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ISSN 2313-8254 (English ed. Online)
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ISSN 2309-1681 (Russian ed. Online)
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BURDENKO'S JOURNAL
OF NEUROSURGERY
Media Sphera
114 BURDENKO'S JOURNAL OF NEUROSURGERY 6, 2019
Reviews
The article is devoted to analysis of long-term outcomes of
surgical treatment of cervical spine degeneration. Considering
increased life expectancy of people in developed countries, greater
number of patients with degenerative spine diseases is expected.
New surgical technologies appear in response to this tendency.
First of all, effectiveness of certain technology is determined by
postoperative outcomes. The authors performed a meta-analysis
of long-term outcomes of surgical treatment of patients with
cervical spine degeneration and compared two technologies —
total arthroplasty and anterior cervical spinal fusion surgery.
A meta-analysis enrolled 9 randomized controlled clinical trials
comprising 2439 patients with cervical spine degeneration. Long-
term postoperative results were analyzed. The study was carried
out in accordance with international recommendations for
systematic reviews and meta-analyses (PRISMA). It should be
noted that the authors use the Review Manager 5.3 software
“Research Bias Risk Assessment” to evaluate each study included
in this meta-analysis. The authors showed that total arthroplasty
is characterized by significantly better clinical efficacy in patients
with cervical spine degeneration in long-term postoperative
period. I would like to note that consideration of arthroplasty as
a secondary approach, in my opinion, is not entirely correct.
The same is true for the term "gold standard". The last decade has
clearly shown that medicine is becoming more personalized (“4P
medicine”). Today we have the opportunity to choose a treatment
strategy considering the goals and individual characteristics of a
particular patient. In this context, similar safety of both methods
is more important than data on superiority of one method over
another. In general, the article is devoted to a relevant issue due
to thorough methodology and evidence-based analysis. The report
may be recommended for the use in educational programs and
lectures as an example of correct approach.
A.G. Nazarenko (Moscow, Russia)
Commentary
115
BURDENKO'S JOURNAL OF NEUROSURGERY 6, 2019
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In search of an effective algorithm for rhythmic transcranial magnetic
stimulation in neurorehabilitation after severe traumatic brain injury
© M.M. KOPACHKA1, E.V. SHAROVA2, E.V. ALEKSANDROVA1, E.M. TROSHINA1, O.S. ZAYTSEV1,
A.D. KRAVCHUK1, A.A. POTAPOV1
1Burdenko Neurosurgical Center, Moscow, Russia;
2Institute of Higher Nervous Activity and Neurophysiology, Moscow, Russia
ABSTRACT
Rehabilitation of patients with severe traumatic brain injury (sTBI) is a topical medical and social issue because this pathology is
one of the main causes of mortality and disability in the young working age population [1]. The most common sTBI consequences
include motor and cognitive impairment as well as depression of consciousness [2, 3]. Despite significant progress in treatment of
the consequences of severe traumatic brain injury, there are no treatment and rehabilitation standards for these patients, and the
used rehabilitation measures are not always effective. These circumstances substantiate the need for the development of additional
methods of neurotherapy.
Over the past decade, transcranial electrical and magnetic stimulation (TMS) has been increasingly used as neuromodulatory treat-
ment in clinical practice [4―12]. The accumulated experience has shown that transcranial neurostimulation methods require a
more individualized approach in terms of both careful selection of patients and choice of exposure parameters.
This review is based on an analysis of the most significant publications and recommendations recognized in the scientific com-
munity, as well as on reports of domestic and foreign authors presented at dedicated congresses in comparison with experience
of our own research on transcranial stimulation. The paper discusses the main problems of using this method in medical practice
of sTMI and their possible solutions.
Keywords: rhythmic transcranial magnetic stimulation (rTMS), severe traumatic brain injury (sTBI), impaired consciousness and
motor activity, neurorehabilitation.
INFORMATIONS ABOUT THE AUTHORS:
Kopachka M.M. — https://orcid.org/0000-0003-2907-4030;
Sharova E.V. — https://orcid.org/0000-0003-4994-4187;
Aleksandrova E.V. — https://orcid.org/0000-0001-5327-314X;
Troshina E.M. — https://orcid.org/0000-0002-6863-5868, e-mail: ETroshina@nsi.ru;
Zaytsev O.S. — https://orcid.org/0000-0003-0767-879X;
Kravchuk A.D. — https://orcid.org/0000-0002-3112-8256;
Potapov A.A. — https://orcid.org/0000-0001-8343-3511
Corresponding author: Troshina E.M. — e-mail: ETroshina@nsi.ru
TO CITE THIS ARTICLE:
Kopachka MM, Sharova EV, Aleksandrova EV, Troshina EM, Zaytsev OS, Kravchuk AD, Potapov AA. In search of an effective algorithm for
rhythmic transcranial magnetic stimulation in neurorehabilitation after severe traumatic brain injury. Burdenko’s Journal of Neurosurgery = Zhurnal
voprosy neirokhirurgii imeni N.N. Burdenko. 2019;83(6):115-123. (In Russ.). https://doi.org/10.17116/neiro201983061115
Burdenko's j ournal of n eurosurgery
2019, №6, pp. 115-123
https://doi.org/10.17116/neiro201983061115
Introduction
Rehabilitation of patients with severe traumatic
brain injury (BMI) is an urgent medical and social
problem, since this pathology remains one of the
main causes of mortality and disability of
the population of young working age [1]. The most
common consequences of PMTCT include motor
and cognitive impairment, as well as depression of
consciousness [2, 3]. Over the past decade,
transcranial electrical and magnetic stimulation
(TMS) has been increasingly used as a
neuromodulatory effect in clinical practice [4—12].
Historical reference
TMS has been used as a diagnostic tool since 90s
of the twentieth century. This method is recognized
as informative procedure for assessing anatomical
integrity of corticospinal tract and functional state of
human nervous system. The first foreign and national
researches of TMS concerned analysis of motor
cortex excitability and conduction along
corticospinal pathways [4, 13, 14]. These studies
showed that TMS is sensitive and perspective
method, its diagnostic and curative capabilities are
much wider and also related to functional assessment
116 BURDENKO'S JOURNAL OF NEUROSURGERY 6, 2019
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of visual cortex, speech and memory centers in both
neurological and mental diseases [15]. TMS may be
valuable to evaluate integrity and functional state of
nervous pathways in various forms of central nervous
system pathology [16]. Moreover, stimulation of
different cortical areas in a healthy person and
analysis of concomitant functional effects are useful
to clarify structural and functional organization of
the brain [17]. The last one is important for
theoretical and scientific purposes.
Transcranial and peripheral rhythmic magnetic
stimulation was observed to be effective curative
measure besides diagnosis [18].
Currently, rhythmic TMS (rTMS) is one of the
most common and popular procedures not only in
neurology, but also in neurobiology as a whole.
Significant increase of interest in this approach in
recent years is shown in Fig. 1.
According to the PubMed database, the number
of reports devoted to rTMS only for neurological
diseases has been increased from single ones to 360—
400 per year since 1988 (Fig. 1). Reviews account up
to 20% of these publications (Fig. 2).
This report is based on analysis of the most
significant publications and recommendations
recognized by the scientific community. We also
consider the reports of national and foreign authors
and own experience of transcranial stimulation.
The use of rTMS is comprehensively described
in reviews [4, 17, 18, 19]. rTMS is effective for relief
of various neurogenic pain syndromes including
phantom pain, post-stroke thalamic pain,
compression cervical and lumbar pain syndromes,
etc. [16, 18, 20]. Exposure points are various parts of
the brain and spinal segments, as well as peripheral
nervous system depending on zone of interest and
expected functional effects. This method is used in
the treatment of depression, pathological neurogenic
tinnitus, epilepsy, migraine and migraine-like
symptoms [4]. TMS is also applied to alleviate
clinical manifestations of Parkinson's disease [21,
22]. Antispastic effect of some modes of magnetic
stimulation is used for the management of spasticity,
overactive bladder syndrome, hemifacial spasm,
cerebral palsy and other diseases with similar
pathogenesis [4]. Perhaps, rTMS is very actively used
for the treatment of depression [23], neurogenic pain
syndromes, as well as to compensate motor
deficiency in patients with limb paresis [24]. There
are effective rTMS modes for treatment of
consequences of stroke [4, 25—27], including
protocols incorporated into international
guidelines [28]. rTMS protocols for head injury are
less clear [5, 29, 30]. rTMS for restoration of patients
with impaired consciousness after severe TBI is being
studied [7, 29, 25, 31—33].
TMS mechanisms
Therapeutic effect of rTMS is based on change
of cortical excitability, depolarization of neurons
with subsequent appearance and distribution of
action potential (AD) [4, 13]. TMS combines the
advantages of non-invasiveness and painlessness.
Moreover, this method is also characterized by more
local effect compared to electrical stimulation [13,
19, 34]. More recent studies revealed that TMS
affects some other processes such as redistribution
of cerebral blood flow [36], release of brain-derived
neurotrophic factor and dopamine, activity of some
enzymes [17] besides excitation and inhibition per
se [4, 35]. Perhaps, “non-electric” effects of TMS
are associated with its initial action at the molecular,
atomic and subatomic (quantum) levels [37, 38].
Rhythmic TMS allows non-invasive stimulation
of brain neuronal structures with short magnetic
pulses. Comprehensive studies using EEG and
diffusion-tensor magnetic resonance imaging (DT
MRI) showed improved functional and structural
communications and integrative activity after brain
stimulation [39].
Modern devices are capable to create 4 T
electromagnetic fields and stimulation frequency
over 100 Hertz. Magnetic impulse is generated in a
plane perpendicular to the coil and non-invasively
penetrates through the body’s tissues (skin, muscles,
bone, etc.) to a depth of 10—15 centimeters. This
impose causes own excitation of neuronal structures
with subsequent spread of action potential [24].
Methodological features of rTMS
The effects of rTMS are determined by
characteristics of electromagnetic field of the
inductors. These features largely depend on the
shape, dimensions, design of electromagnetic coil
and its orientation in relation to the patient’s head.
Annular, 8- and H-shaped coils of various diameters
are the most common. Annular coils result quite
powerful, but relatively poorly localized stimulation.
At the same time, dual 8-shaped coils produce more
focal (with an accuracy of 1 cm) but slightly less
powerful pulses. Stimulation of the structures close
to the scalp surface, for example cerebral cortex or
cerebellum, may be performed using 8-shaped coil.
In case of tangential placement of the coil in relation
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to scalp, the probability of stimulation is maximum
in those areas oriented parallel to central segments
of the coil [19]. Stimulation of larger areas is carried
out using annular coils. Special H-shaped coils are
used for stimulation of deep brain structures
(hippocampus, subcortical structures, brain
stem) [40]. Dual coils have recently appeared. In this
devices, single Faraday’s coils are placed under
certain angle to each other rather in parallel fashion.
Development of stimulation technique and new coils
for TMS is continued [4, 41].
Shape of magnetic pulse is important physical
characteristic. It is monophasic or biphasic as
a rule [34]. Monophasic impulses are preferable for
basic researches, since it is believed that such stimuli
excite relatively uniform columns of neurons in
certain zone. Thus, more clear and obvious
functional effects are obtained due to less
involvement of adjacent structures [4, 13]. However,
generation of this impulse requires complex magnetic
stimulator. In addition, significant energy
Fig. 2. Number of reviews devoted to application of rTMS in neurology (PubMed database).
Fig. 1. Number of publications devoted to application of rTMS in neurology (PubMed database).
118 BURDENKO'S JOURNAL OF NEUROSURGERY 6, 2019
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consumption also limits the widespread use of
monophasic TMS.
Currently, foreign and national manufacturers
offer various modifications of magnetic stimulators.
It is necessary to emphasize separately the navigation
systems for TMS. These systems are used to visualize
stimulation zones. These complexes make it possible
to load previously performed MRI scans of the brain
into the system with subsequent 3D reconstruction
using special cameras and sensors on the patient’s
head and the coil. This system allows on-line virtual
projection of coil position on the surface of cerebral
cortex with fairly high accuracy after computer
processing and special calibration to take into
account errors and soft tissue thickness. These
complexes open up new possibilities for both
scientific researches and precise clinical use of TMS.
The most significant drawbacks of such systems are
extremely high cost (ten times more expensive than
conventional “blind” TMS systems) and need to
involve large personnel and time resources
(specialists for radiation diagnosis). Until now, above
described TMS navigation systems are used only in
few laboratories [17, 27, 32].
Recommendations for therapeutic rhythmic
transcranial magnetic stimulation: accumulated
questions
Most of TMS effects as well as basic ideas about
nature of impulses were obtained in researches of
motor cortex in animals and, subsequently, humans
as the most accessible system for evaluation and
analysis. Clear, topographically determined motor
response, determining its threshold for selection of
individual stimulus power and relatively good
reproducibility of the effects justified the choice of
this zone for stimulation. Current guidelines [4, 13,
42] concern mainly diagnostic and therapeutic
stimulation of motor cortex. At the same time,
significant problems are associated with sensitivity
threshold determination and stimulation intensity
selection for other brain structures in the absence of
a distinct functional (behavioral) response. Analysis
of bioelectrical activity of the brain during rTMS may
be perspective solution of this problem [11, 36, 43].
However, this method is not generally accepted.
Probably for this reason, some researchers use
TMS parameters effective for the motor cortex
during stimulation of various cortical zones that is
not entirely correct. The problem is very relevant for
pathology followed by with increased and reduced
cortical excitability when interpretation of results and
their comparison with normative data are difficult
[4, 12].
TMS can cause the effect of short-term excitation
and inhibition since TMS-induced action potential
in a neuron propagates along the axon and is able to
activate many surrounding neurons of various
modalities through the synapses [40]. Certain general
principles of therapeutic stimulation have been
developed for a long follow-up period (2000—2015)
and published in guidelines with various evidence
levels [4, 18, 42].
Methodological issues also include the choice of
rTMS intensity: suprathreshold, threshold or
subthreshold. The last one varies in different studies
from 90—80% [33, 27] to 50% of the motor
threshold. Moreover, various researchers conduct
stimulation using a wide range of power parameters
in accordance with modern guidelines on TMS
safety [45]. Therefore, significant variability in
stimulation protocols is obtained.
Two rTMS frequency modes were distinguished
(“inhibitory” and “activating”) according to the
results of theoretical and practical studies in the
90s—2000s. The first mode was stimulation with a
frequency of less than 2 Hz causing the so-called
LTD effects (long-term depression), the second
mode — stimulation with a frequency over 2—5 Hz
causing LTP effects (long-term potentiation). These
ideas became the basis for development of various
rTMS protocols implying different frequencies and
stimulation powers, as well as the number of stimuli
(it is assumed that greater number of stimuli cause
more persistent effects) and intervals between
stimulus packets (different types of theta-burst
stimulation) [4, 45, 46].
However, multiple rTMS data have been
accumulated which do not fit into this scheme [47,
48]. A certain positive effect of rTMS was noted by
various authors regardless of stimulation mode [5,
26, 39]. A.V. Chervyakov et al. [27] compared the
effects of TMS of the motor cortex with frequencies
of 1 Hz and 10 Hz in patients with stroke. The
authors reported positive effect of various modes on
motor functions. Some foreign authors confirmed
these results [49, 50]. Thus, the idea about exciting
physiological effects of high-frequency rTMS and
inhibitory ones of low-frequency stimulation turned
out to be very simplified [15, 48].
Perhaps, functional effects of rTMS are largely
determined by the basal state of the brain tissue and
its excitability. The last one may be significantly
altered in patients with brain diseases including
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severe TBI. This assumption is consistent with the
ideas of classical neurophysiology and confirmed by
some recent trials. It is shown that potentiation or
inhibition effect of stimulation substantially depends
on initial functional state of neural networks (so-
called “resting-state condition”). This condition
depends on many factors which seem insignificant
at first glance even in healthy people: sleep
deprivation on the eve of the procedure, emotional
state, hormone levels, dependence on circadian
rhythms, etc.
In this regard, even recognized leading experts
are currently reviewing the above-mentioned initial
principles of rTMS although these approaches were
considered fundamental 10—15 years ago [35]. There
is a tendency towards refusal strictly regulated
protocols to obtain reproducible effects in favor of
predominantly individualized approach. This method
considers initial cortical excitability [51] and ensures
selection of rTMS parameters taking into account
features and functional characteristics of initial state
of central nervous system [52]. For example, reduced
or absent reactivity in response to TMS in those brain
areas with PET-confirmed metabolic impairment is
described in the literature [53].
The protocols with different duration, power and
number of sessions are used for most stimulation
zones due to the absence of clear recommendations.
The only common aspects for most of them are
adherence to guidelines on safety of rTMS of the
International Federation of Clinical Neurophysiology
(IFCN) [44] and selection of TMS frequency in
accordance with the above-described principle
(classic LTP-LTD technique). Stimulation protocols
for the treatment of neuropathic pain and
depression are characterized by the highest evidence
level (class A) [4].
An important problem of rTMS in patients with
severe TBI followed by impaired motor sphere and
consciousness is the choice of the “target” for
stimulation.
Thus, positive effects of stimulation of primary
motor and prefrontal cortex were reported in patients
with motor disorders [17]. Stimulation of sagittal
parts of motor area was effective in patients with
Parkinson's disease [4]. Isolated potentiation rTMS
of the motor cortex [4, 27, 30] in damaged
hemisphere or in combination with inhibitory
stimulation of the intact hemisphere [4, 25] is used
after stroke. More recent studies have shown that the
most effective motor recovery after stroke is ensured
by stimulation of either both hemispheres [27,47] or
low-frequency rTMS of only intact hemisphere [54].
It should be emphasized once again that these
protocols are actively being reviewed [49, 50].
Inconsistencies in attempts to use standardized
approaches have been previously noted. For example,
Pino et al [55] proposed a bimodal balance model of
stimulation where the choice of mode is associated
with intact structural reserve.
Stimulation of occipital area [7], prefrontal
cortex [33], as well as unilateral stimulation of
primary motor cortex with more significant positive
effect of left hemispheric stimulation are used [4, 31]
for recovery of impaired consciousness [56]. rTMS
of gyrus angularis was described and more significant
effect was noted in patients with minimum
consciousness rather vegetative state [32]. rTMS of
sagittal parts of premotor cortex is perspective for
activation of voluntary attention and motor sphere
in case of vegetative state and akinetic mutism [29,
57]. Some authors note moderate positive effects of
stimulation. Complications of rTMS [27] and
individual characteristics of damaged brain response
to stimulation are less commonly analyzed [53].
Considering above-mentioned references, the
choice of a “target” for rTMS is often determined by
general ideas about topographic anatomy or
neurophysiology of impaired function. At the same
time, an important but not always taken into account
aspect of stimulation (largely due to insufficient
knowledge) is functional integrity and features of
interaction of stimulated structures with other ones
that makes impossible the use of "mechanistic"
approach. We cannot argue that functional effects of
stimulation of certain brain area are due solely to
direct effect on the structures in projection of
magnetic coil. Interaction of individual brain areas,
functional communications and pathways,
orthodromic and antidromic TMS-induced spread
of excitation, as well as accumulation effect should
be also considered. Considering hierarchical
organization of nervous system, stimulation of higher
systems followed by functional modulation of
underlying structures and vice versa are discussed
within the concepts of positive and negative
feedback [4,18].
It is important to emphasize that the problems
of network and hierarchical organization of central
nervous system in norm and disease are among the
urgent for neuroscience. In this regard, various
questions concerning systemic brain responses to
stimulation, rTMS protocols for various CNS
diseases (including the choice of individual “targets”
120 BURDENKO'S JOURNAL OF NEUROSURGERY 6, 2019
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for stimulation), as well as evaluation of results are
still of significant research interest [4, 11, 58].
Conclusion
Thus, the prospects of rTMS and need for its
further development and clinical introduction are
obvious despite some problems of the use of rTMS
in neurorehabilitation of patients with TBI. In our
opinion, the priority should be given to individualized
selection of stimulation parameters to resolve this
problem. Stimulation mode should be based not only
on patient’s clinical condition and localization of
lesions, but also on analysis of cerebral bioelectric
activity. This is especially true for patients with severe
TBI followed by multi-focal or diffuse lesion as a
rule.
The authors acknowledge scientific secretary of the
Burdenko Research Center of Neurosurgery, associate
professor of the Department of Neurosurgery with
neuroscience courses, doctor, Ph.D. Gleb Valerievich
Danilov for assistance in preparing the diagrams.
This research was supported by the RFBR grant 16-
29-08304 ofi_m.
The authors declare no conflict of interest.
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Received 22.04.19
