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      Towards human exploration of space: the THESEUS review series on muscle and bone research priorities

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          Abstract

          Without effective countermeasures, the musculoskeletal system is altered by the microgravity environment of long-duration spaceflight, resulting in atrophy of bone and muscle tissue, as well as in deficits in the function of cartilage, tendons, and vertebral disks. While inflight countermeasures implemented on the International Space Station have evidenced reduction of bone and muscle loss on low-Earth orbit missions of several months in length, important knowledge gaps must be addressed in order to develop effective strategies for managing human musculoskeletal health on exploration class missions well beyond Earth orbit. Analog environments, such as bed rest and/or isolation environments, may be employed in conjunction with large sample sizes to understand sex differences in countermeasure effectiveness, as well as interaction of exercise with pharmacologic, nutritional, immune system, sleep and psychological countermeasures. Studies of musculoskeletal biomechanics, involving both human subject and computer simulation studies, are essential to developing strategies to avoid bone fractures or other injuries to connective tissue during exercise and extravehicular activities. Animal models may be employed to understand effects of the space environment that cannot be modeled using human analog studies. These include studies of radiation effects on bone and muscle, unraveling the effects of genetics on bone and muscle loss, and characterizing the process of fracture healing in the mechanically unloaded and immuno-compromised spaceflight environment. In addition to setting the stage for evidence-based management of musculoskeletal health in long-duration space missions, the body of knowledge acquired in the process of addressing this array of scientific problems will lend insight into the understanding of terrestrial health conditions such as age-related osteoporosis and sarcopenia.

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          Cortical and trabecular bone mineral loss from the spine and hip in long-duration spaceflight.

          We measured cortical and trabecular bone loss using QCT of the spine and hip in 14 crewmembers making 4- to 6-month flights on the International Space Station. There was no compartment-specific loss of bone in the spine. Cortical bone mineral loss in the hip occurred primarily by endocortical thinning. In an earlier study, areal BMD (aBMD) measurements by DXA showed that cosmonauts making flights of 4- to 12-month duration on the Soviet/Russian MIR spacecraft lost bone at an average rate of 1%/month from the spine and 1.5%/month from the hip. However, because DXA measurements represent the sum of the cortical and trabecular compartments, there is no direct information on how these bone envelopes are affected by spaceflight. To address this, we performed a study of crewmembers (13 males and 1 female; age range, 40-55 years) on long-duration missions (4-6 months) on the International Space Station (ISS). We used DXA to obtain aBMD of the hip and spine and volumetric QCT (vQCT) to assess integral, cortical, and trabecular volumetric BMD (vBMD) in the hip and spine. In the heel, DXA was used to measure aBMD, and quantitative ultrasound (QUS) was used to measure speed of sound (SOS) and broadband ultrasound attenuation (BUA). aBMD was lost at rates of 0.9%/month at the spine (p < 0.001) and 1.4-1.5%/month at the hip (p < 0.001). Spinal integral vBMD was lost at a rate of 0.9%/month (p < 0.001), and trabecular vBMD was lost at 0.7%/month (p < 0.05). In contrast to earlier reports, these changes were generalized across the vertebrae and not focused in the posterior elements. In the hip, integral, cortical, and trabecular vBMD was lost at rates of 1.2-1.5%/month (p < 0.0001), 0.4-0.5%/month (p < 0.01), and 2.2-2.7%/month (p < 0.001), respectively. The cortical bone loss in the hip occurred primarily by cortical thinning. Calcaneal aBMD measurements by DXA showed smaller mean losses (0.4%/month) than hip or spine measurements, with SOS and BUA showing no change. In summary, our results show that ISS crewmembers, on average, experience substantial loss of both trabecular and cortical bone in the hip and somewhat smaller losses in the spine. These results do not support the use of calcaneal aBMD or QUS measurements as surrogate measures to estimate changes in the central skeleton. Copyright 2004 American Society for Bone and Mineral Research
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            One week of bed rest leads to substantial muscle atrophy and induces whole-body insulin resistance in the absence of skeletal muscle lipid accumulation.

            Short (<10 days) periods of muscle disuse, often necessary for recovery from illness or injury, lead to various negative health consequences. The present study investigated mechanisms underlying disuse-induced insulin resistance, taking into account muscle atrophy. Ten healthy, young males (age: 23±1 y, BMI: 23.0±0.9 kg·m(-2)) were subjected to one week of strict bed rest. Prior to and after bed rest, lean body mass (DXA) and quadriceps cross-sectional area (CSA; CT) were assessed, and VO2peak and leg strength were determined. Whole-body insulin sensitivity was measured using a hyperinsulinemic-euglycemic clamp. Additionally, muscle biopsies were collected to assess muscle lipid (fraction) content and various markers of mitochondrial and vascular content. Bed rest resulted in 1.4±0.2 kg lean tissue loss and a 3.2±0.9% decline in quadriceps CSA (both P<0.01). VO2peak and 1RM declined by 6.4±2.3 (P<0.05) and 6.9±1.4% (P<0.01), respectively. Bed rest induced a 29±5% decrease in whole-body insulin sensitivity (P<0.01). This was accompanied by a decline in muscle oxidative capacity, without alterations in skeletal muscle lipid content or saturation level, markers of oxidative stress, or capillary density. In conclusion, one week of bed rest substantially reduces skeletal muscle mass and lowers whole-body insulin sensitivity, without affecting mechanisms implicated in high-fat diet-induced insulin resistance.
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              Exercise in space: human skeletal muscle after 6 months aboard the International Space Station.

              The aim of this investigation was to document the exercise program used by crewmembers (n = 9; 45 +/- 2 yr) while aboard the International Space Station (ISS) for 6 mo and examine its effectiveness for preserving calf muscle characteristics. Before and after spaceflight, we assessed calf muscle volume (MRI), static and dynamic calf muscle performance, and muscle fiber types (gastrocnemius and soleus). While on the ISS, crewmembers had access to a running treadmill, cycle ergometer, and resistance exercise device. The exercise regimen varied among the crewmembers with aerobic exercise performed approximately 5 h/wk at a moderate intensity and resistance exercise performed 3-6 days/wk incorporating multiple lower leg exercises. Calf muscle volume decreased (P < 0.05) 13 +/- 2% with greater (P < 0.05) atrophy of the soleus (-15 +/- 2%) compared with the gastrocnemius (-10 +/- 2%). Peak power was 32% lower (P < 0.05) after spaceflight. Force-velocity characteristics were reduced (P < 0.05) -20 to -29% across the velocity spectrum. There was a 12-17% shift in myosin heavy chain (MHC) phenotype of the gastrocnemius and soleus with a decrease (P < 0.05) in MHC I fibers and a redistribution among the faster phenotypes. These data show a reduction in calf muscle mass and performance along with a slow-to-fast fiber type transition in the gastrocnemius and soleus muscles, which are all qualities associated with unloading in humans. Future long-duration space missions should modify the current ISS exercise prescription and/or hardware to better preserve human skeletal muscle mass and function, thereby reducing the risk imposed to crewmembers.
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                Author and article information

                Contributors
                Thomas.Lang@ucsf.edu
                Journal
                NPJ Microgravity
                NPJ Microgravity
                NPJ Microgravity
                Nature Publishing Group UK (London )
                2373-8065
                14 February 2017
                14 February 2017
                2017
                : 3
                : 8
                Affiliations
                [1 ]ISNI 0000 0001 2348 0690, GRID grid.30389.31, Department of Radiology and Biomedical Imaging Box 0946, , University of California, ; CA San Francisco, USA
                [2 ]ISNI 0000 0004 0435 165X, GRID grid.16872.3a, DESC (Dutch Experiment Support Center) & 3D InnovationLab, Dept. Oral and Maxillofacial Surgery/Oral Pathology, Dept. Oral Cell BiologyAcademic Centre for Dentistry Amsterdam (ACTA), , VU University Medical Center, ; Amsterdam, Netherlands
                [3 ]ISNI 0000 0004 4687 2082, GRID grid.264756.4, Department of Health & Kinesiology, , Texas A&M University, ; College Station, TX USA
                [4 ]Laboratoire de Biologie Intégrée du Tissu Osseux, LBTO INSERM U1059, University of St. Etienne, St. Etienne, France
                [5 ]ISNI 0000 0001 2186 5845, GRID grid.121334.6, Dynamique musculaire et métabolisme (DMEM) UMR 866 INRA, , University of Montpellier 1, ; Montpellier, France
                [6 ]ISNI 0000 0000 8580 3777, GRID grid.6190.e, Institute of Aerospace Medicine, DLR and Department of Pediatric and Adolescent Medicine, , University of Cologne, ; Cologne, Germany
                [7 ]ISNI 0000000109457005, GRID grid.4793.9, Department of Physical Education and Sports Science, Laboratory of Exercise Physiology and Biochemistry, , Aristotle University of Thessaloniki, ; Thessaloniki, Greece
                [8 ]ISNI 0000 0001 2218 4662, GRID grid.6363.0, , Charite Hospital, ; Berline, Germany
                [9 ]ISNI 0000 0004 0472 1876, GRID grid.416983.1, , UKK Institute for Health Promotion Research, ; Tampere, Finland
                [10 ]Skoltech University, Moscow, Russia
                [11 ]ISNI 0000 0000 8535 6057, GRID grid.412623.0, Department of Orthopedics and Sports Medicine, , University of Washington Medical Center, ; Seattle, WA USA
                Author information
                http://orcid.org/0000-0002-3720-8038
                http://orcid.org/0000-0002-1105-1060
                Article
                13
                10.1038/s41526-017-0013-0
                5445590
                28649630
                196c677f-add2-482b-a80e-0078c681c398
                © The Author(s) 2017

                This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

                History
                : 3 January 2016
                : 28 January 2017
                : 31 January 2017
                Categories
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                © The Author(s) 2017

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