Relationships between Parameters of the Cardiovascular System, Salivary Lactoferrin Level and Body Temperature during a Short-Term Human Whole-Body Exposure to Cold Air

Liliya V. Poskotinova, Elena V. Krivonogova, Olga V. Krivonogova, Denis B. Demin, Irina N. Gorenko, Elena V. Tipisova, Victoria A. Popkova, Alexandra E. Elfimova

International Journal of Biomedicine. 2019;9(2):111-116.
DOI: 10.21103/Article9(2)_OA5
Originally published June 15, 2019  


Background: The problem of maintaining body temperature in people working outdoors in the cold air of the Arctic remains relevant. The purpose of this study was to determine the autonomic nervous mechanisms of regulation of heart rate (HR), blood pressure (BP) and local immunity on the example of the dynamics of salivary lactoferrin during a decrease in body temperature in humans (the core and the skin of hands) during and after a short-term, whole-body exposure to cold air.
Materials and Methods: A total of 15 healthy Russian male volunteers aged between18 and 20 years, born and living in Arkhangelsk, were examined in the winter. Research stages: the registration of indicators before exposure to the cold air  (Stage 1), during the 10-minute exposure to the cold air at -20°C (Stage 2) and after the 10-minute exposure to the cold air (Stage 3). The registration of indicators in Stages 1 and 3 was carried out indoors at an air temperature of +20 °C. HR (bpm), the heart rate variability (HRV) parameters, systolic and diastolic blood pressure (BPsyst, BPdiast, mmHg), salivary lactoferrin level (ng/ml) by ELISA and the body temperature in the ear canal (Tear, °C) and on the skin of the dorsum of the right hand (Tskin, °C) were determined at each stage of the study.
 Results: In Stage 2 with significantly decreased Tear and Tskin, compared to the initial indicators in Stage 1, there was a significant increase in HRV indices reflecting the overall HRV and vagal effects on the heart rhythm. At the same time, HR was significantly decreased, as well as SI. An increase in the total power (TP) of the HRV spectrum was revealed due to a predominant increase in HF  and VLF, and to a lesser degree in LF. Both BPsyst and BPdiast significantly increased. After cooling in Stage 3, HR increased, but remained significantly lower than the initial values. The overall HRV according to SDNN and TP decreased, reaching baseline values. Concentrations of salivary lactoferrin during cooling in Stage 2 tended to increase, which was also maintained in Step 3 after cooling.
Correlation analysis in the entire sample (n=15) revealed a positive correlation between SDNN and Tear in Stage 2 (rs=0.56, p=0.035). In Stage 2, the change in Tskin was significantly correlated with the salivary lactoferrin level (rs=-0.73, p=0.003); this relationship was also found in Stage 3(rs=-0.65, p=0.015).
 Conclusion: The successful return of body temperature after general cooling occurs under the condition of increasing the overall HRV, enhancing vagal influences on the heart rhythm, HF and VLF components of HRV during cooling. An increase in the level of salivary lactoferrin, while maintaining vagal reserves of the vegetative regulation of heart rhythm against a decrease in skin temperature during general cooling, as well as a decrease in the level of lactoferrin against the background of recovery of body temperature after cooling, at least 10 minutes, can be regarded as an adaptive response of the body to exposure to cold temperature with minimal risk of cold inflammation.

heart rate variability • heart rate • blood pressure • salivary lactoferrin • exposure to cold air
  1. Le Blanc J, Dulac S, Cote J, Girard B. Autonomic nervous system and adaptation to cold in man. J ApplPhysiol. 1975;39(2):181-6. doi:10.1152/jappl.1975.39.2.181
  2. Demin DB, Poskotinova LV, Krivonogova EV. [Variants of neurophysiological reactions during short-term experimental hypothermia in humans]. J Biomedical Radioelectronics. 2018;12:48-50. doi: 10.18127/j15604136-201812-06. [Article in Russian].
  3. Mäkinen TM, Mäntysaari M, Pääkkönen T, Jokelainen J, Palinkas LA, Hassi J, Leppäluoto J, Tahvanainen K, Rintamäki H. Autonomic nervous function during whole-body cold exposure before and after cold acclimation. Aviat Space Environ Med. 2008 Sep;79(9):875-82.
  4. Peng RC, Yan WR, Zhou XL, Zhang NL, Lin WH, Zhang YT. Time-frequency analysis of heart rate variability during the cold pressor test using a time-varying autoregressive model. Physiol Meas. 2015 Mar;36(3):441-52. doi: 10.1088/0967-3334/36/3/441.
  5. Patrakeeva VP, Basova EE. Effects of Low Temperatures on the Formation of Adaptive Reactions: a review. International Journal of Biomedicine. 2018;8(2):95-101.   doi: 10.21103/Article8(2)_RA1
  6. Hintsala HE, Kiviniemi AM, Tulppo MP, Helakari H, Rintamämaki H, Mäntysaari M, et al. Hypertension Does Not Alter the Increase in Cardiac Baroreflex Sensitivity Caused by Moderate Cold Exposure. Front Physiol. 2016;7:204. doi: 10.3389/fphys.2016.00204
  7. Kuznetsov IA, Potiyevskaya VI, Kachanov IV, Kuraleva OO. [Laktoferrin's role in biological circles of the person. Modern problems of sciences and education]. 2017:3 [Electronic source] [Article in Russian].
  8. Aleshina GM, Yankelevich IA, Zhakharova ET, Kokryakov VN. [Stress-protective effect of human lactoferrin]. Ross Fiziol Zh Im I M Sechenova. 2016;102(7):846-51. [Article in Russian]
  9. Bosch JA, de Geus EJ, Veerman EC, Hoogstratan J, Nieuw Amerongen AV. Innate secretory immunity in response to laboratory stressors that evoke distinct patterns of cardiac autonomic activity. Psychosom Med. 2003;65(2):245-58.
  10. Thompson RS, Roller R, Mika A, Greenwood BN, Knight R, Chichlowski M, et al. Dietary Prebiotics and Bioactive Milk Fractions Improve NREM Sleep, Enhance REM Sleep Rebound and Attenuate the Stress-Induced Decrease in Diurnal Temperature and Gut Microbial Alpha Diversity. Front Behav Neurosci. 2017;10:240. doi: 10.3389/fnbeh.2016.00240.
  11. Li CY, Hsu GS, Suzuki K, Ko MH, Fang SH. Salivary Immuno Factors, Cortisol and Testosterone Responses in Athletes of a Competitive 5,000 m Race. Chin J Physiol. 2015; 58(4):263-9. doi: 10.4077/CJP.2015.BAE367
  12. He CS, Tsai ML, Ko MH, Chang CK, Fang SH. Relationships among salivary immunoglobulin A, lactoferrin and cortisol in basketball players during a basketball season. Eur J Appl Physiol. 2010;110(5):989-95. doi: 10.1007/s00421-010-1574-8.
  13. Svendsen IS, Hem E, Gleeson M. Effect of acute exercise and hypoxia on markers of systemic and mucosal immunity. Eur J Appl Physiol. 2016;116(6):1219-29. doi: 10.1007/s00421-016-3380-4
  14. Malik M, Bigger J, Camm A, Kleiger R, Malliani A, Moss AJ, Schwartz PJ. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology: Heart rate variability. Standards of measurement, physiological interpretation, and clinical use. Eur Heart J. 1996;17:354–381. doi: 10.1093/oxfordjournals.eurheartj.a014868.
  15. Shaffer F, Ginsberg JP. An Overview of Heart Rate Variability Metrics and Norms. Front Public Health. 2017;5:258. doi: 10.3389/fpubh.2017.00258
  16. Millis RM, Austin RE, Hatcher MD, Bond V, Goring KL. Metabolic energy correlates of heart rate variability spectral power associated with a 900-calorie challenge. J Nutr Metab. 2011;2011:715361. doi: 10.1155/2011/715361.
  17. Kazimierska A, Placek MM, Uryga A, Wachel P, Burzyґnska M, Kasprowicz M. Assessment of Baroreflex Sensitivity Using Time-Frequency Analysis during Postural Change and Hypercapnia. Comput Math Methods Med. 2019:4875231
  18. Hodges GJ, Ferguson SAH, Cheung SS. Cardiac autonomic function during hypothermia and its measurement repeatability. Appl Physiol Nutr Metab. 2019;44(1):31-36. doi: 10.1139/apnm-2018-0248
  19.  Wang JJ, Chen CC. Study of the effect of short-time cold stress on heart rate variability. In: Lim CT, Goh JC (eds) 13th International Conference on Biomedical Engineering. IFMBE Proceedings. 2009: 23: 490-492.
  20. Shinjo T, Sakuraba K, Nakaniida A, Ishibashi T, Kobayashi M, Aono Y, Suzuki Y. Oral lactoferrin influences psychological stress in humans: A single-dose administration crossover study. Biomed Rep. 2018;8(5):426-432. doi: 10.3892/br.2018.1076.

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Received April 28, 2019.
Accepted May 28, 2019.
©2019 International Medical Research and Development Corporation.