Reduction in proximal femoral strength due to long-duration spaceflight
Abstract
Loss of bone mass is a well-known medical complication of long-duration spaceflight. However, we do not know how changes in bone density and geometry ultimately combine to affect the strength of the proximal femur as a whole. The goal of this study was to quantify the changes in proximal femoral strength that result from long-duration spaceflight. Pre-and post-flight CT scan-based patient-specific finite element models of the left proximal femur of 13 astronauts who spent 4.3 to 6.5 months on the International Space Station were generated. Loading conditions representing single-limb stance and a fall onto the posterolateral aspect of the greater trochanter were modeled, and proximal femoral strength (F(FE)) was computed. Mean F(FE) decreased from 18.2 times body weight (BW) pre-flight to 15.6 BW post-flight for stance loading and from 3.5 BW pre-flight to 3.1 BW post-flight for fall loading. When normalized for flight duration, F(FE) under stance and fall loading decreased at mean rates of 2.6% (0.6% to 5.0%) per month and 2.0% (0.6% to 3.9%) per month, respectively. These values are notably greater than previously reported reductions in DXA total femoral bone mineral density (0.4 to 1.8% per month). In some subjects, the magnitudes of the reductions in proximal femoral strength were comparable to estimated lifetime losses associated with aging. Although average post-flight proximal femoral strength is greater than forces expected to occur due to falls or normal activities, some subjects have small margins of safety. If proximal femoral strength is not recovered, some crew members may be at increased risk for age-related hip fractures decades after their missions.
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BMD loss is an established fracture risk factor due to bone weakening, as shown by large epidemiological studies correlating BMD with the incidence of fragility fractures.
“BMD loss is an established fracture risk factor due to bone weakening as measured in large epidemiological studies correlating BMD with the incidence of fragility fractures [2–4].”
From A human mission to Mars: Predicting the bone mineral density loss of astronauts (2020) · cites this paper as [2]
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Hip joint loading during walking and running, measured in two patients
Bergmann, G., Graichen, F., & Rohlmann, A. (1993) · Journal of Biomechanics · doi:10.1016/0021-9290(93)90058-m · Cited by 1,281 · see citing works
Khosla, S., Amin, S., & ORWOLL, E. S. (2008) · Endocrine Reviews · doi:10.1210/er.2008-0002 · Cited by 934 · see citing works
Cortical and Trabecular Bone Mineral Loss From the Spine and Hip in Long-Duration Spaceflight
Lang, T., LeBlanc, A., Evans, H., Lu, Y., Genant, H., & Yu, A. (2004) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.040307 · Cited by 828 · see citing works
Self-citationPrediction of femoral fracture load using automated finite element modeling
Keyak, J. H., Rossi, S. A., Jones, K. A., & Skinner, H. B. (1997) · Journal of Biomechanics · doi:10.1016/s0021-9290(97)00123-1 · Cited by 684 · see citing works
Self-citationBone mineral and lean tissue loss after long duration space flight.
LeBlanc, A., Schneider, V. B., Shackelford, L. C., West, S., Oganov, V. S., Bakulin, A. V., & Voronin, L. I. (2000) · PubMed · Cited by 466 · see citing works
Self-citationFemoral strength is better predicted by finite element models than QCT and DXA
CODY, D. D., Gross, G. J., Hou, F. J., Spencer, H. J., Goldstein, S. A., & Fyhrie, D. P. (1999) · Journal of Biomechanics · doi:10.1016/s0021-9290(99)00099-8 · Cited by 440 · see citing works
Prediction of strength and strain of the proximal femur by a CT-based finite element method
Bessho, M., Ohnishi, I., Matsuyama, J., Matsumoto, T., Imai, K., & Nakamura, K. (2006) · Journal of Biomechanics · doi:10.1016/j.jbiomech.2006.08.003 · Cited by 408 · see citing works
Prediction of Femoral Impact Forces in Falls on the Hip
Robinovitch, S. N., Hayes, W. C., & McMahon, T. A. (1991) · Journal of Biomechanical Engineering · doi:10.1115/1.2895414 · Cited by 319 · see citing works
Improved prediction of proximal femoral fracture load using nonlinear finite element models
Keyak, J. H. (2001) · Medical Engineering & Physics · doi:10.1016/s1350-4533(01)00045-5 · Cited by 313 · see citing works
Self-citationAdaptation of the proximal femur to skeletal reloading after long-duration spaceflight
Lang, T. F., Leblanc, A. D., Evans, H. J., & Lu, Y. (2006) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.060509 · Cited by 302 · see citing works
Self-citationPredicting Proximal Femoral Strength Using Structural Engineering Models
Keyak, J. H., Kaneko, T. S., Tehranzadeh, J., & Skinner, H. B. (2005) · Clinical Orthopaedics and Related Research · doi:10.1097/01.blo.0000164400.37905.22 · Cited by 279 · see citing works
Self-citationBiomechanics of Fracture Risk Prediction of the Hip and Spine by Quantitative Computed Tomography
Hayes, W. C., Piazza, S. J., & Zysset, P. K. (1991) · Radiologic Clinics of North America · doi:10.1016/s0033-8389(22)02675-6 · Cited by 259 · see citing works
Bouxsein, M., Szulc, P., Munoz, F., Thrall, E., Sornay‐Rendu, E., & Delmas, P. D. (2007) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.070309 · Cited by 218 · see citing works
Hip impact velocities and body configurations for voluntary falls from standing height
van den Kroonenberg, A. J., Hayes, W. C., & McMahon, T. A. (1996) · Journal of Biomechanics · doi:10.1016/0021-9290(95)00134-4 · Cited by 182 · see citing works
Kaneko, T. S., Bell, J. S., Pejcic, M. R., Tehranzadeh, J., & Keyak, J. H. (2003) · Journal of Biomechanics · doi:10.1016/j.jbiomech.2003.08.010 · Cited by 169 · see citing works
Self-citationKaneko, T. S., Pejcic, M. R., Tehranzadeh, J., & Keyak, J. H. (2003) · Medical Engineering & Physics · doi:10.1016/s1350-4533(03)00030-4 · Cited by 148 · see citing works
Self-citationEffect of force direction on femoral fracture load for two types of loading conditions
Keyak, J. H., Skinner, H. B., & Fleming, J. A. (2001) · Journal of Orthopaedic Research® · doi:10.1016/s0736-0266(00)00046-2 · Cited by 144 · see citing works
Self-citationComparison of micro-level and continuum-level voxel models of the proximal femur
Verhulp, E. E., van Rietbergen, B., & Huiskes, R. (2005) · Journal of Biomechanics · doi:10.1016/j.jbiomech.2005.10.027 · Cited by 117 · see citing works
Dynamic Models for Sideways Falls From Standing Height
van den Kroonenberg, A. J., Hayes, W. C., & McMahon, T. A. (1995) · Journal of Biomechanical Engineering · doi:10.1115/1.2794186 · Cited by 113 · see citing works
Evaluation of hip fracture risk in relation to fall direction
Nankaku, M., Kanzaki, H., Tsuboyama, T., & Nakamura, T. (2005) · Osteoporosis International · doi:10.1007/s00198-005-1843-2 · Cited by 82 · see citing works
Theoretical Implications of the Biomechanical Fracture Threshold
Keaveny, T. M., & Bouxsein, M. (2008) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.080406 · Cited by 71 · see citing works
Fast Contour Detection Algorithm for High Precision Quantitative CT
Seitz, P., & Ruegsegger, P. (1983) · IEEE Transactions on Medical Imaging · doi:10.1109/tmi.1983.4307627 · Cited by 46 · see citing works
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Smith, S. M., Heer, M. A., Shackelford, L. C., Sibonga, J. D., Ploutz-Snyder, L., & Zwart, S. R. (2012) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.1647 · Cited by 351 · see citing works
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LeBlanc, A., Matsumoto, T., Jones, J., Shapiro, J., Lang, T., Shackelford, L., Smith, S. M., Evans, H., Spector, E., Ploutz-Snyder, R., et al. (2013) · Osteoporosis International · doi:10.1007/s00198-012-2243-z · Cited by 234 · see citing works
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Zysset, P. K., Dall’Ara, E., Varga, P., & Pahr, D. H. (2013) · BoneKEy Reports · doi:10.1038/bonekey.2013.120 · Cited by 188 · see citing works
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Dall’Ara, E., Luisier, B., Schmidt, R., Kainberger, F. M., Zysset, P. K., & Pahr, D. H. (2012) · Bone · doi:10.1016/j.bone.2012.09.006 · Cited by 176 · see citing works
Keyak, J. H., Sigurdsson, S. O., Karlsdottir, G., Oskarsdóttir, D., Sigmarsdottir, A., Zhao, S., Kornak, J., Harris, T. B., Sigurdsson, G. T., Jónsson, B. Y., et al. (2011) · Bone · doi:10.1016/j.bone.2011.03.682 · Cited by 165 · see citing works
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Lang, T., Van Loon, J. J. W. A., Bloomfield, S., Vico, L., Chopard, A., Rittweger, J., Kyparos, A., Blottner, D., Vuori, I., Gerzer, R., et al. (2017) · npj Microgravity · doi:10.1038/s41526-017-0013-0 · Cited by 141 · see citing works
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Ireland, A., Maden‐Wilkinson, T., McPhee, J. S., Cooke, K., Narici, M. V., Degens, H., & Rittweger, J. (2013) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e31828f882f · Cited by 104 · see citing works
Girardi, C., Pittà, C. D., Casara, S., Sales, G., Lanfranchi, G., Celotti, L., & Mognato, M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0031293 · Cited by 100 · see citing works
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Keyak, J. H., Sigurdsson, S. O., Karlsdottir, G., Oskarsdóttir, D., Sigmarsdottir, A., Kornak, J., Harris, T. B., Sigurdsson, G. T., Jónsson, B. Y., Siggeirsdóttir, K., et al. (2013) · Bone · doi:10.1016/j.bone.2013.07.028 · Cited by 99 · see citing works
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Li, Y., Ge, C., Long, J. P., Begun, D. L., Rodriguez, J. A., Goldstein, S. A., & Franceschi, R. T. (2012) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.1574 · Cited by 91 · see citing works
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Dana Carpenter, R., LeBlanc, A. D., Evans, H., Sibonga, J. D., & Lang, T. F. (2010) · Acta Astronautica · doi:10.1016/j.actaastro.2010.01.022 · Cited by 77 · see citing works
Self-citationYang, L., Palermo, L., Black, D. M., & Eastell, R. (2014) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.2291 · Cited by 77 · see citing works
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Alwood, J. S., Yumoto, K., Mojarrab, R., Limoli, C. L., Almeida, E. A. C., Searby, N. D., & Globus, R. K. (2010) · Bone · doi:10.1016/j.bone.2010.05.004 · Cited by 70 · see citing works
Swift, J. M., Nilsson, M. I., Hogan, H. A., Sumner, L. R., & Bloomfield, S. A. (2009) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.090811 · Cited by 70 · see citing works
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Bloomfield, S. A. (2010) · Current Osteoporosis Reports · doi:10.1007/s11914-010-0013-4 · Cited by 59 · see citing works
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Morseth, B., Emaus, N., & Jørgensen, L. (2011) · Norsk Epidemiologi · doi:10.5324/nje.v20i2.1338 · Cited by 58 · see citing works
Wagner, E. B., Granzella, N. P., Saito, H., Newman, D. J., Young, L. R., & Bouxsein, M. (2010) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00014.2009 · Cited by 58 · see citing works
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Riquelme, M. A., Cardenas, E. R., Xu, H., & Jiang, J. X. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21031146 · Cited by 51 · see citing works
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Nelson, E. S., Lewandowski, B., Licata, A., & Myers, J. G. (2009) · Annals of Biomedical Engineering · doi:10.1007/s10439-009-9779-x · Cited by 50 · see citing works
Girardi, C., Pittà, C. D., Casara, S., Calura, E., Romualdi, C., Celotti, L., & Mognato, M. (2014) · BioMed Research International · doi:10.1155/2014/296747 · Cited by 50 · see citing works
Microgravity Stress: Bone and Connective Tissue
Bloomfield, S. A., Martinez, D. A., Boudreaux, R. D., & Mantri, A. V. (2016) · Comprehensive physiology · doi:10.1002/cphy.c130027 · Cited by 54 · see citing works
Bone fracture healing: perspectives according to molecular basis
Ruggieri, I. N. C., Cícero, A. M., Issa, J. P. M., & Feldman, S. (2020) · Journal of Bone and Mineral Metabolism · doi:10.1007/s00774-020-01168-0 · Cited by 50 · see citing works
Opportunistic CT screening predicts individuals at risk of major osteoporotic fracture
Michalski, A. S., Besler, B. A., Burt, L. A., & Boyd, S. K. (2021) · Osteoporosis International · doi:10.1007/s00198-021-05863-0 · Cited by 48 · see citing works
Fifteen days of microgravity causes growth in calvaria of mice
Zhang, B., Cory, E., Bhattacharya, R., Sah, R. L., & Hargens, A. R. (2013) · Bone · doi:10.1016/j.bone.2013.06.009 · Cited by 46 · see citing works
Reduction in Proximal Femoral Strength in Patients With Acute Spinal Cord Injury
Edwards, W. B., Schnitzer, T. J., & Troy, K. L. (2014) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.2227 · Cited by 46 · see citing works
Quantitative Computed Tomography
Lang, T. (2010) · Radiologic Clinics of North America · doi:10.1016/j.rcl.2010.03.001 · Cited by 44 · see citing works
Self-citationMale mice, caged in the International Space Station for 35 days, sire healthy offspring
Matsumura, T., Noda, T., Muratani, M., Okada, R., Yamane, M., Isotani, A., Kudo, T., Takahashi, S., & Ikawa, M. (2019) · Scientific Reports · doi:10.1038/s41598-019-50128-w · Cited by 43 · see citing works
Integrated Therapies for Osteoporosis and Sarcopenia: From Signaling Pathways to Clinical Trials
Girgis, C. M. (2015) · Calcified Tissue International · doi:10.1007/s00223-015-9956-x · Cited by 43 · see citing works
Konda, N. N., Karri, R. S., Winnard, A., Nasser, M., Evetts, S. E., Boudreau, E. A., Caplan, N., Gradwell, D. P., & Velho, R. (2019) · npj Microgravity · doi:10.1038/s41526-019-0073-4 · Cited by 42 · see citing works
Role of follistatin in muscle and bone alterations induced by gravity change in mice
Kawao, N., Morita, H., Obata, K., Tatsumi, K., & Kaji, H. (2017) · Journal of Cellular Physiology · doi:10.1002/jcp.25986 · Cited by 42 · see citing works
Human Response to Space Flight
Baker, E. S., Barratt, M. R., & Wear, M. L. (2008) · Principles of Clinical Medicine for Space Flight · doi:10.1007/978-0-387-68164-1_2 · Cited by 41 · see citing works
Krainski, F., Hastings, J. L., Heinicke, K., Romain, N., Pacini, E. L., Snell, P. G., Wyrick, P., Palmer, M. D., Haller, R. G., & Levine, B. D. (2014) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00803.2013 · Cited by 42 · see citing works
Redox Signaling and Its Impact on Skeletal and Vascular Responses to Spaceflight
Tahimic, C. G. T., & Globus, R. K. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18102153 · Cited by 40 · see citing works
Hu, L., Li, J., Qian, A., Wang, F., & Shang, P. (2014) · Cell Biology International · doi:10.1002/cbin.10391 · Cited by 39 · see citing works
A novel partial gravity ground-based analog for rats via quadrupedal unloading
Mortreux, M., Nagy, J. A., Ko, F. C., Bouxsein, M., & Rutkove, S. B. (2018) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01083.2017 · Cited by 39 · see citing works
Lang, T., Saeed, I., Streeper, T., Carballido‐Gamio, J., Harnish, R. J., Frassetto, L. A., Lee, S. M. C., Sibonga, J. D., Keyak, J. H., Spiering, B. A., et al. (2013) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.2155 · Cited by 37 · see citing works
Self-citationEdwards, W. B., Schnitzer, T. J., & Troy, K. L. (2013) · Bone · doi:10.1016/j.bone.2013.12.012 · Cited by 35 · see citing works
Chen, M., Wang, W., Hao, Z., & Liu, H. (2020) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2020.136972 · Cited by 35 · see citing works
Carpenter, R. D., Saeed, I., Bonaretti, S., Schreck, C., Keyak, J. H., Streeper, T., Harris, T. B., & Lang, T. (2014) · Medical Engineering & Physics · doi:10.1016/j.medengphy.2014.06.010 · Cited by 35 · see citing works
Self-citationMechanical Factors and Bone Health: Effects of Weightlessness and Neurologic Injury
Amin, S. (2010) · Current Rheumatology Reports · doi:10.1007/s11926-010-0096-z · Cited by 35 · see citing works
Transhumeral loading during advanced upper extremity activities of daily living
Drew, A. J., Izykowski, M. T., Bachus, K. N., Henninger, H. B., & Foreman, K. B. (2017) · PLoS ONE · doi:10.1371/journal.pone.0189418 · Cited by 33 · see citing works
Lau, P., Vico, L., & Rittweger, J. (2022) · Biomedicines · doi:10.3390/biomedicines10020342 · Cited by 32 · see citing works
Özçivici, E., & Judex, S. (2014) · Bone · doi:10.1016/j.bone.2014.05.009 · Cited by 31 · see citing works
Partial Weight Bearing Does Not Prevent Musculoskeletal Losses Associated with Disuse
Swift, J. M., Lima, F., Macias, B. R., Allen, M. R., Greene, E. S., Shirazi‐Fard, Y., Kupke, J. S., Hogan, H. A., & Bloomfield, S. A. (2013) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e318299c614 · Cited by 30 · see citing works
Musculoskeletal Response to Space Flight
Shackelford, L. C. (2008) · Springer eBooks · doi:10.1007/978-0-387-68164-1_14 · Cited by 30 · see citing works
Macias, B. R., Lima, F., Swift, J. M., Shirazi‐Fard, Y., Greene, E. S., Allen, M. R., Fluckey, J. D., Hogan, H. A., Braby, L. A., Wang, S., et al. (2016) · Radiation Research · doi:10.1667/rr13579.1 · Cited by 30 · see citing works
Physical Activity for Strengthening Fracture Prone Regions of the Proximal Femur
Fuchs, R. K., Kersh, M. E., Carballido‐Gamio, J., Thompson, W. R., Keyak, J. H., & Warden, S. J. (2017) · Current Osteoporosis Reports · doi:10.1007/s11914-017-0343-6 · Cited by 29 · see citing works
Self-citationDiscordant recovery of bone mass and mechanical properties during prolonged recovery from disuse
Shirazi‐Fard, Y., Kupke, J. S., Bloomfield, S. A., & Hogan, H. A. (2012) · Bone · doi:10.1016/j.bone.2012.09.021 · Cited by 29 · see citing works
Crew-Friendly Countermeasures Against Musculoskeletal Injuries in Aviation and Spaceflight
O’Conor, D. K., Dalal, S. R., Ramachandran, V., Shivers, B. L., Shender, B. S., & Jones, J. A. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.00837 · Cited by 28 · see citing works
Swift, J. M., Swift, S. N., Nilsson, M. I., Hogan, H. A., Bouse, S. D., & Bloomfield, S. A. (2011) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.407 · Cited by 27 · see citing works
Effects of Local Vibration on Bone Loss in Tail-Suspended Rats
Sun, L., Luan, H., Huang, Y., Wang, Y., & Fan, Y. (2014) · International Journal of Sports Medicine · doi:10.1055/s-0033-1358468 · Cited by 28 · see citing works
Effects of Long-Duration Spaceflight on Vertebral Strength and Risk of Spine Fracture
Burkhart, K. A., Allaire, B., Anderson, D., Lee, D. C., Keaveny, T. M., & Bouxsein, M. (2019) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.3881 · Cited by 27 · see citing works
Longitudinal time course of muscle impairments during partial weight-bearing in rats
Mortreux, M., Ko, F. C., Riveros, D., Bouxsein, M., & Rutkove, S. B. (2019) · npj Microgravity · doi:10.1038/s41526-019-0080-5 · Cited by 26 · see citing works
- Authors
- Keyak, J. H., Koyama, A. K., LeBlanc, A., Lu, Y., & Lang, T. F.
- Affiliations
- University of California, Irvine (US)
- University of California, San Francisco (US)
- Universities Space Research Association (US)
- Corresponding author
- Keyak, J.H.
- Venue
- Bone
- Publisher
- Elsevier BV
- Published
- 2009-03
- Volume
- 44
- Issue
- 3
- Pages
- 449-453
- ISSN
- 1873-2763 (ISSN-L)
- 8756-3282
- OpenAlex
- W2119818184
- Cited by
- 236
- References
- 22
- Citations by year
- 2026: 3 · 2025: 8 · 2024: 5 · 2023: 6 · 2022: 14 · 2021: 15 · 2020: 18 · 2019: 19 · 2018: 8 · 2017: 16 · 2016: 8 · 2015: 18 · 2014: 22 · 2013: 24 · 2012: 16
- FWCI
- 8.12
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Bone (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Aeronautics and Space Administration
- Topics
- Health Sciences › Medicine › Physiology › Spaceflight effects on biology
- Health Sciences › Medicine › Orthopedics and Sports Medicine › Bone health and osteoporosis research
- Physical Sciences › Engineering › Aerospace Engineering › Space Exploration and Technology
- Keywords
- long-duration spaceflight, bone loss, astronauts, International Space Station, finite element model, hip fracture risk, bone mineral density, bone geometry, safety margin, aging
- MeSH terms
- Adult, Computer Simulation, Female, Femur, Humans, Male, Middle Aged, Risk Factors, Space Flight, Time Factors, Bone Density, Weight-Bearing, Compressive Strength, Fractures, Bone
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