Cardiac Effects of Repeated Weightlessness During Extreme Duration Swimming Compared With Spaceflight

HomeCirculationVol. 143, No. 15Cardiac Effects of Repeated Weightlessness During Extreme Duration Swimming Compared With Spaceflight Free AccessLetterPDF/EPUBAboutView PDFView EPUBSections ToolsAdd to favoritesDownload citationsTrack citationsPermissions ShareShare onFacebookTwitterLinked InMendeleyReddit Jump toFree AccessLetterPDF/EPUBCardiac Effects of Repeated Weightlessness During Extreme Duration Swimming Compared With Spaceflight James P. MacNamara, Katrin A. Dias, Satyam Sarma, Stuart M.C. Lee, David Martin, Maks Romeijn, Vlad G. Zaha and Benjamin D. Levine James P. MacNamaraJames P. MacNamara Institute for Exercise and Environmental Medicine, Texas Health Presbyterian Hospital, Dallas (J.P.M., K.A.D., S.S., V.G.Z., B.D.L.). Search for more papers by this author , Katrin A. DiasKatrin A. Dias https://orcid.org/0000-0002-2430-9219 Institute for Exercise and Environmental Medicine, Texas Health Presbyterian Hospital, Dallas (J.P.M., K.A.D., S.S., V.G.Z., B.D.L.). Search for more papers by this author , Satyam SarmaSatyam Sarma Institute for Exercise and Environmental Medicine, Texas Health Presbyterian Hospital, Dallas (J.P.M., K.A.D., S.S., V.G.Z., B.D.L.). Search for more papers by this author , Stuart M.C. LeeStuart M.C. Lee https://orcid.org/0000-0001-7065-5182 University of Texas Southwestern Medical Center, Dallas (J.P.M., K.A.D., S.S., V.G.Z., B.D.L.). Search for more papers by this author , David MartinDavid Martin University of Texas Southwestern Medical Center, Dallas (J.P.M., K.A.D., S.S., V.G.Z., B.D.L.). Search for more papers by this author , Maks RomeijnMaks Romeijn KBR, Houston, TX (S.M.C.L., D.M.). Search for more papers by this author , Vlad G. ZahaVlad G. Zaha Vlad G. Zaha, MD, PhD, Cardiology Division, Department of Internal Medicine, University of Texas Southwestern Medical Center, 5323 Harry Hines Boulevard, Dallas, TX 75390. Email E-mail Address: [email protected] https://orcid.org/0000-0003-4878-891X Institute for Exercise and Environmental Medicine, Texas Health Presbyterian Hospital, Dallas (J.P.M., K.A.D., S.S., V.G.Z., B.D.L.). Search for more papers by this author and Benjamin D. LevineBenjamin D. Levine Benjamin D. Levine, MD, Institute of Exercise and Environmental Medicine, University of Texas Southwestern Medical Center, 7232 Greenville Avenue, Dallas, TX 75231; Email E-mail Address: [email protected] https://orcid.org/0000-0001-9064-7251 Institute for Exercise and Environmental Medicine, Texas Health Presbyterian Hospital, Dallas (J.P.M., K.A.D., S.S., V.G.Z., B.D.L.). Search for more papers by this author Originally published29 Mar 2021https://doi.org/10.1161/CIRCULATIONAHA.120.050418Circulation. 2021;143:1533–1535Other version(s) of this articleYou are viewing the most recent version of this article. Previous versions: March 29, 2021: Ahead of Print Benoît Lecomte (B.L.) swam 2821 kilometers over 159 days, and Scott Kelly (S.K.) spent 340 days in space. What do extreme-duration swimming and extreme-duration spaceflight have in common, and how are they different? Both are associated with removal of gravitational loading of the musculoskeletal system and the absence of weight-bearing activities. Water immersion and supine bed rest, ground-based models for spaceflight, initially increase central blood volume as a result of reversed hydrostatic gradients but over time lead to diuresis partially through atrial natriuretic peptide stimulation and antidiuretic hormone inhibition.1,2 During spaceflight, the loss of a gravitational gradient results in a similar short-term rise in preload, followed by a compensatory decrease in blood volume and a long-term reduction in preload.2 Without countermeasures, extended spaceflight results in cardiac atrophy and orthostatic intolerance. In this study, we compare the cardiac effects of extreme-duration swimming and spaceflight to determine whether low-intensity, long-duration exercise counteracts the effects of repeated weightlessness.Both individuals gave permission to identify them in this report. B.L., an elite endurance swimmer who previously swam across the Atlantic Ocean, swam for 159 days (June 5, 2018–November 11, 2018), with breaks of 7 and 32 days because of unfavorable weather. He swam average of 5.8 hours (range, 1.1–9 hours) per swimming day and slept 8 hours a night, resulting in 9 to 17 h/d in the prone or supine position. He did not have a set hydration regimen. S.K. spent 340 days in space (March 27, 2015–March 1, 2016) and was prescribed exercise 6 d/wk that included a combination of cycling, treadmill, or resistive exercise. Two-dimensional and Doppler echocardiograms (Vivid Q, GE) were performed by sonographers before and by remote guidance during their respective campaigns. Left ventricular (LV) mass and LV ejection fraction were measured with the Teichholz method. Diastolic function was assessed by mitral inflow velocity and early diastolic recoil velocity. The study was approved by the institutional review board, and subjects gave informed consent. The data that support the findings of this study are available from the corresponding author on reasonable request.LV mass declined at similar rates in both individuals. B.L.’s mass dropped by 0.72 g/wk (95% CI, −0.14 to 1.58) and S.K.’s mass dropped by 0.74 g/wk (95% CI, 0.13–1.34) when linear regression is applied (Figure). Both subjects had an initial drop in LV diastolic diameter to a lower steady state through the campaign (B.L., 5 cm to average 4.7 cm; S.K., 5.3 cm to average 4.6 cm), suggesting an initial volume loss that was greater with spaceflight, although biological variability cannot be excluded. LV ejection fraction and markers of diastolic function did not consistently change in either individual throughout their campaign.Download figureDownload PowerPointFigure. Individual data for Benoît Lecomte and Scott Kelly across their respective campaigns. The overall trend of left ventricular (LV) mass was similar between Benoît Lecomte (▴) and Scott Kelly (○) (Top, left). Linear regression equation and best-fit line are shown. LV diastolic diameter shows an initial decline in Scott Kelly (Top, right). Ejection fraction (Bottom, left), diastolic recoil (e’, Bottom, middle), and E/A ratio (Bottom, right) show no consistent trend. BL indicates Benoît Lecomte; LV, left ventricular; and SL, Scott Kelly.Both individuals lost LV mass over the duration of their campaigns despite substantial amounts of exercise. Full-time bed rest studies, which serve as analogs to weightlessness, have shown reductions in plasma volume, cardiac mass, and orthostatic tolerance.2 B.L.’s awake time out of the water and ad libitum hydration were likely insufficient to completely preserve his plasma volume. Daily lower-body negative pressure (partially reinstating hydrostatic gradients) does not preserve plasma volume.3 We anticipated that a long duration of swimming exercise would have been enough of a stimulus to result in increases in LV mass and volume. Swim training of 1 to 3 hours daily at high intensity is associated with increased LV size and mass.4 It is surprising that low-intensity, long-duration swimming was insufficient to overcome the effects of repeated exposure to a weightlessness analog, leading to a cardiac adaptation similar to that in prolonged spaceflight. This study was limited by real-world issues, including delays between initial scans, interruptions of B.L.’s swim (for his safety), lack of body mass and blood volume measures, and reliance on the Teichholz method to estimate mass, limited the study. Both subjects meet the geometric assumptions of the Teichholz method, and S.K.’s results, including the initial decline in LV mass, are consistent with prior studies of bed rest and spaceflight.2These individuals and their extraordinary feats provide unique insight into the effects of extreme duration swimming and spaceflight. Extended loss of gravitational hydrostatic gradients through weightlessness or prone positioning in water immersion without proper countermeasures resulted in loss of cardiac mass. Consistent, low-intensity exercise may be insufficient to prevent cardiac atrophy during extreme-duration swimming, though further study is needed.AcknowledgmentsThe authors acknowledge the many people at the National Aeronautics and Space Administration, The Longest Swim, and the Institute for Exercise and Environmental Medicine for supporting these unprecedented human achievements. The authors express their utmost gratitude and admiration for B.L. and S.K. for their accomplishments.Disclosures None.Footnoteshttps://www.ahajournals.org/journal/circBenjamin D. Levine, MD, Institute of Exercise and Environmental Medicine, University of Texas Southwestern Medical Center, 7232 Greenville Avenue, Dallas, TX 75231; Email [email protected]orgVlad G. Zaha, MD, PhD, Cardiology Division, Department of Internal Medicine, University of Texas Southwestern Medical Center, 5323 Harry Hines Boulevard, Dallas, TX 75390. Email vlad.[email protected]eduReferences1. Anderson JV, Millar ND, O’Hare JP, Mackenzie JC, Corrall RJ, Bloom SR. Atrial natriuretic peptide: physiological release associated with natriuresis during water immersion in man.Clin Sci (Lond). 1986; 71:319–322. doi: 10.1042/cs0710319CrossrefMedlineGoogle Scholar2. Perhonen MA, Franco F, Lane LD, Buckey JC, Blomqvist CG, Zerwekh JE, Peshock RM, Weatherall PT, Levine BD. Cardiac atrophy after bed rest and spaceflight.J Appl Physiol (1985). 2001; 91:645–653. doi: 10.1152/jappl.2001.91.2.645CrossrefMedlineGoogle Scholar3. Dias KA, Hearon CM, Babu G, Marshall JE, MacNamara JP, Leidner J, Gillespie M, Peters K, Levine BD. Nightly lower body negative pressure redistributes blood volume and prevents maladaptive vascular remodeling induced by microgravity.Circulation. 2020; 142:A14436. Abstract.LinkGoogle Scholar4. Wasfy MM, Weiner RB, Wang F, Berkstresser B, Deluca J, Hutter AM, Picard MH, Baggish AL. Myocardial adaptations to competitive swim training.Med Sci Sports Exerc. 2019; 51:1987–1994. doi: 10.1249/MSS.0000000000002022CrossrefMedlineGoogle Scholar Previous Back to top Next FiguresReferencesRelatedDetailsCited By Martin T, Juarros M and Leinwand L (2023) Regression of cardiac hypertrophy in health and disease: mechanisms and therapeutic potential, Nature Reviews Cardiology, 10.1038/s41569-022-00806-6 Fischer M, Moralez G, Sarma S, MacNamara J, Cramer M, Huang M, Romero S, Hieda M, Shibasaki M, Ogoh S and Crandall C (2022) Altered cardiac β1 responsiveness in hyperthermic older adults, American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 10.1152/ajpregu.00040.2022, 323:4, (R581-R588), Online publication date: 1-Oct-2022. Whittle R, Stapleton L, Petersen L and Diaz-Artiles A (2021) Indirect measurement of absolute cardiac output during exercise in simulated altered gravity is highly dependent on the method, Journal of Clinical Monitoring and Computing, 10.1007/s10877-021-00769-y, 36:5, (1355-1366), Online publication date: 1-Oct-2022. Van Akin M, Lantz O, Fellows A, Toutain-Kidd C, Zegans M, Buckey J and Anderson A (2022) Acute effects of postural changes and lower body positive and negative pressure on the eye, Frontiers in Physiology, 10.3389/fphys.2022.933450, 13 Zhao Y, Zhong G, Du R, Zhao D, Li J, Li Y, Xing W, Jin X, Zhang W, Sun W, Liu C, Liu Z, Yuan X, Kan G, Han X, Li Q, Chang Y, Li Y and Ling S (2022) Ckip-1 3′-UTR Attenuates Simulated Microgravity-Induced Cardiac Atrophy, Frontiers in Cell and Developmental Biology, 10.3389/fcell.2021.796902, 9 Pollock R, Hodkinson P and Smith T (2021) Oh G: The x, y and z of human physiological responses to acceleration, Experimental Physiology, 10.1113/EP089712, 106:12, (2367-2384), Online publication date: 1-Dec-2021. Kumar A, Tahimic C, Almeida E and Globus R (2021) Spaceflight Modulates the Expression of Key Oxidative Stress and Cell Cycle Related Genes in Heart, International Journal of Molecular Sciences, 10.3390/ijms22169088, 22:16, (9088) April 13, 2021Vol 143, Issue 15 Advertisement Article InformationMetrics © 2021 American Heart Association, Inc.https://doi.org/10.1161/CIRCULATIONAHA.120.050418PMID: 33775108 Originally publishedMarch 29, 2021 KeywordsweightlessnessexercisePDF download Advertisement SubjectsExercise