以俄罗斯东北部与北高加索地区为例，探讨神经植物性调节的区域特性

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BACKGROUND

Today, analysis of heart rate variability (HRV) is one of the most popular methods worldwide for studying and evaluating heart function, the functional performance of the body as a whole and the condition of various parts of the autonomic nervous system (ANS) [1]. HRV, which is a change in the time intervals between consecutive heart beats [2], is widely known as an effective tool for assessing the autonomic regulation of the heart [3, 4]. The conventional interpretation of HRV includes an analysis of the parasympathetic and sympathetic activity of the ANS, their balance, and relationship and analysis of some other related parameters [5]. HRV can be used as a health index and a measure of the integration of the ANS and the central nervous system [6, 7]. The neurovisceral integration model suggests that higher control levels of vagal cardiac activity are associated with more effective self-regulation of the body in general, including better health [8]. Various HRV parameters are used for in-depth description of the sympathetic-parasympathetic interaction of the ANS in the cardiovascular regulation and control. The level of regulation can be used to characterize the functional abilities of the cardiovascular system and the adaptation abilities of the body. HRV is a highly sensitive indicator of the dynamic change in the autonomic balance in response to exogenous influences, including climatic and geographical factors [9].

In characterizing the climatic and geographical differences of the studied regions, it is worth noting that Magadan (59°34´ N, 150°47´ E) is located in the temperate climate zone within the coastal climatic zone characterized by a combination of marine and monsoon influences. The climate of the northern part of the Northeast region, including most of the Magadan Region, is considered the harshest in the Russian Far East [10]. Average temperature reflects its obvious seasonality (−26.0 °C in January and + 13.4 °C in July).

Vladikavkaz (Republic of North Ossetia-Alania) is located in a temperate climate zone (43°02´ N, 44°39´ E) with orographic moderation due to the proximity of mountain ranges. The average temperature in January is − 1.9 °C and + 20.7 °C in July. In addition to climatic differences, it is worth noting that Vladikavkaz is located in the foothills zone of the Greater Caucasus, in the North Ossetian Trench framed by the offsets of the Sunzhensky and Terskiy Ridges. The terrain is characterized by deep differentiation with absolute marks from 600 to 1,000 m and average height of about 670 m above sea level, which corresponds to low-mountain relief, according to the contemporary geomorphological classification. Magadan is located in the coastal climate zone and characterized by low-lying relief with absolute heights not exceeding 100 m above sea level. Such hypsometric conditions create a specific complex of factors affecting the physiological adaptation of the human body.

AIM: To study regional differences and differences in the autonomic control of the circulatory system based on HRV in individuals living in different climate zones, such as the Northeast (Magadan) and the North Caucasus (Vladikavkaz), which differ in both climatic conditions and relief (lowland and low mountain).

METHODS

The study involved 89 young men, including 41 natives of the Northeast region (Magadan; mean age: 19.8 ± 0.5 years) and 48 natives of the North Caucasus (Vladikavkaz; mean age: 20.8±0.8 years). The study was conducted in the spring (April, May) of 2024.

Inclusion criteria: males in their young adulthood; no acute chronic diseases and health complaints, and a signed informed consent. All participants included in the sample had comparable living conditions (students) and physical activity (physical education classes as part of the educational institution’s curriculum) and permanently resided in the studied region.

All study participants underwent an analysis of HRV using the Varicard suite and VARICARD-KARDi and ISCIM-6 software. The subjects had the following HRV parameters recorded in the time and frequency domains: heart rate (HR, bpm); mode (Mo, ms); difference between maximum and minimum RR intervals, or variation range (MxDMn, ms); root mean square of successive differences (RMSSD, ms); standard deviations of all NN intervals (SDNN, ms); stress index (regulatory stress index; SI, relative units); total power (TP, ms²); total high-frequency (HF) HRV in the range of 0.4–0.15 Hz (respiratory waveforms; HF, ms²); low-frequency (LF) HRV in the range of 0.15–0.04 Hz (vascular waveforms; LF, ms²), very low-frequency (VLF) HRV in the range of 0.04–0.015 Hz (VLF, ms²). In addition, we analyzed the centralization index (IC, relative units [RU]) and the activity index of regulatory systems (IARS, RU) [11]. The subjects’ type of autonomic regulation was determined based on the variation range (MxDMn) and stress index (SI) at rest. Normotonic individuals included participants with MxDMn in the range of 200–300 ms and SI of 70–140 RUs; sympathotonic individuals included participants with MxDMn below the specified range and SI higher than 140 RUs; vagotonic individuals included participants with MxDMn above the specified range and SI less than 70 RUs [12].

The study was approved by the Ethics Committees of the Institute of Biomedical Research, a branch of the Federal State Budgetary Scientific Institution Vladikavkaz Scientific Center of the Russian Academy of Sciences (protocol No. 3 dated February 20, 2022), and the Federal State Budgetary Scientific Institution Arctic Research Center of the Far Eastern Branch of the Russian Academy of Sciences (Opinion No. 002/021 dated November 26, 2021).

Statistical data processing was performed by standard methods of mathematical statistics in the Statistica 7.0 software. To test the normality of the quantitative variables, we used the Shapiro–Wilk and Kolmogorov–Smirnov tests. The analyzed variables are presented as median (Me) and interquartile range [q25%; q75%]. The significance of differences in the analyzed variables was determined using the Mann–Whitney U test. The difference was considered significant at p=0.05; 0.01; 0.001.

RESULTS

The study involved a comprehensive analysis of autonomic cardiovascular regulation based on the HRV time and frequency domains in groups of young men from different regions, including northeast Russia (Magadan) and the North Caucasus (Vladikavkaz, Republic of North Ossetia-Alania). The distribution of types of autonomic heart rate regulation in young men living in different environment and climate with significant gradients of meteorological parameters and altitude above sea level is shown in Fig. 1. It is evident that among natives of the northeast, the share of vagotonic individuals is 59.0%, the share of normotonic individuals is 27.0%, and the share of sympathotonic individuals is 14.0%. On the contrary, the share of vagotonic individuals among natives of the North Caucasus is 20.8%, the share of normotonic individuals is 29.2%, and the share of sympathotonic individuals is 50.0%.

 

Fig. 1. Distribution of types of vegetative regulation HR in young men, living in different natural and climatic zones: the North-East (Magadan) and the North Caucasus (Vladikavkaz).

 

The basic HRV parameters and significance of differences between groups in the samples of young men living in different climate and geographic zones of the Russian Federation are shown in Table 1. The study shows that in 15 analyzed HRV parameters, we observed significant differences between groups in seven parameters as clearly shown in Fig. 2.

 

Table 1. Main indicators of heart rate variability and the level of significance of their differences in young men depending on the climatic and geographical conditions of residence

Parameters	Me (q25; q75)		р
	Magadan Region (n=41)	Republic of North Ossetia-Alania (n=48)
HR, beats/min	74.72 (65.21; 84.38)	85.20 (76.34; 93.48)	0.001
MxDMn, msec	255.00 (203.00; 366.00)	231.00 (182.00; 301.00)	0.114
RMSSD, msec	40.58 (29.73; 64.11)	34.17 (23.36; 49.69)	0.043
pNN50, %	13.58 (7.09; 35.63)	8.35 (2.63; 19.47)	0.020
SDNN, msec	49.20 (38.70; 70.92)	51.33 (41.12; 65.50)	0.955
Mo, msec	808.00 (707.00; 905.00)	688.00 (635.00; 747.00)	0.001
AMo50, msec	43.23 (26.02; 52.66)	49.57 (34.60; 58.95)	0.083
SI, arb. units	112.21 (38.77; 165.33)	139.70 (70.46; 232.35)	0.053
TP, msec2	2481.76 (1510.57; 4874.63)	2107.10 (987.70; 3075.40)	0.050
HF, msec2	730.25 (401.88; 1348.17)	526.47 (253.84; 844.77)	0.050
LF, msec2	1151.12 (729.14; 2112.35)	1007.59 (582.80; 1656.63)	0.202
VLF, msec2	411.46 (255.11; 926.64)	336.36 (149.52; 625.370	0.105
LF/HF, arb. units	1.68 (1.15; 2.61)	1.94 (1.19; 3.02)	0.429
IC, arb. units	2.44 (1.72; 3.50)	2.82 (1.61; 4.02)	0.524
PARS, arb. units	4.00 (3.00; 6.00)	5.00 (4.00; 7.00)	0.135

Note. HR is the heart rate; MxDMn is the difference between the maximum and minimum values of the cardiointervals, or the variation range; RMSSD is the square root of the sum of the differences in a consecutive series of cardiointervals; pNN50 is the number of pairs of cardiointervals with a difference of more than 50 ms, % of the total number of cardiointervals; SDNN is the standard deviation of the full array of cardiointervals; Mo is the mode; AMo is the amplitude of the mode; SI is the stress index (voltage index of regulatory systems); TP is the total power of the spectrum of time values of R-R heart rate intervals.; HF is the spectral power of the high–frequency component of heart rate variability in the range of 0.4–0.15 Hz (respiratory waves); LF is the spectral power of the low–frequency component of heart rate variability in the range of 0.15–0.04 Hz (vascular waves); VLF is the spectral power of the very low–frequency component of heart rate variability in the range of 0.04-0.015 Hz;. LF/HF is an indicator of sympathovagal balance; IC is an index of centralization, PARS is an indicator of the activity of regulatory systems; p is the level of statistical significance.

 

Fig. 2. Intergroup differences in heart rate variability in young men of the North Caucasus and North-Eastern regions of Russia. * Statistically significant intergroup differences are indicated. Blue color range — the value is higher for representatives of the north-eastern region, red color range — the value is higher for representatives of the North Caucasus.

 

It was found that the group of young men from the northeast Russia had significantly higher RMSSD (p=0.043), pNN50 (p=0.020), and Mo (p=0.001) backed by lower SI (p=0.053) and HR (p=0.001).

An analysis of the HRV frequency between the study groups showed that the total power (TP), reflecting the total activity of the body’s regulatory systems, was lower in the group of young men from the North Caucasus due to a lower HF HRV (p=0.050).

DISCUSSION

The intragroup analysis of the types of autonomic heart rate regulation shows the proportional distribution of individuals with different types of regulation. This analysis clearly demonstrates the intergroup differences, namely the predominant sympathotonic type of HRV in young male natives of the North Caucasus (Vladikavkaz), parasympathetic type of HRV in natives of the northeast Russia (Magadan), thereby reflecting the population levels of rhythm variability in the studied age and sex groups. Analysis of the obtained data showed significant differences between both groups in some key HRV parameters (HR, Mo, RMSSD, pNN50, SI, HF, and TP). The study reveals a predominant parasympathetic type of cardiac activity control in the northeastern population compared to residents of the North Caucasus Region. For example, participants from the Northeast region tended to have a greater heart rate variability (TP) with a higher median RMSSD and pNN50, which together indicate the predominance of parasympathetic type of the ANS regulation. It is known that at physiological rest, predominantly parasympathetic activity provides the optimum economization of the body’s functions and bioenergetic processes. An inverse relationship is observed with initial sympathicotonia: increased tone of the sympathetic ANS correlates with functional physiological stress and lower adaptation abilities, limiting the range of possible compensatory reactions when exposed to disturbing factors [13].

It has been shown that young natives of the Republic of North Ossetia-Alania have a significant predominance of HR, IC, SI, and IARS. The data reveal a pronounced vagal dominance in relation to the reduced sympathetic modulation observed with a relatively increased overall heart rate variability in young men from the northeast Russia. These differences may be interpreted as population specificity of the autonomic balance under chronic exposure to extreme climatic factors of the northern regions manifested in the activation of parasympathetic cardiac regulation. The findings are consistent with the data on the effect of low temperatures on HRV causing lower sympathetic activity and, consequently, a higher HRV [14]. They are also consistent with our previous studies showing that the identified parasympathetic activation of the ANS improves gas exchange in the context of cardiovascular stress in Northern conditions and may indicate increased cold resistance [15, 16].

The interpretation of IARS values indicates that young men in the Northeast region have moderate regulatory stress; whereas, the North Caucasus sample has a high regulatory stress caused by the active mobilization of the sympathetic (adrenal) system and the pituitary-adrenal system [17–19].

CONCLUSION

The study involved a comprehensive analysis of time and frequency domains of HRV in two groups of young men permanently residing in contrasting climate and geographic zones of the Russian Federation. The findings significantly expand the contemporary understanding of neurovegetative adaptations to various extreme environmental factors. The study demonstrates fundamentally different autonomic control patterns in response to combined mountain climatic factors, manifested by the persistent sympathicotonic dominant and lower parasympathetic activation in autonomic regulation. In the conditions of northeast Russia, the opposite adaptation manifested by a higher overall variability and parasympathetic activation in the autonomic circulatory regulation. The revealed autonomic differences in the vegetative cardiovascular regulation patterns based on climatic and geographic parameters demonstrate the specificity of the autonomic response.

Our data demonstrate the diagnostic value of HRV for monitoring physiological acclimatization and identifying individual characteristics of autonomic regulation in various environments. These observations support the hypothesis that climatic and geographic factors are important for the development of individual autonomic cardiovascular regulation system. The findings require further study to specify the interaction mechanisms of external factors and internal regulatory processes and development of methods to improve public health in various climate zones.

This study has some limitations as it involved young males, which does not allow a full description of the corresponding populations.

ADDITIONAL INFORMATION

Author сontributions: V.A. Belyayeva: study concept and design, data analysis, writing and editing the manuscript; I.V. Averyanova: study concept and design, preparation of the first version of the manuscript, literature analysis, approval of the final version of the manuscript. All authors approved the manuscript (the version for publication), and also agreed to be accountable for all aspects of the work, ensuring proper consideration and resolution of questions related to the accuracy and integrity of any part of it.

Ethics approval: The study was approved by the Ethical Committees of the Institute of Biomedical Research, a branch of the Federal State Budgetary Institution of Science, the Vladikavkaz Scientific Center of the Russian Academy of Sciences (Protocol No. 3 dated 02/20/2022) and the Federal State Budgetary Institution of Science, the Arctic Research Center of the Far Eastern Branch of the Russian Academy of Sciences (conclusion No. 002/021 dated 11/26/2021).

Consent for publication: All participants provided written informed consent prior to inclusion in the study.

Funding sources: The work has been fulfilled with Institute of Biomedical Investigations – the Affiliate of Vladikavkaz Scientific Center of the RAS, under the financial support of the Russian Federation budget within the framework of the project “Study of molecular-genetic mechanisms of stress, inflammatory and metabolic disorders in cardiovascular and bronchopulmonary pathology in the experiment and clinic in the dynamics of medical and environmental monitoring in the Republic of North Ossetia-Alania, development of technologies for prevention and correction (experimental and clinical study)” (registration number 125030603222-0). The work has been fulfilled with Arktika Scientific Research Center, Far East Branch of the Russian Academy of Sciences, under the financial support of the Russian Federation budget within the framework of the project “Study of intersystem and intrasystem mechanisms involved in developing functional and adaptive reserves of the northern type man at different stages of ontogenesis under discomfort and extreme conditions of residence with the determination of health integral informative indices” (registration number, АААА-А21-121010690002-2).

Disclosure of interests: The authors have no relationships, activities, or interests for the last three years related to for-profit or not-for-profit third parties whose interests may be affected by the content of the article.

Statement of originality: No previously published material (text, images, or data) was used in this work.

Data availability statement: The editorial policy regarding data sharing does not apply to this work, as no new data was collected or created.

Generative AI: No generative artificial intelligence technologies were used to prepare this article.

Provenance and peer review: This paper was submitted unsolicited and reviewed following the standard procedure. The peer review process involved two external reviewers, a member of the editorial board, and the in-house scientific editor.

作者简介

Victoria A. Belyayeva

Institute of Biomedical Investigations of Vladikavkaz Scientific Centre of the Russian Academy of Sciences, North Ossetia-Alania

编辑信件的主要联系方式.
Email: pursh@inbox.ru
ORCID iD: 0000-0002-8126-5275
SPIN 代码: 8202-1922

Cand. Sci. (Biology)

俄罗斯联邦, v. Mikhailovskoye, North Ossetia-Alania

Inessa V. Averyanova

Scientific Research Center «Arktika» Far Eastern Branch of the Russian Academy of Sciences

Email: inessa1382@mail.ru
ORCID iD: 0000-0002-4511-6782
SPIN 代码: 9402-0363

Dr. Sci. (Biology), Professor

俄罗斯联邦, Magadan

参考

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