Biphasic change and disuse-mediated regression of canal network structure in cortical bone of growing rats

Bone

Volumn 41, Issue 2, 2007, Pages 239-246

  Matsumoto, T ^a   Yoshino, M ^a   Uesugi, K ^b   Tanaka, M ^a  

^a OSAKA UNIVERSITY   (Japan)

^b JAPAN SYNCHROTRON RADIATION RESEARCH INSTITUTE   (Japan)

Author keywords

Biphasic change; Canal network; Cortical bone; Monochromatic synchrotron radiation; Sciatic neurectomy

Indexed keywords

ABSORPTION; ANIMAL TISSUE; ARTICLE; BONE DENSITY; BONE GROWTH; BONE STRUCTURE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CORTICAL BONE; DIAPHYSIS; HINDLIMB; MALE; NEURECTOMY; NONHUMAN; RAT; SCIATIC NERVE; STRUCTURE ANALYSIS; TIBIA;

ANIMALS; BONE DEVELOPMENT; BONE RESORPTION; MALE; RATS; RATS, WISTAR; SYNCHROTRONS; TIBIA; TOMOGRAPHY, X-RAY COMPUTED;

EID: 34347221165     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2007.04.192     Document Type: Article

References (57)

1. Brookes M., and Revell W.J. Blood supply of bone: scientific aspects (1998), Springer-Verlag, London 108-141
2. Lieberman D.E., Pearson O.M., Polk J.D., Demes B., and Crompton A.W. Optimization of bone growth and remodeling in response to loading in tapered mammalian limbs. J Exp Biol 206 (2003) 3125-3138
3. Parfitt A.M. The two faces of growth: benefits and risks to bone integrity. Osteoporos Int 4 (1994) 382-398
4. Petrtyl M., Hert J., and Fiala P. Spatial organization of the haversian bone in man. J Biomech 29 (1996) 161-169
5. Williams B., Waddington D., Murray D.H., and Farquharson C. Bone strength during growth: influence of growth rate on cortical porosity and mineralization. Calcif Tissue Int 74 (2004) 236-245
6. Arsenault A.L. Vascular canals in bovine cortical bone studied by corrosion casting. Calcif Tissue Int 47 (1990) 320-325
7. Stout S.D., Brunsden B.S., Hildebolt C.F., Commean P.K., Smith K.E., and Tappen N.C. Computer-assisted 3D reconstruction of serial sections of cortical bone to determine the 3D structure of osteons. Calcif Tissue Int 65 (1999) 280-284
8. Cooper D.M., Turinsky A.L., Sensen C.W., and Hallgrimsson B. Quantitative 3D analysis of the canal network in cortical bone by micro-computed tomography. Anat Rec B New Anat 274 (2003) 169-179
9. Wachter N.J., Augat P., Krischak G.D., Mentzel M., Kinzl L., and Claes L. Prediction of cortical bone porosity in vitro by microcomputed tomography. Calcif Tissue Int 68 (2001) 38-42
10. Peyrin F., Salome M., Nuzzo S., Cloetens P., Laval-Jeantet A.M., and Baruchel J. Perspectives in three-dimensional analysis of bone samples using synchrotron radiation microtomography. Cell Mol Biol (Noisy-le-grand) 46 (2000) 1089-1102
11. Thurner P.J., Wyss P., Voide R., Stauber M., Stampanoni M., Sennhauser U., et al. Time-lapsed investigation of three-dimensional failure and damage accumulation in trabecular bone using synchrotron light. Bone 39 (2006) 289-299
12. Bonse U., and Busch F. X-ray computed microtomography (μCT) using synchrotron radiation (SR). Prog Biophys Mol Biol 65 (1996) 133-169
13. Nuzzo S., Peyrin F., Cloetens P., Baruchel J., and Boivin G. Quantification of the degree of mineralization of bone in three dimensions using synchrotron radiation microtomography. Med Phys 29 (2002) 2672-2681
14. Sone T., Tamada T., Jo Y., Miyoshi H., and Fukunaga M. Analysis of three-dimensional microarchitecture and degree of mineralization in bone metastases from prostate cancer using synchrotron microcomputed tomography. Bone 35 (2004) 432-438
15. Colleran P.N., Wilkerson M.K., Bloomfield S.A., Suva L.J., Turner R.T., and Delp M.D. Alterations in skeletal perfusion with simulated microgravity: a possible mechanism for bone remodeling. J Appl Physiol 89 (2000) 1046-1054
16. LeBlanc A., Marsh C., Evans H., Johnson P., Schneider V., and Jhingran S. Bone and muscle atrophy with suspension of the rat. J Appl Physiol 58 (1985) 1669-1675
17. Ito M., Ejiri S., Jinnai H., Kono J., Ikeda S., Nishida A., et al. Bone structure and mineralization demonstrated using synchrotron radiation computed tomography (SR-CT) in animal models: preliminary findings. J Bone Miner Metab 21 (2003) 287-293
18. Matsumoto T., Yoshino M., Asano T., Uesugi K., Todoh M., and Tanaka M. Monochromatic synchrotron radiation μCT reveals disuse-mediated canal network rarefaction in cortical bone of growing rat tibiae. J Appl Physiol 100 (2006) 274-280
19. Hildebrand T., and Rüegsegger P. A new method for the model-independent assessment of thickness in three-dimensional images. J Microsc (Oxford) 185 (1997) 67-75
20. Toriwaki J., and Mori K. Distance transformation and skeletonization of 3D pictures and their applications to medical images. In: Bertrand G., Imiya A., and Klette R. (Eds). Digital and image geometry (2001), Springer, Tokyo 412-428
21. Bousson V., Peyrin F., Bergot C., Hausard M., Sautet A., and Laredo J.D. Cortical bone in the human femoral neck: three-dimensional appearance and porosity using synchrotron radiation. J Bone Miner Res 19 (2004) 794-801
22. Martin-Badosa E., Amblard D., Nuzzo S., Elmoutaouakkil A., Vico L., and Peyrin F. Excised bone structures in mice: imaging at three-dimensional synchrotron radiation micro CT. Radiology 229 (2003) 921-928
23. Martin-Badosa E., Elmoutaouakkil A., Nuzzo S., Amblard D., Vico L., and Peyrin F. A method for the automatic characterization of bone architecture in 3D mice microtomographic images. Comput Med Imaging Graph 27 (2003) 447-458
24. Sissons H.A., Jowsey J., and Stewart L. The microradiographic appearance of normal bone tissue at various ages. In: Engstrom A., Cosslett V., and Pattee H. (Eds). X-ray microscopy and X-ray microanalysis (1960), Elsevier, Amsterdam 199-205
25. Barou O., Mekraldi S., Vico L., Boivin G., Alexandre C., and Lafage-Proust M.H. Relationships between trabecular bone remodeling and bone vascularization: a quantitative study. Bone 30 (2002) 604-612
26. Gerber H.P., Vu T.H., Ryan A.M., Kowalski J., Werb Z., and Ferrara N. VEGF couples hypertrophic cartilage remodeling, ossification and angiogenesis during endochondral bone formation. Nat Med 5 (1999) 623-628
27. Kirkeby O.J., and Berg-Larsen T. Regional blood flow and strontium-85 incorporation rate in the rat hindlimb skeleton. J Orthop Res 9 (1991) 862-868
28. Whiteside L.A., Simmons D.J., and Lesker P.A. Comparison of regional bone blood flow in areas with differing osteoblastic activity in the rabbit tibia. Clin Orthop Relat Res 124 (1977) 267-270
29. Brandi M.L., and Collin-Osdoby P. Vascular biology and the skeleton. J Bone Miner Res 21 (2006) 183-192
30. Parfitt A.M. The mechanism of coupling: a role for the vasculature. Bone 26 (2000) 319-323
31. Boivin G., and Meunier P.J. The degree of mineralization of bone tissue measured by computerized quantitative contact microradiography. Calcif Tissue Int 70 (2002) 503-511
32. Parfitt A.M. The physiologic and clinical significance of bone histomorphometric data. In: Recker R.R. (Ed). Bone histomorphometry: techniques and interpretation (1983), CRC Press, Boca Raton, FL 143-223
33. Wakley G.K., Baum B.L., Hannon K.S., and Turner R.T. The effects of tamoxifen on the osteopenia induced by sciatic neurotomy in the rat: a histomorphometric study. Calcif Tissue Int 43 (1998) 383-388
34. Zeng Q.Q., Jee W.S.S., Bigornia A.E., King J.G., D'Souza S.M., Li X.J., et al. Time responses of cancellous and cortical bones to sciatic neurectomy in growing female rats. Bone 19 (1996) 13-21
35. Nakamura H., Morita S., Kumei Y., Aoki K., Shimokawa H., Ohya K., et al. Effects of neurectomy and tenotomy on the bone mineral density and strength of tibiae. Acta Astronaut 49 (2001) 179-190
36. Yonezu H., Ikata T., Takata S., and Shibata A. Effects of sciatic neurectomy on the femur in growing rats: application of peripheral quantitative computed tomography and Fourier transform infrared spectroscopy. J Bone Miner Metab 17 (1999) 259-265
37. Doty S.B., Morey-Holton E.R., Durnova G.N., and Kaplansky A.S. Cosmos 1887: morphology, histochemistry, and vasculature of the growing rat tibia. FASEB J 4 (1990) 16-23
38. Fujino H., Kohzuki H., Takeda I., Kiyooka T., Miyasaka T., Mohri S., et al. Regression of capillary network in atrophied soleus muscle induced by hindlimb unweighting. J Appl Physiol 98 (2005) 1407-1413
39. Oni O.O., and Gregg P.J. The relative contribution of individual osseous circulations to diaphyseal cortical blood supply. J Orthop Trauma 4 (1990) 441-448
40. Stewart J.M., Karman C., Montgomery L.D., and McLeod K.J. Plantar vibration improves leg fluid flow in perimenopausal women. Am J Physiol 288 (2005) R623-R629
41. Judex S., and Zernicke R.F. High-impact exercise and growing bone: relation between high strain rates and enhanced bone formation. J Appl Physiol 88 (2000) 2183-2191
42. Thomas C.D., Feik S.A., and Clement J.G. Regional variation of intracortical porosity in the midshaft of the human femur: age and sex differences. J Anat 206 (2005) 115-125
43. Knothe Tate M.L. Whither flows the fluid in bone? An osteocyte's perspective. J Biomech 36 (2003) 1409-1424
44. Klein-Nulend J., Bacabac R.G., and Mullender M.G. Mechanobiology of bone tissue. Pathol Biol 53 (2005) 576-580
45. Klein-Nulend J., Nijweide P.J., and Burger E.H. Osteocyte and bone structure. Curr Osteoporos Rep 1 (2003) 5-10
46. Rubin J., Rubin C., and Jacobs C.R. Molecular pathways mediating mechanical signaling in bone. Gene 367 (2006) 1-16
47. Carano R.A., and Filvaroff E.H. Angiogenesis and bone repair. Drug Discov Today 8 (2003) 980-989
48. 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
49. Bakker A., Klein-Nulend J., and Burger E. Shear stress inhibits while disuse promotes osteocyte apoptosis. Biochem Biophys Res Commun 320 (2004) 1163-1168
50. Noble B.S., Peet N., Stevens H.Y., Brabbs A., Mosley J.R., Reilly G.C., et al. Mechanical loading: biphasic osteocyte survival and targeting of osteoclasts for bone destruction in rat cortical bone. Am J Physiol 284 (2003) C934-C943
51. Chenu C., and Marenzana M. Sympathetic nervous system and bone remodeling. Joint Bone Spine 72 (2005) 481-483
52. de Souza R.L., Pitsillides A.A., Lanyon L.E., Skerry T.M., and Chenu C. Sympathetic nervous system does not mediate the load-induced cortical new bone formation. J Bone Miner Res 20 (2005) 2159-2168
53. Kondo H., Nifuji A., Takeda S., Ezura Y., Rittling S.R., Denhardt D.T., et al. Unloading induces osteoblastic cell suppression and osteoclastic cell activation to lead to bone loss via sympathetic nervous system. J Biol Chem 280 (2005) 30192-30200
54. Suzue N., Nikawa T., Onishi Y., Yamada C., Hirasaka K., Ogawa T., et al. Ubiquitin ligase Cbl-b downregulates bone formation through suppression of IGF-I signaling in osteoblasts during denervation. J Bone Miner Res 21 (2006) 722-734
55. Chantraine A., van Ouwenaller C., Hachen H.J., and Schinas P. Intra-medullary pressure and intra-osseous phlebography in paraplegia. Paraplegia 17 (1979) 391-399
56. Kodama Y., Dimai H.P., Wergedal J., Sheng M., Malpe R., Kutilek S., et al. Cortical tibial bone volume in two strains of mice: effects of sciatic neurectomy and genetic regulation of bone response to mechanical loading. Bone 25 (1999) 183-190
57. Takeuchi A., Uesugi K., Takano H., and Suzuki Y. Submicrometer-resolution three-dimensional imaging with hard x-ray imaging microtomography. Rev Sci Instrum 73 (2002) 4246-4249