Vol 15, No 4 (2021)

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Full Issue

Original articles

Repetitive transcranial magnetic stimulation in the treatment of mild cognitive impairment due to cerebral small vessel disease

Lagoda D.Y., Dobrynina L.A., Suponeva N.A., Bakulin I.S., Poydasheva A.G., Tsypushtanova M.M., Kadykov A.S., Piradov M.A.


Introduction. Mild cognitive impairment (MCI) negatively affects patients’ quality of life and is a risk factor for dementia. One of the main causes of MCI is cerebral small vessel disease (CSVD). The previously established link between decreased activity in the supplementary motor area (SMA) and cognitive impairment in patients with CSVD makes it possible to consider repetitive transcranial magnetic stimulation (rTMS) of the SMA with functional magnetic resonance imaging (fMRI)-assisted positioning as a promising method for treating MCI caused by CSVD.

The aim of the study was to evaluate the efficacy and tolerability of fMRI-guided rTMS of the SMA in patients with MCI caused by CSVD.

Materials and methods. Twenty patients were randomly assigned to the intervention (SMA stimulation; n = 10) and the control (vertex stimulation; n = 10) groups. All patients underwent 10 sessions of high-frequency rTMS. The MoCA scale, trail making test, Tower of London test, and copying and delayed recall in the Rey–Osterrieth complex figure test were used to assess treatment effect. Testing was conducted before, immediately after and 3 months post rTMS.

Results. The intervention group demonstrated a significant improvement in the MoCA, the Tower of London test and delayed recall in the Rey–Osterrieth complex figure test immediately after rTMS. Statistically significant improvement in the MoCA and the Tower of London test results was maintained after 3 months. No statistically significant improvements were found in the control group. Groups were comparable in the incidence of headache during and in the 24-hour period after the stimulation session, and in unpleasant sensations during the session.

Conclusion. fMRI-guided rTMS of the SMA is an effective and promising treatment method for MCI caused by CSVD, with effects lasting three or more months, and good tolerability.

Annals of Clinical and Experimental Neurology. 2021;15(4):5-14
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Hybrid revascularization of the heart and brain: which carotid endarterectomy is preferable?

Kazantsev A.N., Vinogradov R.A., Artyukhov S.V., Roshkovskaya L.V., Matusevich V.V., Bagdavadze G.S., Lider R.Y., Janelidze M.O., Chikin A.E., Zaitseva T.E., Linets Y.P.


The aim of this study was to analyse the inpatient and long-term results of hybrid surgery, incorporating percutaneous coronary intervention (PCI) and different types of carotid endarterectomy (CEA).

Materials and methods. A prospective, open-label cohort comparison study was conducted in 2018–2020 and included 363 patients with atherosclerosis of both the internal carotid artery (ICA) and coronary artery, who underwent hybrid revascularization of the brain and myocardium. All patients were divided into four groups based on the revascularization strategy: group 1 (n = 107; 29.5%) — PCI + eversion CEA; group 2 (n = 98; 27%) — PCI + classic CEA with patch angioplasty; group 3 (n = 72; 19.8%) — PCI + glomus-sparing CEA according to R.A. Vinogradov; and group 4 (n = 86; 23.7%) — PCI + glomus-sparing CEA according to A.N. Kazantsev. The follow-up period was 20.8 ± 8.0 months.

The patient received a loading dose of clopidogrel (300 mg) before the PCI, and the procedure was then performed in an endovascular operating room. A radial artery catheter was inserted, and the patient received 10,000 IU of intravenous heparin before the procedure. After the PCI, the patient was taken to the vascular operating room, where they underwent the CEA. The patient received 5,000 IU of intravenous heparin before artery clamping. Glomus-sparing CEA according to A.N. Kazantsev was performed as follows: an arteriotomy was conducted along the internal edge of the external carotid artery (ECA), adjacent to the carotid sinus and 2–3 cm above the ostium, and extending to the common carotid artery (CCA) (also 2–3 cm below the ECA ostium), depending on the size of the atherosclerotic plaque. The ICA was transected in the area bound by the ECA and CCA walls. Eversion CEA of the ICA was performed, followed by open CEA of the ECA and CCA. The ICA was implanted in its previous position in the preserved area.

Results. No mortality was recorded during the inpatient follow-up period. All cases of myocardial infarction occurred after eversion and classic CEA: 3 in group 1 (2.8%) and 1 in group 2 (1.02%); р = 0.2. No ischaemic stroke was recorded only in patients who underwent CAE according to A.N. Kazantsev (р = 0.66); however, ischaemic stroke occurred in two patients in group 1 (1.8%), in two patients in group 2 (2.04%) and in one patient in group 3 (1.38%). The highest number of cardiovascular events occurred in group 1, due to carotid glomus injury, which led to poorly controlled hypertension during the inpatient stay. This tendency influenced the composite endpoints (death + myocardial infarction + ischaemic stroke), which were highest in group 1 (5 or 4.6%) compared to 3 (3.06%), 1 (1.38%) and 0 in groups 2–4, respectively (р = 0.18). The groups were comparable in the frequency of long-term complications. However, the incidence of ICA restenosis was lowest and no ECA thrombosis/occlusion was observed after glomus-sparing CEA according to R.A. Vinogradov and A.N. Kazantsev.

Conclusion. A hybrid PCI + CEA for brain revascularization should be glomus-sparing. CEA according to A.N. Kazantsev was characterized by lack of procedural arteriotomy complications. This procedure enables blood pressure monitoring in the postoperative period, thus minimizing the risk of cardiovascular complications.

Annals of Clinical and Experimental Neurology. 2021;15(4):15-26
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EEG features in patients with Parkinson's disease during directional perception of olfactory stimuli

Kozhevnikov S.P., Ivanova I.L., Komissarova N.V., Shubina A.V., Vlasov M.A.


Introduction. Olfactory dysfunction is considered to be an early and relatively important marker of Parkinson's disease (PD). Olfactory studies using objective neurophysiological methods may become one of the diagnostic tests to identify individuals with a high risk of developing PD.

The aim of the study was to assess the spectral and topographic characteristics of bioelectrical brain activity in patients with PD during directional perception of olfactory stimuli.

Materials and methods. This study included 30 patients with PD (mean age was 66.5 ± 6.5 years). The control group consisted of 20 people without PD (mean age was 65.3 ± 8.5 years). Lavender oil, clove oil, camphor oil and β-mercaptoethanol solution (an aversive stimulus) were used for olfactory stimulation, while distilled water was used as a control test. The test subject sat with their eyes closed and inhaled the presented smell for 30 seconds, while an EEG recording was made during this time.

Study results. Olfactory stimulation in patients with PD showed increased synchronicity of the α3 rhythm in the right hemisphere, as well as the θ rhythm in the parieto-occipital regions of both hemispheres. These changes indicate significant activation of internal (endogenous) attention, increased overall, non-specific readiness potential, as well as the involvement of the limbic-reticular complex in olfactory perception. Olfactory perception in the control group was accompanied by reduction in the α1 rhythm amplitude in the parieto-occipital regions bilaterally, which may indicate moderate activation of external (exogenous) attention and the posterior attention system responsible for simple perception processes.

Conclusion. Increased α3 rhythm amplitude in the right hemisphere and increased θ rhythm amplitude, observed during directional olfactory perception, may indicate olfactory dysfunction and should be viewed as an additional indicator when establishing a diagnosis of Parkinson’s disease.

Annals of Clinical and Experimental Neurology. 2021;15(4):27-35
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Surgical results for hypertensive intracerebral hemorrhagesdepending on intervention timing

Dashyan V.G., Godkov I.M., Prokop’ev L.V., Grin A.A., Krylov V.V.


Study aim. To analyse the surgical outcomes in patients with haemorrhagic stroke depending on the timing of surgery.

Materials and methods. We performed a retrospective analysis of 500 patients (335 (67%) men and 165 (33%) women), who underwent surgical treatment of hypertensive intracranial hemorrhages at the N.V. Sklifosovsky Research Institute for Emergency Medicine between 1997 and 2020. The mean patient age was 53.1 ± 12.2 years. The mean time until surgery was 3.3 ± 2.6 days. Outcomes were assessed on day 30 from disease onset using the modified Rankin Scale (mRS).

Results. In the total sample, outcomes as measured by the mRS were as follows: type 0 — 84 (16.8%) patients, type 1 — 37 (7.4%), type 2 — 46 (9.2%), type 3 — 38 (7.6%), type 4 — 43 (8.6%), type 5 — 142 (28.4%) and type 6 — 110 (22.0%). Treatment results were better when surgery was delayed (χ2 = 64.4; p < 0.00001). Mortality was 36.4% after surgery conducted in the first day after haemorrhage, while mRS scores of 0–2 made up 18.6%. Mortality was 20.4% after surgery conducted on the second or third day, and mRS scores of 0–2 made up 29.6%. Mortality was 17.4% after surgery conducted on day 4–7, and mRS scores of 0–2 outcomes were present in 49.0% of subjects. Mortality was 8.8% when surgery was performed on day 8 or later, and favourable outcomes were present in 48.5% of patients.

Conclusion. Intracerebral haematoma excision on day 2–3 leads to better outcomes in patients with reduced levels of alertness up to sopor, while surgery after day 3 leads to better results in alert patients and those with obtundation.

Annals of Clinical and Experimental Neurology. 2021;15(4):36-43
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Structural pharmacology of GABAА receptors

Rossokhin A.V., Sharonova I.N.


Gamma-aminobutyric acid (GABA) is the main inhibitory neurotransmitter in the mammalian central nervous system (CNS), activating the inotropic type A receptors (GABAА receptors) to provide fast inhibition. GABAА receptors are the main target for various groups of drugs that are widely used in the treatment of CNS disorders.

This review examines the relationship between the physiological effects of GABAА receptor activation and modulation by various substances (including medicinal compounds), the receptor's structure, and the interaction of these substances with specific modulatory sites. Recent advances in cryogenic electron microscopy have led to fundamental improvements in understanding the detailed organization and function of GABAА receptors. This review is based on both the latest structural data obtained from cryogenic electron microscopy and the results of biochemistry and electrophysiology studies, as well as molecular modelling.

Annals of Clinical and Experimental Neurology. 2021;15(4):44-53
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The quality of artificial intelligence algorithms for identifying manifestations of multiple sclerosis on magnetic resonance imaging (systematic review)

Chernyaeva G.N., Morozov S.P., Vladzimirskyy A.V.


A systematic review was undertaken to summarize the data regarding accuracy and effectiveness of artificial intelligence algorithms for identifying MRI manifestations of multiple sclerosis. The review included 39 papers, whose authors put forth a multitude of corresponding algorithms and mathematical models. However, quality assessment of these developments was limited by retrospective testing on repeat data sets. Clinical test results were almost entirely absent, and there were no prospective independent studies of accuracy and applicability. The relatively high values obtained for the main measures (similarity, sensitivity and specificity coefficients, which were 75–85%) were offset by the methodological errors when creating the baseline data sets, and lack of validation using independent data. Due to small sample sizes and methodological errors when measuring the result accuracy, most of the studies did not meet the criteria for evidence-based research. Studies with the highest methodological quality had algorithms that achieved a sensitivity of 51.6–77.0%, with a Sørensen–Dice coefficient of 53.5–56.0%. These numbers are not high, but they indicate that automatic identification of multiple sclerosis manifestations on magnetic resonance imaging may be achievable. Further development of computer-aided analysis requires the creation of clinical use scenarios and testing methodology, and prospective clinical testing.

Annals of Clinical and Experimental Neurology. 2021;15(4):54-65
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Primary progressive aphasias: clinical and genetic heterogeneity and diagnostic difficulties

Litvinenko I.V., Kolmakova К.A., Emelin А.Y., Lobzin V.Y.


This systematic review describes primary progressive aphasia (PPA) variants and includes the authors' own clinical observations. Over 20 genes have now been identified, with mutations that are directly involved in the development of the behavioural variant of frontotemporal dementia, as well as other forms of PPA. Pathomorphological markers of Alzheimer's disease were identified in 76% of cases of logopenic PPA, while signs of frontotemporal dementia associated with TDP-43 were identified in 80% of cases of the semantic variant, and those associated with TDP-43/tau were identified in 64% of cases of agrammatic PPA. The clinical diagnosis of PPA is based on a history of long-term, progressive speech disturbances and identifying a particular variant: agrammatic, semantic or logopenic. The primary variant of the speech disorder cannot be identified in approximately 30% of cases. The focus should be on the main and additional clinical signs (presence of agrammatism, object naming, word comprehension, preserved repetition), as well as neuroimaging (presence of asymmetrical frontal and/or temporal lobe atrophy).

The article also provides key aspects of differential diagnosis of the PPA variants, and puts forth a stepwise diagnostic algorithm. It examines features of PPA progression, with possible development of corticobasal syndrome, illustrated by a clinical case. A dissociation between neuroimaging findings and clinical disease variant is also demonstrated to be possible. Different neuropsychological assessments of patients with aphasia and methods of determining the severity of speech dysfunction are presented. Standardized aphasia assessment tools and the adapted PPA severity scale are provided.

Annals of Clinical and Experimental Neurology. 2021;15(4):66-77
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Electrophysiological assessment of the cranial reflexes

Seliverstov Y.A., Abramova A.A., Evdokimov K.M., Broutian A.G., Maximova M.Y., Illarioshkin S.N., Piradov M.A.


Electrophysiological assessment methods play a key role in the diagnosis of various neurological disorders. Electrophysiological evaluation of cranial reflexes is particularly valuable for neurologists. This article provides an overview of electrophysiological evaluation methods for cranial reflexes, which are most commonly used in clinical practice. They provide objective assessment of the functional integrity of nervous system structures that make up the cranial reflex arc, identify the level and, in some cases, the nature of disease, as well as pathophysiological mechanisms of central and peripheral nervous system disorders. We describe the instruments and main approaches to analysing the results for the standard blink reflex, blink reflex with prepulse inhibition, blink reflex with paired stimuli and recovery curve evaluation, reflex inhibition of the levator palpebrae superioris, jaw jerk reflex, and reflex inhibition (cutaneous silent period) of the masseter muscle.

Annals of Clinical and Experimental Neurology. 2021;15(4):78-85
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Doppler ultrasound assessment of minor atrial septal defects in patients with paradoxical embolism

Karshieva A.R., Chechetkin A.O., Belopasova A.V., Dobrynina L.A.


Minor atrial septal defect (ASD) may be one of the pathways of paradoxical embolism in the brain. Few scientific papers have investigated the relationship between ASD (excluding patent foramen ovale) and the occurrence of ischemic stroke. There is no definite opinion as to how functionally important such shunts are and how the shunt changes with age. The review analyzes modern ideas about the probability of paradoxical embolism in small ASDs from the viewpoint of pathophysiology, and also demonstrates the technological capabilities of assessing the functional significance of such shunts based on our own clinical observations.

Annals of Clinical and Experimental Neurology. 2021;15(4):86-92
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Clinical analysis

Pseudostroke as a manifestation of mediastinal choriocarcinoma in an elderly man

Korneva Y.S., Maslova N.N., Rudenko Y.A., Miloserdov M.A., Shisterova O.A.


We describe a rare clinical case: onset of acute neurological symptoms suggestive of a pesudostroke, caused by an imbalance in cerebral blood flow as a result of internal carotid artery compression by an enlarged lymph node secondary to metastases from a disseminated non-gestational mediastinal choriocarcinoma. This was accompanied by decompensation due to paraneoplastic coagulopathy.

Annals of Clinical and Experimental Neurology. 2021;15(4):93-98
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Case report of Hashimoto encephalopathy in a 21-year-old female patient

Popova T.E., Tappakhov A.A., Davydova T.K., Govorova T.G., Petrova A.Y., Adamova A.E., Steblevskaya A.E.


Hashimoto encephalopathy is a rarely diagnosed autoimmune neurological disorder, associated with the presence of antithyroid antibodies. The variability of clinical presentation, rarity of the disease, and absence of specific diagnostic markers make timely diagnosis very complicated. This article describes a clinical case of a female patient with Hashimoto encephalopathy and discusses diagnosis, differential diagnosis and treatment approaches. We emphasize the importance of establishing a timely diagnosis, considering high efficacy of targeted treatment.

Annals of Clinical and Experimental Neurology. 2021;15(4):99-104
pages 99-104 views

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