intensity current (70 to 100 mA). His unipolar technique deploys a number of pericranial electrodes secured to the scalp, and a unique stimulating anode positioned over the region to be stimulated. But the use of electric stimulation to produce motor evoked potentials (MEP) has been over-shadowed by the development of transcranial magnetic cortical stimulation. In 1985, Barker and co-workers from the University of Sheffield succeeded in producing a muscular response in the hand following transcranial magnetic stimulation of the motor cortex (Barker, FreestonJL, Jalinous, Merton, & Morotn, 1985).
Magnetic stimulation of the nervous system: Background
In 1831, Michael Faraday observed that a changing magnetic field induced a current in a conductor lying in the field. The induced current, also known as
Motor canduction alterations in lumbar spinal stenosis
eddy current, is the first derivative of the current that produced the magnetic field. In 1896, d'Arsonval demonstrated that a changing magnetic field could stimulate excitable tissue (d'Arsonval, 1896). He reported phosphenes, vertigo, and in some persons, syncope after placing the head through ail alternating magnetic field.
Magnetically induced phosphenes became the subject of
considerable interest when alternating currents were being developed for commercial use. Magnussen and Stevens carried out a series of studies on the importance of frequency and field strength in producing phosphenes (Magnussen & Stevens. 1911). They reported that for a given field strength, the phosphenes appeared brighter with 20-30 Hz currents. Polson et al. Used a flat 35 mm diameter coil to stimulate the median nerve in humans and recorded the compound muscle action potentials from the thumb muscles (Polson, Barker, & Freeston, 1982). It was Barker in 1985 who was the first to stimulate the motor cortex transcutaneously using an alternating magnetic field (Barker et al., 1985).
Principles of magnetic induction
Faraday's law states that a current is induced in a conducting loop if the magnetic flux linking the loop changes. The induced electromotive force (EMF) in a single loop is given by EMF = - d@$dt
(1.1)
Motor conduction alterations in lumbar spinal stenosis
where EMF is the electromotive force (in volts) , d@$dt is the change in the magnetic field over time. Lenz's law completes Faraday's law and states that the sense of the induced current is such as to oppose the change in flux which produces it. Additionally, a small coil with (n) turns may be treated as (n) single loops and the total electromotor force (EMF,) induced is given by
-
EMF, = n d@$dt
(1.2)
The intensity of the magnetic field (i.e. the flux density (B)), is measured in teslas (T). The total flux
(a)is the integral of the flux density across the area (A) which
contains the flux. Therefor EMF = - d@$dt = d(B x A)/dt
(1.3)
The total flux generated by the coil is function of the number of turns in the coil (n), the current in each turn (I), and the area of the coil Q=(nxA)xI
(1.4)
Because total flux and current are proportional, the rate of flux change is proportionalto the rate of current change. Therefore, Faraday's law means that the electric field is also proportional to the changing current in the coil. This specific case of the Faraday's law ignores the magnetic field that acts as the carrier, and simplifies the analysis of the coil. The induced voltage actually appears in each turn of the coil because each turn encloses the same amount of flux. Therefore the voltage induced in the coil is EMF = rate of change of current (1.5)
Motor conduction alterations in lumbar spinal stenosis
EMF=(nxAxdVdt)xn
(1-6)
EMF = (n2x A) x dl/dt
(1.7)
where (n x A x dVdt) is the generated flux. The term (nZx A) is the amount the coil resists the changing current, termed coil inductance (L). The energy the coil stores (E,)
is
E,,, = L x l2 The energy supplied to the coil through a capacitor E (),
(14 is
E,=CxV2
(1.9)
where C is the capacitance and V the electric potential across the capacitor. If most of the energy can be transferred from the capacitor to the coil without resistive loss, then equating the energies frorr equations 1.8 and 1.9 gives CxVZ=LxI2
(1.10)
When the coil and the capacitor are connected through the switch, the energy moves rapidly from the capacitor to the coil creating a large magnetic field, then the coil transfers the energy back to the capacitor. If the switch remains closed, the energy moves back and forth from coil to capacitor until it is entirely consumed by resistive loss. The frequency of oscillation (f) is f=
llrn
(1.11)
and the time (1) required for one period is l / f or t=
m
(1.12)
To depolarize a nerve, the current should be strong enough (1-2 pC/cm2) and of sufficient duration (100
- 300 ms).
For a convenient electric stimulation this
Motor conduction alterotiw in lumbar spinal stenoss
would be 10 mA for 100 psec. Increasing either the duration or the amplitude of the stimulation will increase the effectiveness Effectiveness = V,,
xt
(1.13)
For the magnetic stimulator, the duration is fixed by the capacitors and the coil inductance, and so only the amplitude of the stimulus can be varied. By solving for ,V ,,
and t, we get Effectiveness = V,
x
fi
this term is the square root of the energy in equation 1.9.
(1.l4)
Therefore the
effectiveness does not include the inductance, the Teslas generated by the coil,
or the configuration of the current.
Electrophysiology of excitation
Whether excitable tissue is stimulated with conductive or capacitive electrodes, or with a time-varying magnetic field to induce the stimulating current, the same law of excitability applies. The law is embodied in the strength-duration curve described by Lapicque in 1909 (Lapicque, 1909; Lapicque, 1926). The law states that the shorter the duration of the current pulse, the higher the current intensity needed to achieve excitation.
Across the enveloping membrane of an excitable cell, there appears a metabolically driven ionic gradient, the result of which is the resting membrane
Motor conduction alterations in lumbar spinal stenosis
potential (RMP). The charge distribution is such that the exterior of the cell is positive with respect to the interior (Hodgkin & Katz, 1949). The transmembrane potential is less than 100 mV in most excitable cells.
When the resting
membrane potential is reduced to the threshold potential by the stimulating current, the membrane permeability suddenly increases and a regenerative process occurs with a transmembrane flux of ions, the result of which is a characteristic reduction, reversal, and restoration of the transmembrane potential. The time course of this event (i.e. action potential) depends on the type of cell. Figure 1.1 illustrates the action potential initiated by the delivery of a rectangular pulse of current I and of duration d, which diminishes the transmembrane potential by reducing the charge on the capacitance of the cell membrane. The resulting reduction in transmembrane potential is what causes the cell to be excited.
During depolarization and until late repolarization, the cell is inexcitable and does not respond to any external stimulation. This period is called the absolute refractory period (ARP). The duration of the action potential is a rough indicator of the refractory period (Hodgkin & Huxley, 1952). The duration of the action potential in a large mammalian nerve fiber is approximately 0.5 ms. If the excitability of a cell is tested at different instants after the onset of the action potential, it is found that during the downslope of the action potential there is first the ARP where no excitation is possible. Following this period, excitability returns first to a suprathreshold stimulus, then for a subthreshold stimulus and
Motor conductionalterations in lumbar spinal stenosis
finally to a threshold stimulus. Therefore it follows that if the stimulus is a train of pulses with a peliod that is shorter than the ARP, the cell will respond with a submultiple of the stimulus frequency.
STIMULUS = - I
Id1
Figure 1.1: The changes in membrane potential after subjecting the nerve cell to an electric stimulus with an intensity (I) and a duration of (d). The stimulus reduces the resting membrane potential (HMP) to the threshold potential (TP) and triggers the action potential. The cell can only be depolarized again after the membrane potential falls below the absolute refractory period (ARP) indicator.
Motor conductionalterations in lumbar spinal stenosis
As stated previously, for a cell to be excited, a current pulse must reduce the resting membrane potential to the threshold potential. Therefore to achieve excitation the current must be intense enough and last long enough to bring the resting membrane potential to the threshold potential.
Lapicque demonstrated empirically that the excitability of all tissues follows a similar curve revealed by a plot of threshold current (I) versus pulse duration (d) (Lapicque. 1909; Lapicque, 1926). The expression for the Lapicque strengthduration curve is I= b (1 + cld)
(1 .15)
where b is the long-duration current (rheobase), and c is a tissue-dependent constant called the chronaxie (defined as the duration where the threshold current is 2b).
Figure 1.2 describes the Lapicque strength-duration curve
(normalized by dividing the duration by the chronaxie, c). The strength-duration curves for all excitable tissues have a similar fonn, the difference being expressed by the chronaxie. Note that the chronaxie describes the duration region where the current required for excitation rises steeply with decreasing duraiion.
Motor conduction alterations in lumbar spinal stenosis
Figure 1.2: The Lapicque strength-durationcurve for a motor nerve, normalized
by deviding the duration axis by (c), the chronaxie.
Motor conduction alteralions in lumbar spinal stenosis
When a time-varying magnetic field is applied to biological tissue such that the resulting induced current is of appropriate amplitude and duration as stated in Lapicque's law, neuromuscular tissue can be stimulated as though the current had been applied via electrodes. Amassian compared magnetic stimulation with electric stimulation in the peripheral nervous system. He used a round coil to stimulate the ulnar nerve at the elbow and recorded the hypothenar compound muscle action potential (CMAP) response (Amassian, Maccabee, & Cracco, 1989b). He concluded that magnetic stimulation can produce the same response as bipolar or tripolar electrical stimulation. But he noticed that coil orientation had an important effect on the CMAP amplitude. Maccabee et al (Maccabee, Amassian, Cracco, & Cadwell, 1988) analyzed this phenomenon more closely and found that the most effective coil orientation was the orthogonal-longitudinal (with the plane of the coil aligned with the long axis of the nerve). These finding are in agreement with classical findings of minimal excitation if the stimulation current penetrates the axon transversely (Rushton, 1927). Maccabee noted that one disadvantage of magnetic coil stimulation is the imprecision in defining exactly where the distally propagating nerve impulse originates (Maccabee et al., 1988). He found that in different subjects, using maximum output and orthogonal or tilted (to 45 degrees) longitudinal orientations, the calculated site of excitation in the median nerve varied 2-15 mm distal to the midpoint of the contacting edge of the magnetic coil.
Motor conductionalterations in lumbar spinal stelosis
Electric stimulation of the cortex gives rise to a series of descending volleys in the spinal cord which probably are analogous to the D- and I-waves described by Patton in 1954 (Patton & Amassian. 1954). Studies of single motor unit behavior in muscle (Ugawa, Rothwell, Day, Thompson, & Marsden, 1989) and direct recordings from the spinal epidural space during surgery (Boyd et al., 1986; Inghilleri, Berardelli, Cruccu, Priori, & Manfredi, 1989; Katayama, Tsubokawa, Maejina, & Yamarnoto, 1988) appear to confirm this. In Patton's study, surface stimulation of the cat cortex produced multiple positive waves that were recorded from the medullary pyramid and corticospinal tracts. The first of the descending waves was labeled D-wave (direct wave) as it appeared to be due to direct activation of the corticospinal system in the white matter. The later waves were referred to as indirect waves (I-waves) because they appeared to be generated within the motor cortex, activating the pyramidal cells via synaptic connections. It was later shown that the D and I waves traveled the same pyramidal axon and that the I waves were therefore due to reexcitation of the same pyramidal neuron (Kemell & Wu, 1967). Discrete intracortical stimulating techniques were further refined by Asanuma (Asanuma & Sakata. 1967) who demonstrate the simple but overlapping relationship between the outputs of small clusters of cortical neurons and individual limb muscles. Later studies by Jankowska (Jankowska, Padel, & Tanaka, 1975) reaffirmed these findings and showed that intracortical stimulation produced only I waves and that D waves were propagated from the initial segment of the pyramidal tract neuron. These studies have demonstrated in great detail the nature of the motor cortex
Motor conduction alterations in lumbar spinal stenosis
response to suriace or intracortical stimulation and the complexity of its intracortical connections.
They did not, however, reveal how the brain
organizes or executes movement.
The major studies of brain stimulation in humans began with the detailed and systematic surface cortical explorations of Penfield (Penfield & Jasper, 1954) on patients undergoing brain surgery. In these circumstances, his observations were limited to documenting the motor cortical somatotopy.
When Merton
(Mertcn & Morton, 1980) devised his special electrical stimulator and was able to produce transcranial cortical stimulation, he and others after him found similarities between many of the results obtained from cortical stimulation in humans and in animals (Berardelli, Inghilleri, Rothwell. Cmccu, & Manfredi, 1991; Burke et al., 1993; Chapman & Yeomans, 1994; Chomiak, Dvorak, Antinnes, & Sandler, 1995; Cracco, Amassian, Maccabee, & Cracco, 1989; Inghilleri, Berardelli, Cruccu, & Manfredi, 1993; Katz, VandenBerg, Weinberger, & Cadwell, 1990; Liu, Branston, Kawauchi, Jellinek, & Symon, 1992; Mills & Murray, 1986; Rossini et al., 1994; Rothwell et al., 1994; Rothwell, 1991). It is remarkable that these similarities were found despite the complexity of the motor cortex and its corticospinal terminations in the spinal cord. Because transcranial electric stimulation has been studied more extensively than magnetic stimulation, and because it has a more focal point of application, it will be exposed first and then its results extrapolated to magnetic stimulation.
Motor conduction alterations in lumbar spinal stenwis
The site of electric stimulation appears to be at or near the motor cortex. It was found that arm muscles were more readily stimulated when the stimulating electrode was placed more laterally and the leg muscles when the electrode was place more towards the vertex (Rossini, Marciani, Caramia, Roma, & Zarola, 1985b; Rothwell et at., 1994). Unless stimulation was occurring at or near the cerebral cortex, such localization would unlikely occur. As to the effects of cortical stimulation on spinal motoneurons, they are probably mediated by many direct and indirect descending pathways (Berardelli et al., 1991; Cracco, 1987; lnghilleri et al., 1993; Rothwell et at., 1994; Rothwell, 1991; Thompson et al., 1991; Ugawa, Genba-Shimizu, & Kanazawa, 1995; Zentner, 1989). However, there is good evidence that the pathway responsible for the onset of EMG activity is composed of the fast conducting fibers of the corticomotoneuronal component of the corticospinal tract.
The estimate of
corticospinal conduction velocity after cortical stimulation is in the order of 65m/s (Marsden, Merton, & Morton, 1982; Rossini et al., 1985a; Snooks & Swash, 1985). The latency of the responses in the contracting muscle, for all intensities of cortical stimulation is remarkably stable, only varying by no more than 1 to 2 ms over a series of single trials (Rothwell et al., 1987). This is compatible with the intervention of only one to two synapses between the cortical output neuron stimulated and the neuromuscular junction. This does not suggest that other descending pathways may not be activated by the cortical stimulus, either directly or synaptically. lmpulses from other pathways may contribute to the later phases of the compound motor action potentials. The
Motor conduction alterations in lumbar spiml stenosis
reticulospinal tract has both monosynaptic and polysynaptic connections with the spinal cord. It may conduct rapidly in animals, but is distributed bilaterally to innervate predominantly proximal muscles in humans (Peterson, Pitts. & Fukushima, 1979). The lateral vestibulospinal pathways are also monosynaptic and polysynaptic, can conduct rapidly, but innervate the spinal cord predominantly on the ipsilateral side (Nyberg-Hansen & Mascitti, 1964). Because our knowledge of the functional anatomy of the descending pathway in man is limited, the term corticomotoneuron introduced by Bemhard in 1954 (Bernhard & Bohm, 1954) appears to be the most accurate description of the pathway mediating the earliest effects of cortical stimulation.
To analyze which structure is stimulated when the magnetic coil is used, one may compare the motor response and the latency time of cortical magnetic stimulation to that of electric stimulation. It has been reported that the motor evoked potential latency time obtained with magnetic stimulation exceeded that obtained with electrical stimulation by on average 2 ms (Amassian, Cracco, & Maccabee, 1989a; Amassian et at., 198913; Amassian, Quirk, & Stewart, 1990; Day, Dick, Marsden, &Thompson, 1986; Hess, Mills, & Murray, 1987; Maertens de Noordhout et al., 1992; Mills, 1991; Mills, Murray, & Hess, 1987; Rothwell, 1991). Additionally, this reported difference in latency time seems to disappear with higher intensities. The possibility that this latency difference is because magnetic stimulation activates a different slower descending pathway was excluded by Day et al (Day, Thompson, Dick, Nakashima, & Marsden, 1987)
Motor conduction alterations in lumbar spinal stenosis
who demonstrated that single motor units exhibited similar differences in latency. A latency difference of 2 ms in the arrival of excitation at the spinal motoneurons is unlikely due to magnetic stimulation occurring deeper within the brain either. Assuming that the neural fibers are conducting at only 50 d s , this would require activation of the descending pathway at the level of the pons. If this were the case, then even low intensity magnetic stimulation would also be expected to stimulate the cranial nerves directly at that same level; this is not the case. Only very high intensities have been reported to activate these nerves directly (Maccabee et al., 1991a). Another possible explanation for the latency difference is that magnetic cortical stimulation activates a slower conducting descending pathway than anodal stimulation. Although this can be true, the absence of a known anatomical descending pathway that can conduct at a slower speed makes this hypothesis unlikely. In the corticospinal pathway, there is a small diameter component. These fibers where shown to have a conduction velocity of 10-15m/s in the cat (compared with 60-70 d s for the large pyramidal neurons). Such a difference in conduction velocities is too great to produce a small latency difference of 2 ms over the central motor pathway.
The most plausible explanation comes from Amassian and co-
workers (Amassian, Cracco, Maccabee, Bigland, & Cracco, 1991a; Amassian, Eberle, Maccabee, & Cracco, 1992; Amassian et al., 1989b) who suggest that the coil orientation is the clue to solving the 2 ms mystery. Based on Rushton's work on electrical nerve stimulation (Rushton, 1927) and Maccabee's work on coil orientation in the peripheral nervous system (Maccabee et al., 1988;
Motor conduction alterations in lumbar spinal stenosis
Maccabee, Amassian, Cracco, Eberle, 8 Rudell, 1991b; Maccabee, Amassian, Eberle, & Cracco, 1993), they measured the latency time with the coil placed in three specific configurations over the motor cortex (figure 3.1).
The
conventional tangential orientation at the vertex (figure 1.3 right) couples nearly one half of the magnetic flux to the volume conductor of the head, but the predominant direction of induced current is tangential (transverse to most of the radially-oriented corticospinal neurons and their trajectory in white matter). Only a relatively small number of corticospinal neurons in the anterior bank of the central sulcus would be appropriately oriented for direct stimulation (Kuypers, 1981). By contrast, corticocortical axons, especially those derived from the premotor cortex and postcentral gyrus, would be directly excited by the lateral components of the induced current. The deep tangential fibers in the motor cortex would also be excited by the tangentially oriented current. The anterior and posterior components of the current could, if of sufficient magnitude, excite the callosal axons (Amassian et al., 1993a; Amassian et al., 1993b; Amassian et al., 1991b). Regardless of which of these presynaptic inputs are excited by the tangentially-oriented coil, the consequence is a minimum of one synaptic delay plus minor presynaptic conduction time added to the delay of the corticospinal discharge, presumably accounting for the finding of a CMAP latency 2 ms longer than that elicited by electrical stimulation. By contrast, placing the magnetic coil in a sagittal orientation or a coronal orientation (figure 1.3 left), the induced current flow had a significant component parallel to the corticospinal neurons and their trajectories, rising the possibility
Motor conduction alterations in lumbar spinal stenosis
of their direct excitation. Using this configuration, Amassian et al (Amassian et al., 1991a) found that the latency time of CMAP to magnetic stimulation and to electric stimulation was identical. This of course would suggest that the central excitation pathways to the motoneuron are similar.
Motor conductionalterations in lumbar spinal stenosis
Coil at vertex
Cerebral hemispheres (coronal vue)
Figure 1.3:
Different coil orientations in relation to cerebral hemispheres.
Sagittal and coronal orientations (left) induce current fiow that is oriented correspondingly.
The induced currents in these two orientations are
appropriately oriented to excite radially directed corticospinal neurons. The conventional tangential orientation at the vertex (right) induces tangentially oriented currents which preferentially excites corticocortical axons running along the anteroposterior axis.
Motor conductionalterations in lumbar spinal stenosis
Amassian followed up on his work with a more extensive animal study to determine the type and mode of neuronal excitation in the cerebral cortex by recording corticospinal responses to magnetic stimulation in the monkey (Amassian et al., 1990). He placed electrodes in the lateral column so that he can measure both direct and indirect discharge. He reported that an orthogonal coil orientation elicited only direct discharges at weak intensities, and that there was no difference in latency when compared with electrical stimulation. With higher stimulation intensities he was able to elicit indirect discharges.
By
contrast, with tangential orientation at the vertex, indirect discharges alone were elicited until the stimulus intensity was sufficiently increased to elicit a direct discharge.
In conclusion, the characteristics of the magnetic field and the
electric current induced by it depend on the physical properties and orientation of the magnetic field itself. The magnetic field orientation yielding a major component of current flow parallel to the long axis of the neuron excites it much more readily than one yielding current flow transversely across. A traditional tangential coil orientation appears to stimulate corticocortical neurons whereas a coronal or sagittal coil orientation produces true corticospinal stimulation. One drawback to placing the coil in the sagittal or coronal orientation was that it produced involuntary contraction of the facial muscles that some subjects found unpleasant (Tassinari et al., 1990). In terms of descending pathways, magnetic stimulation appears to preferentially activate pyramidal tract cells via synaptic mechanisms when the coil is placed over the vertex. In terms of D and I waves, magnetic stimulation over the vertex produces essentially I waves, and only at
Motor conduction alterations in lumbar spinal stenosis
very high intensities or with coronal or sagittal coil orientation do we obtain D waves.
On the cellular level, cortical stimulation appears to engage mainly the soma and the initial axonal portion of the large Betz cells, whose bodies are buried in the fifth layer of the motor cortex. These are more excitable than the type II Golgi interneurons because of the greater number of shafts contained in the most distal portion of their apical dendrites, projecting toward the superficial cortical layers (Boyd et al., 1986; Ranck, 1975). At the peripheral nerve level, MEPs are mediated by the fast-propagating motor fibers.
This has been
demonstrated with needle recordings during cortical stimulation by Rossini et al (Rossini, Cararnia, & Zarola, 1987).
Motor conductionalterations in lumbar spinal stenosis
The central and the peripheral motor pathways
The descending motor pathway is made up of two anatomically distinct portions; the central motor pathway that extends from the cerebral cortex to the anterior horn cells in the spinal cord, and the peripheral motor pathway that extends from the anterior horn of the spinal cord to the neuromuscular junction. Motor evoked potentials allow us to study the entire motor pathway.
This has its
clinical importance, however, analyzing the two components individually also has important diagnostic capabilities. This is particularly true in the lumbar spine, where the spinal roots exit from the spinal cord a few levels above their exit from the spinal canal. Neurophysiologically, the latency time is the variable used to study and follow motor conduction. The motor evoked potential latency time (MEPLT) is made up of the central motor conduction time (CMCT) and the peripheral motor conduction time (PMCT).
The MEPLT is obtained by
stimulating the motor cortex and recording the CMAP latency time. The PMCT can be measured in two different ways; the direct method by stimulating the spinal roots electrically (or magnetically) in an orthodromic fashion, and the indirect method by antidromic stimulation of the peripheral nerve and recording F-waves. Once the two variable are known, the third can be calculated as follows:
-
CMCT = MEPLT PMCT
Motor conduction alterations in lumbar spinal stenosis
Measuring the peripheral motor conduction time
Stimulating the spinal roots may seem the logical way to measure PMCT, but the anatomical disposition of the spinal cord within the bony confines of the spine makes this task technically challenging.
Electric root stimulation is
performed using surface electrodes, with the cathode placed over the spinal process and the anode about 5 cm cranially. In the lumbar roots, the cathode is placed over the root exit zone and the anode 2-3 vertebral segments more rostra1 (Claus. 1989; Maertens de Noordhout, Rothwell, Thompson, Day, & Marsden, 1988; Mills & Murray, 1986).
The latency of electrically elicited
responses is about 1.2 ms shorter than the spine-to-muscle motor conduction estimated using F wave measurement (indirect PMCT measurement). Assuming that the conduction velocity in the axon is 60 mls, then the stimulation site is about 6-8cm distal to the spinal cord. Electrical stimulation over the spine induces a powerful and sometimes painful contraction of the paraspinal muscles. Magnetic root stimulation is achieved by placing a small magnetic coil over the spinous process such that the stimulation current is clockwise for right side stimulation and counterclockwise for left side stimulation. Here again, it has been shown that the area of stimulation is in the vicinity of the neuroforamina (Evans. Daube, & Litchy. 1990; Maccabee et al., 1991b; Maccabee et al., 1991~).
Motor conduction alterations in lumbar spinal slenosis
The indirect method used to measure PMCT is based on peripheral nerve stimulation and the production of an orthodromic nervous impulse resulting in a muscular contraction or M wave, and an antidromic nerve impulse and an F wave. It was Magladery and McDougal who first described this phenomenon in 1950 (Magladery & McDougal, 1950). They found that a supramaximal electric
stimulation delivered to a nerve often elicited a late response in the innervated muscle. They designated this late response the F wave presumably because they initially recorded it from the foot muscles. The F wave occurs after the direct motor potential. Its latency decreases with more proximal stimulation while the M wave latency increases. This indicates that the impulse destined to elicit the F wave first travels away from the recording electrode towards the spinal cord before it returns to activate the distal muscles. The F wave is elicited in approximately 1 to 5 percent of antidromically activated motor neurons regardless of their peripheral excitability of conduction characteristics. The conduction time from the stimulus point to the spinal cord and back equals F -M where F is the F wave latency time and M is the M wave latency time. Subtracting an estimated delay of 1.0 ms for the tum-around time at the cell and dividing by two
-
(F M -1)/2
represents the conduction time along the proximal segment from the stimulus site to the spinal cord (figure 1.4). Although the exact turn-around time at the anterior cells is not known in man (Trontelj, 1973), animal studies indicate a delay of nearly 1.0 ms (Lloyd, 1943; Renshaw, 1941). The absolute refractory
Motor conductionalterations in lumbar spinal stenosis
period of the fastest human fibers lasts about 1 ms or slightly less (Kimura, Yamada, & Rodnitzky, 1978). The recurrent discharge generated during the refractory period cannot propagate distally beyond the initial segment of the axon.
In evaluating the minimal refractory latency, therefore, it seems
appropriate to assume a turn-around time of at least 1 ms. The PMCT can be calculated according to the following formula: PMCT=(M+F-1)12 this time represents the nervous conduction time from the anterior horn to the muscle (Figure 1.4).
The F wave is usually inhibited in conditions causing a reduction of spinal excitability, such as flaccidity associated with upper motor neuron syndromes (Drory, Neufeld, & Korczyn, 1993; Fierro, Raimondo, & Modica, 1990), REM sleep (Ichikawa & Yokota, 1994), cataplexy attacks (Yokota, Shimizu, Hayashi, Hirose, & Tanabe, 1992), or cerebral stimulation (Fisher & Penn, 1978). In addition, the F wave suffers from inherent latency variability from one trial to the next. In order to determine the F wave latency, a large number of waves are produced and the shortest latency is then used. F waves on the other hand are most effective when there is a unilateral disorder affecting a single nerve. They also help characterize polyneuropathies in general and those associated with proximal disease in particular (Kimura, Yamada, & Stevland, 1979).
Motor conduction alterationsin lumbar spinal stenosis
Muscle
F wave Neuron
+-------------
-.-------------I I I
Stimulus
I
Figure 1. 4: The latency difference between the F wave and the M wave represents the passage of a motor impulse to and from the cord through the proximal segment. The 1 ms represents the turn-around time delay in the motor neuron pool (*).
Motor conduction alterations in lumbar spinal stenosis
The effects of compression and
ischemia
on neural
conduction in the lumbar spine
With the spinal cord ending at the L1112 level, the lower lumbar spinal roots have to run through the spinal canal from the point they leave the spinal cord until they exit from the spinal column through the intervertebral foramen. The spinal roots are vely specialized neural structures.
They constitute the
anatomical connection between the central and the peripheral nervous system. Their initial localization within the spinal canal makes them anatomically more related to the central nervous system.
However, when considering their
functional properties, they are more related to the peripheral nervous system. The spinal roots do not have the same protective connective tissue sheaths that are present around the peripheral nerves. They do however benefit from the protective bony envelope that is the spinal column. It has been suggested that the absence of the protective connective sheath makes them more susceptible to mechanical deformation, compression, and ischemia (Rydevik, Brown, & Lundborg, 1984). It is important to understand the special anatomy of the spinal nerve roots and how compression and ischemia are related in the lumbar spine.
Motor conductionalterations in lumbar spinal stenosb
Neural anatomy of the lumbar spine
The lumbar spine contains the final portion of the spinal cord (conus medullaris) from which extends the filum terminale. In addition, there are five pairs of lumbar roots, five pairs of sacral roots, and one pair of coccygeal roots present in the lumbar spinal canal. The first lumbar root leaves the spinal cord in the lower thoracic region and travels through the spinal column until it exits through the neural foramen at the LllL2 level. There are two different types of nerve roots within the lumbosacral spine; the ventral motor roots and the dorsal sensory roots (figure 1.5). The cell bodies of the motor axons are located in the gray matter in the spinal cord from where they leave it from the ventral side. The dorsal roots mainly comprise of sensory afferent axons whose cell bodies are found in the dorsal root ganglion (figure 1.5). The dorsal root ganglia are located in or close to the intervertebral foramina (Hasue, Kunogi, Konno, & Kikuchi, 1989). Unlike the nerve roots, the dorsal root ganglia are not enclosed by the cerebrospinal fluid (CSF) and the meninges. Instead they are enclosed by both a multilayered connective tissue sheath similar to the perineurium of the peripheral nerve and a loose connective tissue layer, the epineurium (McCabe & Low, 1969).
The spinal nerve roots are surrounded by CSF and enclosed within the meninges (Rauschning, 1983). The most central nerve roots are located within a common dural cylinder and are usually referred to as intrathecal nerve roots.
Motor conduction alterations in lumbar spinal stenosis
The nerve roots that are about to leave the spinal canal are located in separate extensions of the spinal dura, the root sleeves. This location of the nerve roots is generally called extrathecal. In each root sleeve there is a motor and a sensory nerve root coming from the same segment. The root sleeve with its contents of meninges, CSF, and nerve tissue is referred to as the nerve root complex (Rauschning, 1987).
When the nerve root approaches the intervertebralforamen, the root sleeve gradually encloses the nerve tissue more tightly. The subarachnoid space and the amount of CSF surrounding each nerve root pair will thus become gradually reduced in the caudal direction. Compression injury of a nerve root may induce an increase in permeability of the endoneurial capillaries which may result in edema formation (Rydevik, Myers, & Powel, 1989). This can lead to an increase in the intraneural pressure with a subsequent impairment of the nutritional transport to the nerve roots (Low, Dyck, & Schmeltzer, 1982; Lundborg, Myers, & Powell, 1983). Such a mechanism might be particularly important at locations
where the nerve roots are tightly enclosed within the connective tissue. There is an enhanced risk of an entrapment syndrome within the intervertebral foramen (Rydevik et al., 1989) while the dorsal root ganglia which is tightly enclosed within the meninges is more susceptible to edema formation
Motor conduction alterations in lumbar spinal stenosis
The microanatomy of the nerve root and that of the peripheral nerve is rather similar (Gamble, 1964). The nerve root endoneurium contains the axons, collagen fibers, fibroblasts, and blood vessels. The amount of collagen within the nerve root endoneurium is reported to be five times less than that of the peripheral nerve, but six times more than that surrounding the spinal cord (Stodieck, Beel, & Luttges, 1986). The increased amount of collagen fibers in the peripheral nerve gives it more mechanical strength and allows it to better resist mechanical forces and deformation.
The nerve root can be divided microscopically into two distinct areas, proximal and distal. The proximal region contains a central glial segment comprising glial cells that resembles the microscopic organization of the spinal cord. A few millimeters from the cord, the glial segment transforms to a non-glial segment at a dome-shaped junction (Berthold, Carlstedt, & Comeliuson, 1984). The nonglial segment is organized in the same manner as the peripheral nerves with Schwann cells replacing the glial cells (Tarlov, 1937). In the endoneurium, the axons are separated from the CSF by a thin layer of connective tissue called the root sheath. The proximal part of this sheath has a similar structure to the pia matter that covers the spinal cord (figure 1.5) while the distal part resembles that of the arachnoid (McCabe & Low, 1969). The root sheath has an inner layer of cells that resembles that of the perineurium of the peripheral nerves. Finally the spinal dura encloses the nerve roots and the CSF. When the two layers of the cranial dura enter the spinal canal, the outer layer blends with periosteum of the
Motor conduction alterations in lumbar spinal stenosis
part of the laminae facing the spinal canal. The inner layers join the arachnoid and become the spinal dura. In contrast to the root sheath, the spinal dura is an effective diffusion barrier (McCabe 8 Low, 1969).
The blood supply to the nerve roots is essentially from the segmental arteries. Those divide into three branches when they approach the foramen; an anterior branch, a posterior branch, and an intermediate branch.
It is this last
intermediate branch that supplies the blood to the contents of the spinal canal (Crock & Yoshizawa, 1976). Upon entering the spinal canal, this artery divides into three branches; anterior spinal canal branch, a posterior spinal canal branch, and a nervous system branch. It is this latter that will accompany the nerve roots both proximally towards the spinal cord and distally. When the nervous system branch joins the nerve root at the dorsal root level, it trifurcates and gives rise to arteries that go to the ventral root, the dorsal root and one to the vasa corona of the spinal cord (called medullary arteries). The medullary arteries are inconsistent. The best known and most consistent one is the medullary artery of the thoracic region discovered by Adamkiewicz in 1881 and still holds his name (Adamkiewicz, 1881). The medullary artery runs parallel to the nelve roots, but a direct connection between the medullary arteries and the blood vessels of the nerve root proper has not been found in humans (Parke & Watanabe, 1985). The medullary feeder system is referred to as the extrinsic vascular system of the cauda equina (Parke, Gamell, & Rothman, 1981). The vasculature of the nerve roots is formed by branches from the intermediate
Motor conduction alterations in lumbar spinal stenosis
segmental artery distally and by branches from the vasa corona of the spinal cord proximally. This system is referred to as the intrinsic vascular system of the cauda equina (Parke et al., 1981). The nerve root is supplied by two separate vascular systems, one coming from the distal direction and one coming from the proximal direction. The two systems anastomize at about two thirds length distal to the spinal cord (Parke et al., 1981). This location corresponds to an area of reduced vasculature which may render it particularly vulnerable.
Neuropathophysiology of lumbar compression
The lumbar spinal column protects the nerve roots from outside trauma, however, when there is an insult originating from within, the thin layer of connective tissue surrounding the roots is incapable of protecting the nerve roots like the connective tissue layer of the peripheral nerves does. Compression of nervous tissue can induce clinical symptoms such as numbness, pain, and muscle weakness (Sunderland, 1978). The biological basis for such functional changes has been extensively investigated (Bentley & Schlapp, 1943; Denny-Brown & Brenner, 1944; Fowler, Danta, & Gilliatt, 1972; Grundfest, 1936; Lundborg, 1975; Meek & Leaper, 1911; Rydevik, Lundborg, & Bagge, 1981; Rydevik & Nordborg, 1980). Compression of the nerve induces direct mechanical effects on the nerve fibers and indirect effects due to impairment of the blood supply to the nerve. Grundfest in 1936 subjected nerve tissues to high pressures in a compression chamber (Grundfest, 1936). He
Motor conduction alterations in lumbar spinal stenosis
found that if a high oxygen concentration is present, the neural function was preserved. Denny-Brown performed similar experiments in 1944 and found that nerve function deteriorated rapidly in the absence of an adequate oxygen supply even though the nerve was not subjected to any form of compression. Although these experiments demonstrate the role ischemia plays in nerve injury, they were, however, in vitro studies of isolated nerve segments and did not fully replicate in vivo situations.
Mechanical compression of a nerve have been shown to produce deformation of the nerve fibers, displacement of the nodes of Ranvier, and invagination of the paranodal myelin sheaths (Edwards & Cattell, 1928; Ochoa, Fowler, & Gilliat, 1972). These observations have been made under high levels of compression that exceeded 200 mm Hg. Low level compression studies have been undertaken to evaluate the effect of low-grade compression on peripheral nerves. Lundborg in 1982 found that at a pressure of 30 mm Hg on the median nerve in the carpal tunnel, healthy volunteers started to show signs of functional impairment (Lundborg, Gelberman, & Minteer-Convery, 1982). He concluded that the viability may be at risk during long compression periods (4 -6 hours) at this pressure level.
Rydevik showed that at this level of compression,
intraneural blood flow may be impaired (Rydevik et al., 1981) and Gelberman found a mean carpal tunnel pressure of 32 mm Hg in patients with carpal tunnel syndrome while it was only 2 mm Hg in healthy controls (Gelberman, Hergenroeder, & Hargens, 1981).
Motor conductionalterations in lumbar spinal stenosis
Pressures close to the mean arterial pressure will stop the blood flow through the intrinsic vascular system of the nerve root causing ischemia (Rydevik, McLean. Sjostrand, & Lundborg, 1980). Even when the pressure is released after two hours, there is a reflow through the vasculature.
When higher
pressure levels are used (200-400 mm Hg), the nerve function deteriorated rapidly even when the pressure is applied for short periods indicating that there may be nerve injury and not ischemia (Rydevik & Nordborg, 1980). It is also thought that compression will induce changes in the permeability of the intraneural vessels.
This results in a leakage of macromolecules and
subsequent edema formation. Compression at 50 mm Hg has been shown to produce such changes in the endothelial cells in the peripheral nerves (Smith, Kobrine, & Riuoli, 1977). The vessels located in the epineurium may show changes in vascular permeability after only 2 hours of compression at 50 mm Hg. The effects of local compression are most pronounced at the edge of the compressed segment (Bentley & Schlapp, 1943; Edwards & Cattell, 1928). This "edge effect" is probably due to the displacement of the compressed nerve tissue toward the uncompressed parts of the nerve. The effect is pronounced at the edge where not only is there direct mechanical compression, but also compression due to the displacement of the neural structures.
Studies comparing nerve root compression with peripheral nerve compression have shown that the nerve root is more susceptible (Geflan & Tarlov, 1956). However no critical pressure levels for compression-induced impairment of
Molor conduction alterations in lumbar spinal stenosis
nerve nutrition or function were determined. More recently an animal model for in vivo analysis of the effects of compression was developed by Olmarker (Olmarker, Holm, Rosenqvist, & Rydevik, 1991). His model allows to study the effect of graded compression on various physiological events such as blood flow, nutritional supply and nerve conduction (Olmarker, Rydevik, Hansson, & Holm, 1990; Olmarker, Rydevik, & Holm, 1989a; Olmarker, Rydevik, Holm, & Bagge, 1989b). In this model, compression was induced by inflating a plastic balloon placed over the porcine cauda equina.
By increasing the balloon
pressure incrementally, he was able to determine the critical pressure required to stop the blood flow in the different vascular components (Olmarker et at., 1989b). This study showed that the arterial occlusion occurred at pressures close to the mean arterial blood pressure. Venular blood flow on the other hand was stopped at around 10 mm Hg. The blood flow in the capillaries was dependent on an efficient blood flow in the adjacent venules. Sunderland had suggested that that retrograde capillaly stasis due to venular congestion played an important role in peripheral nerve compression (Sunderland, 1967). Olmarker observed a similar mechanism in the spinal nerve roots since there was a very low venular occlusion pressure for some of the nerve roots h e tested.
As for nutrient transport to the nerve root, it has been found that there are two sources; the intrinsic blood vessels and via diffusion from the CSF (Byrod et al., 1995). This means that the nutrition of the nerve roots may be secured through
Motor eonduction alterations in lumbar spinal stenosis
diffusion when the root is under compression and the intrinsic pathway is occluded. However studies performed on the effects of compression on the transport of intravenously injected 3~-labeled methylglucose to the nerve roots, which reflects both the contribution from the blood and from the cerebrospinal fluid, have shown that very low pressures impair the overall nutritional transport to the nerve roots (Olmarker et al., 1990). A pressure of as little as 10 mm Hg was sufficient to reduce the amount of methylglucose transported to the nerve root by as much as 30%.
Compression may also induce changes in the
permeability of the endoneurial capillaries of the nerve roots causing edema (Olmarker et at., 1989a). lntraneural edema may increase the endoneurial fluid pressure (Low & Dyck, 1977; Lundborg et al., 1983). Such increased pressure may impair the endoneurial capillary blood flow and in this way impair the nutrition of the nerve root (Low et al., 1982). Because the edema will persist for some time after the removal of the compressive agent, it may affect the nerve root negatively for a longer period than the compression itself.
Few studies have attempted to monitor and analyze the effect of compression on neural conduction in the nerve roots. Pedowitz used the porcine model developed by Olmarker (Olmarker et al., 1989a) to study the effect of graded compression on the efferent and afferent pathways (Pedowitz et al., 1992). He found that there was no conduction anomalies when the roots were subjected to 50 mm Hg. Higher compression (100-200 mm Hg) increased conduction time until there was a complete block of sensory conduction followed by a near
Motor conduction alterations in lumbar spinal stenosis
complete block of motor conduction. The recovery period of 1.5 hours saw the motor conduction return to quasi normal values while the sensory conduction did not show any important recovery pattern.
Clinical correlation
From our knowledge of the various mechanisms involved in nerve root compression, we can only speculate as to what these mechanisms translate clinically. The altered neural conduction can explain abnormalities such as loss of sensory and motor function. Pain may be a general reaction to tissue injury recorded by the central nervous system or even as dysfunction of normal inhibitory axons. Neural conduction was not found to be affected when the compression is less than 50 mm Hg, but nutritional transport appeared to be impaired at pressures of 10 mm Hg and less (Olmarker et al., 1990). This may occur minutes after the onset of compression leading to an acute deficit since the nerve cells have very little nutritional reserves.
Central spinal stenosis is characterized by low compression pressure levels (Magnaes, 1982), pain within minutes after the onset of exercise and rapid recovery upon cessation of activity (Verbiest, 1954; Watanabe & Parke, 1986). A possible mechanism for spinal stenosis would be impairment of nerve root
nutrition which is induced by exercise.
During compression that leads to
nutritional impairment which mainly concerns venular and capillary congestion,
Motor conduction alterations in lumbar spinal slenosis
Bb
there will probably be an accumulation of metabolites in the nerve tissue. These substances may cause pain well before the compression can induce nerve conduction changes that can be clinically visible such as motor weakness and sensory deficit. The cessation of the exercise will reduce the congestion and edema and a wash-out of the metabolites can then take place.
From the work of Kobnne we know that there are focal increases in blood flow to stimulated regions in the spinal cord (Kobrine, Evans, & Riuoli, 1976; Kobrine, Evans, & Riuoli, 1978). Compression of the nerve roots by a stenotic process could still permit sufficient blood flow in the nerve roots at rest. However, if the nerve blood flow cannot increase during exercise due to compression by the stenotic process, there would be an ischemic condition as well as an impaired nutritional state in the nervous tissue. This functional ischemia would thus be present only when the increased demands of the nervous tissue are not met and therefore will only produce the symptoms under physical stress.
Animal studies have helped us understand many of the pathophysiological processes taking place following acute compression. They do not however address more chronic problems which are of clinical relevance. How does, for example, nerve conduction change after the removal of a chronic stenotic process? And how long does it take before, if ever, neural conduction comes back to normal? Does exercise increase motor conduction velocity in normal subjects and how does it affect patient with lumbar spinal stenosis. Is the effect
Motor condudion alterations in lumbar spinal stenosis
of ischemia measurable in electrophysiological terms in humans like it is in the animal model? Additionally, animal studies can not help us understand the mechanisms behind the subjective symptoms of patients. This point is of capital importance since the purpose of treatment is not only to improve the clinical signs but the symptoms as well. For those reasons, in vivo studies should be designed to address these questions of clinical importance.
In the following two chapters we will attempt to answer some of those questions. In chapter 2, we study the effect of transient ischemia brought on by exercise on motor conduction in patients suffering from lumbar spinal stenosis. We also evaluate the sensitivity of motor evoked potentials (MEP) in detecting motor conduction abnormalities before and after the onset of neurogenic claudication. We also evaluate the relationship between the patients' symptoms and motor conduction.
In chapter 3, we study the relationship between spinal decompression and motor conduction in humans. decompression?
How does motor conduction change after
And does that correspond to changes in the patients'
symptoms?. We will also evaluate the power of motor evoked potentials to predict clinical outcome in an attempt to develop a new follow-up protocol that will help the physician provide better care earlier for patients following surgery.
Motor conduction alterations in lumbar spinal slenosis
Testing setup
To test these working hypotheses, and to answer the above-mentioned questiones, we developed a motor evoked potential testing protocol.
This
protocol is now in use on a regular basis at the electrophysiological testing laboratory of the Jewish General Hospital. The initial protocol employed at the laboratory was as follows: Self-adhesive pellet electrodes (Graphic Controls, Gananoque, Ontario) are placed in a belly-tendon montage over the desired muscles. Motor evoked potentials are produced using a Magstim 200 magnetic stimulator (Novamatrix Inc., Whitland, Wales) with a custom-made figure-of-eight cone coil producing 2.1 Tesla (figure 1.6). The stimulator intensity used is at 10% above threshold. The coil is placed so that the center is 2-3 cm lateral to the vertex. This position is ideal for lower extremity stimulation because the lower extremity projection on the motor cortex lies around the central sulcus. The magnetic field has a frontto-back direction so that the induced current has a back-to-front direction for optimal cortical stimulation (Amassian et al., 1989a).
Attention is given to provide a high common mode rejection ratio of the amplifier circuit, especially at the 60 Hz frequency. Band pass filtering is used to avoid low frequency drift and/or aliasing during digital data acquisition. The individual amplifier outputs (up to eight channels) are connected to the digital data acquisition board (NB-MIO-16XL, National Instruments, Austin TX).
Motor conduction alterations in lumbar spinal stenosis
The channels are multiplexed and AID converted on the data acquisition board with a sampling rate of up to 4096 Hz.
The magnetic stimulator has a parallel remote input/output allowing full control of the stimulator's activitylstatus by the computer software (Labview 3.01, National Instruments, Austin TX). In order to read the latency time, the computer triggers the stimulator 100 ms after the data acquisition starts.
Repetitive evoked responses are recorded. When finished, the computer is used to rectify the EMG signals and calculate the envelope shape of the curve by using a digital Butterworth filter (figure 1.7). Curves of individual evoked responses at the level of each EMG channel are extracted out of the series of multiple responses (done within the same data acquisition run) and plotted in rows for each channel (figure 1.8).
The individual responses are vertically
aligned with respect to the stimulation time and visually compared. Some of the measurements might be repeated, until the investigator accepts them for further processing. The shortest latency time of five successive stimuli (figure 1.8) is used as the motor evoked potential latency time (MEPLT). The motor response is recorded using a DISA 15C01 EMG amplifier (DISA Electronik, Skovlunde, Denmark). Nerve conduction studies are performed to the EDB and the AH muscles using a TD20 EMGIEP machine (TECA. Pleasantville, NY) and M- and F-wave are recorded. The peripheral motor conduction times (PMCT) of the
Motor conduction alterations in lumbar spinal stenosis
deep peroneal nerve (EDB) and the tibia1 nerve (AH) are calculated according to the following formula (Kimura, 1974): PMCT=(M+F- 1)/2
where M is the M-wave latency time and F is the F-wave latency time. Peripheral conduction is defined as neural conduction from the anterior horn cell in the spinal cord to the peripheral muscle. The 1 msec represents the tumaround time of the neural signal in the spinal cord. The PMCT is used to calculate the central motor conduction time
(CMCT)to L5 and S1 in the
following manner: CMCT = MEPLT - PMCT Central conduction represents nerve conduction from the motor cortex to the anterior horn cell in the spinal cord.
Motor conduction alterations in lumbar spinal stenosis
netic field B
Magnetic field B
\--
Magnetic field 28
Figure 1.6: a figure-of-eight magnetic coil has enough power in the middle section (a combined magnetic field 28) to easily stimulate the deeper lower extremity projections on the motor cortex.
a
M
nducllon alleratlons in spinal stenosls
Figure 1.8: five successive motor evoked responses of the abductor hallucis to transcranial magnetic stimulation. The shortest latency was used for data analysis.
Motor conduction alterations in lumbar spinal stenosis
Chapter 2
Motor Conduction Alterations In Patients With Lumbar Spinal Stenosis Following The Onset Of Neurogenic Claudication. Hani G. Baramki, MD, Max Aebi, MD
Motor conduction alterations in lumbar spinal stenosis
Preface
Chapter 2 will b e prepared in a slightly modified fashion and submitted for publication.
Motor conduction alterations in lumbar spinal stenosis
Abstract
Neurogenic claudication is often seen in patients with lumbar spinal stenosis (LSS). The pathogenesis of neurogenic claudication is thought to be due to relative ischemia of cauda equina roots during exercise. It is important to distinguish between neurogenic claudication and vascular claudication because of the different treatment modality of each condition.
Objectives: We will study the effect of transient ischemia brought on by exercise on motor conduction in patients suffering from LSS. We will also evaluate the sensitivity of motor evoked potentials (MEP) in detecting motor conduction abnormalities before and after the onset of neurogenic claudication.
Methods: Thirty patients with LSS and nineteen healthy volunteers were enrolled in the study.
All LSS patients had a history of neurogenic claudication and the
diagnosis was confirmed with a CT myelogram. Both groups underwent the same electrophysiological evaluation which consisted of nerve conduction studies and motor evoked potentials to the lower extremities. The motor evoked potential latency time (MEPLT), the peripheral motor conduction time (PMCT), and the central motor conduction time (CMCT), were measured. The subjects were asked to walk on a flat surface until their symptoms were reproduced or for
Motor conductionalterations in lumbar spinal stenosis
15 minutes whichever came first. Following, a new set of electrophysiological tests was done.
Results: The patient group was divided into two sub-groups according to the presence or absence of signs of neurological deficit. Exercise did not produce claudication in any of the control group subjects.
Twenty seven patients did have
claudication. The pre-exercise MEPLT and nerve conduction studies in the control group fell within the normal range. In the patient group, nineteen patients had increased baseline values for MEPLT to at least one muscle. The nerve conduction studies to the EDB and the AH did not reveal any abnormal latency times. The paired t-test showed that there was a statistically significant difference between the MEPLT and the PMCT values measured before and after the exercise in the patients with signs of neurological deficit (t-test pc0.0001). This difference was not found to be statistically significant in patients without neurological deficits (t-test p>0.05).
Conclusions: The presence of an abnormal MEPLT helps distinguish between neurogenic claudication and vascular claudication when the radiological image is not conclusive. Exercise appeared to increase the sensitivity of MEPs in LSS when there are signs of neurological deficit associated with neurogenic claudication.
Motor conductionalterations in lumbar spinal stenosis
Introduction: Lumbar spinal stenosis (LSS) is defined as any type of narrowing of the spinal canal, nerve root canal, or intervertebral foramen (Amoldi et al., 1976). Symptoms of spinal stenosis include pain in the lower back andlor radiating pain that extends down to the lower extremities (Paine, 1976). Neurogenic claudication is characterized by intermittent pain and dysfunction brought on by exercise. The location of the pain in the lower extremity has a lumbo-sacral distribution (Hall et al., 1985). Neurogenic claudication has been reported in various affections (Bergman, 1950; Dejerine, 1911; Ehni, 1969; Madsen & Heros, 1988), but it is generally associated with LSS (Verbiest, 1954). The pathogenesis of intermittent claudication is thought to be due to relative ischemia of active cauda equina roots during exercise (Blau & Louge, 1961; Evans, 1964; Hanai, 1980; Matsuda et al., 1979; Tsuji et al., 1985).
The distinction between neurogenic claudication and vascular claudication is not always clear because the symptoms are similar and patients with LSS may also suffer from vascular insufficiency and vice versa.
The differentiation
between these two entities is important because of the different treatment modalities involved. The radiological evaluation (plain radiographs, CT scan, CT myelography, MRI) allows for the visualization of the spinal canal, but it does not offer any information on the functional state of the neural structures within. The scientific literature is abundant with reports of controversial findings on
Motor conduction aheratiom in lumbar spinal stenosis
radiological examinations (Boden, Davis, Dina, Patronas, & Wiesel, 1990a; Boden et al., 1990b; Hitselberger & Witten, 1968; Teresi et al., 1987; Wiesel, Tsourmas, Feffer, Citrin, & Patronas, 1984).
Teresi for example found
radiological evidence of spinal compression in asymptomatic individuals and vice versa (Teresi et al., 1987).
In order to evaluate the functional state of the spinal cord and roots, different electrophysiological testing protocols have been put forward and tested for accuracy and reliability. Radiculopathies are the single most common cause of patient referral to electromyography (EMG) and nerve conduction laboratories (Johnson, Stocklin, & LaBan, 1965).
The use of somatosensory evoked
potentials (SSEP) on the other hand has been rather disappointing in assessing root compression in the lumbar spine. The reason for this is that the peripherai nerve stimulated to produce the SSEP often comprises many roots and thus a monoradiculopathy is easily masked by normal responses mediated by the intact roots (Katifi & Sedgwick, 1986).
Stimulation of individual
dermatomes through dermatomal SSEPs has proven more promising in lumbar spinal compression (Green, Gildemeister, & Hazelwood, 1983; Nicpon, Sedgwick, Brice, & Docherty, 1983; Scarff, Dallmann, & Bunch, 1981; Sedgwick, Katifi, Docherty, & Nicpon, 1985), yet its use is still rather limited (Aminoff, Goodin, Barbaro, Weinstein, & Rosenblum, 1985).
Motor conduction alterations in lumbar spinal stenosis
Transcranial motor evoked potentials (MEP) were first described by Merton and Morton in 1980 (Merton & Morton, 1980).
The technique they introduced
consisted of percutaneous stimulation of the motor cortex using electrical shocks produced by discharging a 0.1 pF condenser charged up to 2000 V through two electrodes applied to the scalp regions overlying the motor cortex. Transcutaneous electrical stimulation has not achieved wide
clinical
acceptability because of the scalp discomfort incurred. In 1985, Barker and coworkers produced MEP through magnetic stimulation of the human brain (Barker et al., 1985). They used a custom made electromagnet that produced brief magnetic pulses that induced the formation of an electric capable of stimulating the motor cortex..
MEPs are currently used to evaluate the
functional state of the entire descending motor pathway from cortex to muscle. It has been shown that motor conduction is altered in clinical conditions resulting in spinal cord and root compression (Dvorak, Herdmann, Theiler, & Grob, 1991; Glassman, Zhang, Shields, Linden, & Johnson, 1995; Herdmann, Dvorak, & Vohanka, 1992b; Kameyama, Shibano, Kawakita, & Ogawa, 1995; Linden & Berlit, 1994; Tavy et al., 1994; Ueta, Owen, & Sugioka, 1992).
Few studies have evaluated the effects the ischemic process that produces claudication on the various electrophysiological parameters.
London and
England (London & England, 1991) studied the effect of claudication on the Fwave and reported that there is an increase in the F-wave latency time in the two cases they studied. Kondo studied the effect of claudication on the nerve
Motor conduction allerationsin lumbar spinal slenosis
conduction along the sensory pathway (Kondo, Matsuda, Kureya, & Shimazu, 1989). He performed somatosensory evoked potentials (SEP) on patients with
spinal stenosis and reported altered SSEPs following the onset of claudication.
By using transcranial magnetic MEPs, this study will assess the effect of the transient ischemic process that brings along claudication on motor conduction along the entire motor pathway. Additionally, it will test the hypothesis that the sensitivity of MEPs to detect motor dysfunction is increased if the test is performed after the occurrence of claudication.
Material & Method: In a cross-sectional study, thirty patients with lumbar spinal stenosis and nineteen healthy volunteers were enrolled in the study which was approved by the local ethics committee.
All LSS patients had a history of neurogenic
claudication and the diagnosis was confirmed with a CT myelogram.
Both
groups underwent the same electrophysiological evaluation which consisted of nerve conduction studies and motor evoked potentials to the lower extremities. Exclusion criteria for the study included prior spinal or brain surgery and known or suspected peripheral vascular disease. The study hypothesis and protocol were explained to each participant by a clinical coordinator.
Motor conduction alterations in lumbar spinal stenosis
Clinical Evaluation: All patients and controls gave a complete history and underwent a thorough physical examination.
Specific attention was given to the neurological
examination which included a complete motor and sensory evaluation.
Electrophysiological evaluation: Self-adhesive pellet electrodes (Graphic Controls, Gananoque, Ontario) were placed in a belly-tendon montage over the following muscles bilaterally: vastus lateralis (VL); tibialis anterior (TA); extensor digitorum brevis (EDB); abductor hallucis (AH). Motor evoked potentials were produced using a Magstim 200 magnetic stimulator (Novamatrix Inc., Whitland, Wales) with a custom-made figure-of-eight cone coil producing 2.1 Tesla (figure 1.6).
The stirnulztor
intensity used was at 10% above threshold. The shortest latency time of five successive stimuli (figure 1.8) was used as the motor evoked potential latency time (MEPLT). The coil was placed over the motor cortex so that the resulting induced current had a back-to-front direction along the motor cortex (Amassian et al., 1989a). The motor response (figure 1.7) was recorded using a DISA 15C01 EMG amplifier (DISA Electronik, Skovlunde, Denmark).
Nerve
conduction studies were performed using a TD20 EMG/EP machine (TECA, Pleasantville, NY). Nerve conduction studies were performed to the EDB and the AH muscles using a TD20 EMG/EP machine (TECA, Pleasantville, NY) and
Motor conduction alterationsin lumbar spinal stenosis
M- and F-wave were recorded. The peripheral motor conduction times (PMCT) of the deep peroneal nerve (EDB) and the tibia1 nerve (AH) were calculated according to the following formula (Kimura. 1974):
where M is the M-wave latency time and F is the F-wave latency time. Peripheral conduction is defined as neural conduction from the anterior horn cell in the spinal cord to the peripheral muscle. The 1 msec represents the turnaround time of the neural signal in the spinal cord. The PMCT was used to calculate the central motor conduction time (CMCT) to L5 and S1 in the following manner:
-
CMCT= MEPLT PMCT Central conduction represents nerve conduction from the motor cortex to the anterior horn cell in the spinal cord. After performing this initial electrophysiological evaluation and recording the various resting latency times, the subject was asked to walk on a flat surface until hislher symptoms were reproduced or for 15 minutes whichever came first. Following the appearance of claudication or after 15 minutes, a new set of electrophysiologicaltests (MEP, nerve conduction) was performed and the postexercise MEPLT, PMCT , and CMCT were obtained.
Motor conduction alterations in lumbar spinal stenosis
Data Analysis: MEPLTs were compared to previously published results (Claus, 1990; Dvorak et al., 1991). An analysis of variance (ANOVA) was used to evaluate the effect of side (left, right), exercise, and neurological symptoms on the MEPLT, CMCT, and PMCT of the four muscles. In addition, a paired t-test was used to compare the pre-exercise with the post-exercise MEPLTs, PMCT, CMCTs in the patient group and in the control group.
Motor conductionalterations in lumbar spinal stenosis
Results: The LSS group consisted of 19 males and 11 females and had a mean age of 66.6 years (range: 38.3
-
89.3).
The control group (healthy volunteers)
consisted of 10 males and 9 females and had an average age of 62.18 years (range: 41.1
- 85.9).
The clinical examination did not reveal any neurological
abnormalities in any of the controls. The patient group was divided into two sub-groups according to the presence (sub-group P, n 4 0 ) or absence (subgroup A, n= 20) of signs of neurological deficit. In the sub-group P, six patients had a predominantly motor deficit. Their clinical signs included weak or absent deep tendon reflexes (patellar n = 3, achelian n = 4) , distal muscular weakness (L4: n = 2, L5: n = 5, S1: n = 5). The remaining four patients in the
P sub-group
had predominantly a loss of light touch sensation along the L4 dermatome (n = I), along the L5 dermatome (n = 3) and along the S1 dermatome (n = 4).
Exercise did not produce claudication in any of the control group subjects. Twenty seven patients did have claudication (17 in the A subgroup, 10 in the P subgroup).
The pre-exercise MEPLT and nerve conduction studies in the control group fell within the normal range. Table 2.1 shows the pre- and post-exercise results for the left AH muscle in the control group. A paired t-test comparing the pre-and post-exercise values of MEPLT, PMCT, and CMCT did not show any statistically
Motor conducl'on alterations in lumbar spinal slenosis
significant difference in the pre-and post-exercise values (p= 0.7483, 0.9189, 0.9734 respectively).
In the patient group, nineteen patients had increased baseline values for MEPLT and PMCT (7110 in the P sub-group , 12/20 in the A sub-group) to at least one muscle. The nerve conduction studies (M-wave) to the ED6 and the AH did not reveal any abnormal latency times. The ANOVA model did not detect a statistically significant effect for side or exercise on the latency times when the patients were not separated according to their neurological signs. The paired t-test showed that there was a statistically significant difference between the MEPLT and the PMCT values measured before and after the exercise in the patients with signs of neurological deficit (t-test pc0.0001). This difference was not found to be statistically significant in patients without neurological deficits (t-test p>0.05). Tables 2.2a and 2.2b show as an example the pre- and post-exercise results for the left AH muscle in the patient group (P sub-group and A sub-group respectively). Table 2.3 presents the pooled values for the different parameters and the absolute and relative differences between the pre-and post-exercisein the patient group.
Motor conductionalterations in lumbar spinal stenosis
Table 2.1: The control group's pre-exercise and the post-exercise MEPLTs, PMCTs, and CMCTs to the left AH (in rnsec).
Motor conductionalterations in lumbar spinal stenosis
Table 2.2a: TI
pre-exerciseand the post-exe
se MEPLTs, PMCTs, and
CMCTs to the left AH (in ms) in the patients with signs of neurological deficit (subgroup P).
Motor conduction alterations in lumbar spinal stenosis
Table 2.2b: The pre-exercise and the post-exercise MEPLTs, PMCTs, and CMCTs to the left AH (in msec) in the patients with no neurological deficit (subgroup A).
1
'
1
MUSCLE PRE-EXERCISE MEPLT POST-EXERCISE MEPLT MEPLT ABSOLUTE DIFFERENCE. MEPLT RELATIVE DIFFERENCE PRE-EXERCISE PMCT POST-EXERCISE PMCT PMCT ABSOLUTE DIFFERENCE PMCT RELATIVE DIFFERENCE PRE-EXERCISE CMCT POST-EXERCISE CMCT CMCT ABSOLUTE DIFFERENCE CMCT RELATIVE DIFFERENCE
Table 2.3: Fooled values for all measured parameters (msec) in the patient group. The absolute difference (ms) and the relative difference (%) compared to the initial baseline value are also shown.
Motor conductionalterations in lumbar spinal stenosis
Discussion: The purpose of the study was to test if a MEP test would be sensitive enough to detect the presence of a functional deficit on a given neural pathway.
In
addition, we wanted to evaluate the effect of ischemia and the onset of claudication on motor conduction. spectacular,
the
While symptoms of LSS are often
physical examination
usually
renders
few
findings
(Schonstrom, Bolender, & Spengler, 1985). The radiological evaluation plays an important role when planning for surgical decompressive. Unfortunately the presence of multilevel compression and the false positive results seen with computed tomography (Tavy et al., 1994; Wiesel et al., 1984) reduce the overall accuracy of the radiological evaluation.
When clinical findings are not
conclusive, electrophysiological investigations may be of clinical value. Various studies have shown that the different electrophysiological tests available are sensitive in detecting neural damage (Chistyakov, Soustiel, Hafner, & Feinsod, 1995; Dvorak et al., 1991; Glassman et al., 1995; Herdmann, Dvorak, & Bock, 1992a; Kondo et al., 1989; Linden & Berlit, 1995). In the present study we found that 63% (19130) of patients with LSS had abnormal MEPLTs.
This is
comparable with what has been reported by others (Dvorak et al., 1991). In all these patients, peripheral nerve conduction to the EDB and the AH as well as signal transmission across the neuromuscular junction to the same muscles was normal (M-wave latencies within the normal limits). The increase in the PMCT was the result of an increase in the F-wave latency time due to
Motor conduclion alterations in lumbar spinal stenosis
decreased nerve conduction velocity within the spinal canal caused by neural compression. This resulted in the observed increase in the MEPLT. There was an observed increase in the MEPLT of the VL and TA muscles in patients with L4 injury. Here again one would suspect that the increase was a result of an increase in the PMCT due to nerve root compression within the spinal canal. although this could not be stated with certitude because peripheral nerve conduction was not measured.
In an effort to increase the sensitivity of the MEP test, the patients were asked to walk until they produced their symptoms.
The stress test increased the
abnormal MEPLTs to 76% (23130). When we separated the patients into the two clinical subgroups, we found that in the P subgroup, the number of patients with pathological results increased from 70% (7110) to 100% (10110) while in the A subgroup it went from 60% (12120) to 65% (13MO). This result is not surprising as we were measuring motor conduction in a group of patients with signs of neural deficit.
Although the pathogenesis of neurogenic claudication is complex and not entirely clear, it is generally accepted that nerve root ischemia plays a major role in its genesis (Blau & Louge, 1961; Evans, 1964; Hanai, 1980; Matsuda et al., 1979; Tsuji et al., 1985).
The symptoms usually start with sensory
disturbances such as numbness, paresthesia, or dysesthesia prior to the development of motor disturbances (Spengler, 1987). This may explain the
Motor conductionalterations in lumbar spinal stenosis
lack of motor symptoms in the majority of the current cohort. In the present study we found that the onset of claudication increased the MEPLT in the patients who have signs of neural deficit. This group of patients has a documented neural compression that produced an increase in their MEPLT before the onset of claudication. When these patients were asked to reproduce their symptoms, the MEPLT was found to increase even further, indicating the occurrence of an acute process that overlays a chronic one. We believe that the mechanical compression is responsible for the chronic increase in latency time, but it is the ischemic process that further increases the MEPLT. This is in agreement with what Kobrine and colleagues (Kobrine, Evans, & Riuoli, 1979) found concerning ischemia affecting neural conduction in the spinal cord of the monkey and Rydevik in the pig cauda equina (Rydevik et al., 1991). As to why only 73% of patients with symptoms of claudication did have abnormal MEPLTs and 27% had normal MEPLTs, we believe that in the 27% that had normal MEPLTs their chronic mechanical compression might be below threshold and so the ischemic process was not important enough to produce prolonged latency times. This is in agreement with Rydevik's finding (Rydevik et al., 1991) that there was a threshold pressure of 50 mm Hg below which no alteration in neural conduction could be induced.
The presence of an abnormal MEPLT will help distinguish neurogenic claudication from vascular claudication when the radiological image is not
0
conclusive. Exercise appeared to increase the sensitivity of MEPs in LSS when
Motor conduction alterations in lumbar spinal stenosis
there are signs of neurological deficit associated with neurogenic claudication. When lumbar stenosis is not accompanied by a neurological deficit, exercise does not appear to significantly increase the sensitivity of the MEP test. The MEPLT of the VL muscle may be helpful in evaluating motor conduction along the L4 pathway, but the impossibility to obtain M and F-waves makes it less interesting than the MEPLTs of the EDB and AH muscles.
Motor conduction alterations in lumbar spinal stenosis
Chapter 3
Motor Conduction Changes Following Spinal Decompression And Their Value As Predictors Of Clinical Outcome. Hani G. Baramki, MD, Max Aebi, MD
Motor conduclion alleralions in lumbar spinal stenosis
Preface
In chapter 2, the effects of acute ischemia on motor conduction were studied in the lumbar spinal stenosis model. We had found that the acute ischemic process that is brought on by exercise reduces the motor conduction velocity along the affected pathway. In chapter 3 we use the same model to monitor the changes in motor conduction that are brought on by decompression of the spinal roots. This is in effect a reversal of the stenotic process that takes place over a certain time period. In addition, we will evaluate the effect of decompression on the clinical signs of the patients and correlate those findings with changes in motor conduction velocity. This chapter will be prepared in a slightly modified fashion and submitted for publication.
Molor conduction atternlionsin lumbar spinal stenosis
Abstract Motor evoked potentials (MEP) to the lower extremities have been shown to be altered in lumbar spinal compression. Animal experiments have studied the effect of acute compression on motor conduction along the cauda equina. They demonstrated the presence of a direct relationship between the removal of compression and the normalization of the motor conduction time.
Objectives: We will study the relationship between spinal decompression and motor conduction in humans. We will also evaluate the power of motor evoked potentials to predict clinical outcome in an attempt to develop a new follow-up protocol.
Methods: Thirty-five patients with symptomatic LSS and abnormal MEP will be recruited before they undergo decompressive surgery. They will be examined clinically and electrophysiologicallyonce pre-operatively and four times post-operatively at one week, one month, two months, and six months. Their clinical condition will be evaluated using the American Spinal Injury Association (ASIA) neurological score. Their functional state will be evaluated using a modified functional independence measure (FIM) score.
Motor conduction will be
measured with transcranial magnetic cortical stimulation to the EDB and AH muscles. The motor conduction time at one month and two months will be used
Motor Conduction alterations in lumbar spinal stenosis
to predict the clinical outcome at six months as evaluated with the ASIA and the FIM scores.
Results: MEP at one month was able to predict clinical outcome at six months (multiple regression, 12= 0.326 for L5 and I2 = 0.379 for S1). Using the MEP data at one week and preoperatively increased the predictive power considerable (I2
.
0.503). There was a gradual decrease in MEP latency time over the six month period and at the end of the study only 14% of the patients had abnormal latency times.
Conclusions: Motor evoked potentials have shown to be excellent outcome predictors following decompressive surgery. They are more sensitive than the clinical examination and their objective results are both reproducible and reliable.
Motor conduction alterations in lumbar spinal stenosis
Introduction: Over the past few decades, there has been a steady increase in the number of electrophysiological examinations available to assess spinal cord and spinal root dysfunction. Somatosensory evoked potentials (SSEP) have been the predominant type used to assess spinal cord integrity and to follow-up on the patient's clinical condition (Arninoff, 1984; Eisen, 1982; Fehlings, Tator, & Linden, 1989; Nash & Brown, 1989). The SSEP test evaluates the afferent sensory pathways in the dorsal column (Cusick, Myklebust, Larson, & Sances, 1979). It does not provide any information on the efferent anterior motor pathways.
The development of motor evoked potentials (MEP) through
transcranial electrical stimulation of the motor cortex (Merton & Morton, 1980) allowed physicians to evaluate the central motor pathways (Cascino, Ring, King, Brown, & Chiappa, 1988; Cracco, 1987; Rossini et al., 1994), and study the electrophysiological phenomena resulting from neural insults (Baskin & Simpson, 1987; Fehlings et al., 1989; Fehlings, Tator, Linden, & Piper, 1987; Levy, MacCaffrey, Hagichi, & Siaviash., 1987; Patil, Nagaraj, & Mehta, 1985; Young & Cracco, 1985; Zentner, 1989). This type of cortical stimulation is however painful and requires sedation of the patient. Barker and colleagues (Barker et al., 1985) used brief high-intensity focal magnetic fields to induce the production of electric currents deep within the skull. This new method was painless and easy to use. Using the method proposed by Kimura (Kimura, 1974) to measure the peripheral motor conduction time (PMCT), Robinson and
Motor conduction alterations in lumbar spinal stenosis
colleagues (Robinson, Jantra, & Maclean. 1988) expressed the MEP latency time as central motor conduction time (CMCT) and PMCT. This process is particularly important when motor conduction to the lower extremities is being evaluated since the spinal cord (and hence the central motor system) ends at the L11L2 level.
Motor evoked potentials have been shown to be altered in various condition affecting the spinal cord and the nerve roots (Chang & Lien, 1991; Chistyakov et al., 1995; Dvorak et al., 1991; Glassman et al., 1995; Kameyama et al., 1995; Linden & Berlit, 1995; Uozumi, Tsuji, & Murai, 1991; Wilbourn & Aminoff, 1388; Wohrle, Kammer, Steinke, & Hennerici, 1995).
Animal experiments have
demonstrated that motor conduction is altered almost instantaneously when the neural structure is subjected to mechanical compression (Pedowitz et al., 1992; Rydevik, 1992), or ischemia (Kobrine et al.. 1979). but returns to normal when the noxious stimulus is removed. Although these observations are assumed to be similar in humans, it is not clear how chronic compression affects motor conduction and how does its removal alter motor conduction. Additionally, to what does the normalization of motor conduction translate to in terms of changes in the patient's functional state and clinical condition.
In this study, patients undergoing spinal decompression will be monitored clinically and electrophysiologically over a period of six months.
The
relationship between MEPs and the patient's clinical and functional state
Motor conductionalterations in lumbar spinal stenosis
following surgery will be investigated. Additionally, we will explore the power of MEP measurement in the early post-operative period to predict clinical outcome at six months.
Materials & Method:
Thirty five patients with lumbar spinal stenosis (LSS) were enrolled in the study which was approved by the institution's ethics committee.
The study group
consisted of 24 males and 11 females and had an average age of 65.3 years (range 38.3 - 82.4). The clinical diagnosis was confirmed by CT scan andlor CT myelogram. Because the study's purpose is to investigate the natural course of abnormal MEPs following decompression, only the patients with abnormal MEPLT on the pre-operative MEP test were asked to pacicipate. The study's exclusion criteria were previous spinal surgery or neurosurgery, epileptic seizures, and known peripheral neuropathy.
Each subject was examined
clinically and electrophysiologically at five well-defined time intervals (To,T,, T, T3 ,T,).
The first series (To) was performed as part of the patient's pre-operative
work-up. Four other series of examinations were performed post-operatively at 1 week (T,), 1 month (T,), two months (T,), and at six months (T,).
Each series of
examinations consisted of a clinical examination (including history and physical), a neurological examination, and an electrophysiologicalexamination. The American Spinal Injury Association's (ASIA) neurological examination score was used to rate each patient's neurological signs (annex 3.1). The three neurological scores (motor, pin prick, light touch) were noted for each level. A
Motor conductionalterations in lumbar spinal stenosis
modified functional independence measure (FIM) (Ditunno, Young, Donovan. & Creasey, 1994) was used to assess the functional state of each patient (annex 3.2).
This consists of a seven-point scale and was used to evaluate eight
different items (bathing, dressing, toileting, mobility, locomotion/walking, locomotion/stairs, bladder management, bowel management).
The electrophysiological evaluation consisted of a motor evoked potential test and a nerve conduction test.
The two tests were to the extensor digitorurn
brevis (EDB) and the abductor hallucis (AH) muscles. Motor evoked potentials were produced using a Magstim 200 magnetic stimulator (Novamatrix Inc., Whitland, Wales) with a custom-made figure-of-eight cone coil producing 2.1 Tesla (figure 1.6).
The coil was placed over the motor cortex so that the
resulting induced current had a back-to-front direction along the motor cortex (Amassian et al., ). The stimulation intensity was 10% above threshold. The motor response was recorded using a DISA 15C01 EMG amplifier (DISA Electronik, Skovlunde, ilenmark).
Pellet electrodes (Graphic Controls,
Gananoque, Ontario) were placed over the EDB and the AH muscles in a bellytendon montage. The motor response was processed using custcrn software on a Macintosh Quadra 650 (Apple Computers, Cupertino, CA). The motor evoked potential latency times (MEPLT) of five successive stimuli were recorded and the shortest one used for the data analysis (figure 1.8). The nerve conduction studies were performed using a TD20 EMGlEP machine (TECA, Pleasantville, NY).
The deep peroneal nerve and the tibia1 nerve were
Motor conduction alterationsin lumbar spinal stenosis
stimulated and the M- and the F-waves were recorded from the ED6 and AH muscles. The penpheral motor conduction time (PMCT) was calculated as follows (Kimura, 1974):
PMCT=(M+F- 1)/2 where M is the M-wave latency time and F is the F-wave latency time. Peripheral conduction is defined as neural conduction from the anterior horn cell in the spinal cord to the penpheral muscle. The 1 msec represents the tumaround time of the neural signal in the spinal cord. The PMCT was used to calculate the central motor conduction time (CMCT) to L5 and S1 in the following manner:
-
CMCT = MEPLT PMCT Central conduction represents nerve conduction from the motor cortex to the anterior horn cell in the spinal cord. The surgery was performed by the same surgeon and consisted of lumbar spinal decompression. All patients had the same rehabilitation program postoperativelly.
Data analysis:
Four root-specific electrophysiological and clinical datasets were collected from each patient (L5 and S1 bilaterally ). The data from the 140 roots (35 patients) were first split according to level (annex 3.3).
The datasets were further
Motor conduction alterations in lumbar spinal stenosis
subdivided based on their MEPLT at To (normal or abnormal MEPLT). The four motor pathways (L5 right and left, S1 right and left) were analyzed independently for the normal group and the abnormal group.
A repeated
analysis of variance (rANOVA) was used to evaluate the effect of side (left, right) and time
CT,, T,, T,, T,, TJ
on the MEPLT and the PMCT. Throughout the
analysis process, the clinical and electrophysiological data of each root were kept linked together.
A correlation test was used to evaluate the relation between the MEPLT and the
PMCT. A multiple regression model was used to calculate the power of the MEPLT and the PMCT (the independent variables) at To, T,, T,, and T, in predicting the clinical outcome (FIM score) and neurological outcome (the ASlA score) and the electrophysiological outcome (MEPLT) at T, (dependent variables) in the abnormal subgroup. Additionally, a correlation test was used to evaluate the relation between MEPLT and both the FIM and the ASlA scores at each visit.
Mator conductionalterations in lumbar spinal stenosis
Results: Clinical Data:
All patients had symptoms of neural compression at T,. These included lower extremity pain (n = 23), low back pain (n = 29), and neurogenic claudication (n = 24). Five patients had clinical signs of S1 compression, and five had signs of a combined L5IS1 compression. Table 3.1 lists the MEPLT results for all patients and muscles and describes how the values changed for each patient over the six-month study period.
It also describes the clinical findings at T.,
Eight
patients had persistent symptoms at six months post-operatively (T,) and four had persistent signs of neural deficit. All patients underwent posterior spinal decompressive surgery.
In addition to spinal decompression, posterolateral
spinal instrumentation (A0 Internal Fixator with transpedicular screws) with intertransverse process graft was used in twenty-eight patients and autologous bone harvested from the iliac crest was used as graft material. There were no major complications reported. The average hospital stay was 7.2 days (range 4- 10 days). The ASIA score for the normal and abnormal groups for L5 and S1 is shown in figures 3.la and 3.1 b. The FIM score for the entire study population in shown in figure 3.2.
Motor conductionalterations in lumbar spinal stenosis
Figure 3.la 10
Time
Figure 3.1b
~le0peraUve
Iw
k
1 rnonfh
2 months
6 rnonlhr
Time
Figures 3.la & 3.1b: The combined ASIA neurological score for the L5 (figure 3.la) and the S1 (figure 3.lb) roots.
Motor conduction alterations in lumbar spinal stenosb
Time
Figure 3.2: Modified FIM Score for all patients combined.
Electrophysiological Data
Of the seventy motor pathways tested for each level (thirty-five patients, left and right), there were thirty-nine abnormal MEPLT to tho EDB and fifty-one abnormal MEPLT to the AH muscles (table 1). Nerve conduction to the EDB and the AH was normal in all the patients (M-wave latency times within normal limits for age and size). The F-wave and consequently the PMCT was abnormal in the same motor pathways that had the increased MEPLT. The CMCT was
Motor conductionalterations in lumbar sDinal stencsb
normal in all patients. There was a very good correlation between the MEPLT and PMCT (r = 0.996).
After separating the MEPLTs into the normal and
abnormal s~~bgroups at To, no statistically significant difference was found between the left and the right side within each group (rANOVA, p>0.05).
The
left and right sides were therefore pooled for subsequent data analysis. Figures 3.3a and 3.3b depict the MEPLT to the EDB and AH muscles respectively. Figure 3.4 describes the PMCT to these same muscles.
Of the thirty-nine
abnormal MEPLTs to the EDB at To, six remained abnormally high at T, and of the fifty-one abnormal MEPLTs to the AH, seven remained high at TJtable 3.1).
Motor conduction alterations in lumbar spinal stenosis
Figure 3.3a
'-I-.-----
m E m
IrrreaSBa MEPLTat TO
f ---.-
-
- - - - - - - - ---- -JP pre~p~rative
I week
1 monlh
2 months
6 months
Time
Figure 3.3b
preoperalive
1 week
I month
2 monms
6 monms
Time
Figures 3.3a & 3.3b: Normal and anormal MEPLT to the EDB (figure 3.3a) and the AH (Figure 3.3b).
Motor conduction alterations in lumbar spinal stenosis
Figure 3.4.3
- ..
40
-0.
WED6
wPM2T.m
38 36
-' 0
34 32 30
I-
28
24
Time
Time
Figures 3.4a & 3.4b: Normal and abnormal PMCT to the EDB (figure 3.4a) and the AH (figure 3.4b) muscles.
Motor conduction alterationsin lumbar spinal stenosb
Symptoms at To
LBP, RLEP LLEP LBP. RLEP LBP.NC LLEP LBP. NC LBP. RLEP LBP. NC. LLEP LBP. NC. LLEP NC LBP, LBP, LBP. NC, LLEP LLEP LBP, NC, RLEP LBP. NC LBP. LLEP LBP. NC, RLEP LBP, NC LBP. NC, RLEP. LLEP LBP, NC LBP. NC LBP. NC, RLEP LBP. NC, LLEP LBP, NC LBP. NC LBP. NC LBP. NC LBP. NC, RLEP LBP. NC, RLEP LBP. NC, RLEP LBP. NC. RLEP. LLEP LBP, NC, RLEP. LLEP
(
1 /
j
1 ( j
j j j
f
(
j I j
( j
f
/
i
MEPLT Neurologicaldeficit atTo None None Right S1 None None None None None Left L~ISI None Right S1 None None Left L5lS1 None Right S1 None None Right S1 None None Right L5lS1 None None None None None None Right S1 None Right L5lS1 None None Left L5lS1, Right S1 None
I I
Right EDB
1 2 j N
1
; I
N N N
1 2 1 2
I
/
I
p N N N
1 3
I
;
I
N N N
(
4
j
N
I
N N
I
Left EDB
Right
N
N N P
3 N N N N N N P N
4 N 2
3 N N 2 P
2 N
1 4 I 3
4
P N
3
/
I
1 4
I
p N
1
3 4
j
4
j
2 P
N N N 1 3
N
AH
2
N N N N
N
3
4 4 1
N N N
4
3
N P
4 3
2
N
N N N P N 1 P
3
2 2 4 4 3
3 2
2 3 3 4 3
4
2 2 3 3 2 4
1 2 4
1 3
1
3
I
I 1 1 3
/
Left
AH -
P 3 N P
2 4 N
2 P
2 2 2 4 3 N
3 3 3 3 2 4 2
Table 3.1: Flow chart describing the MEPLT for all subjects and for all muscles during the study period. LBP: low back pain; NC: neumgenic claudication; RLEP: right lower extremity pain; LLEP: left lower extremity pain. The MEPLT is described as follows: N = normal MEPLT at To 1 = MEPLT was abnormally high at Toand became normal at T, 2 = MEPLT was abnormally high at Toand became normal at T, 3 = MEPLT was abnormally high at Toand became normal at T, 4 = MEPLT was abnormally high at Toand became normalat T, P = MEPLT remained abnormally high during the entire skdy period.
Motor conduction alterations in lumbar spinal stenosis
Dependent Variabls /
L5 ASlA score Q T,
I
Independent Variable(s)
/
L5 MEPLT Q T,
/
1 Significance i
/
P = 0.0054
I
/
15 MEPLT Q T, P c 0.0001 L5 MEPLT Q T, j
/
L5 MEPLT O To
'
~elationshidAdjusted 3
/
lnverse
1
0.326
I
Inverse
1
0.453
j L5 MEPLT Q T,
f 1 ! L5 MEPLT @ T, I
P c0.0001
/
lnverse
1
0.503
i S1 MEPLT Q T,/
P c 0.0012
/
lnverse
/
0.379
Pc0.0001
I
lnverse
:
1.
SI ASIA score Q T,
1 S1 MEPLT Q T, / / SI MEPLT @ T,! ! S l MEPLT Q T,
I
0.482
j
! S1 MEPLT Q T,I
I S1 MEPLT Q T; /
1
Pc0.0001
I
lnverse
1
0.527
i
Table 3.2. The results of the multiple regressions that were performed on the ASlA scores obtained at T., Findings which were deemed significant are listed.
Motor conduction akerationsin lumbar spinal stenosis
Discussion The purpose of this study is to analyze how changes in neural conduction affect clinical signs and symptoms. Additionally, the study evaluates the ability of electrophysiological testing in predicting clinical outcome. We do not however attempt to evaluate the results of the surgical procedure.
All patients enrolled in the study had to have abnormal MEPLTs because our aim was to compare changes in MEPs with clinical signs and symptoms. From previous studies (chapter 2 table 2.3), (Baramki, Steffen, Rubin, Antoniou, & Aebi, 1996; Dvorak et al., ), we know that about 65% of patients with spinal stenosis have abnormal MEPLTs. This study does not attempt to extrapolate the finding to the general population of LSS patients but rather to the subpopulation of LSS patients with abnormal MEPLTs (about 65% of the total).
The results of the clinical examination had to be quantified to facilitate comparative follow-ups. Although the ASIA score is an ordinal rating scale, its results have been shown to be reproducible and reliable over time (Capaul et al., 1994; Ditunno et al., 1994; Ota et al., 1996). In order to assure consistency, the clinical examination was performed by the main investigator on all of the patients. The FIM score is used to evaluate the patient's functionality and to evaluate hislher progress. In its modified form, it focuses on eight areas that are
Motor canduction alterations in lumbar spinal stenosb
directly affected by lumbar spinal injury. It also evaluates the patient's function as a whole (Ditunno et al., 1994; Ota et al., 1996). All patients had symptoms of LSS but only ten patients (28%) showed clinical signs of neural compression (table 3.1).
The paucity of clinical signs seen in this study is consistent with what has been reported by others (Hall et al., 1985; Schonstrom et al., 1985). Over the sixmonth study period, eight patients remained symptomatic (22%) and 4 (11%) had persistent signs of neural deficit. Figures 3.la and 3.lb show the ASlA score for the patients with neurological deficit at the L5 and S1 levels respectively. There is a slow amelioration in the overall score for these patients. The highest improvement was seen between two months and six months, which indicates a clear time-dependent phenomenon. At the end of the six-month period, the ASlA score did not join that of patients with normal MEPLT times at T.,
Additionally, all patients with neurological deficits had increased MEPLTs
along the affected pathway, confirming the high sensitivity of MEPLTs in detecting neural dysfunction (Chokroverty, Sachdeo, Dilullo, & Duvoisin, 1989; Dvorak et al., 1991; Uozumi et al., 1991; Wilbourn & Aminoff, 1988).
Eight
patients had abnormally high MEPLT in one root each at T, (table 3.1, roots marked P). Of these eight patients only four had clinical signs of neurological deficit.
Motor conductionalterations in lumbar sdnal stenosis
The FIM score was highly influerxed by the surgical procedure because it is based on the patient's functional state (figure 3.2).
Following surgery, the
patients did not perform well in items five and six of the FIM score (locomotion) because of pain at the iliac crest (donor site). The changes in the FIM score at T, were not matched by changes in the neurological or the electrophysiologicai examinations. This has been shown previously in the literature (Ota et al., 1996). The FIM score and the ASIA score do however show a similar change i n the last four months of the follow-up period (between T, and T,).
The motor evoked potential test measures neural conduction time from the motor cortex to the target muscle.
The motor pathway can be divided
anatomically into a central motor pathway which runs form the motor cortex to the anterior horn cells in the spinal cord, and the peripheral motor pathway the stretches from the anterior horn cell to the target muscle. With the spinal cord ending at the L1112 level, compression within the lower lumbar spine does not affect the spinal cord itself but rather the roots. In accordance, we found that all the patients who had a prolonged MEPLT had an increased PMCT as well. The CMCT was normal. The high correlation found between the MEPLT and the PMCT indicates that the two entities could be used interchangeably once peripheral neuropathy has been ruled out. This is particularly useful for the follow-up of patients with conditions that may affect F-wave latencies (Abbruzzese, Vische, Ratto, Abbruzzese, & Favale, 1985; Drory et al., 1993; Eisen & Odusote, 1979; Fierro et al., 1990; Fisher, 1983; Fisher & Penn, 1978;
Motor anduction alterations in lumbar spinal stenosis
Fox & Hitchcock. 1987; McComas, Sica, & Upton, 1970). In parallel, one could hypothesize that the MEPLT could be used to follow progress in the L2, L3, and L4 roots, but precise data on this subject are lacking. Following surgery, there was a rapid improvement in the MEPLTs to both the EDB and the AH (figures 3.3 and 3.4).
MEPLTs to six muscles fell to normal
values at one week post-operatively, and at one month the number of muscles with prolonged MEPLTs had gone down to 60 (from 90 at To). At two m ~ n t h s there were 33 muscles with abnormal MEPLTs. At T4 only thirteen muscles had prolonged MEPLTs. The change in MEPLT appeared to precede that of the neurological examination. The multiple regression model run on the MEPLTs showed that the MEPLTs at T, and T, have an excellent predictive power of MEPLT outcome at T4 (? = 0.762). When the regression model had the ASIA score at T4 as the dependent variable and the MEPLT at variable times as the independent variable (table 3.2), it was found that the MEPLT at T, has a good predictive value (P > 0.326). When the MEPLTs at To and T, were added, this improved the predictive power considerably (P s 0.503). When the FIM score was used as the dependent variable in the same model, the MEPLT failed to predict outcome (? = 0.124). From these models, it can be said that MEPLT at one month post-operatively can be used to predict both the MEPLT and the clinical outcome at six months. Patients are usually seen for the last time at one month post-operatively unless there are post-operative complications. A simple electrophysiological examination can now help the physician decide on a line
Motor conduction alterations in lumbar spinal stenosis
of action. If the MEPLTs zre not improved at one month, the patient can be scheduled for more aggressive rehabilitation and follow-up.
The power of MEPs in detecting neural dysfunction varies according to the study and the affection. Jaskolski reported abnormal CMCTs in 63% of patients with cervical spondylotic myelopathy (Jaskolski, Jarratt. & Jukubowski, 1989). In a larger study, Maertens de Noordhout (Maertens de Noordhout, Remacle, Pepin, Born, & Delwaide, 1991) reported that 84% of their spondylotic myelopathy patients had altered CMCT.
Dvorak reported that 65% of his
patients with spinal stenosis had prolonged MEPs but also that about 20% of subjects with increased MEP latency times did not have any clinical signs of neural dysfunction (Dvorak et al., 1991). asymptomatic
patients with
Tavy reported that 25% of
isolated radiological evidence
of
spinal
compression had altered MEPs (Tavy et al., 1994). A direct relation between clinical signs and increased latency times has not been established.
Nerve
conduction studies (including MEP and SSEP) evaluate the general quality of the nerve fibers and are particularly affected by demyelinating processes. The clinical examination on the other hand is more quantity-dependent. In this study we found that the MEPLTs showed a faster recuperation rate than the clinical signs and the functional state of the patient. All four patients with persistent signs of neural deficit at T4 had prolonged MEPLTs while only one of the eight with persistent symptoms had prolonged MEPLTs. The clinical condition of the patient and the MEPLT data showed good correlation at TO and at T4, when the
Motor conductionalterations in lumbar spinal stenosis
two clinical condition was at the extreme of the spectrum. The last half of the study showed the largest change in clinical signs while the MEPLT had a more rapid change in the beginning of the study. This observation should be further investigated before conclusion can be reached because of the rather small number of subjects in this study.
In conclusion, this study has clearly demonstrated the clinical value of MEPs i n the follow-up of patients after spinal decompression. MEPs were able to predict the clinical outcome as early as one month post-operatively. This should help the physician plan a more suitable rehabilitation program based on objective parameters. MEPs were found to be more sensitive to changes in motor conduction than the clinical examination and the two did show good agreement at the end of the six-month study period.
Molar conductionallerationsin spinal stenos*
Annex 3.1
Motor crrnduaion alteahns in lumbar spinal stenosis
Annex 3.2 FlM Form
Date: Hospital #:
Visit:
Pre-op
post-op 1
post-op 2
post-op 3
post-op 4
1. Bathing 2. Dressing
3. Toileting 4. Mobility (transfer to bed/chair/toilet/shower)
5. Locomotion/walking 6. Locomotion/stairs
7. Bladder management 8. Bowel management
7 = Complete independence: the activity is performed safely, without modification, assistive devices or aids, and within a reasonabletime. 6 = Modified independence: the activity requires an assistive device and/or more than reasonable time and/or is not performed safely. 5 =Supervision or special setup: no physical assistance is needed. but cueing. coaxing or special setup is required. 4 = Minimal contact assistance: subject requires no more than touching and expends 75% of the effort required in the activity. 3 = Moderate assistance: subject requires more than touching and expends 50-75% of the effort requires in the activity. 2 = Maximal assistance: subject expends 25-50% of the effort required in the activity. 1 = Total assistance: subject expends 0-25% of the effort required in the activity.
Motor conduction alterationsin lumbar spinal stenosis
ANNEX 3.3
: 140 Root-specific :Datasets placed in normal and abnormal 35 Patients at To :datasets separated: subgroups following MEPLT results at TO :into L5 & S1 groups
:
31 L5 roots with normal MEPLT at TO L5
S1
39 W roots with abnormal MEPLT at To
L5
19 S1 roots with normal MEPLT at To
SI
-
* :.
51 S1 roots with abnormal MEPLT at TO
Organisational chart: The data from the 35 patients were separated into two groups (L5, SI). The root-specific data was then separated into normal and abnormal subgroups according to the MEPLT result at TO.
Motor condudion alterations in lumbar spinal stenosis
Chapter 4
Motor conduction alterations in lumbar spinal stenosis
Summary and Conclusions The passage of knowledge from the bench to the bedside is not an easy task. In vitro tests are usually conducted under ideal condition with every variable accounted for, stratified, and then normalized. The findings are then extrapolated and applied to in vivo situations. In spite of that, in vitro methods have given us great insight on the physiological mechanisms involved in many areas, especially in electrophysiology. The Cole and Curtis studies on the giant axon of the squid is just one example of such experiments (Cole & Curtis, 1939). Hodgkin and Katz brought forward the idea of ion channels and the importance of the cell membrane in generating action potentials (Hodgkin & Katz, 1949). With that, it became easier to understand and explain the effects of noxious stimuli, such as mechanical compression and ischemia, on nerve conduction (Kobrine et al., 1979; Olmarker et al., 1990; Owen et al., 1989; Owen, Naito, & Bridwell, 1990a; Owen, Naito, Bridwell, & Oakley, 1990b; Pedowitz, Nordborg, Rosenqvist, & Rydevik, 1991; Rydevik, 1993). The difficulty in designing in vivo experiments is the lack of adequate models. In addition, no subjective data can be obtained from such studies. Using humans in in vivo studies has many limitations both physically and morally.
In the first study, we chose a human modei to conduct our motor conduction studies. Patients with confirmed lumbar spinal stenosis were recruited. By using transcranial magnetic MEPs, this study assessed the effect of the transient
Motor conductionalterations in lumbar spinal stenosis
ischemia brought on by claudication on motor conduction along the entire motor pathway. From the work of Olmarker and Rydevik (Olmarker et at., 1991; Olmarker et al., 1989b; Rydevik, 1992), nerve root compression appears to be more of an ischemic process than due to direct compression. Owen and coworkers and Kai and coworkers (Kai, Owen, Allen, Dobras, & Davis, 1994; Kai et al., 1993; Owen et al., 1988; Owen et al.. 199Gb) have demonstrated that ischemia causes changes in motor conduction. Our results showed that motor conduction velocity decreased significantly after exercise. This is consistent with the ischemic hypothesis brought on by Rydevik (Rydevik, 1993). What remains to be understood is the exact mechanism of pain genGration during claudication. The ischemic theory could also be evoked here. Pain could be the result of accumulation of metabolic biproducts that are noxious in nature, and due to the reduced blood flow, are not washed out quick enough.
In the second study, patients undergoing spinal decompression were monitored clinically and electrophysiologically over a period of six months.
The
relationship between MEPs and the patient's clinical and functional state following surgery was investigated. The idea here was that motor conduction is more sensitive to changes than clinical signs. In order for the clinical signs to improve, an important number of nerve fibers must improve. Improvement i n nerve conduction can be observed more rapidly because of neural summation and recruitment at more distal locations ensuring the production of an evoked response. We found that there were improvements in motor conduction as early
Motor conduction alterations in lumbar spinal stenosis
as one week post decompression. The earliest signs of clinical improvement came at one month post decompression and the most part was at six months.
We explored the power of MEPs measured in the early post-operative period to predict clinical outcome at six months. Here again the MEP test had excellent predictive powers. The multiple regression model run on the MEPLTs showed that the MEPLTs at one week and at one month have an excellent predictive power of MEPLT outcome at six months. In addition, MEPLT at one month postoperatively showed an excellent power to predict both the MEPLT and the clinical outcome at six months. Patients are usually seen for the last time at one month post-operatively unless there are post-operative complications. A simple electrophysiological examination can now help the physician plan the postoperative period. If the MEPLTs are not improved at one month, the patient can be scheduled for more aggressive rehabilitation and follow-up.
Motor evoked potentials through magnetic stimulation of the motor cortex is non-invasive and easy to use. They have now become part of the neurological work-up of patients undergoing spinal decompression. The test itself takes about 30 minutes and is usually coupled with the nerve conduction tests. It has been shown that it is a good diagnostic tool, and now we have shown its prognostic capabilities. Motor evoked potentials through magnetic stimulation however can not replace peripheral nerve conduction studies. The areas
Motor conduction alterations in lumbar spinal stenosis
stimulated in the motor cortex are not focal enough so that polyphasic wave forms are often seen (figures 1.7 and 1.8). Supramaximal stimulation can not be achieved and so the amplitude of the contraction can not be used for quantification. But it is an excellent tool to measure central motor conduction and conduction along nerve roots where conventional stimulation is not possible.
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Motor conduction alterations in lumbar spinal stenosis
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Motor conduction alterations in lumbar spinal stenosis
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