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Cited by 127Spaceflight effects on biologyBone health and osteoporosis researchBone Metabolism and Diseases

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One-month spaceflight compromises the bone microstructure, tissue-level mechanical properties, osteocyte survival and lacunae volume in mature mice skeletons

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Gerbaix, Maude, Gnyubkin, Vasily, Farlay, Delphine, Olivier, Cécile, Ammann, Patrick, Courbon, Guillaume, Laroche, Norbert, Genthial, Rachel, Follet, Hélène, Peyrin, Françoise, Shenkman, Boris, Gauquelin-Koch, Guillemette, Vico, Laurence·2017·Scientific Reports
DOI 10.1038/s41598-017-03014-2PMC PMC5453937
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Abstract

The weightless environment during spaceflight induces site-specific bone loss. The 30-day Bion-M1 mission offered a unique opportunity to characterize the skeletal changes after spaceflight and an 8-day recovery period in mature male C57/BL6 mice. In the femur metaphysis, spaceflight decreased the trabecular bone volume (−64% vs. Habitat Control), dramatically increased the bone resorption (+140% vs. Habitat Control) and induced marrow adiposity invasion. At the diaphysis, cortical thinning associated with periosteal resorption was observed. In the Flight animal group, the osteocyte lacunae displayed a reduced volume and a more spherical shape (synchrotron radiation analyses), and empty lacunae were highly increased (+344% vs. Habitat Control). Tissue-level mechanical cortical properties (i.e., hardness and modulus) were locally decreased by spaceflight, whereas the mineral characteristics and collagen maturity were unaffected. In the vertebrae, spaceflight decreased the overall bone volume and altered the modulus in the periphery of the trabecular struts. Despite normalized osteoclastic activity and an increased osteoblast number, bone recovery was not observed 8 days after landing. In conclusion, spaceflight induces osteocyte death, which may trigger bone resorption and result in bone mass and microstructural deterioration. Moreover, osteocyte cell death, lacunae mineralization and fatty marrow, which are hallmarks of ageing, may impede tissue maintenance and repair.

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Figures

Figure 1 Effect of spacecraft housing conditions, spaceflight and recovery on (A) body mass, and (B) femur marrow adipocyte density (black arrows) in the metaphysis trabecular compartment (representative Haematoxylin/Eosin stained longitudinal sections). Data are presented as clusters of individual points (bars = median). *p < 0.017, **p < 0.003.
Figure 1 Effect of spacecraft housing conditions, spaceflight and recovery on (A) body mass, and (B) femur marrow adipocyte density (black arrows) in the metaphysis trabecular compartment (representative Haematoxylin/Eosin stained longitudinal sections). Data are presented as clusters of individual points (bars = median). *p < 0.017, **p < 0.003.CC BY · PubMed Central
Figure 2 Effects of spacecraft housing conditions, spaceflight and recovery on (A) L3 and T12 vertebrae microarchitecture parameters, (B) trabecular osteoblast surfaces (Ob.S/BS) and osteoclast surfaces (Oc.S/BS). (C) Tartrate resistant acid phosphatase staining of osteoclastic cells (black arrows). Trabecular (Tb) parameters include bone volume fraction (BV/TV), trabecular number (Tb.N), trabecular thickness (Tb.Th), and connectivity density (Conn.D). Data are presented as clusters of individual points (bars = median). *p < 0.017, **p < 0.003.
Figure 2 Effects of spacecraft housing conditions, spaceflight and recovery on (A) L3 and T12 vertebrae microarchitecture parameters, (B) trabecular osteoblast surfaces (Ob.S/BS) and osteoclast surfaces (Oc.S/BS). (C) Tartrate resistant acid phosphatase staining of osteoclastic cells (black arrows). Trabecular (Tb) parameters include bone volume fraction (BV/TV), trabecular number (Tb.N), trabecular thickness (Tb.Th), and connectivity density (Conn.D). Data are presented as clusters of individual points (bars = median). *p < 0.017, **p < 0.003.CC BY · PubMed Central
Figure 4 Effect of spacecraft housing conditions, spaceflight and recovery on (A) the femur total microarchitecture, (B) the metaphysis trabecular (Tb) microarchitecture, and (C) the cortex at mid-diaphysis. A panel thickness colour map of representative 3D reconstructions illustrates the decrease in bone mass, Tb volume and cortical (Ct) thickness induced by microgravity and after Earth recovery. (D) Tb microarchitecture parameters and (E) Ct parameters. Tb parameters include bone volume fraction (BV/TV), trabecular number (Tb.N), trabecular thickness (Tb.Th), and connectivity density (Conn.D). Ct bone parameters include Ct thickness (Ct.Th), Ct area (Ct.Ar), tissue mineral density (TMD), and marrow area (Ma.Ar). Data are presented as clusters of individual points (bars = median). *p < 0.017, **p < 0.003.
Figure 4 Effect of spacecraft housing conditions, spaceflight and recovery on (A) the femur total microarchitecture, (B) the metaphysis trabecular (Tb) microarchitecture, and (C) the cortex at mid-diaphysis. A panel thickness colour map of representative 3D reconstructions illustrates the decrease in bone mass, Tb volume and cortical (Ct) thickness induced by microgravity and after Earth recovery. (D) Tb microarchitecture parameters and (E) Ct parameters. Tb parameters include bone volume fraction (BV/TV), trabecular number (Tb.N), trabecular thickness (Tb.Th), and connectivity density (Conn.D). Ct bone parameters include Ct thickness (Ct.Th), Ct area (Ct.Ar), tissue mineral density (TMD), and marrow area (Ma.Ar). Data are presented as clusters of individual points (bars = median). *p < 0.017, **p < 0.003.CC BY · PubMed Central
Figure 3 Effects of spacecraft housing conditions, spaceflight and recovery on (A) L1 vertebra biomechanical properties. The polarized light image on the right illustrates the two regions of interest for biomechanical analyses within vertebra trabeculae (B) L2 FTIRM parameters and (C) L2 DMB. Data are presented as clusters of individual points (bars = median). *p < 0.017, **p < 0.003. (D) Representative schema of the investigated zones in femur.
Figure 3 Effects of spacecraft housing conditions, spaceflight and recovery on (A) L1 vertebra biomechanical properties. The polarized light image on the right illustrates the two regions of interest for biomechanical analyses within vertebra trabeculae (B) L2 FTIRM parameters and (C) L2 DMB. Data are presented as clusters of individual points (bars = median). *p < 0.017, **p < 0.003. (D) Representative schema of the investigated zones in femur.CC BY · PubMed Central
Figure 5 Effect of spacecraft housing conditions, spaceflight and recovery on (A) femur trabecular osteoblast surfaces (Ob.S/BS) and osteoclast surfaces (Oc.S/BS), and (B) cortical osteoclast surfaces. Tartrate resistant acid phosphatase staining of osteoclastic cells (black arrows) in the trabecular compartment (C), in the endocortical surface (Ec) and in the periosteal surface (Ps) (D). Data are presented as clusters of individual points (bars = median). p < 0.017, **p < 0.003.
Figure 5 Effect of spacecraft housing conditions, spaceflight and recovery on (A) femur trabecular osteoblast surfaces (Ob.S/BS) and osteoclast surfaces (Oc.S/BS), and (B) cortical osteoclast surfaces. Tartrate resistant acid phosphatase staining of osteoclastic cells (black arrows) in the trabecular compartment (C), in the endocortical surface (Ec) and in the periosteal surface (Ps) (D). Data are presented as clusters of individual points (bars = median). p < 0.017, **p < 0.003.CC BY · PubMed Central
Figure 6 Effects of spacecraft housing conditions, spaceflight and recovery on (A) femur cortical biomechanical properties, (B) femur cortical mineralization parameters in the lateral zone (schema in the upper right corner illustrates the regions of analysis), and (C) cortical FTIRM parameters. Data are presented as clusters of individual points (bars = median). *p < 0.017, **p < 0.003.
Figure 6 Effects of spacecraft housing conditions, spaceflight and recovery on (A) femur cortical biomechanical properties, (B) femur cortical mineralization parameters in the lateral zone (schema in the upper right corner illustrates the regions of analysis), and (C) cortical FTIRM parameters. Data are presented as clusters of individual points (bars = median). *p < 0.017, **p < 0.003.CC BY · PubMed Central
Figure 7 Effects of spacecraft housing conditions, spaceflight and recovery on osteocyte lacunae volume and shape. (A) A 3D colour map reconstruction of synchrotron radiation imaging showing total bone, total lacunae, and magnification of posterior zones in one Flight and Habitat Control mouse. (B,C) Lacunae total volume and shape (Lc.L1/Lc.L2), (D,E) lacunae mean volume and distribution, and (F) empty lacunae fraction measured by histomorphometry. Data are presented as clusters of individual points (bars = median). p < 0.017, **p < 0.003.
Figure 7 Effects of spacecraft housing conditions, spaceflight and recovery on osteocyte lacunae volume and shape. (A) A 3D colour map reconstruction of synchrotron radiation imaging showing total bone, total lacunae, and magnification of posterior zones in one Flight and Habitat Control mouse. (B,C) Lacunae total volume and shape (Lc.L1/Lc.L2), (D,E) lacunae mean volume and distribution, and (F) empty lacunae fraction measured by histomorphometry. Data are presented as clusters of individual points (bars = median). p < 0.017, **p < 0.003.CC BY · PubMed Central

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Research works printed but not linked: 1

  1. Seeman, E., John, P. B., Lawrence, G. R., T. John MartinA2-John P. Bilezikian, L. G. R. & Martin, T. J. Principles of Bone Biology (Third Edition) 1943–1972 (Academic Press, San Diego, 2008).

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Metadata

Authors
Gerbaix, M., Gnyubkin, V., Farlay, D., Olivier, C., Ammann, P., Courbon, G., Laroche, N., Genthial, R., Follet, H., Peyrin, F., Shenkman, B., Gauquelin-Koch, G., & Vico, L.
Affiliations
  • Inserm (FR)
  • Lyon 1 Université (FR)
  • University of Geneva (CH)
  • Centre National d'Études Spatiales (FR)
  • Centre National de la Recherche Scientifique (FR)
  • Russian Academy of Sciences (RU)
Corresponding author
Vico, Laurence
ORCID
Venue
Scientific Reports
Publisher
Springer Science and Business Media LLC
Published
2017-06-01
Volume
7
Issue
1
Pages
13078-13078
ISSN
2045-2322 (ISSN-L)
DOI
10.1038/s41598-017-03014-2
PMC
PMC5453937
OpenAlex
W2619099565
Cited by
127
References
54
Citations by year
2026: 11 · 2025: 15 · 2024: 8 · 2023: 11 · 2022: 16 · 2021: 19 · 2020: 19 · 2019: 16 · 2018: 10 · 2017: 1
FWCI
9.31
Type
journal article
Language
en
Update notices
erratum (2017-10-12)
Open access
Licence
Locations
  • Scientific Reports (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, other-oa)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Archive ouverte UNIGE (University of Geneva) (publishedVersion, other-oa)
  • HAL (submittedVersion, other-oa)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Archive ouverte UNIGE (University of Geneva) (submittedVersion, cc-by)
Funders
  • Agence Nationale de la Recherche (ANR-11-LABX-0063)
  • European Synchrotron Radiation Facility
  • Centre National d’Etudes Spatiales
  • Université de Lyon (ANR−11-LABX−0063)
  • LabEx PRIMES (ANR-11-LABX-0063))
  • Russian Academy of Sciences
Topics
  • Health Sciences › Medicine › Physiology (medical) › Spaceflight effects on biology
  • Health Sciences › Medicine › Orthopedics and Sports Medicine › Bone health and osteoporosis research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bone Metabolism and Diseases
Keywords
spaceflight, microgravity, bone loss, osteocyte death, osteocyte lacunae, trabecular bone volume, cortical bone thinning, bone resorption, marrow adiposity, bone mechanical properties, bone recovery, bone aging
MeSH terms
Animals, Biomechanical Phenomena, Bone and Bones, Bone Resorption, Femur, Male, Mice, Inbred C57BL, Osteocytes, Space Flight, Spine, Weightlessness, Bone Density

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