Decreased bone turnover with balanced resorption and formation prevent cortical bone loss during disuse (hibernation) in grizzly bears (Ursus arctos horribilis)

Bone

Volumn 42, Issue 2, 2008, Pages 396-404

  McGee, Meghan E ^a   Maki, Aaron J ^a   Johnson, Steven E ^a   Nelson, O Lynne ^b   Robbins, Charles T ^b   Donahue, Seth W ^a  

^a Michigan Technological University   (United States)

^b WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Bone mechanics; Bone remodeling; Cortical bone; Disuse osteoporosis; Grizzly bear

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEAR; BIOMECHANICS; BONE ATROPHY; BONE MINERALIZATION; BONE REGENERATION; BONE STRENGTH; BONE STRUCTURE; BONE TURNOVER; CONTROLLED STUDY; CORTICAL BONE; FEMALE; FEMUR; HIBERNATION; MALE; NONHUMAN; OSSIFICATION; OSTEOLYSIS; POROSITY;

ANIMALS; BONE AND BONES; BONE DENSITY; BONE RESORPTION; FEMALE; HIBERNATION; MALE; OSTEOGENESIS; OSTEOPOROSIS; URSIDAE;

EID: 38049042984     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2007.10.010     Document Type: Article

References (54)

1. Takata S., and Yasui N. Disuse osteoporosis. J Med Invest 48 (2001) 147-156
2. Caillot-Augusseau A., Lafage-Proust M.H., Soler C., Pernod J., Dubois F., and Alexandre C. Bone formation and resorption biological markers in cosmonauts during and after a 180-day space flight (Euromir 95). Clin Chem 44 (1998) 578-585
3. Weinreb M., Rodan G.A., and Thompson D.D. Osteopenia in the immobilized rat hind limb is associated with increased bone resorption and decreased bone formation. Bone 10 (1989) 187-194
4. Zerwekh J.E., Ruml L.A., Gottschalk F., and Pak C.Y. The effects of twelve weeks of bed rest on bone histology, biochemical markers of bone turnover, and calcium homeostasis in eleven normal subjects. J Bone Miner Res 13 (1998) 1594-1601
5. Li C.Y., Price C., Delisser K., Nasser P., Laudier D., Clement M., et al. Long-term disuse osteoporosis seems less sensitive to bisphosphonate treatment than other osteoporosis. J Bone Miner Res 20 (2005) 117-124
6. Shackelford L.C., LeBlanc A.D., Driscoll T.B., Evans H.J., Rianon N.J., Smith S.M., et al. Resistance exercise as a countermeasure to disuse-induced bone loss. J Appl Physiol 97 (2004) 119-129
7. Vico L., Chappard D., Alexandre C., Palle S., Minaire P., Riffat G., et al. Effects of a 120 day period of bed-rest on bone mass and bone cell activities in man: attempts at countermeasure. Bone Miner 2 (1987) 383-394
8. Wronski T.J., and Morey E.R. Inhibition of cortical and trabecular bone formation in the long bones of immobilized monkeys. Clin Orthop Relat Res (1983) 269-276
9. Bain S.D., and Rubin C.T. Metabolic modulation of disuse osteopenia: endocrine-dependent site specificity of bone remodeling. J Bone Miner Res 5 (1990) 1069-1075
10. Rubin C., Gross T., Qin Y.X., Fritton S., Guilak F., and McLeod K. Differentiation of the bone-tissue remodeling response to axial and torsional loading in the turkey ulna. J Bone Joint Surg Am 78 (1996) 1523-1533
11. Lang T.F., Leblanc A.D., Evans H.J., and Lu Y. Adaptation of the proximal femur to skeletal reloading after long-duration spaceflight. J Bone Miner Res 21 (2006) 1224-1230
12. Modlesky C.M., Slade J.M., Bickel C.S., Meyer R.A., and Dudley G.A. Deteriorated geometric structure and strength of the midfemur in men with complete spinal cord injury. Bone 36 (2005) 331-339
13. Garber M.A., McDowell D.L., and Hutton W.C. Bone loss during simulated weightlessness: a biomechanical and mineralization study in the rat model. Aviat Space Environ Med 71 (2000) 586-592
14. Kaneps A.J., Stover S.M., and Lane N.E. Changes in canine cortical and cancellous bone mechanical properties following immobilization and remobilization with exercise. Bone 21 (1997) 419-423
15. Kanis J., Oden A., and Johnell O. Acute and long-term increase in fracture risk after hospitalization for stroke. Stroke 32 (2001) 702-706
16. Vestergaard P., Krogh K., Rejnmark L., and Mosekilde L. Fracture rates and risk factors for fractures in patients with spinal cord injury. Spinal Cord 36 (1998) 790-796
17. Weinreb M., Patael H., Preisler O., and Ben-Shemen S. Short-term healing kinetics of cortical and cancellous bone osteopenia induced by unloading during the reloading period in young rats. Virchows Arch 431 (1997) 449-452
18. Leblanc A.D., Schneider V.S., Evans H.J., Engelbretson D.A., and Krebs J.M. Bone mineral loss and recovery after 17 weeks of bed rest. J Bone Miner Res 5 (1990) 843-850
19. Harvey K.B., and Donahue S.W. Bending properties, porosity, and ash fraction of black bear (Ursus americanus) cortical bone are not compromised with aging despite annual periods of disuse. J Biomech 37 (2004) 1513-1520
20. Donahue S.W., McGee M.E., Harvey K.B., Vaughan M.R., and Robbins C.T. Hibernating bears as a model for preventing disuse osteoporosis. J Biomech 39 (2006) 1480-1488
21. McGee M.E., Magic K.W., Miller D.L., Maki A.J., and Donahue S.W. Black bear femoral porosity decreases and mechanical properties increase with age despite annual periods of disuse (hibernation). Eng Frac Mech 74 (2007) 1942-1952
22. McGee M.E., Miller D.L., Auger J., Black H.L., and Donahue S.W. Black bear femoral geometry and cortical porosity are not adversely affected by ageing despite annual periods of disuse (hibernation). J Anat 210 (2007) 160-169
23. Pardy C.K., Wohl G.R., Ukrainetz P.J., Sawers A., Boyd S.K., and Zernicke R.F. Maintenance of bone mass and architecture in denning black bears (Ursus americanus). J Zool Lond 263 (2004) 359-364
24. Floyd T., Nelson R.A., and Wynne G.F. Calcium and bone metabolic homeostasis in active and denning black bears (Ursus americanus). Clin Orthop 8 (1990) 301-309
25. McGee M.E., Castillo A.B., Nelson O.L., Robbins C.T., and Donahue S.W. The effects of disuse (hibernation) on trabecular architecture and mineral density in grizzly bear (Ursus arctos horribilis) femurs. 52nd annual meeting of the Orthopaedic Research Society (2006), Orthopaedic Research Society, Chicago, IL pp. Poster #1609
26. Donahue S.W., Galley S.A., Vaughan M.R., Patterson-Buckendahl P., Demers L.M., Vance J.L., et al. Parathyroid hormone may maintain bone formation in hibernating black bears (Ursus americanus) to prevent disuse osteoporosis. J Exp Biol 209 (2006) 1630-1638
27. Blanchard B.M. Size and growth patterns of the Yellowstone grizzly bear. International Conference on Bear Research and Management 7 (1987) 99-107
28. Troyer W.A., and Hensel R.J. The brown bear of Kodiak Island. U.S. Department of the Interior, Bureau of Sport Fish and Wildlife, Branch of Wildlife Refuges (1969)
29. Pearson A.M. The northern grizzly bear Ursus arctos L (report series no. 34) (1975), Canadian Wildlife Service, Ottawa
30. Schwartz C.C., Miller S.D., and Haroldson M.A. Grizzly bear. In: Feldhamer G.A., Thompson B.C., and Chapman J.A. (Eds). Wild mammals of North America: biology, management, and conservation (2003), Johns Hopkins University Press, Baltimore 556-586
31. Turner C.H., and Burr D.B. Basic biomechanical measurements of bone: a tutorial. Bone 14 (1993) 595-608
32. Hori M., Takahashi H., Konno T., Inoue J., and Haba T. A classification of in vivo bone labels after double labeling in canine bones. Bone 6 (1985) 147-154
33. Metz L.N., Martin R.B., and Turner A.S. Histomorphometric analysis of the effects of osteocyte density on osteonal morphology and remodeling. Bone 33 (2003) 753-759
34. Vajda E.G., Kneissel M., Muggenburg B., and Miller S.C. Increased intracortical bone remodeling during lactation in beagle dogs. Biol Reprod 61 (1999) 1439-1444
35. Gross T.S., and Rubin C.T. Uniformity of resorptive bone loss induced by disuse. J Orthop Res 13 (1995) 708-714
36. Jaworski Z.F., Liskova-Kiar M., and Uhthoff H.K. Effect of long-term immobilisation on the pattern of bone loss in older dogs. J Bone Joint Surg Br 62-B (1980) 104-110
37. Zerath E., Grynpas M., Holy X., Viso M., Patterson-Buckendahl P., and Marie P.J. Spaceflight affects bone formation in rhesus monkeys: a histological and cell culture study. J Appl Physiol 93 (2002) 1047-1056
38. Zerath E., Novikov V., Leblanc A., Bakulin A., Oganov V., and Grynpas M. Effects of spaceflight on bone mineralization in the rhesus monkey. J Appl Physiol 81 (1996) 194-200
39. Smith S.M., Wastney M.E., O'Brien K.O., Morukov B.V., Larina I.M., Abrams S.A., et al. Bone markers, calcium metabolism, and calcium kinetics during extended-duration space flight on the mir space station. J Bone Miner Res 20 (2005) 208-218
40. Keyak J., Koyama A., LeBlanc A., Lu Y., and Lang T. Reduction in proximal femoral strength after long-duration spaceflight. 53rd annual meeting of the Orthopaedic Research Society (2007), Orthopaedic Research Society, San Diego, CA 15
41. Lang T., LeBlanc A., Evans H., Lu Y., Genant H., and Yu A. Cortical and trabecular bone mineral loss from the spine and hip in long-duration spaceflight. J Bone Miner Res 19 (2004) 1006-1012
42. Maimoun L., Couret I., Micallef J.P., Peruchon E., Mariano-Goulart D., Rossi M., et al. Use of bone biochemical markers with dual-energy X-ray absorptiometry for early determination of bone loss in persons with spinal cord injury. Metabolism 51 (2002) 958-963
43. de Bruin E.D., Herzog R., Rozendal R.H., Michel D., and Stussi E. Estimation of geometric properties of cortical bone in spinal cord injury. Arch Phys Med Rehabil 81 (2000) 150-156
44. Harvey K.B., Drummer T.D., and Donahue S.W. The tensile strength of black bear (Ursus americanus) cortical bone is not compromised with aging despite annual periods of hibernation. J Biomech 38 (2005) 2143-2150
45. Shaw S.R., Zernicke R.F., Vailas A.C., DeLuna D., Thomason D.B., and Baldwin K.M. Mechanical, morphological and biochemical adaptations of bone and muscle to hindlimb suspension and exercise. J Biomech 20 (1987) 225-234
46. Nguyen-Yamamoto L., Rousseau L., Brossard J.H., Lepage R., Gao P., Cantor T., et al. Origin of parathyroid hormone (PTH) fragments detected by intact-PTH assays. Eur J Endocrinol 147 (2002) 123-131
47. Brossard J.H., Cloutier M., Roy L., Lepage R., Gascon-Barre M., and D'Amour P. Accumulation of a non-(1-84) molecular form of parathyroid hormone (PTH) detected by intact PTH assay in renal failure: importance in the interpretation of PTH values. J Clin Endocrinol Metab 81 (1996) 3923-3929
48. Monier-Faugere M.C., Geng Z., Mawad H., Friedler R.M., Gao P., Cantor T.L., et al. Improved assessment of bone turnover by the PTH-(1-84)/large C-PTH fragments ratio in ESRD patients. Kidney Int 60 (2001) 1460-1468
49. Divieti P., John M.R., Juppner H., and Bringhurst F.R. Human PTH-(7-84) inhibits bone resorption in vitro via actions independent of the type 1 PTH/PTHrP receptor. Endocrinology 143 (2002) 171-176
50. Nguyen-Yamamoto L., Rousseau L., Brossard J.H., Lepage R., and D'Amour P. Synthetic carboxyl-terminal fragments of parathyroid hormone (PTH) decrease ionized calcium concentration in rats by acting on a receptor different from the PTH/PTH-related peptide receptor. Endocrinology 142 (2001) 1386-1392
51. Langub M.C., Monier-Faugere M.C., Wang G., Williams J.P., Koszewski N.J., and Malluche H.H. Administration of PTH-(7-84) antagonizes the effects of PTH-(1-84) on bone in rats with moderate renal failure. Endocrinology 144 (2003) 1135-1138
52. Dufour C., Holy X., and Marie P.J. Skeletal unloading induces osteoblast apoptosis and targets alpha5beta1-PI3K-Bcl-2 signaling in rat bone. Exp Cell Res 313 (2007) 394-403
53. Aguirre J.I., Plotkin L.I., Stewart S.A., Weinstein R.S., Parfitt A.M., Manolagas S.C., et al. Osteocyte apoptosis is induced by weightlessness in mice and precedes osteoclast recruitment and bone loss. J Bone Miner Res 21 (2006) 605-615
54. McGee M.E., Galley S.A., Nelsen M.P., Tsai C.J., and Donahue S.W. Synthetic black bear (Ursus americanus) PTH 1-34 upregulates c-fos and decreases the ratio of Bax/Bcl-2 in MC-3T3 osteoblastic cells. 53rd annual meeting of the Orthopaedic Research Society (2007), Orthopaedic Research Society, San Diego, CA pp. Poster #1289