Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Skeletal changes during and after spaceflight

Nature Reviews Rheumatology volume 14, pages 229–245 (2018)Cite this article

Subjects

Key Points

  • Low-orbit spaceflight induces bone fragility at weight-bearing skeletal sites and increases bone resorption.

  • Bone that is lost during space sojourns is not fully regained, and bone density can continue to deteriorate after landing, possibly owing to osteocyte death.

  • Physical activities and other interventions (known as countermeasures) designed to reduce loss of bone are not completely effective.

  • Cartilaginous tissues, such as intervertebral discs, lose structure and function in space and require effective countermeasures to facilitate re-adaptation to gravity upon landing.

  • Galactic and solar radiation in deep-space environments can contribute to bone loss, and radiation countermeasures are urgently needed.

Abstract

Space sojourns are challenging for life. The ability of the human body to adapt to these extreme conditions has been noted since the beginning of human space travel. Skeletal alterations that occur during spaceflight are now better understood owing to tools such as dual-energy X-ray densitometry and high-resolution peripheral quantitative CT, and murine models help researchers to understand cellular and matrix changes that occur in bone and that are difficult to measure in humans. However, questions remain with regard to bone adaptation and osteocyte fate, as well as to interactions of the skeleton with fluid shifts towards the head and with the vascular system. Further investigations into the relationships between the musculoskeletal system, energy metabolism and sensory motor acclimatisation are needed. In this regard, an integrated intervention is required that will address multiple systems simultaneously. Importantly, radiation and isolation-related stresses are gaining increased attention as the prospect of human exploration into deep space draws nearer. Although space is a unique environment, clear parallels exist between the effects of spaceflight, periods of immobilization and ageing, with possibly irreversible features. Space travel offers an opportunity to establish integrated deconditioning and ageing interventions that combine nutritional, physical and pharmaceutical strategies.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Hazards of spaceflight.
Figure 2: Changes in bone mineral density of cosmonauts after flights on the Mir space station.
Figure 3: Devices for load generation and fluid shift prevention for use during spaceflight.

Similar content being viewed by others

References

  1. Futterer, B. et al. in Generation and Applications of Extra-Terrestrial Environments on Earth (eds Beysens, D. A. & van Loon, J. J. W. A.) Ch. 9 (River Publishers, Netherlands, 2015).

    Google Scholar 

  2. Hackney, K. J. & English, K. L. Protein and essential amino acids to protect musculoskeletal health during spaceflight: evidence of a paradox? Life 4, 295–317 (2014).

    PubMed  PubMed Central  Google Scholar 

  3. Iwaniec, U. T. & Turner, R. T. Influence of body weight on bone mass, architecture and turnover. J. Endocrinol. 230, R115–R130 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Genc, K. O. et al. Foot forces during exercise on the International Space Station. J. Biomech. 43, 3020–3027 (2010).

    CAS  PubMed  Google Scholar 

  5. Vogel, J. M. & Whittle, M. W. Proceedings: bone mineral content changes in the Skylab astronauts. AJR Am. J. Roentgenol. 126, 1296–1297 (1976).

    CAS  PubMed  Google Scholar 

  6. Leach, C. S. & Rambaut, P. C. in Biomedical Results from Skylab (eds Johnston, R. S. & Dietlein, L F.) 204–216 (NASA, WA, USA, 1977).

    Google Scholar 

  7. Smith, M. C. Jr, Rambaut, P. C., Vogel, J. M. & Whittle, M. W. in Biomedical Results from Skylab (eds Johnston, R. S. & Dietlein, L F.) 183–190 (NASA, WA, USA, 1977).

    Google Scholar 

  8. Whedon, G. D. et al. Effect of weightlessness on mineral metabolism; metabolic studies on Skylab orbital space flights. Calcif. Tissue Res. 21 (Suppl.), 423–430 (1976).

    PubMed  Google Scholar 

  9. Orwoll, E. S. et al. Skeletal health in long-duration astronauts: nature, assessment, and management recommendations from the NASA Bone Summit. J. Bone Miner. Res. 28, 1243–1255 (2013).

    PubMed  Google Scholar 

  10. Oganov, V. S. The Skeletal System, Weightlessness, and Osteoporosis 88 (Slovo, Moscow, 2006).

    Google Scholar 

  11. LeBlanc, A. et al. Bone mineral and lean tissue loss after long duration space flight. J. Musculoskelet. Neuronal Interact. 1, 157–160 (2000).

    CAS  PubMed  Google Scholar 

  12. Smith, S. M. et al. Benefits for bone from resistance exercise and nutrition in long-duration spaceflight: evidence from biochemistry and densitometry. J. Bone Miner. Res. 27, 1896–1906 (2012).

    CAS  PubMed  Google Scholar 

  13. Cosman, F. et al. Clinician's guide to prevention and treatment of osteoporosis. Osteoporos. Int. 25, 2359–2381 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Oganov, V. S., Cann, C., Rakhmanov, A. S. & Ternovoi, S. K. Study of the musculoskeletal system of the spine in humans after long-term space flights by the method of computerized tomography [Russian]. Kosm. Biol. Aviakosm. Med. 24, 20–21 (1990).

    CAS  PubMed  Google Scholar 

  15. Bousson, V. et al. Volumetric quantitative computed tomography of the proximal femur: relationships linking geometric and densitometric variables to bone strength. Role for compact bone. Osteoporos. Int. 17, 855–864 (2006).

    CAS  PubMed  Google Scholar 

  16. Bala, Y., Zebaze, R. & Seeman, E. Role of cortical bone in bone fragility. Curr. Opin. Rheumatol. 27, 406–413 (2015).

    PubMed  Google Scholar 

  17. Humbert, L., Whitmarsh, T., Craene, M. D., Del Río Barquero, L. M. & Frangi, A. F. Technical note: comparison between single and multiview simulated DXA configurations for reconstructing the 3D shape and bone mineral density distribution of the proximal femur. Med. Phys. 39, 5272–5276 (2012).

    PubMed  Google Scholar 

  18. Lang, T. et al. Cortical and trabecular bone mineral loss from the spine and hip in long-duration spaceflight. J. Bone Miner. Res. 19, 1006–1012 (2004).

    PubMed  Google Scholar 

  19. Lang, T. F., Leblanc, A. D., Evans, H. J. & Lu, Y. Adaptation of the proximal femur to skeletal reloading after long-duration spaceflight. J. Bone Miner. Res. 21, 1224–1230 (2006).

    PubMed  Google Scholar 

  20. Vico, L. et al. Effects of long-term microgravity exposure on cancellous and cortical weight-bearing bones of cosmonauts. Lancet 355, 1607–1611 (2000).

    CAS  PubMed  Google Scholar 

  21. Stagi, S., Cavalli, L., Cavalli, T., de Martino, M. & Brandi, M. L. Peripheral quantitative computed tomography (pQCT) for the assessment of bone strength in most of bone affecting conditions in developmental age: a review. Ital. J. Pediatr. 42, 88 (2016).

    PubMed  PubMed Central  Google Scholar 

  22. European Space Agency. EXPERIMENT RECORD N° 9517 EDOS 2 – Early Detection of Osteoporosis in Space. Erasmus Experiment Archive http://eea.spaceflight.esa.int/portal/exp/?id=9517 (2018).

  23. Vico, L. et al. 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. 32, 2010–2021 (2017).

    CAS  PubMed  Google Scholar 

  24. Burghardt, A. J. et al. A longitudinal HR-pQCT study of alendronate treatment in postmenopausal women with low bone density: relations among density, cortical and trabecular microarchitecture, biomechanics, and bone turnover. J. Bone Miner. Res. 25, 2558–2571 (2010).

    PubMed  PubMed Central  Google Scholar 

  25. Government of Canada. TBone: effects of microgravity on bones. Canadian Space Agency http://www.asc-csa.gc.ca/eng/sciences/tbone.asp (2017).

  26. Smith, S. M. et al. Calcium metabolism before, during, and after a 3-mo spaceflight: kinetic and biochemical changes. Am. J. Physiol. 277, R1–10 (1999).

    CAS  PubMed  Google Scholar 

  27. Smith, S. M. et al. Collagen cross-link excretion during space flight and bed rest. J. Clin. Endocrinol. Metab. 83, 3584–3591 (1998).

    CAS  PubMed  Google Scholar 

  28. Caillot-Augusseau, A. et al. Bone formation and resorption biological markers in cosmonauts during and after a 180-day space flight (Euromir 95). Clin. Chem. 44, 578–585 (1998).

    CAS  PubMed  Google Scholar 

  29. Caillot-Augusseau, A. et al. Space flight is associated with rapid decreases of undercarboxylated osteocalcin and increases of markers of bone resorption without changes in their circadian variation: observations in two cosmonauts. Clin. Chem. 46, 1136–1143 (2000).

    CAS  PubMed  Google Scholar 

  30. Collet, P. et al. Effects of 1- and 6-month spaceflight on bone mass and biochemistry in two humans. Bone 20, 547–551 (1997).

    CAS  PubMed  Google Scholar 

  31. Leblanc, A. et al. Bisphosphonates as a supplement to exercise to protect bone during long-duration spaceflight. Osteoporos. Int. 24, 2105–2114 (2013).

    CAS  PubMed  Google Scholar 

  32. Smith, S. M. et al. Space flight calcium: implications for astronaut health, spacecraft operations, and Earth. Nutrients 4, 2047–2068 (2012).

    PubMed  PubMed Central  Google Scholar 

  33. Smith, S. M. et al. Men and women in space: bone loss and kidney stone risk after long-duration spaceflight. J. Bone Miner. Res. 29, 1639–1645 (2014).

    PubMed  Google Scholar 

  34. Spatz, J. M. et al. Serum sclerostin increases in healthy adult men during bed rest. J. Clin. Endocrinol. Metab. 97, E1736–E1740 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Frings-Meuthen, P. et al. Sclerostin and DKK1 levels during 14 and 21 days of bed rest in healthy young men. J. Musculoskelet. Neuronal Interact. 13, 45–52 (2013).

    CAS  PubMed  Google Scholar 

  36. Smith, S. M. et al. Bone metabolism and renal stone risk during International Space Station missions. Bone 81, 712–720 (2015).

    CAS  PubMed  Google Scholar 

  37. Gerbaix, M., Vico, L., Ferrari, S. L. & Bonnet, N. Periostin expression contributes to cortical bone loss during unloading. Bone 71, 94–100 (2015).

    CAS  PubMed  Google Scholar 

  38. Cresswell, E. N., Goff, M. G., Nguyen, T. M., Lee, W. X. & Hernandez, C. J. Spatial relationships between bone formation and mechanical stress within cancellous bone. J. Biomech. 49, 222–228 (2016).

    CAS  PubMed  Google Scholar 

  39. Lutwak, L., Whedon, G. D., Lachance, P. A., Reid, J. M. & Lipscomb, H. S. Mineral, electrolyte and nitrogen balance studies of the Gemini-VII fourteen-day orbital space flight. J. Clin. Endocrinol. Metab. 29, 1140–1156 (1969).

    CAS  PubMed  Google Scholar 

  40. Rambaut, P. C., Leach, C. S. & Whedon, G. D. A study of metabolic balance in crewmembers of Skylab IV. Acta Astronaut. 6, 1313–1322 (1979).

    CAS  PubMed  Google Scholar 

  41. Smith, S. M. et al. Bone markers, calcium metabolism, and calcium kinetics during extended-duration space flight on the Mir space station. J. Bone Miner. Res. 20, 208–218 (2005).

    CAS  PubMed  Google Scholar 

  42. Grigor'ev, A. I., Larina, I. M. & Morukov, B. V. Calcium metabolism characteristics in microgravity [Russian]. Ross. Fiziol. Zh. Im. I M Sechenova 85, 835–846 (1999).

    CAS  PubMed  Google Scholar 

  43. Rambaut, P. C., Leach, C. S. & Johnson, P. C. Calcium and phosphorus change of the Apollo 17 crew members. Nutr. Metab. 18, 62–69 (1975).

    CAS  PubMed  Google Scholar 

  44. Drummer, C., Cirillo, M. & De Santo, N. G. History of fluid balance and kidney function in space. J. Nephrol. 17, 180–186 (2004).

    PubMed  Google Scholar 

  45. Hughes-Fulford, M. Review of the biological effects of weightlessness on the human endocrine system. Receptor 3, 145–154 (1993).

    CAS  PubMed  Google Scholar 

  46. Morey-Holton, E. R. et al. Vitamin D metabolites and bioactive parathyroid hormone levels during Spacelab 2. Aviat. Space Environ. Med. 59, 1038–1041 (1988).

    CAS  PubMed  Google Scholar 

  47. Whitson, P. A., Pietrzyk, R. A. & Sams, C. F. Space flight and the risk of renal stones. J. Gravitat. Physiol. 6, 87–88 (1999).

    Google Scholar 

  48. Willey, J. S. et al. Spaceflight-relevant challenges of radiation and/or reduced weight bearing cause arthritic responses in knee articular cartilage. Radiat. Res. 186, 333–344 (2016).

    CAS  PubMed  Google Scholar 

  49. Liphardt, A.-M. et al. Vibration training intervention to maintain cartilage thickness and serum concentrations of cartilage oligometric matrix protein (COMP) during immobilization. Osteoarthritis Cartilage 17, 1598–1603 (2009).

    PubMed  Google Scholar 

  50. Tagliaferri, C., Wittrant, Y., Davicco, M.-J., Walrand, S. & Coxam, V. Muscle and bone, two interconnected tissues. Ageing Res. Rev. 21, 55–70 (2015).

    CAS  PubMed  Google Scholar 

  51. Sayson, J. V. & Hargens, A. R. Pathophysiology of low back pain during exposure to microgravity. Aviat. Space Environ. Med. 79, 365–373 (2008).

    PubMed  Google Scholar 

  52. Wilke, H. J., Neef, P., Caimi, M., Hoogland, T. & Claes, L. E. New in vivo measurements of pressures in the intervertebral disc in daily life. Spine 24, 755–762 (1999).

    CAS  PubMed  Google Scholar 

  53. Krag, M. H., Cohen, M. C., Haugh, L. D. & Pope, M. H. Body height change during upright and recumbent posture. Spine 15, 202–207 (1990).

    CAS  PubMed  Google Scholar 

  54. Andersson, G. B., Murphy, R. W., Ortengren, R. & Nachemson, A. L. The influence of backrest inclination and lumbar support on lumbar lordosis. Spine 4, 52–58 (1979).

    CAS  PubMed  Google Scholar 

  55. Tyrrell, A. R., Reilly, T. & Troup, J. D. Circadian variation in stature and the effects of spinal loading. Spine 10, 161–164 (1985).

    CAS  PubMed  Google Scholar 

  56. Malko, J. A., Hutton, W. C. & Fajman, W. A. An in vivo magnetic resonance imaging study of changes in the volume (and fluid content) of the lumbar intervertebral discs during a simulated diurnal load cycle. Spine 24, 1015–1022 (1999).

    CAS  PubMed  Google Scholar 

  57. Adams, M. A. & Hutton, W. C. The effect of posture on the fluid content of lumbar intervertebral discs. Spine 8, 665–671 (1983).

    CAS  PubMed  Google Scholar 

  58. Hutton, W. C., Malko, J. A. & Fajman, W. A. Lumbar disc volume measured by MRI: effects of bed rest, horizontal exercise, and vertical loading. Aviat. Space Environ. Med. 74, 73–78 (2003).

    PubMed  Google Scholar 

  59. Bailey, J. F. et al. From the International Space Station to the clinic: how prolonged unloading may disrupt lumbar spine stability. Spine J. 18, 7–14 (2018).

    PubMed  Google Scholar 

  60. Harrison, M. F. et al. Preflight, in-flight, and postflight imaging of the cervical and lumbar spine in astronauts. Aerosp. Med. Hum. Perform. 89, 32–40 (2018).

    PubMed  Google Scholar 

  61. Chang, D. G. et al. Lumbar spine paraspinal muscle and intervertebral disc height changes in astronauts after long-duration spaceflight on the International Space Station. Spine 41, 1917–1924 (2016).

    PubMed  PubMed Central  Google Scholar 

  62. Ishihara, H., McNally, D. S., Urban, J. P. & Hall, A. C. Effects of hydrostatic pressure on matrix synthesis in different regions of the intervertebral disk. J. Appl. Physiol. 80, 839–846 (1996).

    CAS  PubMed  Google Scholar 

  63. Horner, H. A. & Urban, J. P. Effect of nutrient supply on the viability of cells from the nucleus pulposus of the intervertebral disc. Spine 26, 2543–2549 (2001).

    CAS  PubMed  Google Scholar 

  64. Kasra, M. et al. Effect of dynamic hydrostatic pressure on rabbit intervertebral disc cells. J. Orthop. Res. 21, 597–603 (2003).

    PubMed  Google Scholar 

  65. Morey-Holton, E. R., Hill, E. L. & Souza, K. A. Animals and spaceflight: from survival to understanding. J. Musculoskelet. Neuronal Interact. 7, 17–25 (2007).

    CAS  PubMed  Google Scholar 

  66. Kaplansky, A. S., Durnova, G. N., Burkovskaya, T. E. & Vorotnikova, E. V. The effect of microgravity on bone fracture healing in rats flown on Cosmos-2044. Physiologist 34 (Suppl.), S196–S199 (1991).

    CAS  PubMed  Google Scholar 

  67. Vico, L. et al. Trabecular bone remodeling after seven days of weightlessness exposure (BIOCOSMOS 1667). Am. J. Physiol. 255, R243–R247 (1988).

    CAS  PubMed  Google Scholar 

  68. Kaplansky, A. S., Durnova, G. N., Sakharova, Z. F. & Ilyina-Kakueva, E. Histomorphometric analysis of rat bones after spaceflight aboard Cosmos 1667 biosatellite. Space Biol. Med. 21, 33–40 (1987).

    Google Scholar 

  69. Vico, L., Bourrin, S., Genty, C., Palle, S. & Alexandre, C. Histomorphometric analyses of cancellous bone from COSMOS 2044 rats. J. Appl. Physiol. 75, 2203–2208 (1993).

    CAS  PubMed  Google Scholar 

  70. Yagodovsky, V. S., Triftanidi, L. A. & Gorokhova, G. P. Space flight effects on skeletal bones of rats (light and electron microscopic examination). Aviat. Space Environ. Med. 47, 734–738 (1976).

    CAS  PubMed  Google Scholar 

  71. Lafage-Proust, M. H. et al. Space-related bone mineral redistribution and lack of bone mass recovery after reambulation in young rats. Am. J. Physiol. 274, R324–R334 (1998).

    CAS  PubMed  Google Scholar 

  72. Morey, E. R. & Baylink, D. J. Inhibition of bone formation during space flight. Science 201, 1138–1141 (1978).

    CAS  PubMed  Google Scholar 

  73. Montufar-Solis, D., Duke, P. J. & Durnova, G. Spaceflight and age affect tibial epiphyseal growth plate histomorphometry. J. Appl. Physiol. 73, 19S–25S (1992).

    CAS  PubMed  Google Scholar 

  74. Sibonga, J. D. et al. Effects of spaceflight and simulated weightlessness on longitudinal bone growth. Bone 27, 535–540 (2000).

    CAS  PubMed  Google Scholar 

  75. Westerlind, K. C. & Turner, R. T. The skeletal effects of spaceflight in growing rats: tissue-specific alterations in mRNA levels for TGF-β. J. Bone Miner. Res. 10, 843–848 (1995).

    CAS  PubMed  Google Scholar 

  76. Wronski, T. J., Morey-Holton, E. R., Doty, S. B., Maese, A. C. & Walsh, C. C. Histomorphometric analysis of rat skeleton following spaceflight. Am. J. Physiol. 252, R252–R255 (1987).

    CAS  PubMed  Google Scholar 

  77. Vailas, A. C. et al. Effects of spaceflight on rat humerus geometry, biomechanics, and biochemistry. FASEB J. 4, 47–54 (1990).

    CAS  PubMed  Google Scholar 

  78. Zerath, E. et al. Spaceflight inhibits bone formation independent of corticosteroid status in growing rats. J. Bone Miner. Res. 15, 1310–1320 (2000).

    CAS  PubMed  Google Scholar 

  79. Wronski, T. J. et al. Lack of effect of spaceflight on bone mass and bone formation in group-housed rats. J. Appl. Physiol. 85, 279–285 (1998).

    CAS  PubMed  Google Scholar 

  80. Vajda, E. G., Wronski, T. J., Halloran, B. P., Bachus, K. N. & Miller, S. C. Spaceflight alters bone mechanics and modeling drifts in growing rats. Aviat. Space Environ. Med. 72, 720–726 (2001).

    CAS  PubMed  Google Scholar 

  81. Vico, L., Chappard, D., Bakulin, A. V., Novikov, V. E. & Alexandre, C. Effects of 7-day space flight on weight-bearing and non-weight-bearing bones in rats (Cosmos 1667). Physiologist 30 (Suppl.), S45–S46 (1987).

    CAS  PubMed  Google Scholar 

  82. Mechanic, G. L. et al. Regional distribution of mineral and matrix in the femurs of rats flown on Cosmos 1887 biosatellite. FASEB J. 4, 34–40 (1990).

    CAS  PubMed  Google Scholar 

  83. Patterson-Buckendahl, P. et al. Fragility and composition of growing rat bone after one week in spaceflight. Am. J. Physiol. 252, R240–R246 (1987).

    CAS  PubMed  Google Scholar 

  84. Vailas, A. C. et al. Adaptations of young adult rat cortical bone to 14 days of spaceflight. J. Appl. Physiol. 73, 4S–9S (1992).

    CAS  PubMed  Google Scholar 

  85. Hatton, D. C. et al. Calcium metabolism and cardiovascular function after spaceflight. J. Appl. Physiol. 92, 3–12 (2002).

    CAS  PubMed  Google Scholar 

  86. Zhang, B., Cory, E., Bhattacharya, R., Sah, R. & Hargens, A. R. Fifteen days of microgravity causes growth in calvaria of mice. Bone 56, 290–295 (2013).

    PubMed  PubMed Central  Google Scholar 

  87. McCarthy, I. D. Fluid shifts due to microgravity and their effects on bone: a review of current knowledge. Ann. Biomed. Eng. 33, 95–103 (2005).

    PubMed  Google Scholar 

  88. Ghosh, P., Stabley, J. N., Behnke, B. J., Allen, M. R. & Delp, M. D. Effects of spaceflight on the murine mandible: possible factors mediating skeletal changes in non-weight bearing bones of the head. Bone 83, 156–161 (2016).

    PubMed  Google Scholar 

  89. Cavolina, J. M. et al. The effects of orbital spaceflight on bone histomorphometry and messenger ribonucleic acid levels for bone matrix proteins and skeletal signaling peptides in ovariectomized growing rats. Endocrinology 138, 1567–1576 (1997).

    CAS  PubMed  Google Scholar 

  90. Keune, J. A., Branscum, A. J., Iwaniec, U. T. & Turner, R. T. Effects of spaceflight on bone microarchitecture in the axial and appendicular skeleton in growing ovariectomized rats. Sci. Rep. 5, 18671 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  91. Tavella, S. et al. Bone turnover in wild type and pleiotrophin-transgenic mice housed for three months in the International Space Station (ISS). PLoS ONE 7, e33179 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  92. Lloyd, S. A. et al. Osteoprotegerin is an effective countermeasure for spaceflight-induced bone loss in mice. Bone 81, 562–572 (2015).

    CAS  PubMed  Google Scholar 

  93. Blaber, E. A. et al. Microgravity induces pelvic bone loss through osteoclastic activity, osteocytic osteolysis, and osteoblastic cell cycle inhibition by CDKN1a/p21. PLoS ONE 8, e61372 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  94. Berg-Johansen, B. et al. Spaceflight-induced bone loss alters failure mode and reduces bending strength in murine spinal segments. J. Orthop. Res. 34, 48–57 (2016).

    PubMed  Google Scholar 

  95. Gerbaix, M. et al. One-month spaceflight compromises the bone microstructure, tissue-level mechanical properties, osteocyte survival and lacunae volume in mature mice skeletons. Sci. Rep. 7, 2659 (2017).

    PubMed  PubMed Central  Google Scholar 

  96. Lin, C. et al. Sclerostin mediates bone response to mechanical unloading through antagonizing Wnt/β-catenin signaling. J. Bone Miner. Res. 24, 1651–1661 (2009).

    CAS  PubMed  Google Scholar 

  97. Tu, X. et al. Sost downregulation and local Wnt signaling are required for the osteogenic response to mechanical loading. Bone 50, 209–217 (2012).

    CAS  PubMed  Google Scholar 

  98. Britz, H. M. et al. Prolonged unloading in growing rats reduces cortical osteocyte lacunar density and volume in the distal tibia. Bone 51, 913–919 (2012).

    PubMed  Google Scholar 

  99. Busse, B. et al. Decrease in the osteocyte lacunar density accompanied by hypermineralized lacunar occlusion reveals failure and delay of remodeling in aged human bone. Aging Cell 9, 1065–1075 (2010).

    CAS  PubMed  Google Scholar 

  100. Milovanovic, P. et al. The formation of calcified nanospherites during micropetrosis represents a unique mineralization mechanism in aged human bone. Small 13, 1602215 (2017).

    Google Scholar 

  101. Zérath, E. et al. Effects of Bion 11 14-day space flight on monkey iliac bone. J. Gravitat. Physiol. 7, S155–156 (2000).

    Google Scholar 

  102. Zérath, E. et al. Spaceflight affects bone formation in rhesus monkeys: a histological and cell culture study. J. Appl. Physiol. 93, 1047–1056 (2002).

    PubMed  Google Scholar 

  103. Rodionova, N. V., Oganov, V. S. & Zolotova, N. V. Ultrastructural changes in osteocytes in microgravity conditions. Adv. Space Res. 30, 765–770 (2002).

    CAS  PubMed  Google Scholar 

  104. Oganov, V. S., Bakulin, A. V., Novikov, V. E. & Murashko, L. M. Change and recovery of bone mass and acoustic properties of rhesus monkeys after Bion 11 spaceflight. J. Gravitat. Physiol. 7, S163–S168 (2000).

    CAS  Google Scholar 

  105. Arnaud, S. B. et al. Calcium metabolism in Bion 11 monkeys. J. Gravitat. Physiol. 7, S153 (2000).

    CAS  Google Scholar 

  106. Chatani, M. et al. Microgravity promotes osteoclast activity in medaka fish reared at the International Space Station. Sci. Rep. 5, 14172 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  107. Chatani, M. et al. Acute transcriptional up-regulation specific to osteoblasts/osteoclasts in medaka fish immediately after exposure to microgravity. Sci. Rep. 6, 39545 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  108. Gopalakrishnan, R. et al. Muscle volume, strength, endurance, and exercise loads during 6-month missions in space. Aviat. Space Environ. Med. 81, 91–102 (2010).

    PubMed  Google Scholar 

  109. Lee, S. M. C. et al. WISE-2005: Countermeasures to prevent muscle deconditioning during bed rest in women. J. Appl. Physiol. 116, 654–667 (2014).

    PubMed  Google Scholar 

  110. Trappe, S. et al. Exercise in space: human skeletal muscle after 6 months aboard the International Space Station. J. Appl. Physiol. 106, 1159–1168 (2009).

    PubMed  Google Scholar 

  111. Lee, S. M. C., Moore, A. D., Everett, M. E., Stenger, M. B. & Platts, S. H. Aerobic exercise deconditioning and countermeasures during bed rest. Aviat. Space Environ. Med. 81, 52–63 (2010).

    PubMed  Google Scholar 

  112. Kozlovskaya, I. B. & Grigoriev, A. I. Russian system of countermeasures on board of the International Space Station (ISS): the first results. Acta Astronaut. 55, 233–237 (2004).

    PubMed  Google Scholar 

  113. Alkner, B. A. & Tesch, P. A. Knee extensor and plantar flexor muscle size and function following 90 days of bed rest with or without resistance exercise. Eur. J. Appl. Physiol. 93, 294–305 (2004).

    PubMed  Google Scholar 

  114. Lee, S. M. C. et al. Supine LBNP exercise maintains exercise capacity in male twins during 30-d bed rest. Med. Sci. Sports Exerc. 39, 1315–1326 (2007).

    PubMed  Google Scholar 

  115. Holt, J. A. et al. WISE 2005: Aerobic and resistive countermeasures prevent paraspinal muscle deconditioning during 60-day bed rest in women. J. Appl. Physiol. 120, 1215–1222 (2016).

    PubMed  Google Scholar 

  116. Schneider, S. M., Lee, S. M. C., Macias, B. R., Watenpaugh, D. E. & Hargens, A. R. WISE-2005: exercise and nutrition countermeasures for upright V˙O2pk during bed rest. Med. Sci. Sports Exerc. 41, 2165–2176 (2009).

    PubMed  Google Scholar 

  117. Hargens, A. R. & Vico, L. Long-duration bed rest as an analog to microgravity. J. Appl. Physiol. 120, 891–903 (2016).

    PubMed  Google Scholar 

  118. Hargens, A. R. & Richardson, S. Cardiovascular adaptations, fluid shifts, and countermeasures related to space flight. Respir. Physiol. Neurobiol. 169 (Suppl. 1), S30–S33 (2009).

    PubMed  Google Scholar 

  119. Kwon, R. Y., Meays, D. R., Tang, W. J. & Frangos, J. A. Microfluidic enhancement of intramedullary pressure increases interstitial fluid flow and inhibits bone loss in hindlimb suspended mice. J. Bone Miner. Res. 25, 1798–1807 (2010).

    PubMed  PubMed Central  Google Scholar 

  120. Hillsley, M. V. & Frangos, J. A. Bone tissue engineering: the role of interstitial fluid flow. Biotechnol. Bioeng. 43, 573–581 (1994).

    CAS  PubMed  Google Scholar 

  121. Clément, G. & Ngo-Anh, J. T. Space physiology II: adaptation of the central nervous system to space flight — past, current, and future studies. Eur. J. Appl. Physiol. 113, 1655–1672 (2013).

    PubMed  Google Scholar 

  122. Van Ombergen, A. et al. Spaceflight-induced neuroplasticity in humans as measured by MRI: what do we know so far? NPJ Micrograv. 3, 2 (2017).

    Google Scholar 

  123. Thornton, W. E. & Bonato, F. Space motion sickness and motion sickness: symptoms and etiology. Aviat. Space Environ. Med. 84, 716–721 (2013).

    PubMed  Google Scholar 

  124. Black, F. O. et al. Disruption of postural readaptation by inertial stimuli following space flight. J. Vestib. Res. Equilib. Orientat. 9, 369–378 (1999).

    CAS  Google Scholar 

  125. Vignaux, G., Ndong, J. D., Perrien, D. S. & Elefteriou, F. Inner ear vestibular signals regulate bone remodeling via the sympathetic nervous system. J. Bone Miner. Res. 30, 1103–1111 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  126. Reschke, M. F. et al. Effects of sex and gender on adaptation to space: neurosensory systems. J. Womens Health 23, 959–962 (2014).

    Google Scholar 

  127. Petersen, N. et al. Postflight reconditioning for European astronauts — a case report of recovery after six months in space. Musculoskelet. Sci. Pract. 27 (Suppl. 1), S23–S31 (2017).

    PubMed  Google Scholar 

  128. Smith, S. M. et al. Fifty years of human space travel: implications for bone and calcium research. Annu. Rev. Nutr. 34, 377–400 (2014).

    CAS  PubMed  Google Scholar 

  129. Shackelford, L. C. et al. Resistance exercise as a countermeasure to disuse-induced bone loss. J. Appl. Physiol. 97, 119–129 (2004).

    CAS  PubMed  Google Scholar 

  130. Barer, A. S., Kozlovskaia, I. B., Tikhomirov, E. P., Sinigin, V. M. & Letkova, L. I. Effect of loading suit 'Penguin' on human metabolism during movements [Russian]. Aviakosmicheskaia Ekol. Meditsina Aerosp. Environ. Med. 32, 4–8 (1998).

    CAS  Google Scholar 

  131. Sologubov, E. G., Iavorskii, A. B. & Kobrin, V. I. The significance of visual analyzer in controlling the standing posture in individuals with the spastic form of child cerebral paralysis while wearing 'Adel' suit [Russian]. Aviakosmicheskaia Ekol. Meditsina Aerosp. Environ. Med. 30, 8–13 (1996).

    CAS  Google Scholar 

  132. Yamashita-Goto, K. et al. Maximal and submaximal forces of slow fibers in human soleus after bed rest. J. Appl. Physiol. 91, 417–424 (2001).

    CAS  PubMed  Google Scholar 

  133. Carvil, P. A., Attias, J., Evetts, S. N., Waldie, J. M. & Green, D. A. The effect of the gravity loading countermeasure skinsuit upon movement and strength. J. Strength Cond. Res. 31, 154–161 (2017).

    PubMed  Google Scholar 

  134. Hamilton, D. R. et al. Cardiac and vascular responses to thigh cuffs and respiratory maneuvers on crewmembers of the International Space Station. J. Appl. Physiol. 112, 454–462 (2012).

    PubMed  Google Scholar 

  135. Smith, S. M. et al. Evaluation of treadmill exercise in a lower body negative pressure chamber as a countermeasure for weightlessness-induced bone loss: a bed rest study with identical twins. J. Bone Miner. Res. 18, 2223–2230 (2003).

    PubMed  Google Scholar 

  136. Smith, S. M. et al. Effects of artificial gravity during bed rest on bone metabolism in humans. J. Appl. Physiol. 107, 47–53 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  137. Iwase, S. et al. Effect of centrifuge-induced artificial gravity and ergometric exercise on cardiovascular deconditioning, myatrophy, and osteoporosis induced by a -6 degrees head-down bedrest. J. Gravitat. Physiol. 11, 243–244 (2004).

    Google Scholar 

  138. Rittweger, J. et al. Short-arm centrifugation as a partially effective musculoskeletal countermeasure during 5-day head-down tilt bed rest—results from the BRAG1 study. Eur. J. Appl. Physiol. 115, 1233–1244 (2015).

    PubMed  Google Scholar 

  139. Naumann, F. L., Bennell, K. L. & Wark, J. D. The effects of +Gz force on the bone mineral density of fighter pilots. Aviat. Space Environ. Med. 72, 177–181 (2001).

    CAS  PubMed  Google Scholar 

  140. Naumann, F. L., Grant, M. C. & Dhaliwal, S. S. Changes in cervical spine bone mineral density in response to flight training. Aviat. Space Environ. Med. 75, 255–259 (2004).

    CAS  PubMed  Google Scholar 

  141. Vico, L., Barou, O., Laroche, N., Alexandre, C. & Lafage-Proust, M. H. Effects of centrifuging at 2 g on rat long bone metaphyses. Eur. J. Appl. Physiol. 80, 360–366 (1999).

    CAS  Google Scholar 

  142. Canciani, B. et al. Effects of long time exposure to simulated micro- and hypergravity on skeletal architecture. J. Mech. Behav. Biomed. Mater. 51, 1–12 (2015).

    PubMed  Google Scholar 

  143. Gnyubkin, V. et al. Effects of chronic hypergravity: from adaptive to deleterious responses in growing mouse skeleton. J. Appl. Physiol. 119, 908–917 (2015).

    CAS  PubMed  Google Scholar 

  144. Ikawa, T. et al. Hypergravity suppresses bone resorption in ovariectomized rats. Adv. Space Res. 47, 1214–1224 (2011).

    CAS  Google Scholar 

  145. Spengler, D. M., Morey, E. R., Carter, D. R., Turner, R. T. & Baylink, D. J. Effects of spaceflight on structural and material strength of growing bone. Proc. Soc. Exp. Biol. Med. 174, 224–228 (1983).

    CAS  PubMed  Google Scholar 

  146. Turner, R. T. et al. Spaceflight results in formation of defective bone. Proc. Soc. Exp. Biol. Med. 180, 544–549 (1985).

    CAS  PubMed  Google Scholar 

  147. Zhang, L.-F. & Hargens, A. R. Spaceflight-induced intracranial hypertension and visual impairment: pathophysiology and countermeasures. Physiol. Rev. 98, 59–87 (2018).

    PubMed  Google Scholar 

  148. Heer, M., De Santo, N. G., Cirillo, M. & Drummer, C. Body mass changes, energy, and protein metabolism in space. Am. J. Kidney Dis. 38, 691–695 (2001).

    CAS  PubMed  Google Scholar 

  149. Heer, M. et al. Effects of high-protein intake on bone turnover in long-term bed rest in women. Appl. Physiol. Nutr. Metab. 42, 537–546 (2017).

    CAS  PubMed  Google Scholar 

  150. Heer, M. et al. Nutrient supply during recent European missions. Pflugers Arch. 441, R8–R14 (2000).

    CAS  PubMed  Google Scholar 

  151. Bloomfield, S. A., Martinez, D. A., Boudreaux, R. D. & Mantri, A. V. Microgravity stress: bone and connective tissue. Compr. Physiol. 6, 645–686 (2016).

    PubMed  Google Scholar 

  152. Varsavsky, M. et al. Recommended vitamin D levels in the general population. Endocrinol. Diabetes Nutr. 64 (Suppl. 1), 7–14 (2017).

    PubMed  Google Scholar 

  153. Schneider, V. S. & McDonald, J. Skeletal calcium homeostasis and countermeasures to prevent disuse osteoporosis. Calcif. Tissue Int. 36 (Suppl. 1), S151–S144 (1984).

    PubMed  Google Scholar 

  154. Shane, E. et al. Atypical subtrochanteric and diaphyseal femoral fractures: second report of a task force of the American Society for Bone and Mineral Research. J. Bone Miner. Res. 29, 1–23 (2014).

    PubMed  Google Scholar 

  155. Fantasia, J. E. The role of antiangiogenic therapy in the development of osteonecrosis of the jaw. Oral Maxillofac. Surg. Clin. N. Am. 27, 547–553 (2015).

    Google Scholar 

  156. Poubel, V. L. do N., Silva, C. A. B., Mezzomo, L. A. M., De Luca Canto, G. & Rivero, E. R. C. The risk of osteonecrosis on alveolar healing after tooth extraction and systemic administration of antiresorptive drugs in rodents: a systematic review. J. Craniomaxillofac. Surg. 46, 245–256 (2018).

    PubMed  Google Scholar 

  157. Wood, J. et al. Novel antiangiogenic effects of the bisphosphonate compound zoledronic acid. J. Pharmacol. Exp. Ther. 302, 1055–1061 (2002).

    CAS  PubMed  Google Scholar 

  158. Macias, B. R. et al. Simulated resistance training, but not alendronate, increases cortical bone formation and suppresses sclerostin during disuse. J. Appl. Physiol. 112, 918–925 (2012).

    CAS  PubMed  Google Scholar 

  159. Eastell, R. et al. Postmenopausal osteoporosis. Nat. Rev. Dis. Primers 2, 16069 (2016).

    PubMed  Google Scholar 

  160. Tella, S. H., Kommalapati, A. & Correa, R. Profile of abaloparatide and its potential in the treatment of postmenopausal osteoporosis. Cureus 9, e1300 (2017).

    PubMed  PubMed Central  Google Scholar 

  161. Ferrari, S. L. Osteoporosis: Romosozumab to rebuild the foundations of bone strength. Nat. Rev. Rheumatol. 14, 128 (2018).

    PubMed  Google Scholar 

  162. Weivoda, M. M., Youssef, S. J. & Oursler, M. J. Sclerostin expression and functions beyond the osteocyte. Bone 96, 45–50 (2017).

    CAS  PubMed  Google Scholar 

  163. Spatz, J. M. et al. Sclerostin antibody inhibits skeletal deterioration in mice exposed to partial weight-bearing. Life Sci. Space Res. 12, 32–38 (2017).

    CAS  Google Scholar 

  164. Mehta, P. & Bhayani, D. Impact of space environment on stability of medicines:challenges and prospects. J. Pharm. Biomed. Anal. 136, 111–119 (2017).

    CAS  PubMed  Google Scholar 

  165. Wood, S. J., Loehr, J. A. & Guilliams, M. E. Sensorimotor reconditioning during and after spaceflight. NeuroRehabilitation 29, 185–195 (2011).

    CAS  PubMed  Google Scholar 

  166. Sibonga, J. D. et al. Recovery of spaceflight-induced bone loss: bone mineral density after long-duration missions as fitted with an exponential function. Bone 41, 973–978 (2007).

    CAS  PubMed  Google Scholar 

  167. Ozcivici, E. & Judex, S. Trabecular bone recovers from mechanical unloading primarily by restoring its mechanical function rather than its morphology. Bone 67, 122–129 (2014).

    PubMed  Google Scholar 

  168. Shanbhogue, V. V., Brixen, K. & Hansen, S. Age- and sex-related changes in bone microarchitecture and estimated strength: a three-year prospective study using HRpQCT. J. Bone Miner. Res. 31, 1541–1549 (2016).

    PubMed  Google Scholar 

  169. Schneider, V. et al. Bone and body mass changes during space flight. Acta Astronaut. 36, 463–466 (1995).

    CAS  PubMed  Google Scholar 

  170. Leblanc, A. D., Schneider, V. S., Evans, H. J., Engelbretson, D. A. & Krebs, J. M. Bone mineral loss and recovery after 17 weeks of bed rest. J. Bone Miner. Res. 5, 843–850 (1990).

    CAS  PubMed  Google Scholar 

  171. Uebelhart, D. et al. Modifications of bone and connective tissue after orthostatic bedrest. Osteoporos. Int. 11, 59–67 (2000).

    CAS  PubMed  Google Scholar 

  172. Shirazi-Fard, Y. et al. Previous exposure to simulated microgravity does not exacerbate bone loss during subsequent exposure in the proximal tibia of adult rats. Bone 56, 461–473 (2013).

    PubMed  Google Scholar 

  173. Shirazi-Fard, Y. et al. Moderate intensity resistive exercise improves metaphyseal cancellous bone recovery following an initial disuse period, but does not mitigate decrements during a subsequent disuse period in adult rats. Bone 66, 296–305 (2014).

    PubMed  Google Scholar 

  174. Allen, M. R., Hogan, H. A. & Bloomfield, S. A. Differential bone and muscle recovery following hindlimb unloading in skeletally mature male rats. J. Musculoskelet. Neuronal Interact. 6, 217–225 (2006).

    CAS  PubMed  Google Scholar 

  175. Manske, S. L. et al. Extending rest between unloading cycles does not enhance bone's long-term recovery. Med. Sci. Sports Exerc. 47, 2191–2200 (2015).

    PubMed  Google Scholar 

  176. Tse, K. Y., Macias, B. R., Meyer, R. S. & Hargens, A. R. Heritability of bone density: regional and gender differences in monozygotic twins. J. Orthop. Res. 27, 150–154 (2009).

    PubMed  Google Scholar 

  177. Sabik, O. L. & Farber, C. R. Using GWAS to identify novel therapeutic targets for osteoporosis. Transl Res. J. Lab. Clin. Med. 181, 15–26 (2017).

    CAS  Google Scholar 

  178. García, A. et al. Post-ISS plans: what should be done? REACH Rev. Hum. Space Explor. 1, 63–73 (2016).

    Google Scholar 

  179. Maalouf, M., Durante, M. & Foray, N. Biological effects of space radiation on human cells: history, advances and outcomes. J. Radiat. Res. 52, 126–146 (2011).

    PubMed  Google Scholar 

  180. Ingber, D. E., Wang, N. & Stamenovic, D. Tensegrity, cellular biophysics, and the mechanics of living systems. Rep. Prog. Phys. Phys. Soc. G. B. 77, 046603 (2014).

    Google Scholar 

  181. Ulrich, D., van Rietbergen, B., Laib, A. & Rüegsegger, P. The ability of three-dimensional structural indices to reflect mechanical aspects of trabecular bone. Bone 25, 55–60 (1999).

    CAS  PubMed  Google Scholar 

  182. Johnston, S. L., Campbell, M. R., Scheuring, R. & Feiveson, A. H. Risk of herniated nucleus pulposus among U.S. astronauts. Aviat. Space Environ. Med. 81, 566–574 (2010).

    PubMed  Google Scholar 

  183. Tian, Y. et al. The impact of oxidative stress on the bone system in response to the space special environment. Int. J. Mol. Sci. 18, E2132 (2017).

    PubMed  Google Scholar 

  184. Kondo, H. et al. Total-body irradiation of postpubertal mice with (137)Cs acutely compromises the microarchitecture of cancellous bone and increases osteoclasts. Radiat. Res. 171, 283–289 (2009).

    CAS  PubMed  Google Scholar 

  185. Willey, J. S. et al. Early increase in osteoclast number in mice after whole-body irradiation with 2 Gy X rays. Radiat. Res. 170, 388–392 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  186. Alwood, J. S. et al. Ionizing radiation stimulates expression of pro-osteoclastogenic genes in marrow and skeletal tissue. J. Interferon Cytokine Res. 35, 480–487 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  187. Yumoto, K. et al. Short-term effects of whole-body exposure to (56)Fe ions in combination with musculoskeletal disuse on bone cells. Radiat. Res. 173, 494–504 (2010).

    CAS  PubMed  Google Scholar 

  188. Alwood, J. S. et al. Heavy ion irradiation and unloading effects on mouse lumbar vertebral microarchitecture, mechanical properties and tissue stresses. Bone 47, 248–255 (2010).

    CAS  PubMed  Google Scholar 

  189. Macias, B. R. et al. Simulating the lunar environment: partial weightbearing and high-LET radiation-induce bone loss and increase sclerostin-positive osteocytes. Radiat. Res. 186, 254–263 (2016).

    CAS  PubMed  Google Scholar 

  190. Yu, K. et al. Mimicking the effects of spaceflight on bone: Combined effects of disuse and chronic low-dose rate radiation exposure on bone mass in mice. Life Sci. Space Res. 15, 62–68 (2017).

    Google Scholar 

  191. Alwood, J. S. et al. Dose- and ion-dependent effects in the oxidative stress response to space-like radiation exposure in the skeletal system. Int. J. Mol. Sci. 18, E2117 (2017).

    PubMed  Google Scholar 

Download references

Acknowledgements

The work of L.V. is supported in part by the Centre National d'Etudes Spatiales (CNES) and by the European Space Agency (ESA). The work of A.H. is supported in part by NASA (National Aeronautics and Space Administration), grant numbers NNX14AP25G, NNX13AM89G and NNX13AJ12G.

Author information

Authors and Affiliations

  1. INSERM, U1059 Sainbiose, Université de Lyon–Université Jean Monnet, Faculté de Médecine, Campus Santé Innovation, Saint-Étienne, France

    Laurence Vico

  2. Department of Orthopaedic Surgery, University of California, San Diego, La Jolla, CA, USA

    Alan Hargens

Authors
  1. Laurence Vico
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alan Hargens
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Both authors researched the data for the article, provided substantial contributions to discussions of its content, wrote the article and reviewed and/or edited the manuscript before submission.

Corresponding author

Correspondence to Laurence Vico.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary information S1 (table)

Duration of spaceflight and variations in animal conditions of experiments used to understand the effects of spaceflight on bone. (PDF 389 kb)

PowerPoint slides

Glossary

Countermeasures

Interventions designed to protect the health of crewmembers during spaceflights.

Strain energy

The energy stored by a system undergoing deformation; when the applied force is released, the whole system returns to its original shape.

Ground reaction force

The force supplied by the ground in reaction to the force the body exerts on the ground; an important external force exerted on the body.

T-score

The number of standard deviations above or below the mean for a healthy 30-year-old adult of the same sex and ethnicity as the patient.

Areal bone mineral density

A measure of the bone mineral content (as measured by dual-energy X-ray absorptiometry) divided by the bone size, given as g/cm2.

Resistive exercise device

A device that enables exercise for all of the major muscle groups, focusing on squats, dead lifts and calf raises.

Volumetric bone mineral density

A measure of the bone mineral content (as measured by quantitative CT) divided by the bone volume, given as g/cm3.

Ultimate load

The maximum load the bone can bear before fracture.

Head-down tilt (HDT) bed rest

A physiological human analogue for weightlessness that mimics fluid shift and decreases bodily movements and power, in which healthy volunteers are in a bed with a 4–6 degree head-down tilt, usually for periods of several days to two months.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Vico, L., Hargens, A. Skeletal changes during and after spaceflight. Nat Rev Rheumatol 14, 229–245 (2018). https://doi.org/10.1038/nrrheum.2018.37

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrrheum.2018.37

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing