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Features of Hemodynamics of Pulmonary Circulation During the Diving Reflex

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Features of Hemodynamics of Pulmonary Circulation During the Diving Reflex FULL COMMUNICATIONS PHYSIOLOGY Features of hemodynamics of pulmonary circulation during the diving reflex Ekaterina Podyacheva1, Tatyana Zemlyanukhina1, Lavrentij Shadrin2, and Tatyana Baranova1 1Department of General Physiology, Faculty of Biology, Saint Petersburg State University, Universitetskaya nab., 7–9, Saint Petersburg, 199034, Russian Federation 2Department of Physical Culture and Sports, Saint Petersburg State University, Universitetskaya nab., 7–9, Saint Petersburg, 199034, Russian Federation Address correspondence and requests for materials to Ekaterina Podyacheva, [email protected] Abstract The adaptive cardiovascular reactions of the human diving reflex were studied. The diving reflex was activated by submerging a face in cold water under labo- ratory conditions. Forty volunteers (aged 18–24) were examined. ECG, arterial blood pressure (ABP) and central blood flow were recorded by the impedance rheography method in resting state, during diving simulation (DS) and after apnea. During DS there is a statistically significant decrease in the dicrotic in- dex (DCI), which reflects a decrease in the resistive vessel tone and as well as diastolic index (DSI), characterizing lung perfusion. A comparison of the latent periods (LP) of an increase in ABP and a drop in DCI showed that a decrease in pulmonary vascular tone develops faster than ABP begins to increase. The LP for lowering DCI is from 0.6 to 10 s; for an increase in ABP — from 6 to 30 s. A short LP for DCI and the absence of a correlation between a decrease in ABP and DCI suggests that a decrease in pulmonary vascular tone during DS occurs reflexively and independently of a change in ABP. Keywords: diving reflex, systemic circulation, pulmonary circulation, impedan- ce rheography, plethysmography. Citation: Podyacheva, E., Zemlyanukhina, T., Shadrin, L., and Baranova, T. 2020. Features Introduction of hemodynamics of pulmonary circulation during the diving reflex. Bio. Comm. 65(3): 244–251. https://doi.org/10.21638/ Resistance to extreme environmental factors is determined by the adaptive po- spbu03.2020.304 tential of the body, its protective mechanisms. One of these mechanisms is the Authors’ information: Ekaterina Podyacheva, Master of Sci. in Biology, diving reflex inherent in humans and animals (Ilardo, 2018). The diving reflex is Student, orcid.org/0000-0002-0365-3301; an interconnected set of respiratory and cardiovascular signaling reflexes aimed Tatyana Zemlyanukhina, Master of Sci. in Biology, Student, orcid.org/0000-0003- at economizing oxygen consumption while diving (Campbell et al, 1969; Ponga- 2651-8521; Lavrentij Shadrin, PhD, Head of Laboratory, orcid.org/0000-0003-0199-4417; nis, 2011). Tatyana Baranova, Dr. of Sci. in Biology, In both animals and humans, when the head is immersed in water, breathing Researcher, orcid.org/0000-0003-0524-2933 reflexively stops, heart rhythm decelerates, and constriction occurs in the periph- Manuscript Editor: Michael Firsov, Sechenov Institute of Evolutionary eral vessels of the skin, muscles, and the gastrointestinal tract (Ramirez et al., Physiology and Biochemistry, Russian 2007). Blood is redistributed to those organs which are most vulnerable to hy- Academy of Sciences, Saint Petersburg, Russia poxia (the brain, heart and lungs) (Andersen, 1966; Galantsev, 1977, 1982, 1986; Received: December 9, 2019; Elsner et al., 1964; Elsner, 1970; Thompson et al., 1993; Butler et al., 2007). The Revised: June 5, 2020; peculiarities of the realization of this reflex in animals are determined by species, Accepted: June 25, 2020. and in humans are determined by features of vegetative regulation and psycho- Copyright: © 2020 Podyacheva et al. physiological status (Galantsev, 1995; Baranova, 2004). This is an open-access article distributed under the terms of the License Agreement The phenomenon of the diving reflex has been described quite well, but the with Saint Petersburg State University, which permits to the authors unrestricted mechanisms of the diving reflex are complicated and still far from full under- distribution, and self-archiving free of standing. For example, there are conflicting data about blood flow in pulmonary charge. circulation during diving (or diving simulation). According to some researchers, No funding information provided. Funding: blood flow decreases in the lungs and oxygen extraction decreases from the lungs Competing interests: The authors have declared that no competing interests exist. (Anderssen et al., 1998). At first glance, this seems reasonable, since hypoxia, hy- BIOLOGICAL COMMUNICATIONS, vol. 65, issue 3, July–September, 2020 | https://doi.org/10.21638/spbu03.2020.304 245 percapnia and a decrease in pH provoke constriction of from the test (financial rewards, educational require- the pulmonary vessels (Dawson, 1984). Data from other ments or credits). Information about the general results researchers, in contrast, indicate dilatation of the pul- of the research or personal data was provided to inter- monary vessels when diving. The authors explain this ested individuals. At the time of the experiment, none by the fact that filling the lungs with blood prevents the of the volunteers had arteriosclerosis or diabetes or were compression of the alveoli (Linér et al., 2008), but they taking any drugs. The study was approved by the Saint are convinced that the cause of this effect is the baromet- Petersburg State University Ethics Review Committee ric factor. Pulmonary capillary stress failure represents a for human studies (No. 40 from 07.03.2012), and all of continuum of conditions from a low-permeability, hy- the volunteers signed an informed agreement. drostatic type of pulmonary edema at slightly elevated Exposures and sampling procedures. The activation capillary pressures, to a high-permeability form of ede- of the diving reflex was performed using face submer- ma or even frank hemorrhage at high capillary pressures sion in cold water under laboratory conditions (diving (West et al., 1991, 1992). It is believed (Linér et al., 2008) simulation). It is well known that a 10° C gradient be- that the mechanism of these disorders is associated with tween the air temperature and the water temperature is an increase in intrathoracic blood volume and, conse- optimal for the manifestation of the diving reflex (Glo- quently, the increase of pulmonary capillary transmural tov et al., 2007), and in our experiments, the water tem- pressure. With the usual holding of breath without im- perature was 13.2 ± 0.4 °С and the air temperature was mersion in water during inspiration, the intrathoracic 22.6 ± 0.3 °С. The procedure was performed on subjects pressure is increased relative to ambient due to the elas- lying in a ventricumbent position on a couch with their tic inward recoil of the chest wall (Ferrigno et al., 1987). arms along their body (Fig. 1). During the experimen- The increased intrathoracic pressure hinders venous re- tal procedure, all of the subjects kept their hands at the turn, resulting in decreased pulmonary blood flow and heart line, did not change this position, and did not cardiac output, as well as decreased intrathoracic blood move their fingers with a finger sensor. Six face submer- volume, cardiovascular changes that would not bring sions on a normal exhale were performed in cold water. about pulmonary edema. In contrast, when a breath- The duration of the first submersion was limited by the hold diver descends to depth during a dive, the lung gas feeling of first discomfort. The duration of the remaining volume decreases due to increased ambient pressure, ac- submersions was performed on volitional breath-hold cording to Boyle’s law. When the lung gas volume de- until a maximum time. The pause between submersions creases, the intrathoracic pressure drops relative to am- was from 2 to 3 min. bient pressure. This depth-related drop in intrathoracic Electrocardiogram records were taken for the re- pressure results in increased venous return, pulmonary sting state, during diving simulation and after apnea. PHYSIOLOGY blood flow, and cardiac output, as well as increased in- During the whole experiment, heart rate was continu- trathoracic blood volume compared with breath holding ously recorded with the Poly-Spectrum-8/E Supermin- without immersion in water. These changes cause the iature 12-channel Digital ECG System (by Neurosoft). pulmonary capillary transmural pressure to increase, Arterial blood pressure was recorded with a sphygmo- leading to the development of pulmonary edema. manometer with the cuff on the right shoulder (B. Well The aim of this study was to study hemodynam- WA-33). Also, arterial blood pressure was measured us- ics (in particular, pulmonary blood flow) during diving ing the Finometer-pro (FMS, Holland) throughout the simulation by immersing the face in chilled water. Such diving simulation procedure. The minute volume of a model of diving simulation is usually used to study blood flow (MVBF, liter per min (l/min)) and the stroke this phenomenon in laboratory conditions (Scholander, volume (SV, ml) were determined for these states using 1962; Elsner et al., 1963; Irving, 1963; Gooden, 1994; the impedance rheography method (RGPA-6/12 “Re- Andersson et al., 1998, 2002, 2004). We suggest that dur- an-Poly,” Medicom-MTD, Russia). Blood supply to pe- ing diving simulation, the tone of the pulmonary vessels ripheral vessels was measured indirectly using the pulse can change under the influence of local reflex reactions, wave amplitude (PWA, per mille
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