Clinical Value of Functional MRI in the Diagnosis of Cognitive

Disorders in Patients with Arteriovenous Malformations

N. V. Korno

, N. E. Ivanova

, A. Yu Ivanov

, G. E. Trufanov

, N. N. Semibratov

, D. N. Iskhakov

A. V. Sokolov

, A. S. Lepekhina

and A. Yu Efimtsev

Almazov National Medical Research Centre, Akkuratova Str. 2, Saint-Petersburg, Russia

St.-Petersburg State Pediatric Medical University, Litovskaya Str. 2, Saint-Petersburg, Russia

Keywords: Functional Magnetic Resonance Imaging, Arteriovenous Malformations, Bold Contrast, Cognitive

Impairment.

Abstract: Cognitive impairment that develops in acute and chronic cerebral pathology, including arteriovenous

malformations, is one of the most frequent and prognostically unfavorable complications. Late detection of

severe forms of cognitive impairment, including dementia, leads to a lack of early preventive and therapeutic

correction, a decrease in the effectiveness of rehabilitation and the quality of life of patients with AVM. A

comprehensive assessment of cognitive impairment may be a diagnostic criterion for assessing the severity

of neurological symptoms at the endovascular treatment stages. A significant contribution to the study of the

pathophysiology of CN formation in patients with AVM is made by fMRI, providing knowledge about the

functional organization of the brain. The results of functional mapping of the brain in 11 patients with

arteriovenous malformations are presented. The structure of cognitive impairment was evaluated using

advanced neuropsychological testing and structural-functional restructuring in the cerebral cortex using fMRI.

To obtain images, an echoplanar tomography technique using BOLD contrast was used. The data obtained

indicate complex neurodynamic disorders of the cognitive sphere in patients with AVM in several areas of

both the right and left hemisphere: dorsal, ventral and medial front-striatal thalamic and fronto-parietal

cerebellar networks.

1 INTRODUCTION

Cerebral arteriovenous malformations (AVM) are a

malformation of cerebral vessels belonging to the

group of congenital and progressive vascular diseases

of the central nervous system (Robert,2007; Berman,

2007; Lin et al, 2012).

AVMs are a significant source of disability and

mortality in the working age population among

various forms of cerebrovascular abnormalities. Up to

4% of all intracranial volume formations, 9% are

causes of non-traumatic subarachnoid hemorrhages,

1% are ischemic strokes (Robert, 2017).

Information on the frequency of occurrence of

cerebral AVM in the population is contradictory and

depends on the sources of information. Some studies

indicate that the prevalence of the disease in the adult

population is 19 per 100,000 people, and the

frequency of surgical interventions for AVM of the

cerebral vessels is 0.9 per 100 thousand of the

population per year (Laakso et al., 2010; Lunsford,

2009; Laakso et al. A2012).

The clinical manifestation of AVM most often

occurs in people 20-50 years old, and the long-term

prognosis without surgical treatment is unfavorable:

23% of patients die, in 48% the disease leads to

disability, which indicates the social significance of

this problem (Robert, 2017).

One of the most frequent and maladaptive

manifestations of AVM is cognitive impairment (CI)

(Marshall et al., 2003; Steinvorth et al., 2002, Lazar

et al. 1996; Steinvorth, 2002; Andrea et al.,2014;

Buklina, 2001).

Considering that AVM is a congenital pathology,

CI at the stage of mild disorders often remain

underestimated, thereby transforming into more

severe forms, leading to significant limitations in

work, the social sphere, and patient self-care (Ernst et

al.,2017; Charidimou et al., 2017)

The cerebral cortex is a complex integrated

system that combines a large number of different

parts of the nervous system, each of which performs

Korno, N., Ivanova, N., Ivanov, A., Trufanov, G., Semibratov, N., Iskhakov, D., Sokolov, A., Lepekhina, A. and Eﬁmtsev, A.

Clinical Value of Functional MRI in the Diagnosis of Cognitive Disorders in Patients with Arteriovenous Malformations.

DOI: 10.5220/0008973003790386

In Proceedings of the 13th International Joint Conference on Biomedical Engineering Systems and Technologies (BIOSTEC 2020) - Volume 1: BIODEVICES, pages 379-386

ISBN: 978-989-758-398-8; ISSN: 2184-4305

379

a specific function. At the same time, these

departments interact with each other, participating in

the implementation of one or another program, in the

framework of which the information entering the

brain is constantly processed by centers structurally

and functionally interconnected (Yakhno et al., 2014;

Luria, 2000, Mendoza et al., 2014)

The quantitative and qualitative characteristics of

cognitive impairment are extremely important in the

diagnostic work of neurologists, neurosurgeons,

therapists and doctors of other specialties. The

identification and clinical analysis of the cognitive

impairment features in patients with AVM is

necessary for the correct syndromal and topical

diagnosis, for assessing the severity of neurological

symptoms at the stages of endovascular treatment of

AVM. Extensive neuropsychological testing and

conventional neuroimaging are not enough to

describe the general picture of AVM, because even if

it can provide accurate anatomical localization, it

does not provide any information about the functional

organization of the brain.

A significant contribution to the study of the

pathophysiology of cognitive impairment formation

in patients with AVM is made by modern methods of

neuroimaging, one of which is fMRI, because it

allows you to simultaneously obtain data on

metabolism, blood flow and structural and functional

characteristics of the brain (Ellis, 2016).

The first work on the use of fMRI in brain

research appeared in 1992 (Bandettini, 1992). FMRI

has become the standard for determining the activity

of brain neurons in humans, since it is a non-invasive

method, has reliable localization of responses, and

high spatial resolution, compared to the earlier

developed technologies, such as positron emission

tomography (PET) (Odinak, 2006; Lazar et al., 2010).

Considering that the hemodynamic characteristics

of AVM is a decrease in pressure in the arteries

involved in the blood supply to AVM, a unified

system of blood circulation equilibrium is being

displaced, and as a result — arteriovenous bypass

surgery has a damaging effect on the cerebral cortex.

According to the mechanism of intensive venous

discharge, areas of reduced microcirculation are

formed, both in the affected vascular pool and in the

opposite hemisphere. Due to the structural and

functional reorganization of the cerebral cortex, that

occurs against the background of insufficient blood

circulation, cortical functions from certain parts of the

brain are rearranged to adjacent parts of the brain,

which leads to their later manifestation in patients

with AVM (Ishikawa et al., 2017; Moretti et. Al.,

2017).

Functional magnetic resonance imaging is

considered as a way of studying the "functional

architecture" of the brain. The most widely used

fMRI technique is based on the sensitivity of the pulse

sequence of the gradient echo to changes in the

oxygenation of brain tissue - the BOLD effect

(Barbay et. al., 2017, Keefe et. al., 2017).

With this sequence, changes in the magnetic

resonance signal in the same part of the brain under

conditions of rest and activation occur due to

differences in the paramagnetic properties of

deoxyhemoglobin and oxyhemoglobin. It is believed

that when exposed to an irritant, the degree of

increase in regional blood flow exceeds the tissue's

oxygen demand, which leads to local hyperoxemia

and, consequently, to a decrease in the concentration

of deoxyhemoglobin. Due to a decrease in the degree

of local inhomogeneity of the magnetic field, an

increase in the magnetic resonance signal occurs.

Areas that change the signal intensity in accordance

with the shape and duration of the stimulus are

detected using special statistical processing, are

selected in the form of activation maps and combined

with anatomical images of the brain.

Regarding the study of the cognitive status of

patients with AVM, there are only a few studies. In

2013, a team of researchers led by R.L. Piana showed

how the combined use of different imaging

techniques can be useful in understanding

neuroplasticity and hemodynamics in patients with

AVM at the endovascular treatment stages. Valuable

information in this case is that the structural and

functional organization of the brain in patients with

complex AVMs has a number of features, and it can

be obtained using a more systematic and extensive

imaging protocol that combines perfusion with

complex analyzes of functional MRI (fMRI) and

anatomical MRI for the purpose of mapping brain

activations at the stages of endovascular treatment of

vascular abnormalities (Roberta La Piana, 2013).

In the works of J.C. Lin, T.H.Le described cases

of regression of neurological deficit after

microsurgical removal of malformation due to

compensatory rearrangement of cortical functions.

A study conducted in Japan between 1977 and

1994 described dynamic changes in activation zones

for stimulus tasks. This pattern was presumably

associated with either hemorrhage or ischemic

disorders that correlated with changes in MRI

(hemosiderin deposition, hypoperfusion zones

associated with the “robbery phenomenon”) (Kida,

1994).

A number of foreign fMRI studies have shown

that the functional activity of the cerebral cortex is

NDNSNT 2020 - Special Session on Non-invasive Diagnosis and Neuro-stimulation in Neurorehabilitation Tasks

380

specifically impaired in patients with depressive and

anxiety disorders (Bremner et al., 2002; Cotter et al.,

2001).

Using fMRI methods, Russian researchers have

demonstrated the effects of activation of

neuroplasticity under the influence of

neuroelectrostimulation in patients with depressive

disorder. The use of modern methods of data analysis

of fMRI revealed a significant improvement in the

functioning of the basic working network and brain

connectivity in the studied patients (Kublanov, 2018;

Kublanov, 2019).

To assess cognitive impairment in patients with

AVM, a comprehensive examination is necessary,

including not only the identification of structural

changes using modern neuroimaging methods, but

also a qualitative analysis of integrative changes

using neuropsychological examination. In routine

practice, CI in patients with AVM often remains

unrecognized due to the lack of a standard

examination protocol and the possibility of long-term

monitoring of this category of patients (Skrobot et al.,

2018; Behrman, 2017).

2 PURPOSE

The aim of our study was to assess the clinical

significance of modern functional neuroimaging in

the diagnosis of cognitive impairment in patients with

arteriovenous malformations of the brain, who

underwent embolization of the AVM with the non-

adhesive ONYX composition.

3 MATERIALS AND METHODS

3.1 Study Population

The main criterion for inclusion in the study was the

presence of AVM of supratentorial localization,

confirmed by the history, neurological examination,

and the results of a routine neuroimaging

examination. The study included 11 patients with

arteriovenous malformations of the brain who have

been treated at the Russian National Pedagogical

Institute. prof. A.L. Polenova from January 2014 to

December 2017, who performed embolization of the

AVM with the non-adhesive ONYX composition,

and 18 healthy right-handed volunteers (healthy

controls), who were stratified by gender and age. The

average age of patients with AVM was 36.6 years.

Analysis of the results was made with a maximum

follow-up of 12 months. The structure of cognitive

impairment was evaluated using advanced

neuropsychological testing and structural and

functional restructuring in the cerebral cortex using

fMRI. To activate various areas of the cerebral cortex

during fMRI, patients were asked to perform special

tasks-paradigms. The following were used: the

standard speech block paradigm (speech test), the

generation of counting operations according to the

indifferent counting series presented with the help of

headphones (counting test), the activation of optical-

spatial functions and visual memory using simple

(non-plot) pictures presented on the screen (visual

stimuli).

3.2 MR Imaging Protocol

To obtain images, we used the echoplanar

tomography technique using BOLD contrast.

Postprocessing included the elimination of artifacts,

statistical analysis of BOLD signals, the construction

and combination of t-maps of activation zones with

T1 of the brain and their transformation into the MNI

coordinate space (Montreal Neurological Institute -

Montreal Neurological Institute). The study was

performed using 1.5 Tesla MR scanner. The

observations were dominated by the epileptic type of

course - 8 (41.1%), hemorrhagic type was found in 3

patients (33.56%).

The majority of patients with AVM in the amount

of 6 (54.5%) cases were assigned to Spetzler-Martin

Grade III and V, with the exception of 1 (9.1%)

patient of Grade IV. In the studied group of patients,

AVM localization in the left hemisphere prevailed - 6

(54.5%) patients. Of these, in an amount of 4 (36.4%)

in the left parietal lobe, temporal lobe -1 (9.1%), in

the left occipital lobe -1 (9.1%). In the right

hemisphere, the main localization of the AVM is in

the parietal lobe and occipital lobe 2 (18.2%), in one

case (9.1%) in the frontal lobe.

The principle of multi-stage, complex treatment

was used in all patients - the maximum possible AVM

fragments were embolized during one surgical

intervention (60% approx. of the whole volume of

AVM).

3.3 Results

When performing intragroup analysis (healthy

volunteers) at the stages of interaction of neuronal

structures for recognizing the presented images, a

decrease in activation was detected in the prefrontal

cortex, the Broadman area (BA) 10, as well as in the

projection of BA17 and BA18 (MNI coordinates: -36 -

Clinical Value of Functional MRI in the Diagnosis of Cognitive Disorders in Patients with Arteriovenous Malformations

381

90 14). At the same time, an increase in activation was

observed in the isthmus of the cingulate gyrus - BA31

(MNI coordinates: 6 -62 32), in the insula (MNI

coordinates: 4 40 38) and the parahippocampal gyrus

(MNI coordinates: 32 -36 -12). Local patterns of

processing visual information, recognizing visual

images and transmitting information to other

departments of the visual analyzer that are involved in

providing emotional-volitional decisions, the

formation of motivation, cognitive flexibility, short-

Figure 1: The control group. Activation sites (response to a

visual stimulus) in the projection of brain structures: the

isthmus of the cingulate gyrus, insular cortex,

parahippocampal gyrus, Broca and Wernicke areas —

bilaterally.

term memory and neurodynamics, which is the main

function of the thalamo lenticular complex (Figure 1),

were found. The topical importance of the

parahippocapal complex is to create complex cognitive

patterns, form short-term memory, while being the

basis of neurodynamic thinking, forming connections

with cortical, subcortical, stem formations of the brain.

As it can be seen in Figure 2, when performing a

speech test, there were activations in the region of the

parahippocampal complex in the projection of the

fusiform gyrus (MNI coordinates: 30 -34 20), upper

and lower temporal gyri on the right (MNI coordinates:

52 64 22; 54 -18 -22), upper frontal gyrus on the right,

caudate nuclei (MNI coordinates: 6 8 -6), insular lobes

(MNI coordinates: 34 -22 10).

Figure 2: The control group. Activation sites (response to a

speech test) in the projection of brain structures: the isthmus

of the cingulate gyrus, insular lobes and parahippocampal

gyri.

Presenting a ”count” stimuli resulted in activation areas

in the projection of the middle frontal gyri bilaterally,

insular cortex on the right (MNI coordinates: 40 - 14

8), the upper frontal gyrus on the left (MNI

coordinates: -14 48 48), precentral gyrus bilaterally

(MNI coordinates: 38 -14 50; -24 -24 62). All these

zones are parts of the working network of the brain

at rest and carry out complex, including logical,

processing of information of various nature, are

responsible for short-term and long-term memory,

fluency of speech, neurodynamics, and error control

NDNSNT 2020 - Special Session on Non-invasive Diagnosis and Neuro-stimulation in Neurorehabilitation Tasks

382

Figure 3: The control group. Activation sites (response to a

count test): in the projection of brain structures: medial

prefrontal cortex, BA9, BA46, BA31, BA32.

Figure 4: Results of intergroup analysis. Activation sites

(response to the visual stimuli) presented in the patient

group compared to the control group. Increased severity

(blue): in the projection of PB 6, PB 10, parietal cortex,

prefrontal and cingulate cortex, (p <0.001).

(Figure 3).

The dynamical intergroup analysis was aimed to

establishing statistically significant differences

between the volume of activations to compare

functional changes in the cerebral cortex in patients

with AVM and healthy volunteers. In patients with

AVM, fewer activation sites were detected in

response to certain cognitive tasks. Recognition of the

presented images, storing and fixing of repeated

images on the images presented on the screen

revealed an increase in the activation of the following

areas of the brain in patients with AVM: on the left is

the region of the central gyrus, subcortical structures

BA6 (MNI coordinates: -2 8 -25), BA10 (MNI

coordinates: 23 55 7); parietal cortex (MNI

coordinates: 23 -38 52), on the right - the lower

parietal cortex (MNI coordinates: -24 -50 -40), the

prefrontal cortex (MNI coordinates: 17 44 2) and the

cingulate cortex (MNI coordinates: 4 23 22), p

<0.001, (Figure 4).

When performing a speech test, in patients,

comparing to the control group, a decrease in

activation was found in the following areas: lower

parietal lobe bilaterally, insular lobules on the left

(BA13, MNI coordinates: -42 4 -1), lower frontal

gyrus on the left (MNI coordinates: -32 47 -1),

caudate nucleus (MNI coordinates: 14 10 11) on the

left, parahippocampal gyrus on the left (MNI

coordinates: 24 -9 -4). There was also a statistically

significant increase in activation in the projection of

the superior frontal gyrus on the left (BA 10, MNI

coordinates: 12 49 4), the medial prefrontal cortex

and the anterior cingulate gyrus, p <0.001, (Figure 5).

The main functions of these zones are organization of

complex cognitive circuits, the substrate of short-term

memory, the basis of neurodynamic thinking. They

form connections with cortical, subcortical, stem

structures in the brain.

When performing count test (repeated count

operations), in patients, comparing to the control

group, a statistically significant increase in

activations was established in the following areas:

inferior parietal lobe, BA32 bilaterally (MNI

coordinates: -10 46 11; 14 40 11) , BA7 (MNI

coordinates: 23-60 60), BA9 on the right (MNI

coordinates: 35 39 31), insula (MNI coordinates: 44 4

10), middle frontal gyrus (MNI coordinates: 30 47

11), waist gyrus on the left (MNI coordinates: -3 36

11), p <0.001, (Figure 6).

In the structure of cognitive impairment within the

group of patients with AVM at the stages of

endovascular treatment (ONYX embolization),

cognitive impairments of a mixed structure

(dysfunction of the fronto-subcortical formations of

the brain; structures of the hippocampal circle;

temporal-parietal-occipital region) were revealed -

90%; dysfunction of the structures of the hippocampi

- 10%. In 70%, cognitive impairment was noted at the

Clinical Value of Functional MRI in the Diagnosis of Cognitive Disorders in Patients with Arteriovenous Malformations

383

Figure 5: Intergroup analysis results. Activation sites

(response to the presented speech test) in the patient group

compared to the control group. Increased (blue): in the

projection BA10 on the left. Decrease (red): in the

projection of the lower frontal gyrus on the left, the insula

on the left, the caudate nucleus, the parahippocampal gyrus

on the left (p <0.001).

level of the first functional block (block of regulation

of brain activity) - nonspecific structures of the brain

(thalamo-reticular complex) and the third functional

block (level of regulation, control of activities). In all

patients in the group with AVM, a defeat of the

second functional block (block of reception,

processing and storage of ectoceptive information

(modally specific processes) was noted. Focal

neurological symptoms in the form of oculomotor

disorders, homonymous hemianopsia and

coordinating disorders were revealed in 60% of cases.

About 30% of patients showed mild hemiparesis and

pyramidal symptoms, and 20% had Vincent's

symptom (BA4, BA6) and mild sensitive disorders.

Figure 6: Intergroup analysis results. Activation sites

(response to the presented sample test) in the patient group

compared to the control group: Increased (blue): in the

projection, left inferior parietal lobe BA9, left middle

frontal gyrus (p <0.001).

4 CONCLUSIONS

The clinical significance of modern functional

neuroimaging plays an important role in the diagnosis

of cognitive impairment. The results of our fMRI

study in patients with AVM using the diagnostic

algorithms indicate complex neurodynamic disorders

of the cognitive sphere in several areas, such as the

right and left hemispheres of the dorsal, ventral and

medial fronto-striato-thalamic and fronto-parieto-

cerebellar networks, responsible for control,

attention, reaction speed of choice. In addition, there

is growing evidence of a decrease in activation in

patients with AVM at the endovascular treatment

stages in the prefrontal and limbic regions, which

provide motivation and control of emotions.

Pathogenetic features of cognitive impairment,

assessment of modern methods of neuroimaging and

diagnosis using advanced neuropsychological testing

are currently a promising area. However, features in

the field of correlation between functional research

methods and early identification of cognitive

impairment using advanced neuropsychological

testing have not been investigated. The study of the

structure of cognitive impairment using fMRI in

combination with neuropsychological testing can

help take a fresh look at the vast neuronal

relationships in the central nervous system. The

NDNSNT 2020 - Special Session on Non-invasive Diagnosis and Neuro-stimulation in Neurorehabilitation Tasks

384

inconsistency of numerous literature data confirms

the relevance of this technique to improve the

diagnosis of cognitive impairment in patients with

AVM in order to optimize the therapeutic effect.

CONFLICT OF INTERESTS

The authors declare no conflict of interest.

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