TYPE Original Research

PUBLISHED 12 April 2023

DOI 10.3389/fnhum.2023.996359

Cognitive functions and patterns

OPEN ACCESS of brain activity in patients after
simultaneous coronary and
EDITED BY
Jose Paulo Andrade,
University of Porto, Portugal

REVIEWED BY
Kutlu Kaya,
carotid artery revascularization
Hacettepe University, Türkiye
Joao Rocha-Neves,
University of Porto, Portugal Irina Tarasova1*, Olga Trubnikova1 , Darya S. Kupriyanova1 ,
*CORRESPONDENCE Olga Maleva1 , Irina Syrova1 , Irina Kukhareva1 , Anastasia Sosnina1 ,
Irina Tarasova
[email protected] Roman Tarasov2 and Olga Barbarash3
SPECIALTY SECTION 1
Department of Clinical Cardiology, State Research Institute for Complex Issues of Cardiovascular
This article was submitted to Diseases, Kemerovo, Russia, 2 Department of Cardiac and Vascular Surgery, State Research Institute for
Brain Health and Clinical Neuroscience, Complex Issues of Cardiovascular Diseases, Kemerovo, Russia, 3 Research Institute for Complex Issues of
a section of the journal Cardiovascular Diseases, Kemerovo, Russia
Frontiers in Human Neuroscience

RECEIVED 26 July 2022

ACCEPTED 13 March 2023 Background: On-pump coronary artery bypass grafting (CABG) is associated with
PUBLISHED 12 April 2023
a high risk of neurological complications in patients with severe carotid stenosis.
CITATION
Moreover, early postoperative cognitive dysfunction (POCD) incidence remains
Tarasova I, Trubnikova O, Kupriyanova DS,
Maleva O, Syrova I, Kukhareva I, Sosnina A, high in patients undergoing simultaneous coronary and carotid surgery. Recent
Tarasov R and Barbarash O (2023) Cognitive studies have shown that even moderate carotid stenosis (≥50%) is associated
functions and patterns of brain activity in
with postoperative cognitive decline after CABG. Data on brain health in the
patients after simultaneous coronary and
carotid artery revascularization. postoperative period of simultaneous coronary and carotid surgery are limited.
Front. Hum. Neurosci. 17:996359.
Objectives: This study aimed to analyze early postoperative changes in the
doi: 10.3389/fnhum.2023.996359
cognitive function and patterns of brain electrical activity in patients after
COPYRIGHT
© 2023 Tarasova, Trubnikova, Kupriyanova,
simultaneous coronary and carotid artery revascularization.
Maleva, Syrova, Kukhareva, Sosnina, Tarasov Materials and methods: Between January 2017 and December 2020, consecutive
and Barbarash. This is an open-access article
distributed under the terms of the Creative
patients were assigned to on-pump CABG with or without carotid endarterectomy
Commons Attribution License (CC BY). The use, (CEA) according to clinical indications. An extended neuropsychological and
distribution or reproduction in other forums is electroencephalographic (EEG) assessment was performed before surgery and at
permitted, provided the original author(s) and
the copyright owner(s) are credited and that
7–10 days after CABG or CABG + CEA.
the original publication in this journal is cited, in Results: A total of 100 patients were included [median age 59 (55; 65), 95% men,
accordance with accepted academic practice.
No use, distribution or reproduction is
MMSE 27 (26; 28)], and among these, 46 underwent CEA. POCD was diagnosed
permitted which does not comply with these in 29 (63.0%) patients with CABG + CEA and in 32 (59.0%) patients with isolated
terms. CABG. All patients presented with a postoperative theta power increase. However,
patients with CABG + right-sided CEA demonstrated the most pronounced theta
power increase compared to patients with isolated CABG.
Conclusion: The findings of our study show that patients with CABG + CEA and
isolated CABG have comparable POCD incidence; however, patients with CABG
+ right-sided CEA presented with lower brain activity.

KEYWORDS

simultaneous revascularization, coronary artery bypass grafting, carotid endarterectomy,

postoperative cognitive dysfunction, brain electrical activity

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1. Introduction Researchers have become interested in the topographic features

of brain lesions after cardiac surgery. Cerebral hypoperfusion
Patients with high-grade carotid stenosis or occlusion have a during on-pump cardiac surgery can contribute to the development
high risk of neurological complications during on-pump coronary of mild, multiple lesions in the frontal and parietal brain lobes, the
artery bypass surgery (CABG) (Sahni and Dalton, 2016; Tarasov so-called “watershed areas,” in the terminal branches of adjacent
et al., 2017; Campbell et al., 2021). A possible approach that has large cerebral arteries (Safan et al., 2022). At the same time, it was
been recognized in some cases as an effective treatment modality is found that cerebral blood flow alterations in the frontal and parietal
CABG and simultaneous carotid endarterectomy (CEA) (Tarasov lobes are associated with a decrease in attention and executive
et al., 2017; Aboyans et al., 2018; Silverman, 2019). The risk of control (Hshieh et al., 2017; Wang et al., 2022).
ischemic brain injury increases due to global or local ischemia Data on the brain electrical activity in the postoperative period
and the factors associated with simultaneous coronary and carotid of simultaneous interventions on coronary and carotid stenosis
surgery. Although this procedure is not always complicated by are quite limited. Other authors have shown that patients with
traumatic brain injury (stroke), it may cause a less pronounced, CABG + left-sided CEA had a localized postoperative theta activity
diffuse lesion that later leads to cognitive decline (Weimar et al., increase at 7–10 days after surgery compared to baseline. At the
2017; Maleva et al., 2020). Previous studies have shown that same time, patients with isolated CABG or CABG + right-sided
patients undergoing simultaneous coronary and carotid artery CEA demonstrated a more diffuse theta activity increase (Tarasova
surgery present with a high incidence of postoperative cognitive et al., 2019).
dysfunction (POCD) in the early postoperative period (Maleva The aim of our study was to investigate early postoperative
et al., 2019, 2020). changes in cognitive functions and patterns of brain electrical
Data on the influence of the laterality of CA revascularization activity in patients undergoing simultaneous coronary and carotid
on adverse neurological outcomes are limited (Bossema et al., 2007; surgery. Moreover, we aimed to determine the significance of
Baracchini et al., 2012; Heyer et al., 2015). The study by Bossema the laterality of the CA revascularization side in simultaneous
et al. (2007) demonstrated that cognitive changes, measured by interventions (CABG + CEA) for regional EEG power changes.
neuropsychological tests sensitive to hemispheric specialization, are
irrespective of the side of intervention. Baracchini et al. (2012)
also found no impact of the CEA side on any of the indicators
of cognitive performance. Heyer et al. (2015) investigated the 2. Materials and methods
relationship between the laterality of CEA and fine hand deficits
using the Grooved Pegboard test. The authors demonstrated 2.1. Patients
greater subtle deficits of hand coordination in the non-dominant
hand compared to the dominant hand in patients undergoing CEA This prospective and observational study involved 100 patients
of the opposite carotid artery. with indications for simultaneous coronary and carotid artery
Thus, the issue of selecting the optimal strategy in the surgery or isolated CABG selected from a cohort of cardiac patients
surgical treatment of coronary and carotid atherosclerosis and admitted to the clinic of the Research Institute of Complex Issues of
early diagnosis of brain ischemia during simultaneous coronary Cardiovascular Diseases. Data collection was performed between
and carotid artery surgery is far from being solved and January 2017 and December 2020, and consecutive patients were
necessitates the implementation of highly informative techniques. assigned to on-pump CABG with or without simultaneous carotid
Electroencephalography (EEG) may be a promising method for endarterectomy (CEA) according to clinical indications. This study
obtaining data on specific changes in the brain electrical activity was performed in compliance with the ethical principles of the
in cardiac surgery patients due to high temporal and moderate Declaration of Helsinki. The study protocol received approval from
spatial resolution. The study of spontaneous electrical activity the Institutional Review Board (study protocol No 2/02072019). All
in the brain in various pathological conditions revealed that patients included in the study signed an informed consent form
neuronal oscillatory systems are widely involved and that such (Figure 1).
changes are the earliest evidence of subsequent impairment of The inclusion criteria were as follows: patients who were aged
cognitive functions (Bonanni et al., 2015; Engels et al., 2016; between 45 and 80 years, patients with simultaneous coronary and
Tarasova et al., 2021). The brain’s electrical activity is affected carotid artery revascularization or isolated CABG, and patients who
by temperature management during cardiopulmonary bypass, the were right-handed (to exclude any influence of the laterality on
depth of anesthesia, metabolic disorders, in particular hypo- or cognitive function).
hyperglycemia, and impaired cerebral autoregulation (Howard The exclusion criteria were as follows:
et al., 2012; Sutter et al., 2013). A number of studies have
demonstrated a high diagnostic value of EEG parameters in patients • Life-threatening arrhythmias (at baseline);
undergoing CABG (Tarasova et al., 2021; Trubnikova et al., 2021). • Functional class IV heart failure according to the New York
EEG theta band activity is one of the most sensitive indicators Heart Association (FC NYHA IV) guidelines;
associated with perioperative brain injury. According to other • Chronic obstructive pulmonary disease with persistent
studies, even moderate and small stenosis (≥50%) is associated with breathing difficulty;
pronounced theta activity changes in the early postoperative period • Malignant pathology;
of CABG (Trubnikova et al., 2014). • Diseases of the central nervous system, including stroke;

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FIGURE 1
Design of the study.

• Depressive symptoms [Beck Depression Inventory (BDI-II) testing and EEG recording were conducted at baseline (1–3 days
score ≥ 8]; before surgery) and 7–10 days after surgery.
• Mini-Mental State Examination (MMSE) score <24; Frontal
Assessment Battery (FAB) score < 11; and
• Drugs and alcohol addiction. 2.2.1. The neuropsychological test battery
The extended neuropsychological test battery from
The patients underwent standard physical, instrumental, and psychophysiological software ≪Status PF≫ (Ivanov et al.,
neurological examinations. The clinicians were blind to patients’ 2001) was used to assess three domains of cognitive function
study participation. (psychomotor speed and executive function, attention, and
A total of 46 patients had hemodynamically significant CA short-term memory). Psychomotor speed and executive
stenosis (NASCET criteria) confirmed by digital angiography. The functions were evaluated using the complex visual-motor
patients with simultaneous coronary and carotid surgery were response time test, neural responses to feedback, and brain
divided into groups depending on the CEA side: the CABG + responses to feedback assessments. Bourdon’s test was used to
left-sided CEA group included 25 patients and the CABG + right- assess attention. The visual short-term memory assessment
sided CEA group included 21 patients. The group of patients with consisted of tasks requiring participants to memorize 10
isolated CABG included 54 patients. words, 10 numbers, and 10 non-sense syllables. A detailed
As seen in Table 1, clinical and anamnestic characteristics of description of the neuropsychological test battery is presented
patients before surgery were comparable for most indicators. It in Table 2 (Trubnikova et al., 2021). Alternative versions of the
should be noted that patients with CABG + right-sided CEA neuropsychological tests were used in repeated measurements
were older and had lower MMSE scores. Moreover, the parameters to minimize practice effects. Postoperative changes in cognitive
of the intraoperative period such as the mean cardiopulmonary function were assessed individually in each patient. The percentage
bypass (CPB) time and aorta cross-clamping time were higher of change in indicators was calculated using the formula: [(baseline
in the isolated CABG group compared to the simultaneous value–postoperative value)/baseline value] × 100%. A 20%
intervention groups. decline in postoperative parameters compared to baseline in
20% of the test battery indicates POCD (Trubnikova et al.,
2021).
2.2. Neurophysiological assessment

Cognitive screening tests were performed once at baseline (1–3 2.2.2. EEG recording and processing
days before surgery) in all patients using modified Russian versions EEGs were recorded via a 62-channel Quik-cap (Neuroscan,
of the MMSE and FAB scales. The extended neuropsychological El Paso, TX); scalp electrode locations were based on the

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TABLE 1 Clinical and anamnestic characteristics of the groups of the patients before cardiac surgery.

Variable Isolated CABG CABG + CABG + p-value

n = 54 left-sided CEA right-sided CEA
n = 25 n = 21
1 2 3
Age, years, Me (Q25; Q75) 58.5 (51.5;60.5) 58.5 (56.0;65.0) 69.0 (62.0;74.0) p1–3 ≤ 0.0001

Mini–mental state, scores, Me (Q25; Q75) 28.0 (27.0;28.0) 27.0 (26.0;28.0) 26.0 (25.0;27.0) p1–3 = 0.01

Frontal assessment battery, scores, Me (Q25; Q75) 16.0 (16.0;17.0) 16 (16.0;17.0) 15.0 (14.0;17.0) n/s

BDI–II, scores, Me (Q25; Q75) 2.5 (2.0;4.0) 2.0 (1;4.0) 3.0 (2.0;8.0) n/s

Educational attainment, years, n (%)

8–14 37 (69) 19 (76) 18 (85) n/s

≥15 17 (31) 6 (24) 3 (15)

Functional class of angina, n (%)

I–II 28 (52) 21 (84) 17 (81) p1–2 = 0.025

III 26 (48) 4 (16) 4 (19) p1–3 = 0.1

Functional class NYHA, n (%)

I–II 46 (85) 23 (92) 20 (95) n/s

III 8 (15) 2 (8) 1 (5)

History of myocardial infarction, n (%) 46 (85) 17 (68) 16 (76) n/s

LVEF, %, Me (Q25; Q75) 56.0 (52.0; 62.0) 57.0 (46.0; 67.0) 65.0 (60.0; 68.0) n/s

Type 2 of diabetes mellitus, n (%) 14 (26) 9 (36) 9 (43) n/s

History of hypertension, n (%) 52 (96) 24 (96) 20 (95) n/s

Hyperlipidaemia, n (%) 38 (70) 24 (96) 17 (81) n/s

Degree of operated CS, % - 80.0 (55.0; 99.0) 80.5 (57.0; 99.0) n/s

Patients with significant contralateral CS, n (%) - 17 (68) 16 (76) n/s

Cardiopulmonary bypass time, min, Me (Q25; Q75) 106.0 (100.0; 111.0) 79.0 (51.0; 137.0) 86.0 (52.0; 146.0) p1–2 = 0.01

p1–3 = 0.02

Aorta cross-clamping time, min, Me (Q25; Q75) 58.0 (50.0; 66.0) 50.0 (28.0; 75.0) 51.0 (27.0; 80.0) p1–2 = 0.02

p1–3 = 0.03

CEA time - 25.0 (20.0; 25.0) 26.0 (21.0; 30.0) n/s

Total surgery/anesthesia time 162.0 (140.0; 190.0) 90.0 (60.0; 170.0) 90.0 (62.0; 161.0) p1–2 = 0.01

p1–3 = 0.01
BDI-II, Beck Depression Inventory; NYHA, heart failure by the New York Heart Association; LVEF, left ventricle ejection fraction; CS, carotid stenosis; CEA, carotid endarterectomy.

modified 10/10 system; and a nose bridge electrode was used were averaged within the theta1 (4–6 Hz) range, taking into
as a reference. Bipolar eye movement electrodes were applied to account the results of previous studies indicating the diagnostic
the canthus and cheekbone to monitor eye movement artifacts. significance of low-frequency rhythm changes in the detection
Electrode impedances were <20 kΩ for all electrodes. The EEGs of postoperative ischemic brain injury (Tarasova et al., 2019,
were recorded using a NEUVO-64 system (NeuroScan, El Paso, 2021). The next step was the clustering of data recorded in
TX) in the eyes-closed condition, in a dimly lit, soundproof, 56 leads into five electrode zones symmetrically in the left and
electrically shielded room. The EEG recording length was 5 min. right hemispheres: frontal (F) (Fp1/2, AF3/4, F1/2, Fp3/4, Fp5/6,
The amplifier bandwidths were 1.0 to 50.0 Hz, and EEGs were F7/8), central (C) (FC1/2, FC3/4, FC5/6, C1/2, C3/4, and C5/6),
digitized at 1,000 Hz. Each EEG record was plotted and visually temporal (T) (FT7/8, T7/8, and TP7/8), parietal (P) (CP1/2,
examined and then edited to remove artifacts using the NeuroScan CP3/4, CP5/6, P1/2, P3/4, P5/6, P7/8), and occipital (O) (PO3/4,
4.5 software program (Compumedics, TX, USA). Artifact-free PO5/6, PO7/8, O1/2). In the present study, the frontal and
EEG fragments were divided into 2s epochs and underwent parietal zones were considered as the regions of interest (ROI)
Fourier transformations. For each subject, EEG power values (Figure 2).

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TABLE 2 Cognitive test battery for assessing cognitive function in cardiac surgery patients.

Cognitive tests and Description of the procedure

indicators
Mini-mental state examination 30-point questionnaire for cognitive impairment and dementia screening.
(MMSE)
Scores

Frontal assessment battery (FAB) 18-point questionnaire for frontal lobes dementia screening.
Scores

Complex visual-motor reaction Reaction latencies of the right and left hands to stimuli (different colors of rectangles) when the subject should choose one of
Reaction time, ms the three presented signals (the number of signals in the test is 30).
Errors, n

Level of functional mobility of nervous The previous test is conducted in the feedback mode. The duration of the exposure to the test signal (see above) is changed
processes responses to feedback automatically; the exposure of the next signal is shortened by 20 ms with each correct answer and extended by 20 ms, if the
Reaction time, ms answer is wrong (the number of signals in the test is 120). No response to the appearance of the test signal indicates missed
Errors, n signals.
Missed signals, n

Performance of the brain responses to The previous test is conducted in the feedback mode for a fixed period of time (5 min). It is necessary to process the maximum
feedback number of signals presented with a given exposure.
Reaction time, ms
Errors, n
Missed signals, n

The Bourdon’s test The subject is provided with the alphabetic version of the Bourdon’s test to highlight certain letters for the time of 4 mins.
Processed letters per 1th min, n
Processed letters per 4th min, n

10 words memorizing test, n To remember as many of 10 words presented one after another as possible.

10 numbers memorizing test, n To remember as many of 10 numbers presented one after another as possible.

10 nonsense syllable memorizing To remember as many of 10 nonsense syllables presented one after another as possible.
test, n

2.3. Statistical analysis 3.1.2. After cardiac surgery

Adverse cardiovascular events (myocardial infarction,
The data were analyzed using STATISTICA 10.0 software stroke, death, and repeated unplanned revascularization)
(StatSoft, Tulsa, OK, USA). The Shapiro–Wilk test was used to test were not observed in the examined patients in the early
the normality of data. Most of the data (clinical parameters and post-operative period simultaneous with CABG + CEA or
cognitive indicators) were non-normal; thus, the Mann–Whitney isolated CABG.
test was used to analyze it. Log-transforming EEG power In our cohort, POCD occurred in 29 (63.0%) patients with
spectral data were performed in order to normalize the data. CABG + CEA and in 32 (59.0%) patients with isolated CABG
Further analysis of the EEG data was done by performing a (OR = 1.17, 95 % CI = 0.52–2.63, p = 0.7). Thus, the incidence
repeated measure ANOVA. Planned comparisons were used to of postoperative cognitive deficit was comparable in simultaneous
compare every two tests, a p-value of <0.05 was considered and isolated cardiac surgery.
statistically significant. Postoperative indicators of psychomotor speed and executive
function, attention, and short-term memory were analyzed.
Significant intergroup differences were detected in the indicators of
psychomotor speed and executive function compared to baseline.
3. Results At 7–10 days after surgery, psychomotor speed was higher in
the CABG group compared to the CABG + CEA group in the
3.1. Neuropsychological functioning executive function tests, see Table 4. The isolated CABG patients
also presented with higher indicators of executive control function
3.1.1. Before cardiac surgery at 7–10 days after surgery compared to patients with CABG
Executive functions and psychomotor speed, attention, and + CEA.
short-term memory were analyzed, and significant intergroup
differences at baseline were noted in the indicators of psychomotor
speed and executive function. Increased psychomotor speed was 3.2. EEG data
noted in the CABG group, whereas in the CABG + CEA group, this
indicator was lower, see Table 3. Moreover, CABG + CEA patients For the next stage of the analysis, patients who underwent
made fewer errors in the executive function test. simultaneous CABG + CEA were divided into two groups

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FIGURE 2
Location of the electrodes of EEG recording. Shaded red circles indicate the regions of interest (ROI).

depending on the laterality of CA revascularization. The × AREA × LATERALITY [F(2,97) = 5.12, p = 0.008, η2 =
repeated measure ANOVA with a between-subject factor of 0.1]. The most pronounced theta1 power difference was found
GROUP (3 levels: CABG + left-sided CEA/CABG + right- between the patients with isolated CABG and CABG + right-
sided CEA/isolated CABG), and within-subject factors of sided CEA. The CABG + right-sided CEA group had higher
EXAMINATION TIME (2 levels: before/after surgery), ROI theta1 power values in the left frontal zone compared to patients
(2 levels: frontal and parietal), and LATERALITY (2 levels: with isolated CABG before and after surgery (Figure 5). After
left/right hemisphere) was performed for the indicators of theta1 surgery, the CABG + right-sided CEA group also had higher
rhythm power. theta1 power values in the left parietal zone and the right
The repeated measure ANOVA revealed the significance of frontal zone compared to patients with isolated CABG, as seen in
the factor EXAMINATION TIME—F(2,97) = 61.9, p ≤ 0.0001, Figure 5.
η2 = 0.38. Theta1 power increase was noted at postoperative
7–10 days compared to baseline in both groups. As seen in
Figure 3, the CABG + right-sided CEA group also differed 4. Discussion
from the isolated CABG group at 7–10 days after surgery
(p = 0.04). One of the main findings of this study was the lower
The interaction of factors GROUP × LATERALITY cognitive performance (in terms of psychomotor speed and
[F(2,97) = 3.13, p = 0.047, η2 = 0.06] was deemed to be executive control) in patients with simultaneous intervention
significant. The CABG + left-sided CEA group showed the (CABG + CEA). It was noted before surgery and then it
least difference regarding the laterality of CEA‘s impact on kept worsening in the early postoperative period at 7–10
theta1 power. Patients in the isolated CABG and the CABG + postoperative days.
right-sided CEA groups had higher theta1 power values in the As stated in the review by Piegza et al. (2021), recent
left hemisphere compared to the right hemisphere. This effect studies have highlighted the impact of impaired circulation due
was more pronounced in the CABG + right-sided CEA patients to high-grade carotid stenosis on cognitive deterioration. The
(Figure 4). study hypothesized that cerebral blood flow impairment could
The topography and severity of post-operative changes in be an independent and potentially reversible factor determining
the theta1 power rhythm differed in patients depending on the cognitive decline in patients with severe stenosis (Lattanzi
type of cardiac surgery. Thus, another significant interaction was et al., 2018). Recent studies have also shown that aortic arch
revealed between the factors GROUP × EXAMINATION TIME atheroembolism may play a critical role in brain injury and carotid

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TABLE 3 Cognitive indicators in the patients before cardiac surgery.

Cognitive tests and Isolated CABG CABG+CEA F p (Mann–Whitney U

indicators n = 54 n = 46 test)
Complex visual-motor reaction
Reaction time, ms 564.0 [526.0; 620.0] 621.0 [575.0; 736.0] −3.37 0.0008

Errors, n 2.0 [1.0; 3.0] 2.0 [1.0; 3.0] 0.08 0.93

Level of functional mobility of nervous processes responses to feedback

Reaction time, ms 453.0 [424.0; 482.0] 492.5 [453.5; 527.5] −2.73 0.006

Errors, n 25.0 [22; 27] 25 [19; 28] 0.46 0.65

Missed signals, n 17 [11; 21] 25 [19; 28] −1.32 0.19

Performance of the brain responses to feedback

Reaction time, ms 430.0 [401.0; 460] 454.0 [422.0; 486.0] −1.96 0.049

Errors, n 119.0 [111.0; 137.0] 103.0 [89.0; 121.0] 2.75 0.006

Missed signals, n 57.0 [40.0; 80.0] 72.0 [45.0; 109.0] −1.24 0.21

The Bourdon’s test

Processed letters per 1 th min, 68.0 [52.0; 83.0] 71.0 [53.0; 89.0] −0.39 0.70
n

Processed letters per 4 th min, 88.0 [79.0; 119.0] 94.0 [77.0; 107.0] −0.04 0.97
n

Memory
10 numbers memorizing test, 5.0 [4.0; 5.0] 4.0 [3.0; 5.0] 1.12 0.26
n

10 words memorizing test, n 4.0 [4.0; 5.0] 4.0[3.0; 5.0] 1.76 0.08

10 nonsense syllable 2.0 [2.0;4.0] 3.0 [2.0;4.0] −1.51 0.13

memorizing test, n

disease and can serve as a marker of arch atherosclerosis, thus, indicates cerebral dysfunction and may be a predictor of
increasing the risk of cardioembolism in CPB (Naylor et al., long-term cognitive impairment, meaning it is important for
2002). diagnostic purposes (Tarasova et al., 2018, 2019). In cardiac
Despite the fact that CABG + CEA patients had worse surgery patients, an increase in theta activity can be associated
cognitive performance at baseline, the incidence of POCD was with cerebral ischemia during CPB. Cerebral atherosclerosis
comparable in both simultaneous and isolated cardiac surgery leads to endothelial dysfunction, perivascular nerve damage,
groups. This can be explained by the prolonged CPB and arterial stiffness, and cerebrovascular insufficiency (de la Torre,
operation time in isolated CABG patients. Another reason 2017; Frey et al., 2018). Together, these adverse factors cause
could be the recovery of cerebral circulation following carotid neuronal dysfunction, tissue atrophy, and damage in neural
revascularization (Crespo Pimentel et al., 2022). In the study networks, resulting in cortical suppression by subcortical regions
by Relander et al. (2022), CABG patients more frequently and the domination of low-frequency brain activity (Daulatzai,
presented with short-term postoperative cognitive dysfunction 2017).
compared to CEA patients. According to the authors, POCD is Frontal and parieto-occipital brain zones are particularly
deemed to be a heterogeneous condition. It should also be noted vulnerable to cerebral hypoperfusion and microemboli associated
that the incidence of POCD was estimated based on relative with on-pump cardiac surgery (Pierik et al., 2019). The frontal
differences between the baseline and postoperative cognitive and parietal zones are known as “cerebral watershed areas,”
indicators. Thus, comparable POCD incidence in simultaneous and they are perfused by the most distal branches of two
and isolated cardiac surgery patients could be a manifestation major cerebral arteries (Momjian-Mayor and Baron, 2005;
of the ceiling effect that occurs when an independent factor Amano et al., 2020). Furthermore, frontal brain zones play a
(cardiac surgery) no longer has an effect on a dependent variable key role in cognitive control and executive function (Widge
(cognitive performance). et al., 2019; Friedman and Robbins, 2022). The results of our
The results of the EEG study have shown that the theta study showed significant intergroup differences in the theta
power increased in all patients in the early postoperative power in the left and right frontal zones, in particular, worse
period compared to baseline regardless of the type of cardiac executive function was noted in patients with simultaneous
surgery. The increase in theta activity in resting-state EEG intervention and isolated CABG. Moreover, patients who

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TABLE 4 Cognitive indicators in the patients after cardiac surgery.

Cognitive tests and Isolated CABG CABG+CEA F p (Mann–Whitney U

indicators n = 54 n = 46 test)
Complex visual-motor reaction
Reaction time, ms 511.5 [489.0; 557.5] 624.0 [566.0; 679.0] −4.39 ≤0.00001

Errors, n 2.0 [1.0; 3.0] 2.0 [1.0; 3.0] 0.05 0.96

Level of functional mobility of nervous processes responses to feedback

Reaction time, ms 438.5 [410.0; 461.5] 499.0 [457.5; 516.5] −3.84 0.00006

Errors, n 26.0 [24.0; 30.0] 25.0 [19.5; 28.0] 1.43 0.15

Missed signals, n 12.0 [7.5; 16.5] 25.0 [13.5; 28.0] −3.03 0.002

Performance of the brain responses to feedback

Reaction time, ms 422.0 [403.0; 451.5] 479.0 [430.0; 515.0] −3.65 0.0003

Errors, n 132.0 [113.0; 147.0] 94.0 [76.0; 121.0] 3.27 0.001

Missed signals, n 45.0 [20.0; 90.0] 66.0 [50.0;106] −1.62 0.11

The Bourdon’s test

Processed letters per 1 th min, 70.0 [55.0; 91.0] 69.5 [61.5; 92.0] −0.37 0.97
n

Processed letters per 4 th min, 98.0 [74.0;111.0] 80.0 [74.0; 100.5] 1.17 0.24
n

Memory
10 numbers memorizing test, 5.0 [4.0; 6.0] 4.0 [3.0; 5.0] 1.69 0.09
n

10 words memorizing test, n 4.0 [3.0; 5.0] 4.0 [3.0; 5.0] −1.59 0.11

10 nonsense syllable 3.0 [2.0; 3.0] 4.0 [2.0; 4.0] 0.81 0.42
memorizing test, n

FIGURE 3
Postoperative theta1 rhythm power changes in the patients undergoing isolated CABG and simultaneous intervention (CABG + CEA). Solid red
lines—the preoperative indicators, and dashed blue lines—the postoperative indicators. * indicates the significance level p ≤ 0.05 in the postoperative
indicators of the right-sided CEA + CABG group in comparison to the CABG group.

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Tarasova et al. 10.3389/fnhum.2023.996359

underwent CABG + right-sided CEA demonstrated more CPB is traumatic for the brain regardless of its features.
pronounced theta power changes compared to patients with Therefore, the search for diagnostic markers of the prediction
isolated CABG. of the impact of CABG and simultaneous intervention on
It has been recently reported that severe carotid stenosis brain function, and the implementation of the mandatory
can disturb the hemodynamic balance, illustrated by blood flow assessment of cognitive performance before surgery would
laterality (Zarrinkoob et al., 2021). In the study by Hedberg and be of great assistance to researchers. Further studies are
Engström (2013), the authors showed that stroke occurs more necessary to identify the group of patients who will benefit
frequently in the right hemisphere compared to the left hemisphere the most from simultaneous revascularization. Moreover, we
in the early postoperative period of cardiac surgery. As shown by need more sensitive and specific neuropsychological tests that
the results of our study, contralateral stenosis of CA was observed can assign each symptom to certain brain regions, as well as
in 76% of patients undergoing CABG + right-sided CEA. Thus, modern brain imaging techniques for diagnosis. For example,
worse brain function in patients after CABG + right-sided CEA the sLORETA algorithm has been used to identify brain
may be due to both surgical techniques focusing on right or left electrical patterns associated with various cognitive impairments in
carotid arteries and cerebral blood flow impairment. resting-state EEG.
Summarizing the abovementioned points, the results of
the study allow us to conclude that cardiac surgery with
5. Limitations
It is important to mention some of the limitations of
this study. One limitation is a lack of data regarding cerebral
blood flow laterality and the degree of the recruitment
of collaterals. Another limitation of the study is the
small sample of patients with simultaneous interventions.
Moreover, the surgical procedure (anesthesia) time differed
between the isolated CABG and the CABG + CEA
group. Further research should be conducted to address
these issues.

6. Conclusion
Thus, both CABG and simultaneous CEA and isolated CABG
show comparable POCD incidence. It is important to note
that all types of cardiac surgery resulted in the theta power
increase in the early postoperative period compared to baseline.
FIGURE 4 The CABG + right-sided CEA group is characterized by the
Lateral differences of theta1 power in the patients undergoing most pronounced theta rhythm changes compared to patients
isolated CABG and simultaneous intervention (CABG + CEA). Blue
columns—the power values in the left hemisphere, and red undergoing isolated CABG and CABG + left-sided CEA due to
columns—the power values in the right hemisphere. a higher incidence of bilateral carotid artery stenosis and severe
brain ischemia.

FIGURE 5
Topography of the postoperative theta1 rhythm power changes in the patients undergoing isolated CABG and simultaneous intervention (CABG +
CEA). (A)—Left hemisphere, (B)—right hemisphere; green columns—isolated CABG, blue columns—left-sided CEA + CABG group, red
columns—right-sided CEA+CABG group. + indicates the significance level p ≤ 0.05 in between-group differences.

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Tarasova et al. 10.3389/fnhum.2023.996359

Data availability statement Funding

The data that support the findings of this study are not readily This study was supported by the Federal State Ministry of
available because data sharing is not applicable. Further inquiries Science and Education of the Russian Federation (Fundamental
can be directed to the corresponding author. research topic No. 122012000364-5, dated January 20, 2022). The
funder was not involved in the study design, collection, analysis,
interpretation of data, the writing of this article, or the decision to
Ethics statement submit it for publication.

The studies involving human participants were reviewed

and approved by Ethics Committee of the State Research Conflict of interest
Institute for Complex Issues of Cardiovascular Diseases. The
patients/participants provided their written informed consent to The authors declare that the research was conducted in the
participate in this study. absence of any commercial or financial relationships that could be
construed as a potential conflict of interest.

Author contributions Publisher’s note

IT, OT, and DK: study concept, design, analysis, interpretation All claims expressed in this article are solely those of the
of data, and statistical analysis. IT, DK, OM, IS, IK, AS, authors and do not necessarily represent those of their affiliated
and RT: data collection. OT, RT, and OB: critical revision organizations, or those of the publisher, the editors and the
of the manuscript and study supervision. IT: drafting of the reviewers. Any product that may be evaluated in this article, or
manuscript. All authors contributed to the article and approved the claim that may be made by its manufacturer, is not guaranteed or
submitted version. endorsed by the publisher.

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