Housing in the Animal Enclosure Module Spaceflight Hardware Increases Trabecular Bone Mass in Ground-Control Mice

Shane A Lloyd, Virginia S Ferguson, Steven J Simske, Alexander W Dunlap, Eric W Livingston, Ted A Bateman


During spaceflight, rodents are housed in specially designed cages called the Animal Enclosure Module (AEM), with gravity-independent nutrient delivery and waste management systems. Utilization of this flight hardware may affect the skeletal properties of housed animals, independent of microgravity considerations. We examined the effect of thirteen days of AEM housing on 64 day-old female C57BL/6J mice (AEM: n=12, standard vivarium enclosure: n=12). The effects of AEM housing were most pronounced in the trabecular compartment. AEM mice had 44% and 144% greater trabecular bone volume fraction and connectivity density, respectively, compared to their counterparts housed in standard rodent cages. A similar response was seen in the trabecular bone of the proximal humerus. Tibia trabecular bone formation rate (BFR) was nearly two-fold greater. Osteoclast surface at the tibia was 65% lower in AEM-housed mice versus vivarium. Surprisingly, there was an even greater 79% decrease in osteoblast surface at this same site. The effects of AEM housing on femur cortical bone were modest: there was reduced endocortical BFR and lower femur stiffness due to lower diaphysis mineralization. Overall, we have demonstrated significant effects of AEM housing on ground control mice, particularly in the trabecular bone compartment. Altered behavior and loading in this unique housing environment likely contributed to this complex response profile. Characterization of these effects is critical to elucidating the true effects of microgravity on skeletal parameters and for the proper selection of ground-based controls to spaceflight experiments.


Arnett, T. R. and B. Henderson (1998). Methods in Bone Biology. London, UK, Chapman & Hall.

Bateman, T. A., R. J. Zimmerman, et al. (1998). "Histomorphometric, physical, and mechanical effects of spaceflight and insulin-like growth factor-I on rat long bones." Bone 23(6): 527-535.

Bergwitz, C. and H. Juppner (2010). "Regulation of phosphate homeostasis by PTH, vitamin D, and FGF23." Annu Rev Med 61: 91-104.

Blottner, D., N. Serradj, et al. (2009). "Morphological, physiological and behavioural evaluation of a 'Mice in Space' housing system." J Comp Physiol B 179(4): 519-533.

Bouxsein, M. L., S. K. Boyd, et al. (2010). "Guidelines for assessment of bone microstructure in rodents using micro-computed tomography." J Bone Miner Res 25(7): 1468-1486.

Brooks, K. (1981). Spacelab Life Sciences 1: Animal Enclosure Module (AEM) Crew Training Workbook/Familiarization Manual, NASA Ames Research Center, Space Life Sciences Payloads Office.

Broz, J. J., S. J. Simske, et al. (1993). "Effects of rehydration state on the flexural properties of whole mouse long bones." J Biomech Eng 115(4A): 447-449.

Dalton, P., M. Gould, et al. (2003). "Preventing annoyance from odors in spaceflight: a method for evaluating the sensory impact of rodent housing." J Appl Physiol 95(5): 2113-2121.

Ducher, G., S. Prouteau, et al. (2004). "Cortical and trabecular bone at the forearm show different adaptation patterns in response to tennis playing." J Clin Densitom 7(4): 399-405.

Ferguson, V. L., R. A. Ayers, et al. (2003). "Bone development and age-related bone loss in male C57BL/6J mice." Bone 33(3): 387-398.

Fleming, R. H., C. C. Whitehead, et al. (1994). "Bone structure and breaking strength in laying hens housed in different husbandry systems." Br Poult Sci 35(5): 651-662.

Gluer, C. C., K. E. Scholz-Ahrens, et al. (2007). "Ibandronate treatment reverses glucocorticoid-induced loss of bone mineral density and strength in minipigs." Bone 40(3): 645-655.

Gross, T. S., J. L. Edwards, et al. (1997). "Strain gradients correlate with sites of periosteal bone formation." J Bone Miner Res 12(6): 982-988.

Gundberg, C. M., A. C. Looker, et al. (2002). "Patterns of osteocalcin and bone specific alkaline phosphatase by age, gender, and race or ethnicity." Bone 31(6): 703-708.

Halloran, B. P., V. L. Ferguson, et al. (2002). "Changes in bone structure and mass with advancing age in the male C57BL/6J mouse." J Bone Miner Res 17(6): 1044-1050.

Knowles, T. G. and D. M. Broom (1990). "Limb bone strength and movement in laying hens from different housing systems." Vet Rec 126(15): 354-356.

Lafage-Proust, M. H., P. Collet, et al. (1998). "Space-related bone mineral redistribution and lack of bone mass recovery after reambulation in young rats." Am J Physiol 274(2 Pt 2): R324-334.

Lumachi, F., M. Ermani, et al. (2009). "Changes of bone formation markers osteocalcin and bone-specific alkaline phosphatase in postmenopausal women with osteoporosis." Ann N Y Acad Sci 1173 Suppl 1: E60-63.

Morey, E. R. and D. J. Baylink (1978). "Inhibition of bone formation during space flight." Science 201(4361): 1138-1141.

Morey-Holton, E. R., B. P. Halloran, et al. (2000). "Animal housing influences the response of bone to spaceflight in juvenile rats." J Appl Physiol 88(4): 1303-1309.

Newman, S. and S. Leeson (1998). "Effect of housing birds in cages or an aviary system on bone characteristics." Poult Sci 77(10): 1492-1496.

Parfitt, A. M., M. K. Drezner, et al. (1987). "Bone histomorphometry: standardization of nomenclature, symbols, and units. Report of the ASBMR Histomorphometry Nomenclature Committee." J Bone Miner Res 2(6): 595-610.

Rehman, Q. and N. E. Lane (2003). "Effect of glucocorticoids on bone density." Med Pediatr Oncol 41(3): 212-216.

Silversides, F. G., R. Singh, et al. (2012). "Comparison of bones of 4 strains of laying hens kept in conventional cages and floor pens." Poult Sci 91(1): 1-7.

Simske, S. J., K. M. Guerra, et al. (1992). "The physical and mechanical effects of suspension-induced osteopenia on mouse long bones." J Biomech 25(5): 489-499.

Smith, M., P. Johnson, et al. (1987). Animal enclosure module inflight test. Results of the Life Sciences DSOs Conducted Aboard the Space Shuttle 1981–1986. M. W. Bungo, T. M. Bagian, M. W. Bowman and B. M. Iovetan. Houston, TX, NASA: 75-77.

Sonnenfeld, G. (1999). "Space flight, microgravity, stress, and immune responses." Adv Space Res 23(12): 1945-1953.

Spector, M., R. T. Turner, et al. (1983). "Arrested bone formation during space flight results in a hypomineralized bone defect." The Physiologist 26(S).

Turner, R. T. (1995). "Effects of short-term spaceflight and recombinant human growth hormone (rhGH) on bone growth in young rats." Aviat Space Environ Med 66(8): 763-769.

Turner, R. T., E. R. Morey, et al. (1979). "Altered bone turnover during spaceflight." Physiologist 22(6): S73-74.

Vico, L., S. Bourrin, et al. (1993). "Histomorphometric analyses of cancellous bone from COSMOS 2044 rats." J Appl Physiol 75(5): 2203-2208.

Vico, L., D. Chappard, et al. (1988). "Trabecular bone remodeling after seven days of weightlessness exposure (BIOCOSMOS 1667)." Am J Physiol 255(2 Pt 2): R243-247.

Warner, S. E., J. E. Shea, et al. (2006). "Adaptations in cortical and trabecular bone in response to mechanical loading with and without weight bearing." Calcif Tissue Int 79(6): 395-403.

Whitehead, C. C. (2004). "Overview of bone biology in the egg-laying hen." Poult Sci 83(2): 193-199.

Wronski, T. J., M. Li, et al. (1998). "Lack of effect of spaceflight on bone mass and bone formation in group-housed rats." J Appl Physiol 85(1): 279-285.

Yagodovsky, V. S., L. A. Triftanidi, et al. (1976). "Space flight effects on skeletal bones of rats (light and electron microscopic examination)." Aviat Space Environ Med 47(7): 734-738.

Zerath, E., X. Holy, et al. (2002). "Effects of space food bar feeding on bone mass and metabolism in normal and unloaded rats." Nutr Res 22(11): 1309-1318.

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