The effects of spaceflight microgravity on the musculoskeletal system of humans and animals, with an emphasis on exercise as a countermeasure: a systematic scoping review
Jazyk angličtina Země Česko Médium print
Typ dokumentu časopisecké články, scoping review
PubMed
33992043
PubMed Central
PMC8820585
DOI
10.33549/physiolres.934550
PII: 934550
Knihovny.cz E-zdroje
- MeSH
- časové faktory MeSH
- hodnocení rizik MeSH
- kosmický let * MeSH
- lidé MeSH
- muskuloskeletální nemoci diagnóza etiologie patofyziologie prevence a kontrola MeSH
- muskuloskeletální systém patologie patofyziologie MeSH
- ochranné faktory MeSH
- opatření proti účinkům beztíže * MeSH
- rizikové faktory MeSH
- stav beztíže škodlivé účinky MeSH
- terapie cvičením * MeSH
- výsledek terapie MeSH
- zvířata MeSH
- Check Tag
- lidé MeSH
- mužské pohlaví MeSH
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- scoping review MeSH
The purpose of this systematic review is twofold: 1) to identify, evaluate, and synthesize the heretofore disparate scientific literatures regarding the effects of direct exposure to microgravity on the musculoskeletal system, taking into account for the first time both bone and muscle systems of both humans and animals; and 2) to investigate the efficacy and limitations of exercise countermeasures on the musculoskeletal system under microgravity in humans.The Framework for Scoping Studies (Arksey and O'Malley 2005) and the Cochrane Handbook for Systematic Reviews of Interventions (Higgins JPT 2011) were used to guide this review. The Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) checklist was utilized in obtaining the combined results (Moher, Liberati et al. 2009). Data sources, PubMed, Embase, Scopus, and Web of Science were searched for published articles through October 2019 using the Mesh terms of microgravity, musculoskeletal system, and exercise countermeasures. A total of 84 references were selected, including 40 animal studies and 44 studies with human participants. The heterogeneity in the study designs, methodologies, and outcomes deemed this review unsuitable for a meta-analysis. Thus, we present a narrative synthesis of the results for the key domains under five categories: 1) Skeletal muscle responses to microgravity in humans 2) Skeletal muscle responses to microgravity in animals 3) Adaptation of the skeletal system to microgravity in humans 4) Adaptation of the skeletal system to microgravity in animals 5) Effectiveness of exercise countermeasures on the human musculoskeletal system in microgravity. Existing studies have produced only limited data on the combined effects on bone and muscle of human spaceflight, despite the likelihood that the effects on these two systems are complicated due to the components of the musculoskeletal system being anatomically and functionally interconnected. Bone is directly affected by muscle atrophy as well as by changes in muscle strength, notably at muscle attachments. Given this interplay, the most effective exercise countermeasure is likely to be robust, individualized, resistive exercise, primarily targeting muscle mass and strength.
Zobrazit více v PubMed
AKIMA H, KAWAKAMI Y, KUBO K, SEKIGUCHI C, OHSHIMA H, MIYAMOTO A, FUKUNAGA T. Effect of short-duration spaceflight on thigh and leg muscle volume. Med Sci Sports Exerc. 2000;32:1743–1747. doi: 10.1097/00005768-200010000-00013. PubMed DOI
ALLEN DL, YASUI W, TANAKA T, OHIRA Y, NAGAOKA S, SEKIGUCHI C, HINDS WE, ROY RR, EDGERTON VR. Myonuclear number and myosin heavy chain expression in rat soleus single muscle fibers after spaceflight. J Appl Physiol. 1996;81:145–151. doi: 10.1152/jappl.1996.81.1.145. PubMed DOI
ANTONUTTO G, BODEM F, ZAMPARO P, di PRAMPERO PE. Maximal power and EMG of lower limbs after 21 days spaceflight in one astronaut. J Gravit Physiol. 1998;5:63–66. PubMed
ANTONUTTO G, CAPELLI C, GIRARDIS M, ZAMPARO P, di PRAMPERO PE. Effects of microgravity on muscular explosive power of the lower limbs in humans. Acta Astronaut. 1995;36:473–478. doi: 10.1016/0094-5765(95)00133-6. PubMed DOI
ANTONUTTO G, CAPELLI C, GIRARDIS M, ZAMPARO P, di PRAMPERO PE. Effects of microgravity on maximal power of lower limbs during very short efforts in humans. #x201D; J Appl Physiol (1985) 1999;86:85–92. doi: 10.1152/jappl.1999.86.1.85. PubMed DOI
ARKSEY H, O’MALLEY L. Scoping studies: towards a methodological framework. Int J Soc Res Methodol. 2005;8:19–32. doi: 10.1080/1364557032000119616. DOI
BACKUP P, WESTERLIND K, HARRIS S, SPELSBERG T, KLINE B, TURNER R. Spaceflight results in reduced mRNA levels for tissue-specific proteins in the musculoskeletal system. #x201D; Am J Physiol. 1994;266:E567–573. doi: 10.1152/ajpendo.1994.266.4.E567. PubMed DOI
BAILEY JF, MILLER SL, KHIEU K, O’NEILL CW, HEALEY RM, COUGHLIN DG, SAYSON JV, CHANG DG, HARGENS AR, LOTZ JC. From the international space station to the clinic: how prolonged unloading may disrupt lumbar spine stability. Spine J. 2018;18:7–14. doi: 10.1016/j.spinee.2017.08.261. PubMed DOI PMC
BALDWIN KM, HERRICK RE, MCCUE SA. Substrate oxidation capacity in rodent skeletal muscle: effects of exposure to zero gravity. J Appl Physiol (1985) 1993;75:2466–2470. doi: 10.1152/jappl.1993.75.6.2466. PubMed DOI
BELL GJ, MARTIN TP, ILYINA-KAKUEVA EI, OGANOV VS, EDGERTON VR. Altered distribution of mitochondria in rat soleus muscle fibers after spaceflight. J Appl Physiol (1985) 1992;73:493–497. doi: 10.1152/jappl.1992.73.2.493. PubMed DOI
BODINE-FOWLER SC, ROY RR, RUDOLPH W, HAQUE N, KOZLOVSKAYA IB, EDGERTON VR. Spaceflight and growth effects on muscle fibers in the rhesus monkey. J Appl Physiol (1985) 1992;73(2 Suppl):82S–89S. doi: 10.1152/jappl.1992.73.2.S82. PubMed DOI
BURKHART K, ALLAIRE B, BOUXSEIN ML. Negative effects of long-duration spaceflight on paraspinal muscle morphology. Spine (Phila Pa 1976) 2019;44:879–886. doi: 10.1097/BRS.0000000000002959. PubMed DOI
CAIOZZO VJ, BAKER MJ, HERRICK RE, TAO M, BALDWIN KM. Effect of spaceflight on skeletal muscle: mechanical properties and myosin isoform content of a slow muscle. J Appl Physiol (1985) 2004;76:1764–1773. doi: 10.1152/jappl.1994.76.4.1764. PubMed DOI
CAIOZZO VJ, BAKER MJ, HERRICK RE, TAO M, BALDWIN KM. Microgravity-induced transformations of myosin isoforms and contractile properties of skeletal muscle. #x201D; J Appl Physiol (1985) 1996;81:123–132. doi: 10.1152/jappl.1996.81.1.123. PubMed DOI
CANN CE, ADACHI RR. Bone resorption and mineral excretion in rats during spaceflight. Am J Physiol. 1983;244:R327–331. doi: 10.1152/ajpregu.1983.244.3.R327. PubMed DOI
CAVANAGH PR, GENC KO, GOPALAKRISHNAN R, KUKLIS MM, MAENDER CC, RICE AJ. Foot forces during typical days on the international space station. J Biomech. 2010;43:2182–2188. doi: 10.1016/j.jbiomech.2010.03.044. PubMed DOI
CHANG DG, HEALEY RM, SNYDER AJ, SAYSON JV, MACIAS BR, COUGHLIN DG, BAILEY JF, PARAZYNSKI SE, LOTZ JC, HARGENS AR. Lumbar spine paraspinal muscle and intervertebral disc height changes in astronauts after long-duration spaceflight on the international space station. Spine (Phila Pa 1976) 2016;41:1917–1924. doi: 10.1097/BRS.0000000000001873. PubMed DOI PMC
COLLET P, UEBELHART D, VICO L, MORO L, HARTMANN D, ROTH M, ALEXANDRE C. Effects of 1- and 6-month spaceflight on bone mass and biochemistry in two humans. Bone. 1997;20:547–551. doi: 10.1016/S8756-3282(97)00052-5. PubMed DOI
DAGDEVIREN D, KALAJZIC Z, ADAMS DJ, KALAJZIC I, LURIE A, MEDNIEKS MI, HAND AR. Responses to spaceflight of mouse mandibular bone and teeth. Arch Oral Biol. 2018;93:163–176. doi: 10.1016/j.archoralbio.2018.06.008. PubMed DOI
EDGERTON VR, ZHOU MY, OHIRA Y, KLITGAARD H, JIANG B, BELL G, HARRIS B, SALTIN B, GOLLNICK PD, ROY RR, et al. Human fiber size and enzymatic properties after 5 and 11 days of spaceflight. J Appl Physiol (1985) 1995;78(5):1733–1739. doi: 10.1152/jappl.1995.78.5.1733. PubMed DOI
ENGLISH KL, LEE SMC, LOEHR JA, PLOUTZ-SNYDER RJ, PLOUTZ-SNYDER LL. Isokinetic strength changes following long-duration spaceflight on the ISS. Aerosp Med Hum Perform. 2015;86(12 Suppl):A68–A77. doi: 10.3357/AMHP.EC09.2015. PubMed DOI
ESSER KA, HARDEMAN EC. Changes in contractile protein mRNA accumulation in response to spaceflight. Am J Physiol. 1995;268(2 Pt 1):C466–471. doi: 10.1152/ajpcell.1995.268.2.C466. PubMed DOI
FITTS RH, COLLOTON PA, TRAPPE SW, COSTILL DL, BAIN JL, RILEY DA. Effects of prolonged space flight on human skeletal muscle enzyme and substrate profiles. J Appl Physiol (1985) 2013;115:667–679. doi: 10.1152/japplphysiol.00489.2013. PubMed DOI
FITTS RH, TRAPPE SW, COSTILL DL, GALLAGHER PM, CREER AC, COLLOTON PA, PETERS JR, ROMATOWSKI JG, BAIN JL, RILEY DA. Prolonged space flight-induced alterations in the structure and function of human skeletal muscle fibres. J Physiol. 2010;588(Pt 18):3567–3592. doi: 10.1113/jphysiol.2010.188508. PubMed DOI PMC
FITZGERALD J, ENDICOTT J, HANSEN U, JANOWITZ C. Articular cartilage and sternal fibrocartilage respond differently to extended microgravity. NPJ Microgravity. 2019;5:3. doi: 10.1038/s41526-019-0063-6. PubMed DOI PMC
GAMBARA G, SALANOVA M, CICILIOT S, FURLAN S, GUTSMANN M, SCHIFFL G, UNGETHUEM U, VOLPE P, GUNGA HC, BLOTTNER D. Gene expression profiling in slow-type calf soleus muscle of 30 days space-flown mice. PLoS One. 2017;12:e0169314. doi: 10.1371/journal.pone.0169314. PubMed DOI PMC
GERBAIX M, WHITE H, COURBON G, SHENKMAN B, GAUQUELIN-KOCH G, VICO L. Eight days of earth reambulation worsen bone loss induced by 1-month spaceflight in the major weight-bearing ankle bones of mature mice. Front Physiol. 2018;9:746. doi: 10.3389/fphys.2018.00746. PubMed DOI PMC
GHOSH P, STABLEY JN, BEHNKE BJ, ALLEN MR, DELP MD. Effects of spaceflight on the murine mandible: Possible factors mediating skeletal changes in non-weight bearing bones of the head. Bone. 2016;83:156–161. doi: 10.1016/j.bone.2015.11.001. PubMed DOI
GOODSHIP AE, CUNNINGHAM JL, OGANOV V, DARLING J, MILES AW, OWEN GW. Bone loss during long term space flight is prevented by the application of a short term impulsive mechanical stimulus. Acta Astronautica. 1998;43:65–75. doi: 10.1016/S0094-5765(98)00144-1. PubMed DOI
GOPALAKRISHNAN R, GENC KO, RICE AJ, LEE SM, EVANS HJ, MAENDER CC, ILASLAN H, CAVANAGH PR. Muscle volume, strength, endurance, and exercise loads during 6-month missions in space. Aviat Space Environ Med. 2010;81:91–102. doi: 10.3357/ASEM.2583.2010. PubMed DOI
GUILLIAMS ME, LEE SMC, SHEPHERD B, CHAUVIN J, TADDEO T, SHACKELFORD LC. Upper-body strength and endurance after long-duration spaceflight. Med Sci Sports Exercise. 2003;35(Suppl 1):S262. doi: 10.1097/00005768-200305001-01451. DOI
GUROVSKY NN, GAZENKO OG, ADAMOVICH BA, ILYIN EA, GENIN AM, KOROLKOV VI, SHIPOV AA, KOTOVSKAYA AR, KONDRATYEVA VA, SEROVA LV, KONDRATYEV YI. Study of physiological effects of weightlessness and artificial gravity in the flight of the biosatellite Cosmos-936. Acta Astronaut. 1980;7:113–121. doi: 10.1016/0094-5765(80)90122-8. PubMed DOI
HADDAD F, HERRICK RE, ADAMS GR, BALDWIN KM. Myosin heavy chain expression in rodent skeletal muscle: effects of exposure to zero gravity. J Appl Physiol (1985) 1993;75:2471–2477. doi: 10.1152/jappl.1993.75.6.2471. PubMed DOI
HANSEN G, MARTINUK KJ, BELL GJ, MACLEAN IM, MARTIN TP, PUTMAN CT. Effects of spaceflight on myosin heavy-chain content, fibre morphology and succinate dehydrogenase activity in rat diaphragm. Pflugers Arch. 2004;448:239–247. doi: 10.1007/s00424-003-1230-9. PubMed DOI
HENRIKSEN EJ, TISCHLER ME, WOODMAN CR, MUNOZ KA, STUMP CS, KIRBY CR. Elevated interstitial fluid volume in soleus muscles unweighted by spaceflight or suspension. J Appl Physiol (1985) 1993;75:1650–1653. doi: 10.1152/jappl.1993.75.4.1650. PubMed DOI
HIDES JA, LAMBRECHT G, STANTON WR, DAMANN V. Changes in multifidus and abdominal muscle size in response to microgravity: possible implications for low back pain research. Eur Spine J 25 Suppl. 2016;1:175–182. doi: 10.1007/s00586-015-4311-5. PubMed DOI
HIGGINS JPT, GREEN S, editors. Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0 [updated March 2011] The Cochrane Collaboration;
HOLY X, MOUNIER Y. Effects of short spaceflights on mechanical characteristics of rat muscles. Muscle Nerve. 1991;14:70–78. doi: 10.1002/mus.880140112. PubMed DOI
JEE WS, WRONSKI TJ, MOREY ER, KIMMEL DB. Effects of spaceflight on trabecular bone in rats. Am J Physiol. 1983;244:R310–314. doi: 10.1152/ajpregu.1983.244.3.R310. PubMed DOI
KEYAK JH, KOYAMA AK, LEBLANC A, LU Y, LANG TF. Reduction in proximal femoral strength due to long-duration spaceflight. Bone. 2009;44:449–453. doi: 10.1016/j.bone.2008.11.014. PubMed DOI
KORYAK YA. Architectural and functional specifics of the human triceps surae muscle in vivo and its adaptation to microgravity. J Appl Physiol (1985) 2019;126:880–893. doi: 10.1152/japplphysiol.00634.2018. PubMed DOI
KRAEMER WJ, STARON RS, GORDON SE, VOLEK JS, KOZIRIS LP, DUNCAN ND, NINDL BC, GÓMEZ AL, MARX JO, FRY AC, MURRAY JD. The effects of 10 days of spaceflight on the shuttle Endeavor on predominantly fast-twitch muscles in the rat. Histochem Cell Biol. 2019;114:349–355. doi: 10.1007/s004180000193. PubMed DOI
LALANI R, BHASIN S, BYHOWER F, TARNUZZER R, GRANT M, SHEN R, ASA S, EZZAT S, GONZALEZ-CADAVID NF. Myostatin and insulin-like growth factor-I and -II expression in the muscle of rats exposed to the microgravity environment of the NeuroLab space shuttle flight. J Endocrinol. 2000;167:417–428. doi: 10.1677/joe.0.1670417. PubMed DOI
LAMBERTZ D, PÉROT C, KASPRANSKI R, GOUBEL F. Effects of long-term spaceflight on mechanical properties of muscles in humans. J Appl Physiol (1985) 2001;90:179–188. doi: 10.1152/jappl.2001.90.1.179. PubMed DOI
LANG T, LEBLANC A, EVANS H, LU Y, GENANT H, YU A. Cortical and trabecular bone mineral loss from the spine and hip in long-duration spaceflight. J Bone Miner Res. 2004;19:1006–1012. doi: 10.1359/JBMR.040307. PubMed DOI
LAUGHLIN MS, GUILLIAMS ME, NIESCHWITZ BA, HOELLEN D. Functional fitness testing results following long-duration ISS missions. Aerosp Med Hum Perform. 2015;86(12 Suppl):A87–A91. doi: 10.3357/AMHP.EC11.2015. PubMed DOI
LEBLANC A, SCHNEIDER V, SHACKELFORD L, WEST S, OGANOV V, BAKULIN A, VORONIN L. Bone mineral and lean tissue loss after long duration space flight. J Musculoskelet Neuronal Interact. 2000;1:157–160. PubMed
LI XT, YANG CB, ZHU YS, SUN J, SHI F, WANG YC, GAO Y, ZHAO JD, SUN XQ. Moderate exercise based on artificial gravity preserves orthostatic tolerance and exercise capacity during short-term head-down bed rest. Physiol Res. 2017;66:567–580. doi: 10.33549/physiolres.933493. PubMed DOI
LUCIANO TF, MARQUES SO, PIERI BL, De SOUZA DR, ARAÚJO LV, NESI RT, SCHEFFER DL, COMIN VH, PINHO RA, MULLER AP, De SOUZA CT. Responses of skeletal muscle hypertrophy in Wistar rats to different resistance exercise models. Physiol Res. 2017;66:317–323. doi: 10.33549/physiolres.933256. PubMed DOI
MACAULAY TR, SIAMWALA JH, HARGENS AR, MACIAS BR. Thirty days of spaceflight does not alter murine calvariae structure despite increased Sost expression. Bone Rep. 2017;7:57–62. doi: 10.1016/j.bonr.2017.08.004. PubMed DOI PMC
MACK PB, LACHANCE PA, VOSE GP, VOGT FB. Bone demineralization of foot and hand of gemini-titan IV, V and VII astronauts during orbital flight. Am J Roentgenol Radium Ther Nucl Med. 1967;100(3):503–511. doi: 10.2214/ajr.100.3.503. PubMed DOI
MACK PB, VOGT FB. Roentgenographic bone density changes in astronauts during representative Apollo space flight. Am J Roentgenol Radium Ther Nucl Med. 1971;113:621–633. doi: 10.2214/ajr.113.4.621. PubMed DOI
MARTIN TP, EDGERTON VR, GRINDELAND RE. Influence of spaceflight on rat skeletal muscle. J Appl Physiol (1985) 1988;65:2318–2325. doi: 10.1152/jappl.1988.64.6.2318. PubMed DOI
MAUPIN KA, CHILDRESS P, BRINKER A, KHAN F, ABEYSEKERA I, AGUILAR IN, OLIVOS DJ, 3RD, ADAM G, SAVAGLIO MK, GANESH V, GORDEN R, MANNFELD R, BECKNER E, HORAN DJ, ROBLING AG, CHAKRABORTY N, GAUTAM A, HAMMAMIEH R, KACENA MA. Skeletal adaptations in young male mice after 4 weeks aboard the International Space Station. NPJ Microgravity. 2019;5:21. doi: 10.1038/s41526-019-0081-4. PubMed DOI PMC
McNAMARA KP, GREENE KA, MOORE AM, LENCHIK L, WEAVER AA. Lumbopelvic muscle changes following long-duration spaceflight. Front Physiol. 2019;10:627. doi: 10.3389/fphys.2019.00627. PubMed DOI PMC
McNAMARA KP, GREENE KA, TOOZE JA, DANG J, KHATTAB K, LENCHIK L, WEAVER AA. Neck muscle changes following long-duration spaceflight. Front Physiol. 2019;10:1115. doi: 10.3389/fphys.2019.01115. PubMed DOI PMC
MECHANIC GL, ARNAUD SB, BOYDE A, BROMAGE TG, BUCKENDAHL P, ELLIOTT JC, KATZ EP, DURNOVA GN. Regional distribution of mineral and matrix in the femurs of rats flown on Cosmos 1887 biosatellite. FASEB J. 1990;4:34–40. doi: 10.1096/fasebj.4.1.2295376. PubMed DOI
MIU B, MARTIN TP, ROY RR, OGANOV V, ILYINA-KAKUEVA E, MARINI JF, LEGER JJ, BODINE-FOWLER SC, EDGERTON VR. Metabolic and morphologic properties of single muscle fibers in the rat after spaceflight, Cosmos 1887. FASEB J. 1990;4:64–72. doi: 10.1096/fasebj.4.1.2136839. PubMed DOI
MOHER D, LIBERATI A, TETZLAFF J, ALTMAN DG, PRISMA GROUP. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ. 2009;339:b2535. doi: 10.1136/bmj.b2535. PubMed DOI PMC
MOREY ER, BAYLINK DJ. Inhibition of bone formation during space flight. Science. 1978;201:1138–1141. doi: 10.1126/science.150643. PubMed DOI
MUSACCHIA XJ, STEFFEN JM, FELL RD, DOMBROWSKI MJ. Skeletal muscle response to spaceflight, whole body suspension, and recovery in rats. J Appl Physiol (1985) 1990;69:2248–2253. doi: 10.1152/jappl.1990.69.6.2248. PubMed DOI
OGANOV VS, RAKHMANOV AS, NOVIKOV VE, ZATSEPIN ST, RODIONOVA SS, CANN C. The state of human bone tissue during space flight. Acta Astronautica. 1991;23:129–133. doi: 10.1016/0094-5765(91)90109-I. PubMed DOI
OHIRA Y, JIANG B, ROY RR, OGANOV V, ILYINA-KAKUEVA E, MARINI JF, EDGERTON VR. Rat soleus muscle fiber responses to 14 days of spaceflight and hindlimb suspension. J Appl Physiol (1985) 1992;73(2 Suppl):51S–57S. doi: 10.1152/jappl.1992.73.2.S51. PubMed DOI
PUGLIA I, BALSAMO M, VUKICH M, ZOLESI V. Long-term microgravity effects on isometric handgrip and precision pinch force with visual and proprioceptive feedback. Int J Aerospace Eng. 2018;2018:1–11. doi: 10.1155/2018/1952630. DOI
RADUGINA EA, ALMEIDA EAC, BLABER E, POPLINSKAYA VA, MARKITANTOVA YV, GRIGORYAN EN. Exposure to microgravity for 30 days onboard Bion M1 caused muscle atrophy and impaired regeneration in murine femoral Quadriceps. Life Sci Space Res (Amst) 2018;16:18–25. doi: 10.1016/j.lssr.2017.08.005. PubMed DOI
RAMBAUT PC, JOHNSTON RS. Prolonged weightlessness and calcium loss in man. Acta Astronautica. 1979;6:1113–1122. doi: 10.1016/0094-5765(79)90059-6. PubMed DOI
RICHARDSON WS, WILSON MC, NISHIKAWA J, HAYWARD RS. The well-built clinical question: a key to evidence-based decisions. ACP journal club. 1995;123:A12–13. PubMed
RILEY DA, BAIN JL, THOMPSON JL, FITTS RH, WIDRICK JJ, TRAPPE SW, TRAPPE TA, COSTILL DL. Decreased thin filament density and length in human atrophic soleus muscle fibers after spaceflight. J Appl Physiol (1985) 2000;88:567–572. doi: 10.1152/jappl.2000.88.2.567. PubMed DOI
RILEY DA, ELLIS S, SLOCUM GR, SEDLAK FR, BAIN JL, KRIPPENDORF BB, LEHMAN CT, MACIAS MY, THOMPSON JL, VIJAYAN K, De BRUIN JA. In-flight and postflight changes in skeletal muscles of SLS-1 and SLS-2 spaceflown rats. J Appl Physiol (1985) 1996;81:133–144. doi: 10.1152/jappl.1996.81.1.133. PubMed DOI
SANDONÀ D, DESAPHY JF, CAMERINO GM, BIANCHINI E, CICILIOT S, DANIELI-BETTO D, DOBROWOLNY G, FURLAN S, GERMINARIO E, GOTO K, GUTSMANN M, KAWANO F, NAKAI N, OHIRA T, OHNO Y, PICARD A, SALANOVA M, SCHIFFL G, BLOTTNER D, MUSARÒ A, OHIRA Y, BETTO R, CONTE D, SCHIAFFINO S. Adaptation of mouse skeletal muscle to long-term microgravity in the MDS mission. PLoS One. 2012;7(3):e33232. doi: 10.1371/journal.pone.0033232. PubMed DOI PMC
SCHUENKE MD, REED DW, KRAEMER WJ, STARON RS, VOLEK JS, HYMER WC, GORDON S, PERRY KOZIRIS L. Effects of 14 days of microgravity on fast hindlimb and diaphragm muscles of the rat. Eur J Appl Physiol. 2009;106:885–892. doi: 10.1007/s00421-009-1091-9. PubMed DOI
SHENKMAN BS, BELOZEROVA IN, LEE P, NEMIROVSKAYA TL, KOZLOVSKAYA IB. Effects of weightlessness and movement restriction on the structure and metabolism of the soleus muscle in monkeys after space flight. Neurosci Behav Physiol. 2003;33:717–722. doi: 10.1023/A:1024473126643. PubMed DOI
SMITH MCJ, RAMBAUT PC, VOGEL JM, WHITTLE MW. Biomedical Results from Skylab. 1977:183–190.
SMITH SM, HEER M, SHACKELFORD LC, SIBONGA JD, SPATZ J, PIETRZYK RA, HUDSON EK, ZWART SR. Bone metabolism and renal stone risk during International Space Station missions. Bone. 2015;81:712–720. doi: 10.1016/j.bone.2015.10.002. PubMed DOI
SMITH SM, HEER MA, SHACKELFORD LC, SIBONGA JD, PLOUTZ-SNYDER L, ZWART SR. Benefits for bone from resistance exercise and nutrition in long-duration spaceflight: Evidence from biochemistry and densitometry. J Bone Miner Res. 2012;27(9):1896–1906. doi: 10.1002/jbmr.1647. PubMed DOI
SMITH SM, WASTNEY ME, O’BRIEN KO, MORUKOV BV, LARINA IM, ABRAMS SA, DAVIS-STREET JE, OGANOV V, SHACKELFORD LC. Bone markers, calcium metabolism, and calcium kinetics during extended-duration space flight on the mir space station. J Bone Miner Res. 2005;20:208–218. doi: 10.1359/JBMR.041105. PubMed DOI
SMITH SM, WASTNEY ME, MORUKOV BV, LARINA IM, NYQUIST LE, ABRAMS SA, TARAN EN, SHIH CY, NILLEN JL, DAVIS-STREET JE, RICE BL, LANE HW. Calcium metabolism before, during, and after a 3-mo spaceflight: kinetic and biochemical changes. Am J Physiol. 1999;277:R1–10. doi: 10.1152/ajpregu.1999.277.1.R1. PubMed DOI
TASCHER G, BRIOCHE T, MAES P, CHOPARD A, O’GORMAN D, GAUQUELIN-KOCH G, BLANC S, BERTILE F. Proteome-wide adaptations of mouse skeletal muscles during a full month in space. J Proteome Res. 2017;16:2623–2638. doi: 10.1021/acs.jproteome.7b00201. PubMed DOI
TESCH PA, BERG HE, BRING D, EVANS HJ, LEBLANC AD. Effects of 17-day spaceflight on knee extensor muscle function and size. Eur J Appl Physiol. 2005;93:463–468. doi: 10.1007/s00421-004-1236-9. PubMed DOI
THOMASON DB, MORRISON PR, OGANOV V, ILYINA-KAKUEVA E, BOOTH FW, BALDWIN KM. Altered actin and myosin expression in muscle during exposure to microgravity. J Appl Physiol (1985) 1992;73(2 Suppl):90S–93S. doi: 10.1152/jappl.1992.73.2.S90. PubMed DOI
THORNTON WE, RUMMEL JA. Biomedical Results from Skylab. NASA SP-377. NASA SP-377. 1977:491.
TRAPPE S, COSTILL D, GALLAGHER P, CREER A, PETERS JR, EVANS H, RILEY DA, FITTS RH. Exercise in space: human skeletal muscle after 6 months aboard the International Space Station. J Appl Physiol (1985) 2009;106:1159–1168. doi: 10.1152/japplphysiol.91578.2008. PubMed DOI
TRAPPE SW, TRAPPE TA, LEE GA, WIDRICK JJ, COSTILL DL, FITTS RH. Comparison of a space shuttle flight (STS-78) and bed rest on human muscle function. J Appl Physiol (1985) 2001;91:57–64. doi: 10.1152/jappl.2001.91.1.57. PubMed DOI
VANDENBURGH H, CHROMIAK J, SHANSKY J, Del TATTO M, LEMAIRE J. Space travel directly induces skeletal muscle atrophy. FASEB J. 1999;13:1031–1038. doi: 10.1096/fasebj.13.9.1031. PubMed DOI
VICO L, CHAPPARD D, PALLE S, BAKULIN AV, NOVIKOV VE, ALEXANDRE C. Trabecular bone remodeling after seven days of weightlessness exposure (BIOCOSMOS 1667) Am J Physiol. 1988;255(2 Pt 2):R243–247. doi: 10.1152/ajpregu.1988.255.2.R243. PubMed DOI
VICO L, COLLET P, GUIGNANDON A, LAFAGE-PROUST MH, THOMAS T, REHAILLIA M, ALEXANDRE C. Effects of long-term microgravity exposure on cancellous and cortical weight-bearing bones of cosmonauts. The Lancet. 2000;355:1607–1611. doi: 10.1016/S0140-6736(00)02217-0. PubMed DOI
VICO L, Van RIETBERGEN B, VILAYPHIOU N, LINOSSIER MT, LOCRELLE H, NORMAND M, ZOUCH M, GERBAIX M, BONNET N, NOVIKOV V, THOMAS T, VASSILIEVA G. Cortical and trabecular bone microstructure did not recover at weight-bearing skeletal sites and progressively deteriorated at non-weight-bearing sites during the year following international space station missions. J Bone Miner Res. 2017;32:2010–2021. doi: 10.1002/jbmr.3188. PubMed DOI
VOGEL JM. Bone mineral measurement: Skylab experiment M-078. Acta Astronautica. 1975;2:129–139. doi: 10.1016/0094-5765(75)90049-1. PubMed DOI
WHEDON GD, LUTWAK L. Metabolic studies of the Gemini-7 14 day orbital space flight. NASA (National Aeronautics and Space Administration), Scientific and Technical Aerospace Reports. 1971
ZERATH E, NOVIKOV V, LEBLANC A, BAKULIN A, OGANOV V, GRYNPAS M. Effects of spaceflight on bone mineralization in the rhesus monkey. J Appl Physiol (1985) 1996;81:194–200. doi: 10.1152/jappl.1996.81.1.194. PubMed DOI
ZERNICKE RF, VAILAS AC, GRINDELAND RE, KAPLANSKY A, SALEM GJ, MARTINEZ DA. Spaceflight effects on biomechanical and biochemical properties of rat vertebrae. Am J Physiol. 1990;258(6 Pt 2):R1327–1332. doi: 10.1152/ajpregu.1990.258.6.R1327. PubMed DOI