abdominal and respiratory muscles, as well as stimula tion of the arterial baroreceptors due to the redistribu tion of blood, probably, affect the sensitivity of the res.
ISSN 03621197, Human Physiology, 2013, Vol. 39, No. 7, pp. 767–771. © Pleiades Publishing, Inc., 2013. Original Russian Text © Yu.A. Popova, A.V. Suvorov, A.I. D’yachenko, V.I. Kolesnikov, 2011, published in Aviakosmicheskaya i Ekologicheskaya Meditsina, 2011, Vol. 45, No. 6, pp. 26–31.
EXPERIMENTAL AND THEORETICAL STUDIES
Biomechanics and Regulation of External Respiration under Conditions of FiveDay Dry Immersion Yu. A. Popovaa, A. V. Suvorova, A. I. D’yachenkob, and V. I. Kolesnikova a
b
Institute of Biomedical Problems, Russian Academy of Sciences, Moscow, 123007 Russia Prokhorov Institute of General Physics, Russian Academy of Sciences, Moscow, 117942 Russia Received June 17, 2011
Abstract—The functional state of external respiration and the features of its regulation in healthy persons were studied under conditions of microgravity simulated using dry immersion. The lung volume, the ratio of thoracic and abdominal components during quiet breathing and performing various respiratory maneuvers, as well as the parameters that characterize the regulation of breathing (the duration of breath holding and the ability to voluntarily control respiratory movements), were recorded during the baseline period, on days 2 and 4 of dry immersion, and after the end of the dry immersion. It has been shown that the breathing pattern did not significantly change under conditions of dry immersion compared to the baseline period; however, the inspiratory reserve volume increased (p < 0.05), while the expiratory reserve volume decreased (p < 0.01). Dry immersion did not alter pulmonary ventilation, yet most of the subjects trended toward an increase in the contribution of the abdominal component of breathing movements during quiet breathing and demonstrated a statistically significant increase in this parameter during the lung vital capacity maneuver. The durations of the inspiratory and expiratory maximal breath holding under conditions of immersion did not differ from the background values. During the immersion, the accuracy of voluntary control of breathing increased. We believe that immersion, similar to microgravity, leads to changes in the reserve lung volume, which are partly because of changes in the body position; changes in relative contributions of the thoracic and abdominal components in the breathing movements; and changes in voluntary breath regulation. DOI: 10.1134/S0362119713070153
The respiratory biomechanics altered under condi tions of real and simulated microgravity, afferent impulses from proprioceptors of the lungs, chest, and abdominal and respiratory muscles, as well as stimula tion of the arterial baroreceptors due to the redistribu tion of blood, probably, affect the sensitivity of the res piratory center to chemosensory stimuli, the rhythm and structure of the respiratory cycle (breathing pat tern), and the ability to regulate voluntary and invol untary breathing. Earlier studies on the parameters of spirometry and respiratory metabolism under conditions of immer sion showed phase changes in these parameters during the adaptation of external respiration to experimental conditions [2, 3]. In the review [16], on the basis of Russian studies on the respiratory system under conditions of dry immersion, the possibility of only slight changes, mostly related to a decrease in respiratory volume, has been mentioned. In space flights (SFs) of different durations, an increase in the contribution of the abdominal respira tory component and a decrease in the thoracic com ponent have been recorded [13, 17, 20]. However, the contributions of these components to the respiratory reserve and the forced expiratory vol ume, as well as their coordination during spontaneous
breathing under conditions of simulated microgravity, including the immersion simulation, have not been studied. The regulation of respiration during simulated and natural microgravity has been poorly studied. Changes in the regulation of respiration observed during SFs [13, 18] and under antiorthostatic conditions [1, 4] are supposed to be associated with changes in chemical sensitivity. However, they can also be caused by a decrease in stimulation from the proprioceptors in the absence of gravity loads in natural microgravity and simulation studies. The goal of this study was to evaluate the state of external respiration and to study the features of biome chanics, as well as the regulation of respiration in healthy humans under conditions of microgravity simulated using dry immersion. EXPERIMENTAL The study of the functional state of external respi ration was performed in seven healthy men aged 20– 25 years who participated in an integrated experiment simulating the effects of microgravity by means of five day immersion.
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Characteristics of the breathing pattern during immersion (average ± standard deviation) Parameters PMV, L/min Tidal volume, mL Respiratory rate, cycles/min Duration of inhalation, s Duration of exhalation, s Duration of inhalation/Duration of exhalation
Background (sitting position)
Immersion, day 2
Immersion, day 4
Aftereffect (sitting position)
14.0 ± 3.6 1004 ± 345 15.6 ± 6.5 2.3 ± 1.6 2.6 ± 1.5 0.9 ± 0.1
12.2 ± 2.9 800 ± 355 17.1 ± 7.1 2.0 ± 1.3 2.1 ± 0.9 0.9 ± 0.2
13.4 ± 2.7 814 ± 224 17.9 ± 5.3 1.7 ± 0.6 2.0 ± 0.7 0.8 ± 0.1
17.1 ± 7.5 972 ± 276 19.0 ± 8.6 1.8 ± 1.1 2.3 ± 1.6 0.8 ± 0.1
The parameters of external respiration were recorded under normal conditions and during the fol lowing periods of immersion (the subject was in an immersion bath): one day before the start of experi mental exposure; on days 2 and 4 of immersion; and in the aftereffect period (7–8 h after the end of the expo sure). All subjects signed their informed consent to par ticipate in the experiment; a research program was approved by the Commission on Biomedical Ethics of the Institute of Biomedical Problems, Russian Acad emy of Sciences. The parameters of the system of external respira tion were recorded using a Dykhanie1 module (Bio phizpribor, Russia) [10]. The Dykhanie1 module includes a peak flow meter and thoracic and abdominal belts with builtin sensors to record changes of the perimeters of the chest (at the level of the middle of the sternum) and the lumbarabdominal area (at the level of the hypo chondrium). The calibration of the respiratory flow was performed using a 1L syringe included in the kit. In the prepilot (baseline) and aftereffect periods, the examinations of subjects were performed in the sitting position. In each examination, a subject performed a series of tests in consecutive order, while the following parameters were recorded: the volume and velocity characteristics of the respiratory flow, the contribu tions of thoracic and abdominal components to the respiratory movements, and the time characteristics of the respiratory cycle during quiet breathing and while performing the maneuver to determine the lung vital capacity (LVC). In addition, the durations of maximum expiratory and inspiratory voluntary breath holding and the abil ity of the subject to arbitrarily control respiratory movements (spirocinematography) were evaluated. The method of spirocinematography [9, 10] is based on reproducing respiratory movements with the volume and frequency of breathing set individually. Directly before carrying out this test, the spontaneous breathing of a subject was recorded with automatic recordings of the frequency and volume of respiration (according to the signals from the belts, which
checked the changes in the perimeters of the chest and lumbar–abdominal area). Thereafter, individual curves of the tidal stream were presented on the screen, as set by the program with randomized time intervals between inhalations. The values of the latent period (the period between the presentation of the signal and the start of the move ment) and the deviations of the amplitude of respira tory movements from those given by the program were analyzed during the spirocinematography. To charac terize the difference between the amplitudes, the dif ferences between individual amplitudes of each given and performed breathing movement were evaluated (in arbitrary units). Deviations of the amplitude from the given values that differed from the average value by a factor of two or more were excluded from further analysis. Thus, the set of tests used in this study allowed us to assess in an integrated way the state of external respi ration under experimental conditions, as well as to study under conditions of simulated microgravity fea tures of the regulation of external respiration and res piratory movements, such as the breathing pattern, the contribution and coordination of the thoracic and abdominal components of breathing movements, and the ability to voluntarily control respiratory move ments. Statistical processing of the data was performed using the Statistica 7.0 software for WinXP. The non parametric Friedman and Wilcoxon tests were used for the assessment of the statistical significance of differ ences. The critical level of significance was taken to be p = 0.05. RESULTS AND DISCUSSION Analysis of the parameters of quiet (spontaneous) breathing showed no statistically significant differ ences in the tidal volume (TV), respiratory rate (RR), minute tidal volume (mTV), or the timerelated char acteristics of the respiratory cycle, such as the duration of inspiration (Ti), the duration of expiration (Te) and their ratio (table). HUMAN PHYSIOLOGY
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Thus, generally, the breathing pattern did not change under conditions of immersion compared to the baseline values recorded in the sitting position. The structure of LVC did not change under condi tions of immersion, while the backup tidal volume increased by an average of 36%: 2358 ± 508 mL in the background period; 3201 ± 836 mL and 3096 ± 716 mL on days 2 and 4 of immersion, respectively (Fig. 1). The expiratory reserve volume decreased by a fac tor of about two during the immersion: 1888 ± 647 mL in the sitting position in the prepilot period; 3201 ± 836 mL on day 2 of immersion and 906 ± 321 mL on day 4 of immersion (Fig. 1). The detected changes are statistically significant: p < 0.01 and p < 0.05 when analyzing inspiratory reserve volume and expiratory reserve volume, respectively. Earlier, during SFs and experiments simulating microgravity, a decrease in LVC and similar changes in reserve volumes were recorded. According to several studies, in microgravity, the breathing pattern (the frequency and depth of breath ing at rest) was characterized by a decrease in fre quency and an increase in the depth of breathing [2]. With regard to possible changes in these parameters due to immersion, some authors noted their staging nature: in the period of adaptation, in the first few days of immersion, some researchers observed an increase in the mTV and RR and excessive lung ventilation [2], whereas other authors, on the contrary, recorded a decrease in RR and TV. The authors attributed this to muscular discomfort, such as painful sensations in the spine that block deep and rapid breathing [3]. Nevertheless, both groups of authors note a decrease in the LVC during immersion compared to the horizontal position of the body. It is well known that in the LVC in the supine posi tion is 4.9% less than LVS in the sitting position [11]. A decrease in LVC by 6% during the immersion com pared to the LVC in the sitting position was found in [12]; in addition, decreases in inspiratory and expira tory LVCs by 5.4 and 7%, respectively, were recorded during 1 h of water immersion [6]. In this instance, the intragroup standard deviation of LVC was about 15%; thus, a possible decrease in the LVC due to experimental effects might not be evident. The average increase in the inspiratory RV during the immersion compared to the sitting position recorded in our study is 31–35% (Fig. 1). An increase (by 14.6%) in the inspiratory RV in the supine position of the subject compared to the sitting position was recorded in [11]. Thus, probably, the contribution of additional water pressure to the increase in the inspiratory RV also plays an important role. The expiratory RV in the supine position has been recorded [11] to be 68.6% less than expiratory RV in the sitting position. In this study, expiratory RV HUMAN PHYSIOLOGY
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LVC, mL
7000 6000 5000 4000 3000 2000 1000 0 Background
Day 2
Day 4
Aftereffect
RVin, mL
5000 4000
*
*
3000 2000 1000 0 Background
Day 2
Day 4
Aftereffect
RVex, mL
3000 2500 2000 1500 1000
**
**
Day 2
Day 4
500 0 Background
Aftereffect
Fig. 1. The parameters of lung vital capacity during seven days of dry immersion. * p < 0.05; ** p < 0.01.
decreased by 47–48% from the baseline values (in the sitting position). Taking these data into consideration, a decrease in the expiratory RV was, to a greater extent, due to the changes in body position when immersing into the water bath. Experimental studies showed that immediately after the transition to water immersion, expiratory RV decreased by 47% [6]. A decrease in expiratory RV with increasing inspiratory RV was observed in studies on 3h immersion in the supine position [2]. However, under conditions of water immersion, changes in the lung volumes were still more pro nounced than that during the transition from the standing position to the supine [2]. An increase in the inspiratory RV and a decrease in the expiratory RV in the supine position compared to the sitting position are due to the displacement of the diaphragm in the cranial direction as a result of the effect of gravity on the organs of the abdominal and thoracic cavities. The mechanism of additional
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POPOVA et al. (a) During quiet breathing (individual parameters) 70 60 50 40 30 20 10 0 Background Day 2
Day 4
Aftereffect
(b) During the lung vital capacity maneuver (M ± SD) 60 50 *
40
*
30 20 10 0 Background
Day 2
Day 4
Aftereffect
Fig. 2. The contribution of the abdominal component to breathing movements, %. * p < 0.05.
changes in RVs during the immersion consists of the subsequent displacement of the diaphragm as a result of the water pressure on the chest and abdominal wall [2, 12]. Note that the study in the aftereffect period, 7–8 h after immersion, showed that, after the end of immer sion, these values did not differ from the baseline, con firming the fact that the changes in these parameters recorded during the immersion reflected the effects of mechanical factors and posture. Studying the thoracic and abdominal components of breathing movements appeared to be a novel method of research on respiratory biomechanics dur ing immersion. It is well known that changes in the lung volume with the contraction of different respiratory muscles can be very accurately expressed as the sum of volumes of the thoracic and abdominal components of the res piratory system. This approach is based on the concept of the respi ratory system as a linear system with two degrees of freedom [5]. A significant increase in the contribution of the abdominal component to breathing movements was recorded during short periods of microgravity (parabolic flight), as well as in 180day manned SFs [13, 17, 20].
In this experiment, significant withingroup vari ability in the contribution of the abdominal compo nent, especially during quiet breathing, was observed. Taking this into consideration, individual data on the subjects obtained during the experiment are shown in Fig. 2a. Nevertheless, a trend toward an increase in the abdominal contribution during the immersion was observed in five subjects. During the LVC maneuver, a statistically significant increase in the contribution of the abdominal component was recorded on days 2 and 4 of immersion compared to the measurements in a sitting position during the background and aftereffect periods (Fig. 2b). Apparently, an increase in the amplitude of the movements of the diaphragm and other muscles involved in breathing during this maneuver was accompanied by a more pronounced manifestation of this effect. Increased blood circula tion in the chest cavity and an increase in the flexibility of the abdominal wall under the conditions of immer sion probably led to a more active participation of the abdominal component in the breathing movements. An increase in the contribution of the abdominal component during the immersion, as well as in natural microgravity, is probably due to the increased flexibil ity of the abdominal wall [17] and discoordination in the regulation of muscle activity, which is maintained even on the first day after landing [20]. Since the abdominal muscles are involved in maintaining pos ture [15], their activity may be changed under experi mental conditions, which also leads to increased dis tensibility of the abdominal wall. It has been proven that immersion primarily trig gers changes in the tone of the muscles involved in maintaining posture [8]. Since, in sixmonth SFs [13] and headdown tilted bed rest [1], increases in the durations of inspiratory and expiratory voluntary breath holdings were recorded, these parameters were examined in our study. However, no statistically significant changes in the durations of inspiratory and expiratory voluntary breath holdings were recorded compared to those measured when the subjects were in the sitting posi tion. Analysis of the parameters of voluntary breathing movements showed that the ability of the subjects to voluntarily manageme breathing movements improved under conditions of immersion. When the depth of respiration was set at a level of one tidal volume, a statistically significantly decrease in the latency period from the signal to the start of the movement (Fig. 3) was recorded, while during the aftereffect period this parameter is not different from its baseline values. The difference between the performed and given amplitudes of breathing movements during the immer sion was less pronounced than in the prepilot period: the baseline, 3.98 arb. units; on day 2, 2.67 arb. units; on HUMAN PHYSIOLOGY
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6.
1.0 0.8 0.6
*
0.4
7.
*
0.2 0 Background Day 2
Day 4 Aftereffect
Fig. 3. The expiratory latent period when performing the movements given. * p < 0.05.
day 4, 2.6 arb. units (average values). In our case, the improvement of the performance of a given respiratory pattern can not be attributed to the training effect, because in the early aftereffect period, spirocinemato graphic parameters did not differ from their baseline values. We suggest that a decrease in the latency period, as well as more precise performance of the amplitude of breathing movements during immersion, is due to the greater flexibility of the abdominal wall under conditions of immersion, which was manifested in the greater extent of the participation of the abdom inal wall in breathing movements. Thus, staying in dry immersion leads to changes characteristic of immersion and microgravity in the lung reserve volume (compared to the sitting posi tion), an increase in the contribution of the abdominal component to breathing movements, and an increase in the accuracy of voluntary control over breathing.
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