Neurophysiological and neuroradiological predictors of outcome in postanoxic encephalopathy in children

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Introduction

Postanoxic encephalopathy (PAE) is a rare polyetiological clinical condition for which there is an opinion that favorable clinical outcomes occur more frequently in the pediatric population than in adults [1]. The fact that the injury occurs during the period of incomplete myelination and synaptogenesis has historically been interpreted as a potential ground for (re)habilitation of a child with severe PAE; however, descriptions of individual clinical cases and case series demonstrate the ambiguity of this judgment [2, 3]. The inability to shape a prognosis for recovery in a child with PAE based solely on clinical examination data dictates the need to use functional and imaging diagnostic methods, the scope of which is not standardized. The relationship between the child’s age at the time of injury and the utility of diagnostic modalities has not been determined. Therefore, the study of diagnostic markers for predicting PAE outcomes in children, taking into account the child’s age at the time of injury, is needed.

Study aim: To assess the structural and functional integrity of the corticospinal tract (CST) and thalamocortical projections (TCP) in children with severe PAE and to identify the leading diagnostic markers for predicting clinical outcomes regarding the recovery of voluntary motor function, taking into account the patient’s age at the time of hypoxic injury.

Materials and methods

The study included 12 children (4 girls and 8 boys) aged 1 to 16 years in the intermediate (up to 6 months) and long-term (up to 1 year) periods of PAE, who underwent rehabilitation at the Research Institute of Emergency Pediatric Surgery and Traumatology between 2020 and 2024.

Inclusion criteria:

• diagnosis of PAE;
• signed informed consent from the child’s legal representative.

Exclusion criterion: history of congenital disorder of the central nervous system (CNS) with damage to the CST or TCP.

A partial limitation of the study was implanted devices in the child, particularly a pacemaker, which prevented the use of magnetic field-based investigations (in 2 cases). Also, not all patients were able to complete planned study assessments, namely neuroimaging, including follow-up, in cases of technical malfunction of the MRI during hospitalization, or with a nosocomial infection, when performing an imaging under sedation was not justified. In 3 cases, MRI was performed for patients before hospitalization at an external healthcare facility; however, its quality did not allow for morphometry and tractography of the regions of interest, and repeating the study under sedation at a short interval was not ethically justified.

The study was approved by the local ethics committee of the Research Institute of Emergency Pediatric Surgery and Traumatology (protocol No. 23 dated September 28, 2023).

Based on the age-dependent concept of the formation and consolidation of the locomotor act, which is founded on systemic-functional ideas, including P.K. Anokhin’s theory of afferent synthesis and N.A. Bernstein’s theory of the hierarchical mechanism of movement control, all patients were divided into 3 age groups:

• I (1–6 years) — formation of the locomotor act (n = 7);
• II (6–12 years) — consolidation of the locomotor act (n = 1);
• III (12–16 years) — established locomotor act (n = 4).

All patients underwent a standard neurological examination with assessment of gross motor functions using the Gross Motor Function Classification System (GMFCS)¹. Differential diagnosis of impaired consciousness level was performed by a clinical psychologist using the Dobrokhotova–Zaitsev Consciousness Recovery Scale and the Bykova–Lukyanov Communicative Activity Scale (SCALB) [4]. Electrophysiology studies were performed according to standardized protocols and included: recording of somatosensory evoked potentials upon median nerve stimulation using a two-channel scheme (Erbⁱ/Erb^c and C3’/C4’) with assessment of cortical components according to the Houlden grading system, 19-channel two-hour video-electroencephalographic monitoring with recording of sleep patterns, single-pulse transcranial magnetic stimulation (single-pulse TMS) with assessment of motor evoked potential (MEP) parameters and central motor conduction time (CMCT) along the corticocervical tract with recording of potentials from the m. abductor pollicis brevis bilaterally [5–7].

Neuroimaging studies included a standard structural MRI protocol used at the Research Institute of Emergency Pediatric Surgery and Traumatology. Based on this data, segmentation and morphometry of brain structures were performed using the Vol2Brain software suite, as well as magnetic resonance (MR) tractography of the CST from the supplementary motor area (SMA) and primary motor cortex (PMC). For segmentation and morphometry, three-dimensional T1-weighted brain images obtained on an Achieva dStream 3T MR scanner (Philips) were used. For MR tractography data acquisition, an echo-planar imaging pulse sequence with the following parameters was used: TR = 9431 ms; TE = 70 ms; matrix 120/144 pixels; FOV = 240 mm; voxel size 2 × 2 × 2 mm; EPI factor = 63; slice gap = 0; number of signal averages (NSA) = 2; diffusion gradients were applied in 32 non-collinear directions.

To compare the results of MR tractography with normative data, we recruited a control group consisting of 30 children aged 6–16 years who were seen by an outpatient neurologist and had no anamnestic or clinical data indicating CST involvement.

The system for assessing structural brain damage based on MRI data was developed by analogy with the classification proposed for evaluating structural damage in cerebral palsy, with a focus on motor representation structures [8]. The assessment was performed in the cortical motor areas of both hemispheres — M1, SMA, and PMC:

• 0 — normal;
• 0.5 — mild increase (↑) in T2/FLAIR lesions or mild atrophy (≤ 25%);
• 1.0 — moderate ↑T2/FLAIR or moderate atrophy (25–50%) or a cyst ≤ 1.5 cm;
• 1.5 — pronounced ↑T2/FLAIR or pronounced atrophy (≥ 50%) or a cyst ≥ 1.5 cm).

Furthermore, the CSTs were assessed for degeneration and volume loss:

• 0 — normal;
• 0.5 — mild ↑T2/FLAIR or mild atrophy;
• 1.0 — moderate ↑T2/FLAIR or moderate atrophy or WD;
• 1.5 — pronounced ↑T2/FLAIR or pronounced atrophy/disappearance or direct damage).

Changes in the subcortical motor nodes — the striatum and thalamus on both sides — were also evaluated (0 — normal; 0.5 — mild ↑T2/FLAIR or mild atrophy (≤ 25%); 1.0 — moderate ↑T2/FLAIR or moderate atrophy (25–50%) or lesions; 1.5 — pronounced ↑T2/FLAIR or pronounced atrophy (≥ 50%) or large lesions/cysts).

Results

Out of 12 children, 4 (boys aged 3, 9, 12, and 15 years) one child from age groups I and II each and two children from group III showed significant regression of neurological symptoms in terms of partial recovery of locomotor function while cognitive deficit persisted. The rate of regression was more pronounced in the intermediate period of the disease.

According to the presented data, generalized dystonias predominated in the clinical picture of children with PAE; one child from age group I with an unfavorable clinical outcome exhibited myoclonus (Table 1).

 

Table 1. Clinical data of patients with PAE during the first hospitalization

Patient	Age	Sex	Level of consciousness	GMFCS	Disease period		Clinical phenomena
					intermediate	long-term	generalized dystonia	myoclonus
S.	12	М	Clear consciousness with intellectual-mnestic impairment	3		+	+	–
М.	2	F	MCS–	5	+		+	–
P.	5	М	MCS–	5		+	+	+
B.	5	F	MCS–	5		+	+	–
B.	4	F	MSC+	5	+		+	–
P.	14	М	MSC+	5		+	–	–
B.	9	М	MSC+	5	+		+	–
S.	3	F	MSC+	5	+		+	+
М.	3	М	MSC+	5	+		+	–
М.	1	М	MCS–	5	+		+	–
М.	15	М	Clear consciousness with intellectual-mnestic impairment	3	+		–	–
A.	16	М	MSC+	5	+		–	–

Note. MCS — minimal consciousness state (+/–); GD — generalized dystonia; M — myoclonus; GMFCS — Gross Motor Function Classification System.

 

Diagnostic single-pulse TMS was performed in 10 out of 12 children (2 had a cardioverter-defibrillator implanted), with three children examined dynamically. Significant progress in rehabilitation was observed in 3 out of the 10 examined children (one from each category). Only one of them was examined twice and demonstrated normalization of the motor threshold and MEP amplitude by the long-term period of the disease. In a 3-year-old child with a favorable clinical outcome, we failed to record an MEP during single-pulse TMS (Table 2).

 

Table 2. Parameters of MEP and CMCT during single-pulse TMS in patients with PAE with recording from the m. abductor pollicis brevis bilaterally

Patient

Age, years

Disease period

Parameters of the motor evoked potential of the right hemisphere

Central motor conduction time of the right CST

Parameters of the motor evoked potential of the left hemisphere

Central motor conduction time of the left CST

motor threshold, %

latency, ms

amplitude, mV

area, mV×ms

motor threshold, %

latency, ms

amplitude, mV

area, mV×ms

S.

3

Intermediate

–

–

–

–

–

–

–

–

–

–

S.

4

Long-term

–

–

–

–

–

–

–

–

–

–

B.

9

Intermediate

85*

18.7

3.31

11.3

6.8

85*

19.8

0.977

3

9.01

B.

10

Long-term

75

18.8

1.21

5.4

7.43

75

19.1

0.828

2.2

7.33

P.

14

Long-term

85*

17.2

0.107*

0.4

6.23

85*

29.3*

0.048*

0.4

12*

S.

12

Long-term

60

20.8

0.692

3

10.4*

50

22.1*

2.07

5.9

10.7*

М.

2

Intermediate

–

–

–

–

–

–

–

–

–

–

P.

5

Long-term

–

–

–

–

–

–

–

–

–

–

B.

5

Intermediate

–

–

–

–

–

–

–

–

–

–

B.

4

Intermediate

–

–

–

–

–

–

–

–

–

–

B.

5

Long-term

–

–

–

–

–

–

–

–

–

––

М.

3

Intermediate

–

–

–

–

–

–

–

–

–

–

М.

1

Intermediate

–

–

–

–

–

–

–

–

–

–

Note. *Results deviating from normative values. The normative data provided are derived from age-related dynamics of motor evoked potential parameters and central motor conduction time in children (according to K. Muller et al.²).

 

Brain structure morphometry and segmentation was performed for 7 children (including follow-up assessment in 2 patients). Two patients from groups I and III with a favorable clinical outcome were not included in the study. The child with the best clinical outcome in terms of motor function recovery from group II had unchanged volumes of the studied brain regions both at the initial examination and during follow-up. A decrease in thalamic volume, as well as a deficit in the volume of gyri and thickness of the cortical layer involved in the formation of the CST, was noted in 6 out of 7 examined children (Table 3).

 

Table 3. Results of automatic quantitative volumetric morphometric analysis of brain structures

Patient	Age, years	PAE period	Gyrus volume/cortical thickness						Thalamus/volume
			right hemisphere			left hemisphere
			PrCG	MFG	SMA	PrCG	MFG	SMA
S.	3	Intermediate	9.92*/1.6*	17.88*/2.03*	3.54*/2.19*	10.31*/1.59*	17.21*/2.11*	4.46*/2.13*	5.13*
S.	4	Long-term	12.09*/3.03*	22.48/3.44	4.41*/3.97*	12.36*/2.86	24.14/3.36	4.76*/3.6	7.46*
B.	9	Intermediate	11.24/1.22	16.46/1.61	4.65/1.87	11.1/1.1	17.86/1.52	5.04/1.68	9.07
B.	10	Long-term	13.3/2.37	20.28/3.3	5.51/3.34	12.25/ 2.37	21.17/2.9	5.76/3.1	10.74
P.	14	Long-term	8.46*/1.14*	17.54*/1.63*	4.03*/1.66*	8.38*/1.39*	13.71*/1.54*	4.01*/1.6*	4.78*
S.	12	Long-term	11.43*/1.69*	20.6/2.13*	3.88*/2.56	12.21*/1.53*	19.18*/1.98*	4.5/2.17*	9.05*
P.	5	Long-term	8.04*/2.8*	16.11/2.56	3.26*/3.52*	8.42/2.5*	18.35/2.62	3.42/3.29	6.35*
B.	4	Intermediate	8.46*/1.82	13.13*/2.22*	3.65*/2.14*	9.25*/1.55*	12.55*/2.05*	3.3*/2.23*	6.19*
B.	5	Long-term	9.06*/1.93	14.48*/2.54	3.8*/2.29*	9.51*/1.62*	13.25*/2.29*	3.4*/2.17*	6.96*
М.	1	Intermediate	5.67*/2.73*	9.7*/2.2	2.15*/1.7*	5.02*/2.13	9.2*/2.19	1.41*/1.35*	2.29*

Note. PrCG — precentral gyrus; MFG — middle frontal gyrus. * — volume reduction relative to age norm.

 

MR tractography was performed in 7 patients, including follow-up assessment in 2 patients. Children older than 6 years were compared with the results of the control group. Among children of groups II and III, regardless of clinical outcome, a decrease in the fractional anisotropy (FA) coefficient and an increase in the radial diffusivity (RD) were observed compared to the control group (Table 4).

 

Table 4. Results of MR Tractography of CSTs Originating from the PMC and SMA of Both Hemispheres

Patient	Age, years	Disease period	SMA tract on the left				SMA tract on the right				PMC tract on the left				PMC tract on the right
			volume	length	FA	ADC	volume	length	FA	ADC	volume	length	FA	ADC	volume	length	FA	ADC
S.	3	Intermediate	433	100.5	0.467	0.892	–	–	–	–	–	–	–	–	–	–	–	–
S.	4	Long-term	1194	106.8	0.386	1.039	2061	108.7	0.395	1.097	477	90	0.461	1.04	577	108.5	0.444	1.039
B.	9	Intermediate	–	–	–	–	–	–	–	–	575	110	0.445*	0.906*	1470	125	0.48*6	0.932*
B.	10	Long-term	1561	135	0.478*	0.928*	383*	123	0.481*	0.89*	3072	141	0.476*	0.931*	2200	133	0.447*	0.921*
P.	14	Long-term	1438	104	0.434*	1.1*	2977	138	0.432*	1.012*	1061*	115	0.453*	1.02*	4655	126	0.433*	1.057*
S.	12	Long-term	2955	123	0.483*	0.959*	3338	136	0.389*	0.997*	3672	135	0.47*	0.975*	3505	125	0.448*	0.998*
P.	5	Long-term	1900	124	0.395	1.098	2011	123	0.379	1.154	1961	124	0.402	1.086	1522	105	0.391	1.239
B.	4	Intermediate	1061	130	0.428	0.944	466	99.9	0.396	0.947	1566	127	0.401	1.083	1316	101	0.412	1.215
М.	1	Intermediate	–	–	–	–	–	–	–	–	–	–	–	–	–	–	–	–
N.	6–6		3401.13 ± 2962.45	120.15 ± 22.83	0.69 ± 0.12	0.67 ± 0.085	3714.66 ± 2559.36	120.05 ± 18.96	0.68 ± 0.04	0.67 ± 0.05	6005.44 ± 4819.04	121.73 ± 20.47	0.69 ± 0.05	0.67 ± 0.07	6376.92 ± 6197.41	123.43 ± 14.00	0.68 ± 0.04	0.68 ± 0.08

Note. ADC — apparent diffusion coefficient; blank field — tractography not possible; *abnormal.

 

Assessment of the brain structures atrophy was performed in 10 out of 12 children (including follow-up assessment in 3 patients). The youngest child (a 1-year-old boy) had the most significant volume of structural damage in both hemispheres. Periventricular leukomalacia showed a tendency to resolve during the follow-up, which was observed in 2 out of 3 follow-up studies. Patients from groups II and III with a favorable recovery outcome had ≤ 5 points in the severity assessment of the atrophic changes in the CST, striatum, and thalami. A 3-year-old patient with a favorable outcome had 10 points in the intermediate period of PAE, which was higher than the values of other children from group I with an unfavorable outcome (Table 5).

 

Table 5. Severity assessment for the atrophic changes in the CST and subcortical structures involved in voluntary motor function according to MRI data

Patient

Age, years

Disease period

Left

Right

Total score

M1

PMC

SMA

SCT

striatum

thalamus

score

M1

PMC

SMA

SCT

striatum

thalamus

score

S.

3

Intermediate

++

+

++

2.5

+++

+

++

3

5.5

S.

4

Long-term

++

+

++

2.5

++

+

++

2.5

5

B.

9

Intermediate

+

+

1

+

+

1

2

B.

10

Long-term

+

0.5

+

0.5

1

P.

14

Long-term

+++

++

++

++

++

++

6.5

+++

++

++

++

++

++

6.5

13

S.

15

Long-term

++

+

++

2.5

++

+

++

2.5

5

М.

3

Intermediate

++

+

+

++

++

++

5

++

+

+

++

++

++

5

10

P.

5

Long-term

+

+

+

+

++

++

4

+

+

+

+

++

++

4

8

B.

4

Intermediate

+

+

+

+

+

+

3

+

+

+

+

+

+

3

6

B.

5

Long-term

+

+

+

+

+

+

3

+

+

+

+

+

+

3

6

М.

1

Intermediate

+++

+++

+++

++

++

++

7.5

+++

+++

+++

++

++

++

7.5

15

M.

15

Intermediate

+

++

+

2

++

+

1.5

3.5

А.

16

Long-term

+++

+

+

++

3.5

+++

+

+

++

3.5

7

Note. An empty field — normal; + 0.5 (mild); ++ 1 (moderate); +++ 1.5 (pronounced) degrees of atrophy.

 

Somatosensory evoked potentials (SSEPs) and video-electroencephalographic monitoring (VEEG) were performed in all 12 children (including follow-up assessment in 3 patients). Children with a favorable clinical outcome had preserved sleep patterns, a dominant rhythm, and a score of more than 4 on the Houlden grading system, which corresponds to preserved but altered cortical N20 potentials. Two older boys (12 and 15 years old) had increased latency of the N20 complex, which correlated clinically with the severity of intellectual and mnestic impairment (Table 6).

 

Table 6. Results of cortical SSEP and VEEG in children with PAE

Patient	Age, years	Disease period	Right hemisphere N20		Left hemisphere N20		Houlden score	VEEG
			latency, ms	amplitude, μV	latency, ms	amplitude, μV		epileptiform activity	dominant rhythm	sleep patterns
S.	3	Intermediate	–	–	–	–	1	+	–	–
S.	4	Long-term	–	–	20.5*	1.47	2	+	+	+
B.	9	Intermediate	20.6	4.8	20.2	4.6	4	+	+	+
B.	10	Long-term	15.1	0.385	15.3	0.21	6	–	+	+
P.	14	Long-term	–	–	–	–	1	–	–	–
S.	12	Long-term	21.8*	5.5	17.1	3.28	5	–	+	+
М.	2	Intermediate	13.4	0.414*	–	–	2	+	–	+
P.	5	Long-term	–	–	–	–	1	–	+	NFA
B.	5	Intermediate	–	–	–	–	1	–	–	–
B.	4	Intermediate	–	–	–	–	1	+	–	–
B.	5	Long-term	–	–	–	–	1	+	+	+
М.	3	Intermediate	23.3*	4.24	23.8*	0.138	4	–	+	+
М.	1	Intermediate	21.7*	0.263	–	–	2	–	–	–
М.	15	Intermediate	26.8*	6.82	26.7*	3.55	4	–	+	+
А.	16	Long-term	–	–	–	–	1	–	–	NFA

Note. NFA — child did not fall asleep; * — deviation from normative values.

 

Discussion

Among patients in Group I (the largest group in the study), a favorable outcome in terms of partial regression of neurological deficit was observed in only one child, a 3-year-old with a history of a short-term freshwater drowning episode.

Analysis of Group I patients demonstrates a trend toward a favorable prognosis for recovery in cases of post-hypoxic injury acquired during the period of locomotor skill formation, provided there are cortical components of SSEPs (≥ 4 points on the Houlden grading system) combined with a preserved dominant rhythm and physiological sleep patterns (according to VEEG) in the intermediate period of the disease. Morphometry findings for the cortical motor representation area and thalami showed a high frequency of atrophic changes; however, an increase in the volume of gyri and thickness of the cortical layer over time was not accompanied by restoration of their function. Assessment of structural damage proved less informative for predicting recovery among children in Group I, which may be related to the small number of observations and/or limitations of the method in identifying reparative processes and age-dependent myelination. Diagnostic single-pulse TMS in the intermediate and long-term periods of the disease in children with PAE under 6 years of age is of little value for predicting the recovery of motor function. Epileptiform activity can be recorded both in the intermediate and long-term periods, complicating the child’s rehabilitation process.

Group II, corresponding to the stage of consolidation of the locomotor act, is represented by 1 clinical case. This case demonstrated the best outcome in terms of recovery of locomotor function among all patients with PAE we observed.

The patient demonstrated MEPs upon stimulation of both hemispheres, with an increase in the motor threshold during the intermediate stage of the disease and its subsequent normalization by the long-term period. Afferent TMS was functionally intact, as confirmed by the results of SSEPs (≥ 4 points on the Houlden grading system) and VEEG (dominant rhythm and physiological sleep patterns). According to morphometry, the child showed preserved volumes of the assessed brain structures. Structural assessment of the brain showed that the patient scored less than 2 points in both hemispheres (out of a maximum of 15 in the studied sample — indicating pronounced atrophic changes).

Of the 4 observed children in Group III, 2 had contraindications for the TMS assessments — an implanted pacemaker. As a result, single-pulse TMS was performed on only 2 children, aged 12 and 14 years. In the 14-year-old child, who lacked voluntary movements, we managed to record altered (low-amplitude) MEPs. In the 12-year-old child, who had regained the ability to perform voluntary movements, a bilateral increase in CMCT along the corticocervical tract was noted, with an unchanged MEP threshold. The assessment of brain structures demonstrated a lower score in the 12- and 15-year-old patients with a favorable outcome compared to the 16-year-old patient with an unfavorable recovery outcome. The SSEP results in 2 children with MCS+ who lacked voluntary movements (aged 14 and 16) demonstrated the absence of cortical SSEP components and a dominant rhythm (the brain’s bioelectrical activity had a polyrhythmic pattern). Two children, aged 12 and 15, with positive changes in the recovery of consciousness level from MCS+ to severe intellectual and mnestic impairment and the ability to move independently, demonstrated increased latency of the N20 complexes with a preserved dominant rhythm and sleep patterns. Generalized dystonia was observed in only 1 child (aged 12), and myoclonus was not recorded among the children in the older age group.

In a 14-year-old child with an unfavorable clinical outcome, partial anatomical preservation of the corticospinal tract was accompanied by an increased motor threshold and a decreased MEP amplitude. Furthermore, morphometric data revealed a volume deficit in the studied structures with a conduction block at the central level upon registration of SSEP cortical components.

A decrease in the fractional anisotropy coefficient and an increase in the radial diffusivity of corticospinal projections from the PMC and SMA were found in children of groups II and III compared to the control group, accompanying the course of PAE regardless of the clinical outcome.

Thus, we can assume that favorable outcome with the recovery of voluntary movement function in children over 6 years of age with PAE might be considered in the presence of cortical components of somatosensory evoked potentials (≥ 4 points on the Houlden grading system), physiological sleep patterns and a dominant rhythm according to VEEG (in the intermediate and long-term periods of the disease), ≤ 5 points on the severity scale of atrophic changes in brain structures, and unchanged MEP thresholds or CMCT.

According to our observations, the most vulnerable group for the systemic effect of hypoxia are children under 6 years of age, which is likely due to the physiological immaturity of synaptic structures and, consequently, the formation of network hyperexcitability, as confirmed by frequent observations of paroxysmal motor phenomena and epileptiform discharges, including in our sample predominantly among younger children. The etiological cause of network hyperexcitability under hypoxic conditions is the activation of excitatory cortical synapses after anoxic depolarization [9–17].

Based on the obtained data, we can assume a leading role of the afferent CNS component across all age groups in the recovery of voluntary motor function, the integrity of which can be objectified by functional and neuroimaging studies.

The functional and anatomical integrity of the CST in the younger age group of children is likely fundamental for the subsequent formation of motor behavior; therefore, its severe damage during the period of locomotor act development plays a key role in the inability to perform voluntary movements [18]. In children at the stage of an already formed locomotor act, partial anatomical and functional preservation of only the efferent component, with severe impairment of the afferent ascending system, also does not allow for voluntary movements.

A limitation of our study is the lack of normative data for MR tractography of the CST in the group under 6 years of age, which currently does not allow for definitive conclusions regarding the diagnostic value of the study indicators in children of this age.

Conclusion

The data indicate the importance of preserving the afferent component of the CNS in children with PAE across all age groups and also create a prerequisite for developing recommendations on the scope and timing of investigations depending on the child’s age. The period of locomotor act formation is associated with low diagnostic value of neurophysiological and neuroradiological methods for assessing the anatomical and functional integrity of the CST. Confirmation of the obtained results requires studies with a larger number of clinical observations followed by statistical data processing.

 

¹ Cerebral Palsy Alliance. Gross Motor Function Classification System (GMFCS). URL: https://cparf.org/what-is-cerebral-palsy/severity-of-cerebral-palsy/gross-motor-function-classification-system-gmfcs

² Muller K, Homberg V, Lenard HG. Magnetic stimulation of motor cortex and nerve roots in children. Maturation of cortico-motoneuronal projections. Electroencephalogr Clin Neurophysiol. 1991;81(1):63–70. DOI: http://doi.org/10.1016/0168-5597(91)90105-7

About the authors

Daria S. Kanshina

Research Institute of Emergency Pediatric Surgery and Trauma — Dr. Roshal’s Clinic

Author for correspondence.
Email: dr.d.kanshina@gmail.com
ORCID iD: 0000-0002-5142-9400

Cand. Sci. (Med.), senior researcher, Department of rehabilitation

Russian Federation, Moscow

Ilya A. Melnikov

Research Institute of Emergency Pediatric Surgery and Trauma — Dr. Roshal’s Clinic

Email: melnikov_ia@doctor-roshal.ru
ORCID iD: 0000-0002-2910-3711

Cand. Sci. (Med.), senior researcher, Head, Division of magnetic resonance and computed tomography, Radiology department

Russian Federation, Moscow

Maxim V. Ublinskiy

Research Institute of Emergency Pediatric Surgery and Trauma — Dr. Roshal’s Clinic

Email: maxublinsk@mail.ru
ORCID iD: 0000-0002-4627-9874

Cand. Sci. (Biol.), senior researcher

Russian Federation, Moscow

Dzheikhun A. Ismiev

Research Institute of Emergency Pediatric Surgery and Trauma — Dr. Roshal’s Clinic

Email: ismiev90@mail.ru
ORCID iD: 0000-0003-4283-3505

radiologist, postgraduate student, Radiology department

Russian Federation, Moscow

Daria V. Shmeleva

Research Institute of Emergency Pediatric Surgery and Trauma — Dr. Roshal’s Clinic

Email: ShmelevaDV1@zdrav.mos.ru
ORCID iD: 0009-0000-6772-5346

radiologist, Division of magnetic resonance and computed tomography, Radiology department

Russian Federation, Moscow

Elizaveta A. Kobzeva

Research Institute of Emergency Pediatric Surgery and Trauma — Dr. Roshal’s Clinic

Email: KobzevaEA3@zdrav.mos.ru
ORCID iD: 0000-0002-4705-7771

resident, Radiology department

Russian Federation, Moscow

Sergey B. Ivanov

Lomonosov Moscow State University

Email: ivanov.sergey04@mail.ru
ORCID iD: 0009-0003-6586-108X

participant, Electrochemical nanoengineering group, Inorganic materials science laboratory

Russian Federation, Moscow

Tolibdzhon A. Akhadov

Research Institute of Emergency Pediatric Surgery and Trauma — Dr. Roshal’s Clinic

Email: akhadov@mail.ru
ORCID iD: 0000-0002-3235-8854

Dr. Sci. (Med.), Professor, Head, Department of radiation diagnostics

Russian Federation, Moscow

References

Supplementary files