The Effects of Breathing on Changes in Heart Position in Humans

¹Graduate School of Human-Environment Studies, Kyushu University
²Tottori College
³Kawasaki University of Medical Welfare

ABSTRACT
　Space is different from Earth because of the microgravity, radiation, and closed environment that affect astronauts during space missions.　In the initial phase of a space mission, astronauts experience space motion sickness due to fluid shift causing blood volume in the heart and brain to increase.　The change in the position of a visceral organ can be a trigger for stress.　It was reported that the breath holding stops changes of a heart position.　This indicated that the breathing affects the heart position.　The purpose of this study was to clarify changes in heart position during breathing while standing in water.　Seven healthy young males participated in this study.　We measured heart position, heart rate and blood pressure.　Each subject took a standing on land and at various water levels （i.e., knee, greater trochanter, navel, xiphisternum, and clavicle） for 5 min each.　The heart position changed significantly to the left at clavicle-level water （p < 0.05） compared to control.　During breath-holding, the heart position changed significantly posteriorly at the level of clavicle.　The heart position changed significantly to the right during inhalation on land （p < 0.05） compared to control.　During spontaneous breathing （inhalation）, the heart position changed significantly posteriorly at the water level of the xiphisternum.　The heart position changed significantly to the left at xiphisternum-level water （p < 0.05） and at clavicle-level water （p < 0.05） compared to control.　The heart position changed significantly to the right on land （p < 0.05） compared to control.　The heart position changed significantly to the left at greater trochanter level compared to control （p < 0.05）.　HR decreased significantly at xiphisternum-level water （p < 0.05）.　SBP decreased significantly at navel-level water （p < 0.05）.　The diaphragm moves downward during inhalation and rises during exhalation;it contributes to inhalation more than it does to exhalation.　We considered that the diaphragm could be connected to the pericardium in tandem and that these ligaments could cause a change in heart position while breathing.　Water immersion causes the rib cage to move upper anteriorly and the abdominal viscera to move superiorly, thereby stretching the diaphragm.　From this, we conclude that the water pressure causes the diaphragm to rise, pericardiacophrenic ligament to relax, and heart to shift to the left side.　We and believe that the heart rotated toward the left as venous return increases.　

（Received:23 October, 2021　Accepted:24 March, 2022）

Key words:Ultrasonic diagnostic equipment, Breathing, Standing, Heart position, Heart rate

I.　Introduction
　Space is different from Earth because of the microgravity, radiation, and closed environment that affect astronauts during space missions.　In the initial phase of a space mission^1,8,10,12）, astronauts experience space motion sickness due to fluid shift causing blood volume in the heart and brain to increase^18）.　This suggests that the change in the position of a visceral organ can be a trigger for stress.　
　It was reported that underwater immersion at the level of the xiphisternum─the lowest part of the sternum─closely simulates a microgravity environment¹⁶.　This makes underwater an ideal environment for EVA （Extravehicular Activity） training on Earth to be used in place of a microgravity environment^6）.
　In the heart, water pressure causes the venous return to increase, which increases central circulation^19）.　In addition, microgravity causes a fluid shift in the heart.　We, therefore, focused on heart position to investigate circulatory effects.　We determined that the heart position under clavicle-level water was significantly to the left compared with its position out of water^23）.　We considered that water pressure might cause the diaphragm to elevate in the water.　It was reported that the breath holding stops changes of a heart position^24）.　This indicated that the breathing affects the heart position.　The purpose of this study was to clarify changes in heart position during breathing while standing in water.

II.　Method
　Seven healthy young males with no history of heart disease （age:21.6±0.5 years, height:169.4±5.0 cm, weight:67.7±6.9 kg, % body fat:19.7±4.4%, mean±SD） volunteered to participate in this study.　The study parameters were as follows:room temperature at 24.0±0.8℃ and humidity at 81.8±4.3%.　All study protocols were approved by the ethics board at Kawasaki University of Medical Welfare and conformed to the Declaration of Helsinki （20-067）.
　We measured heart position using ultrasonic diagnostic equipment （SonoSite M-Turbo;FUJIFILM）.　The amount of change in the heart position was measured, with the mitral valve as the starting point.　The ultrasound examinations were performed with a sector probe P21x/5-1 （FUJIFILM）.　Sonic gel was used to improve probe-to-skin contact.　After mitral valve movement was observed, we drew a mark with a red marker and recorded the measurement position.　The mitral valves of all the subjects were measured at the same frequency.　We measured changes in heart position under the following conditions:breath holding, spontaneous respiration, and deep breathing.　Each subject took a standing posture on land and at various water levels （i.e., knee, greater trochanter, navel, xiphisternum, and clavicle） for 5 min each.　The change in heart position was measured, with the mitral valve during breath holding while standing on land as the starting point and as a control.　We measured HR using waterproof electrocardiography （FUKUDA DENSHI Co., Ltd., DS-2202, Japan） with chest bipolar induction after 5 min of rest.　We measured blood pressure after 5 min of rest using an aneroid sphygmomanometer （501;KENZMEDICO）.
　The data was analyzed using SPSS ver.23.0 for MAC using a one-way repeated measures ANOVA.　Subsequently, Dunnett’s post-hoc test was used to identify any interactions.　We set p < 0.05 as the threshold for statistical significance.　

III.　Results
　Figure 1 shows the change in heart position during breath holding at various water levels.　The heart position changed significantly by 13.5±13.8 mm to the left at clavicle-level water （p <0.05） compared to control.　During breath-holding, the heart position changed significantly posteriorly by 5.0±3.4 mm at the water level clavicular position （Figure 2）.　Figure 3 shows the change in heart position during spontaneous respiration （inhalation）.　The heart position changed significantly by 12.5±7.4 mm to the right during inhalation on land （p <0.05） compared to control.　During spontaneous breathing （inhalation）, the heart position changed significantly posteriorly by 4.5±3.3 mm at the water level of the xiphisternum （Figure 4）.　Figure 5 shows the change in heart position during spontaneous respiration （exhalation）.　The heart position changed significantly to the left by 9.0±10.8 mm at xiphisternum-level water （p <0.05） and by 14.7±9.1 mm at clavicle-level water （p <0.05） compared to control.　Figure 7 shows the change in heart position during deep respiration （inhalation）.　The heart position changed significantly by 17.9±6.1 mm to the right on land （p <0.05） compared to control.　Figure 9 shows the change in heart position during deep respiration （exhalation）.　The heart position changed significantly to the left:12.4±8.1 mm at greater trochanter level compared to control （p <0.05）.　The heart position during spontaneous breathing （exhalation）, deep breathing （inhalation）, and deep breathing （expiration） did not change to the anterior-posterior direction （Figure 6, 8, 10）.　Figure 11 shows the echo image of the long axis direction of the mitral valve during deep breathing （exhalation） in water at clavicle level.　Short axis direction is not shown.　Figure 12 shows the change in HR at various water levels compared to that on land.　HR decreased significantly at xiphisternum-level water （p <0.05）.　Figure 13 shows the change in blood pressure at various water levels compared to land condition.　SBP decreased significantly at navel-level water （p <0.05）.


Figure 1　Amount of changes in the heart position during hold breathing at various water level （Lateral Direction）	Figure 2　Amount of changes in the heart position during hold breathing at various water level （Anterior-Posterior）

Figure 3　Amount of changes in the heart position during spontaneous respiration （inhalation） at various water level （Lateral Direction）	Figure 4　Amount of changes in the heart position during spontaneous respiration （inhalation） at various water level （Anterior-Posterior）

Figure 5　Amount of changes in the heart position during spontaneous respiration （exhalation） at various water level （Lateral Direction）	Figure 6　Amount of changes in the heart position during spontaneous respiration （exhalation） at various water level （Anterior-Posterior）

Figure 7　Amounts of changes in the heart position during deep breathing （inhalation） at various water level （Lateral Direction）	Figure 8　Amounts of changes in the heart position during deep breathing （inhalation） at various water level （Anterior-Posterior）

Figure 9　Amounts of changes in the heart position during deep breathing （exhalation） at various water level （Lateral Direction）	Figure 10　Amounts of changes in the heart position during deep breathing （exhalation） at various water level （Anterior-Posterior）

Figure 11　Echo image of long axis direction of mitral valve during deep breathing （exhalation） at water of clavicle level	Figure 12　Changes in heart rate at various water level compared to land condition

Figure 13　Changes in blood pressure at various water level compared to land condition

IV.　Discussion
　This study investigated changes in heart position while breathing during water immersion at various levels.　
　The diaphragm and intercostal muscles are mainly for respiration^9）.　The diaphragm moves downward during inhalation and rises during exhalation;it contributes to inhalation more than it does to exhalation^4）.　The median portion of the diaphragm moves distally during maximal deep breathing^11）.　Furthermore, normal excursion is at least one rib interspace in adults on deep inspiration^14）.
　The pericardium covers the heart.　The upper sternopericardial, vertebro-pericardial （T3-T5）, sternopericardial, and pericardiacophrenic ligaments are all connected to the pericardium.
　The diaphragmatic nerves innervate the diaphragm^8）.　They are located on both sides of the heart^8） and transmit stimulation from the peritoneum and pleura.　When the right side of the diaphragm descends, the mediastinum shifts to the right^21）.　There is similar movement of the two hemidiaphragms, although the motion of the left hemidiaphragm may be slightly greater than that of the right^21）.　We considered that the diaphragm could be connected to the pericardium in tandem and that these ligaments could cause a change in heart position while breathing.
　Water immersion causes the rib cage to move upper anteriorly and the abdominal viscera to move superiorly, thereby stretching the diaphragm^17）.　Chest circumference also significantly decreased at clavicle-level water （compared to that at the level of the navel and fourth rib）^23） and at cervical-level water （compared to that on land）^13）.　Because of this, we considered that the chest wall is compressed by water pressure at levels above the clavicle.
　As the water level increases, the water pressure compresses the chest wall and abdominal cavity, thus raising the diaphragm^17） and increasing the load on respiratory muscles^7,10,19）.　Pulmonary vital capacity, forced expiratory volume during the first second （FEV1.0）, and functional residual capacity （FRC） are all decreased during immersion at the clavicle or cervical level^3,5,15,22）.　It has been reported that the maximum inspiratory muscle strength sharply decreased in clavicle-level water compared to xiphisternum-level water because of the higher water pressure^20）.　On the basis of this information, we considered that the heart changed position when submerged at water at the level of the clavicle.
　We clarified that the heart moved significantly to the left in xiphisternum-level and clavicle-level water compared to that on land^24）.　Moreover, when submerged in water, abdominal breathing occurs because of the effects of water pressure.　From this, we conclude that the water pressure causes the diaphragm to rise, pericardiacophrenic ligament to relax, and heart to shift to the left side.
　In this study, the QRS complex and transitional zone could not examined because we used the bipolar lead.　It was supposed that during exhalation or increasing water level changes the heart position to the left by rising diaphragm.　We considered that lead I is extended, leads II, III, aV_F are shortened, and the QRS axis is near 0°.　In transition zone, first, V1 ～ V3 form r waves and V5 ～ V6 make q waves because the initial excitement of the ventricles faces down.　Second, V1 ～ V3 form S waves and V4 ～ V6 form R waves because the main excitement waves go to the left.　Third, the R wave is the highest at V6 because the apex of the heart points to the left.　It was supposed that during inhalation changes the heart position to the right by descending a diaphragm.　We considered that lead I and III are shortened and leads II, aV_F are extended, and the QRS axis is near 60～90°.　In the transition zone, the R wave is the highest at V2～3 because the apex of the heart points to the center of the body.　The long axis direction of the mitral valve during deep breathing （exhalation） in water at clavicle level was observed.　We assumed that this did not occur only due to rise a diaphragm but also the heart rotated clockwise and anteriorly moved apex simultaneously.　We considered that lead I is extended, and leads II, III and aV_F are shortened and, and the QRS axis is near 0°.　In the transition zone, the R wave is the highest at V6 because the apex of the heart points to left.　What is discussed above is our consideration.　Therefore, it is necessary to clarify it to examine the electrocardiographic changes due to deep breathing in our future experiment.
　At supine posture, we observed the short axis direction of the mitral valve on median line.　Diaphragm rises approximately 4cm and increases in a venous return.　Because the effect of gravity is decreased at supine posture compared to standing.　At the standing, heart position was observed slightly to the left compared to supine postures.
　The HR during immersion at xiphisternum-level water was significantly decreased compared to that on land as well （p < 0.05）.　The water pressure causes an increase in venous return and a decrease in both stroke volume and HR;these variables depend on the water depth^19）.
　SBP decreased significantly in navel-level water.　During neutral temperature immersion, both SBP and DBP significantly decreased 5 min after immersion^2）.　Therefore, the changes in blood pressure can vary depending on the conditions of immersion.
　The diaphragm has three major apertures:the aortic hiatus, esophageal hiatus, and IVC hiatus.　The opening of the IVC hiatus enlarges with inspiration, drawing blood into the heart^14）.　It has been reported that during spontaneous respiration at the supine position, the IVC maximally dilates during exhalation and maximally contracts during inhalation^7）.　The IVC expands in water as the water level increases^19）.　Because of this, at clavicle-level water, water pressure exerts negative pressure on the chest cavity, causing the IVC hiatus to expand.　We thus believe that the heart rotated toward the left as venous return increases.　From the above, heart position changed to secure blood flow and maintain cardiac function.
　When floating in microgravity, the human body causes a fluid shift of blood.　It is considered that this fluid shift in microgravity affects the heart.　In the international space station, microgravity causes the force of the Z-axis to decrease, and thus the pressure on the rib cage is lesser than that on the Earth.　Therefore, we consider that astronauts might take a breath more similar to deep breathing rather than spontaneous breathing to do a regular gas exchange.　We considered that the way to prevent astronauts from getting space sickness was to take a deep breath.
　The heart position in this study was observed in the transverse plane;the change in heart position in the vertical direction was not examined.　The ultrasound diagnostic imaging system can only observe one surface at a time.　In the future, we need to investigate changes in the heart position by using the 12-lead method．

V.　Conclusion
　The heart demonstrated the following positional changes:
1.　The heart moved toward the left side during spontaneous respiration （exhalation） at xiphisternum- and clavicle-level water.
2.　During deep breathing （exhalation） at clavicle-level water, the heart rotated to the left and moved toward the left side.

VI.　Conflict of Interest
　The authors declare that there is no conflict of interest regarding the publication of this article.

VII.　Acknowledgments
　The authors gratefully acknowledge Senior Lecturer Tsukasa Tobaru （Kawasaki University of Medical Welfare） for advice on this research.

Corresponding author:Sho Onodera
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1）	LeBlanc, A., Schneider, V., Shackelford, L., West, S., Oganov, V., Bakulin, A. and Voronin, L.:Bone mineral and lean tissue loss after long duration space flight.　J Musculoskel Neuron Interact, 1（2）, 157-160, 2000.
2）	Sudo, A., Akasaki, F., Yagi, Y., Ijiri, K., Komiya, S., Tsunoda, N. and Watanabe, T.: Effects of the water pressure for the blood pressure in water immersion.　JSPEHSS, 22, 51-58, 2003. （In Japanese）
3）	Craig, A.B. and Dvorak, M.:Comparison of exercise in air and in water of different temperatures.　Med Sci Sports, 1, 124-130, 1969.
4）	Lens, E., Gurney-Champion, O.J., Tekelenburg, D.R., van Kesteren, Z., Parkes, M.J., van Tienhoven, G., Nederveen, A.J., van der Horst, A. and Bel, A.:Abdominal organ motion during inhalation and exhalation breath-holds pancreatic motion at different lung volumes compared.　Radiother.　Oncol., 121, 268-275, 2016.
5）	Ide, H., Akita, K., Fujiya, S., Asanuma, Y., Agishi, Y. and Morizaki, M.:Effects of Hydrostatic Pressure on Cardiac Function in Human.　Hokkaido J Med Sci, 62（1）, 68-73, 1987. （In Japanese）
6）	Bolender, H., Stevenin, H., Bessone, L. and Torres, A.: Preparing for space - EVA training at the European Astronaut Centre.　E.S.A., 128, 32-40, 2006.
7）	Nakahara, H. and Miyachi, M.:Reproducibility of the ultrasonographic morphometry of inferior vena caval cross-sectional area considered the respiratory variability.　Japanese Journal of Physical Fitness and Sports Medicine, 47（5）, 623-628, 1998.
8）	Gosling, J.A., Harris, P.E., Humpherson, J.R., Whitmore, I., Willan, P.L.T. and Yamauchi, A.:HUMAN anatomy text and colour atlas, second ed., Nankodo Co., Ltd, Japan, 1993.
9）	Kocjan, J., Adamek, M., Gzil-Zroska, B., Czyzewski, D. and Rydel, M.:Network of breathing.　Multifunctional role of the diaphragm.　Adv. Respir. Med., 85（4）, 224-232, 2017.
10）	Reason, J.T.:Motion sickness adaptation a neural mismatch model.　J. Roy. Soc. Med., 71, 819-829, 1978.
11）	Tomita, K., Sakai, Y., Monma, M., Ohse, H. and Imura, S.:Dynamic MRI of normal diaphragmatic motions during spontaneous breathing and maximal deep breathing.　Rigakuryoho Kagaku, 19（3）, 237-243, 2004. （In Japanese）
12）	Otsuka, K., Cornelissen, G., Furukawa, S., Kubo, Y., Hayashi, M., Shibata, K., Mizuno, K., Aiba, T., Ohshima, H. and Mukai, C.:Long-term exposure to space’s microgravity alters the time structure of heart rate variability of astronauts.　Heliyon, 2, 1-31, 2016.
13）	Kurabayashi, H.T., Kubota, K. and Tamura, J.:Analysis of the circumferences of chest, abdomen, thigh and calf during head- out water immersion.　Climatol. Phys. Med., 64, 199-202, 2001.
14）	Nason, L.K., Walker, C.M., Mcneeley, M.F., Burivong, W., Fligner, C.L. and Godwin, J.D.:Imaging of the Diaphragm, Anatomy and Function, 2012.
15）	Buono, M.J.:Effect of central vascular engorgement and immersion on various lung volumes.　J. Appl. Physiol. Respir. Environ. Exerc. Physiol., 54（4）, 1094-1096, 1983.
16）	Nishimura, M. and Onodera, S.:Relaxative Effects of Supine Floating on Heart Rate, Blood Pressure and Cardiac Autonomic Nervous System Activity.　J. J. Aerospace Env. Med., 37, 49-56, 2000.
17）	Reid, M.B., Loring, S.H., Banzett, R.B. and Mead, J.: Passive mechanics of upright human chest wall during immersion from hips to neck.　J. Appl. Physiol., 60（5）, 1561-1570, 1986.
18）	Yamauchi, R., Mizuno, N., Itazawa, T., Saitoh, H. and Kawamori, J.:Dosimetric evaluation of deep inspiration breath hold for left-sided breast cancer:analysis of patient-specific parameters related to heart dose reduction.　J Radiat Res., 61（3）, 1-10, 2020.
19）	Onodera, S., Miyachi, M., Nishimura, M., Yamamoto, K., Yamaguchi, H., Takahashi, K., In, J.Y., Amaoka, H., Yoshioka, A., Matsui, T. and Hara, H.:Effects of water depth on abdominal ［correction of abdominails］ aorta and inferior vena cava during standing in water.　J. Gravit. Physiol., 8, 59-60, 2001.
20）	Hong, S.K., Cerretelli, P., Cruz, J.C. and Rahn, H.: Mechanics of respiration during submersion in water.　Journal of applied physiology / American Physiological Society, 27（4）, 535-538, 1969.
21）	Sarnoff, S.J., et al.:Electrophrenic respiration IV, The effectiveness of contralateral ventilation during activity of one phrenic nerve.　J. Thorac. Surg., 13, 929-937, 1949.
22）	Risch, W.D., Koubenec, H.-J., Beckmann, U., Lange, S. and Gauer, O.H.:The Effect of Graded Immersion on Heart Volume, Central Venous Pressure, Pulmonary Blood Distribution, and Heart Rate in Man.　Pflugers Arch., 374, 115-118 （1978）.
23）	Yamashina, Y., Yokoyama, H., Naghavi, N., Hirasawa, Y., Takeda, R., Ota, A., Imai, D., Miyagawa, T. and Okazaki, K.:Forced respiration during the deeper water immersion causes the greater inspiratory muscle fatigue in healthy young men.　J. Phys. Ther. Sci., 28, 412-418, 2016.
24）	Ukida, Y., Wada, T., Giho, S., Ishida, Y. and Onodera, S.:Changes in mitral valve position while standing in and out of water.　J. J. Aerospace Env. Med., 58, 89-94, 2021.