Adaptation reactions of hemodynamic systems on artificially modulated stress in healthy individuals

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The concept of stress includes a complex of non-specific adaptation changes in an organism in response to external and internal factors (stressors). The most prominent response of an individual to stress is considered to be reactions on the part of the nervous system and, as a consequence, of the cardiovascular system; complex measurement of these reactions becomes one of criteria for assessment of adaptation status of an organism. Mechanism of primary (early) reactions to stress studied on healthy individuals, provides the basis for its comparison with similar responses in patients with different pathologies, and as a consequence, the possibility for taking early diagnostic and prognostic decisions.

Aim – to study the influence of stimulated psychoemotional stress on the hemodynamic parameters of the peripheral microcirculation in somatically healthy young individuals.

Materials and Methods

In the experiment 30 somatically healthy individuals (16 men and 14 women) participated. The mean age was 18.2±1.1 years. The study was conducted in compliance with the ethical principles of World Medical Association Declaration of Helsinki (1964, 2013); National Standard of the RF “Good Clinical Practice” (GOST Р 52379-2005). All individuals included into the study, gave voluntary informed consent. The protocol of study was approved by Local ethical committee of Chita State Medical Academy (Protocol № 86 of 01.11.2017).

Experiment was conducted in three stages each lasting 5 minutes:

T1 – resting state,

T2 – modulated stress,

T3 – recovery of resting state.

Each stage was conducted with measurement of parameters of hemodynamics and with assessment of heart rate variability. Stress was created by a color test based on Stroop’s effect. This method was designed to assess establishment of association links between cortical zones responsible for perception of color and of letter form. A mismatch between the color and the meaning of the words leads to conflict of perception and, as a result, to stress.

A sensor of dynamic scattering of light mDLS (miniaturized Dynamic Light Scattering, Elfi-Tech, Rehovot, Israel) senses photons reflected from erythrocytes moving in the neighboring blood flow laminae (shear velocity, or lateral velocity gradient). The sensor was positioned on the index finger on the palm side of the hand. The signal was integrated in the form of three hemodynamic indexes HI. Fast Fourier transform (FFT) was used for spectral decomposition of the signal to frequency components associated with hemodynamic sourсes of different shear velocity of laminae. Low-frequency (1-300 Hz) index (HI1) was determined by slow interlaminar coupling, high-frequency (3000-24000 Hz) region (HI3) characterized fast interlaminar shear processes. HI2 takes intermediate position (precapillary and capillary blood flow). For assessment of redistribution tendency of the blood flow between fast and slow processes, HI1/HI3 ratio was introduced.

Variability of cardiointervals isolated from pulse component was assessed by pulsometry method (Heart Rate Variability, HRV). The following parameters were used: SDNN – Standard Deviation of NN Intervals – standard deviation of all RR intervals (reflects all long-term components and circadian rhythms responsible for variability); LF – power in the low frequency range (0.04-0.15 Hz) defined by the activity of sympathetic division and characterizing delay in baroreflex realization; HF – power in the high frequency range (0.16-0.5 Hz) associated with respiratory movements and mostly provided by vagal activity; LF/HF – ratio of powers indicating the general sympathovagal balance; CVI – Cardiac Vagal Index, non-linear parasympathetic index; CSI – Cardiac Sympathetic Index, non-linear sympathetic index.

Statistical analysis and visualization were implemented in R language (http://cran.r -project.org), 3.4.4 version. Reliability of pair differences of all parameters between stages (T1, T2, T3) was assessed by Wilcoxon test. Hommel correction was used for multiple comparison. Decision on statistical significance of hypotheses was taken at the level of p<0.05. Quantitative presentation of parameters in the tables was implemented in M±SD format (mean value + standard deviation).

Results and Discussion

During the test all participants exhibited a significant increase in pulse, and its complete recovery to the initial values (T3) (Fi-gure 1).

Hemodynamic indexes also exhibited significant changes in response to stress stimulation (Table 1). In the second period (T2) there was a noticeable increase in HI1 index (associated with slow shear velocities and near-wall processes in vessels). In the third period (T3) the index returned to the initial values (Figure 2). We think that increase in HI1 may be attributed to both activation of near-wall processes and dilatation of vessels (increase in the diameter of vessel reduces shear velocity).

From this a significant increase in HI1/HI3 ratio follows characterizing the balance of distribution of interlaminar velocities. In stage T3 a tendency emerged for this index to return to the initial values, but this process lacks statistical confirmation.

Simultaneously, increase in parameters of the total variability was observed (Table 2) characterizing the general tone of the autonomic nervous system. After the test both the high-frequency component HF associated with breathing and provided by the vagal activity, and low-frequency component LF characterizing sympathetic activity and reflecting delay in the baroreflex, considerably increased.

 

Fig. 1. Dynamics of heart rate

Note: additional lines connecting pairs of values are introduces

 

Table 1 Parameters of Microcirculation Hemodynamics in Response to Stress Stimulation  in Somatically Healthy Young Individuals

Parameter	T1	T2	T3	p1	p2	p3
HR, beat/minute	78.7±11.7	90.3±11.2	76.9±11.9	<0.0001	0.013	<0.0001
HI1	158.0±26.4	172.0±25.4	163.0±22.5	0.007	0.070	0.015
HI2	460±166	480±154	460±153	0.61	0.98	0.68
HI3	255±109	246±103	243±98.7	0.64	0.79	0.79
HI1/HI3	0.676±0.270	0.773±0.264	0.752±0.322	0.011	0.096	0.67

Note: Hemodynamic indexes are dimensionless values. HR – heart rate. Statistical significance of comparison of groups by paired Wilcoxon test: p1 – T1 and T2, p2 – T1 and T3, p3 – T2 and T3

 

Fig. 2. Dynamics of HI1 hemodynamic index

Note: additional lines connecting pairs of values are introduces

 

It is known that activation of parasympathetic nervous system in stress reaction is a mechanism of protection against side effects. In our research no significant change in the balance of frequency distribution (LF/HF) was observed. Most significant growth was observed in the non-linear parasympathetic index CVI (Figure 3, Table 2) while non-linear sympathetic index (CSI) remained unchanged (Table 2).

Thus, on the one hand, the results of research once again confirm the role of Stroop effect in modulation of stress condition described earlier and manifested in our work by increase in the heart rate with return to the initial values after cancellation of stimulus.

 

Table 2 Changes of Parameters of Heart Rhythm Variability  and of Condition of Autonomic Nervous System

Parameter	T1	T2	T3	p1	p2	p3
SDNN, msec	68.8±22.5	87.2±26.4	71.5±24.2	0.003	0.45	0.018
LF, msec	1090 ± 628	1390 ± 681	1080±630	0.028	0.94	0.070
HF, msec	732±458	1130±713	740±460	0.021	0.93	0.045
LF/HF	1.62±0.89	1.54±0.77	1.49±0.76	0.96	0.96	0.96
CSI	1.73±0.46	1.79±0.53	1.75±0.53	0.84	0.84	0.84
CVI	4.76±0.31	4.96±0.31	4.8±0.30	0.008	0.47	0.039

Note: statistical significance of comparison of groups by paired Wilcoxon test: p1 – T1 and T2, p2 – T1 and T3, p3 – T2 and T3

 

Fig. 3. Dynamics of non-linear parasympathetic index CVI

Note: additional lines connecting pairs of values are introduces

 

On the other hand, parameters of the interlaminar flow dynamics obtained by method of laser speckle-interferometry, demonstrated a reliable reaction to the stimulated stress in the slow HI1 (near-wall) component, and incomplete recovery in the early period after cancellation of the stimulus. Autonomic regulation of hemodynamics was manifested by increase in the activity of the parasympathetic influence.

Unique character of the research consists in complex assessment of the reaction to stress both in terms of distribution of the interlaminar hemodynamic processes in the microcirculation using non-invasive method of laser speckles, and in terms of the autonomic regulation by analysis of heart rate variability isolated from the pulse component of speckle-signal.

Conclusion

The conducted research permitted to obtain a multifactor picture of changes in the microcirculation parameters and of the autonomic regulation of the heart rhythm specific to adaptive reactions to induced stress.

Hemodynamics is characterized by increase in the cross section (diameter of vessels) of the microcirculatory bed, and, probably, by activation of parietal adhesion processes. Autonomic nervous regulation is characterized by preservation of the balance with simultaneous activation of sympathetic and parasympathetic divisions.

Quantitative criteria of the obtained shifts may be integrated to stress indexes and used in clinical practice. A portable mDLS sensor may be supplemented with specific assessment criteria and used for monitoring of adaptive reactions induced by stressful situations, and for taking early diagnostic and prognostic decisions in the clinical practice, and for self-control of a patient.

About the authors

Yuri N. Smolyakov

Chita State Medical Academy

Author for correspondence.
Email: smolyakov@rambler.ru
ORCID iD: 0000-0001-7920-7642
SPIN-code: 7440-6632
ResearcherId: R-5740-2017

PhD, Head of the Department of Medical Physics and Informatics

Russian Federation, Gorkogo str. 39a, 672000, Chita

Boris I. Kuznik

Chita State Medical Academy

Email: bi_kuznik@mail.ru
ORCID iD: 0000-0002-2502-9411
SPIN-code: 5807-7229
ResearcherId: D-2743-2018

MD, Professor, Honored Scientist of the Russian Federation, Professor of the Department of Normal Physiology

Russian Federation, Gorkogo str. 39a, 672000, Chita

Svetlana A. Kalashnikova

Chita State Medical Academy

Email: sak-2020@yandex.ru
ORCID iD: 0000-0001-8360-4624
SPIN-code: 4030-5496

Senior Lecturer, Department of Medical Physics and Informatics

Russian Federation, Gorkogo str. 39a, 672000, Chita

Nikolay A. Nolfin

Chita State Medical Academy

Email: nol.nikol@mail.ru
ORCID iD: 0000-0003-2570-4293
SPIN-code: 5376-8731

4th year student

Russian Federation, Gorkogo str. 39a, 672000, Chita

Ekaterina V. Fedorenko

Chita State Medical Academy

Email: fedorenko@mail.ru
ORCID iD: 0000-0003-0600-7708
SPIN-code: 4711-2143

4th year student

Russian Federation, Gorkogo str. 39a, 672000, Chita, Russia

Mankhar Mikhailovich Mikhahanov

Chita State Medical Academy

Email: mikhahanov@mail.ru
ORCID iD: 0000-0002-0620-2047
SPIN-code: 6393-8086

4th year student

Russian Federation, Gorkogo str. 39a, 672000, Chita, Russia

References

Supplementary files