Three-dimensional cortical bone microstructure in a rat model of hypoxia-induced growth retardation

Calcified Tissue International

Volumn 88, Issue 1, 2011, Pages 54-62

  Matsumoto, Takeshi ^a   Ando, Nobuaki ^a   Tomii, Tomoko ^b   Uesugi, Kentaro ^c  

^a OSAKA UNIVERSITY   (Japan)

^b OKAYAMA UNIVERSITY   (Japan)

^c JAPAN SYNCHROTRON RADIATION RESEARCH INSTITUTE   (Japan)

Author keywords

Cortical bone; High resolution computed tomography; Hypoxia induced growth retardation; Monochromatic synchrotron radiation; Vascular canal

Indexed keywords

OSTEOCALCIN;

ANATOMICAL VARIATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; BONE DENSITY; BONE GROWTH; BONE MINERALIZATION; BONE STRUCTURE; CONTROLLED STUDY; CORTICAL BONE; GROWTH RETARDATION; HEMATOCRIT; HIGH RESOLUTION COMPUTER TOMOGRAPHY; HYPOXIA; IMAGE ANALYSIS; MALE; MICRO-COMPUTED TOMOGRAPHY; NEWBORN; NONHUMAN; OSSIFICATION; PERFUSION; PRIORITY JOURNAL; RAT; SYNCHROTRON RADIATION; THREE DIMENSIONAL IMAGING; TIBIA; VASCULARIZATION;

ANIMALS; ANIMALS, NEWBORN; ANOXIA; BONE AND BONES; BONE DENSITY; BONE DISEASES, DEVELOPMENTAL; COMPUTER SIMULATION; DISEASE MODELS, ANIMAL; GROWTH DISORDERS; IMAGING, THREE-DIMENSIONAL; MALE; RATS; RATS, SPRAGUE-DAWLEY; SYNCHROTRONS; VALIDATION STUDIES AS TOPIC; X-RAY MICROTOMOGRAPHY;

EID: 78951480514     PISSN: 0171967X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00223-010-9415-7     Document Type: Article

References (55)

1. MA Morris PJ Kelly 1980 Use of tracer microspheres to measure bone blood flow in conscious dogs Calcif Tissue Int 32 69 76 1:STN:280: DyaL3M%2FktFOlsw%3D%3D 10.1007/BF02408523 6775781
2. SA Bloomfield HA Hogan MD Delp 2002 Decreases in bone blood flow and bone material properties in aging Fischer-344 rats Clin Orthop 396 248 257 10.1097/00003086-200203000-00036 11859250
3. PJ Vanderhoef PJ Kelly JM Janes LF Peterson 1963 Growth and structure of bone distal to an arteriovenous fistula: quantitative analysis of tetracycline-induced transverse growth patterns J Bone Joint Surg Br 45 582 596 1:STN:280:DyaF2c%2FhsF2ltA%3D%3D 14058339
4. JF Griffith DK Yeung GE Antonio SY Wong TC Kwok J Woo PC Leung 2006 Vertebral marrow fat content and diffusion and perfusion indexes in women with varying bone density: MR evaluation Radiology 241 831 838 10.1148/radiol. 2413051858 17053202
5. Brookes M, Revell W (1998) Blood supply of bone: scientific aspects. Springer-Verlag, London
6. ML Brandi P Collin-Osdoby 2006 Vascular biology and the skeleton J Bone Miner Res 21 183 192 1:CAS:528:DC%2BD28Xhs1Kmurk%3D 10.1359/JBMR.050917 16418774
7. HP Gerber N Ferrara 2000 Angiogenesis and bone growth Trends Cardiovasc Med 10 223 228 1:CAS:528:DC%2BD3MXitF2kt7g%3D 10.1016/S1050-1738(00)00074-8 11282299
8. MJ Blumer S Longato H Fritsch 2008 Structure, formation and role of cartilage canals in the developing bone Ann Anat 190 305 315 10.1016/j.aanat.2008.02.004 18602255
9. C Leterrier P Constantin 1999 Early bone growth in chickens genetically selected for a high and low growth rate Growth Dev Aging 63 75 84 1:STN:280:DC%2BD3czps1Wlsg%3D%3D 10921500
10. B Williams D Waddington DH Murray C Farquharson 2004 Bone strength during growth: influence of growth rate on cortical porosity and mineralization Calcif Tissue Int 74 236 245 1:CAS:528:DC%2BD2cXjt1Slurw%3D 10.1007/s00223-002-2124-0 14517713
11. DM Cooper CD Thomas JG Clement AL Turinsky CW Sensen B Hallgrímsson 2007 Age-dependent change in the 3D structure of cortical porosity at the human femoral midshaft Bone 40 957 965 10.1016/j.bone.2006.11. 011 17223618
12. T Matsumoto M Yoshino K Uesugi M Tanaka 2007 Biphasic change and disuse-mediated regression of canal network structure in cortical bone of growing rats Bone 41 239 246 1:STN:280:DC%2BD2szpsVChuw%3D%3D 10.1016/j.bone.2007.04.192 17544983
13. CM Schnitzler JM Mesquita JM Pettifor 2009 Cortical bone development in black and white South African children: iliac crest histomorphometry Bone 44 603 611 1:STN:280:DC%2BD1M3gs1Ojug%3D%3D 10.1016/j.bone.2008.12.009 19136082
14. C Hunter EJ Clegg 1973 Changes in skeletal proportions of the rat in response to hypoxic stress J Anat 114 201 219 1:STN:280:DyaE3s3it1WksA%3D%3D 4719657
15. ML Nelson JM Cons 1975 Pituitary hormones and growth retardation in rats raised at simulated high altitude (3800 m) Environ Physiol Biochem 5 273 282 1:CAS:528:DyaE28Xnt1ajtQ%3D%3D 1193040
16. RM Alippi AC Barceló ME Río CE Bozzini 1983 Growth retardation in the early developing rat exposed to continuous hypobaric hypoxia Acta Physiol Lat Am 33 1 5 1:STN:280:DyaL2c7gtVOnsA%3D%3D 6581683
17. RE Peterson GT Wetzel 2004 Growth failure in congenital heart disease: where are we now? Curr Opin Cardiol 19 81 83 10.1097/00001573-200403000-00002 15075730
18. C Witzel N Sreeram S Coburger S Schickendantz K Brockmeier E Schoenau 2006 Outcome of muscle and bone development in congenital heart disease Eur J Pediatr 165 168 174 10.1007/s00431-005-0030-y 16320072
19. KN Vogt C Manlhiot G Van Arsdell JL Russell S Mital BW McCrindle 2007 Somatic growth in children with single ventricle physiology impact of physiologic state J Am Coll Cardiol 50 1876 1883 10.1016/j.jacc.2007.07.050 17980255
20. RG Weintraub S Menahem 1993 Growth and congenital heart disease J Paediatr Child Health 29 95 98 1:STN:280:DyaK3s3lslWrtQ%3D%3D 10.1111/j.1440-1754.1993.tb00457.x 8489807
21. GL Semenza 2007 Regulation of tissue perfusion in mammals by hypoxia-inducible factor 1 Exp Physiol 92 988 991 1:CAS:528:DC%2BD2sXhtlGgsb7K 10.1113/expphysiol.2006.036343 17720748
22. GH Fong 2008 Mechanisms of adaptive angiogenesis to tissue hypoxia Angiogenesis 11 121 140 10.1007/s10456-008-9107-3 18327686
23. K Nakanishi M Inoue E Sugawara S Sano 1997 Ischemic and reperfusion injury of cyanotic myocardium in chronic hypoxic rat model: changes in cyanotic myocardial antioxidant system J Thorac Cardiovasc Surg 114 1088 1096 1:CAS:528:DyaK1cXltVGgtA%3D%3D 10.1016/S0022-5223(97)70024-2 9434704
24. T Matsumoto M Yoshino T Asano K Uesugi M Todoh M Tanaka 2006 Monochromatic synchrotron radiation μCT reveals disuse-mediated canal network rarefaction in cortical bone of growing rat tibiae J Appl Physiol 100 274 280 10.1152/japplphysiol.00495.2005 16141381
25. F Maes A Collignon D Vandermeulen G Marchal P Suetens 1997 Multimodality image registration by maximization of mutual information IEEE Trans Med Imaging 16 187 198 1:STN:280:DyaK2s3lsF2qtQ%3D%3D 10.1109/42.563664 9101328
26. U Bonse F Busch 1996 X-ray computed microtomography (microCT) using synchrotron radiation (SR) Prog Biophys Mol Biol 65 133 169 1:STN:280: DyaK2s7otFyjtQ%3D%3D 10.1016/S0079-6107(96)00011-9 9029944
27. P Schneider M Stauber R Voide M Stampanoni LR Donahue R Müller 2007 Ultrastructural properties in cortical bone vary greatly in two inbred strains of mice as assessed by synchrotron light based micro- and nano-CT J Bone Miner Res 22 1557 1570 10.1359/jbmr.070703 17605631
28. F Peyrin 2009 Investigation of bone with synchrotron radiation imaging: from micro to nano Osteoporos Int 20 1057 1063 1:STN:280:DC%2BD1MzjtFansA%3D%3D 10.1007/s00198-009-0855-8 19340510
29. S Nuzzo F Peyrin P Cloetens J Baruchel G Boivin 2002 Quantification of the degree of mineralization of bone in three dimensions using synchrotron radiation microtomography Med Phys 29 2672 2681 10.1118/1.1513161 12462734
30. GJ Kazakia AJ Burghardt S Cheung S Majumdar 2008 Assessment of bone tissue mineralization by conventional X-ray microcomputed tomography: comparison with synchrotron radiation microcomputed tomography and ash measurements Med Phys 35 3170 3179 1:STN:280:DC%2BD1crhsVGmtA%3D%3D 10.1118/1.2924210 18697542
31. DY Moromisato MY Moromisato JA Brasel DM Cooper 1999 Effect of growth hormone therapy in mitigating hypoxia-induced and food restriction-induced growth retardation in the newborn rat Crit Care Med 27 2234 2238 1:STN:280:DC%2BD3c%2FhsVanuw%3D%3D 10.1097/00003246-199910000-00028 10548213
32. A Tarasiuk Y Segev 2007 Chronic upper airway resistive loading induces growth retardation via the GH/IGF-I axis in prepubescent rats J Appl Physiol 102 913 918 1:CAS:528:DC%2BD2sXjvFOis78%3D 10.1152/japplphysiol.00838.2006 17138834
33. JC Utting SP Robins A Brandao-Burch IR Orriss J Behar TR Arnett 2006 Hypoxia inhibits the growth, differentiation and bone-forming capacity of rat osteoblasts Exp Cell Res 312 1693 1702 1:CAS:528:DC%2BD28Xlt1Clsbg%3D 10.1016/j.yexcr.2006.02.007 16529738
34. A Bozec L Bakiri A Hoebertz R Eferl AF Schilling V Komnenovic H Scheuch M Priemel CL Stewart M Amling EF Wagner 2008 Osteoclast size is controlled by Fra-2 through LIF/LIFreceptor signaling and hypoxia Nature 454 221 225 1:CAS:528:DC%2BD1cXot1ygsrc%3D 10.1038/nature07019 18548006
35. JA Morris-Thurgood MP Frenneaux 2000 Diastolic ventricular interaction and ventricular diastolic filling Heart Fail Rev 5 307 323 1:STN:280: DC%2BD3MvltVGmuw%3D%3D 10.1023/A:1026555012135 11498644
36. SV Gurudevan PJ Malouf WR Auger TJ Waltman M Madani AB Raisinghani AN DeMaria DG Blanchard 2007 Abnormal left ventricular diastolic filling in chronic thromboembolic pulmonary hypertension: true diastolic dysfunction or left ventricular underfilling? J Am Coll Cardiol 49 1334 1339 10.1016/j.jacc.2007.01. 028 17394966
37. DH Bass LP Adams A Tregidga 1994 The effects of arterial interruption on bone growth in a rat model S Afr J Surg 32 149 152 1:STN:280: DyaK2MzitVKksw%3D%3D 7597512
38. AJ Chin P Stephens E Goldmuntz MB Leonard 2009 Serum alkaline phosphatase reflects post-Fontan hemodynamics in children Pediatr Cardiol 30 138 145 10.1007/s00246-008-9292-2 18685798
39. DC Giuliani JC Hall BS Morse 1986 Strategies of hemopoietic stress adaptation within the medullary cavity Anat Rec 216 528 533 1:STN:280: DyaL2s%2Fpsl2rsg%3D%3D 10.1002/ar.1092160410 3800000
40. C Bozzini MI Olivera P Huygens RM Alippi CE Bozzini 2009 Long-term exposure to hypobaric hypoxia in rat affects femur cross-sectional geometry and bone tissue material properties Ann Anat 191 212 217 10.1016/j.aanat.2008.11.002 19249196
41. Parfitt AM (1983) The physiologic and clinical significance of bone histomorphometric data. In: Recker RR (ed) Bone histomorphometry: techniques and interpretation. CRC Press, Boca Raton, FL, pp 143-223
42. G Boivin PJ Meunier 2002 The degree of mineralization of bone tissue measured by computerized quantitative contact microradiography Calcif Tissue Int 70 503 511 1:CAS:528:DC%2BD38XlvV2ktLo%3D 10.1007/s00223-001-2048-0 12019458
43. Jowsey J (1964) Variations in bone mineralization with age and disease. In: Frost HM (ed) Bone biodynamics. Little Brown and Company, Boston, pp 461-479
44. EF Eriksen GZ Eghbali-Fatourechi S Khosla 2007 Remodeling and vascular spaces in bone J Bone Miner Res 22 1 6 1:CAS:528:DC%2BD2sXhtVWntbw%3D 10.1359/jbmr.060910 17040170
45. Y Wang C Wan L Deng X Liu X Cao SR Gilbert ML Bouxsein MC Faugere RE Guldberg LC Gerstenfeld VH Haase RS Johnson E Schipani TL Clemens 2007 The hypoxia-inducible factor alpha pathway couples angiogenesis to osteogenesis during skeletal development J Clin Invest 117 1616 1626 1:CAS:528: DC%2BD2sXmsVWkurY%3D 10.1172/JCI31581 17549257
46. E Schipani C Maes G Carmeliet GL Semenza 2009 Regulation of osteogenesis-angiogenesis coupling by HIFs and VEGF J Bone Miner Res 24 1347 1353 1:CAS:528:DC%2BD1MXhtFaitrvL 10.1359/jbmr.090602 19558314
47. T Kiaer 1994 Bone perfusion and oxygenation. Animal experiments and clinical observations Acta Orthop Scand Suppl 257 1 41 1:STN:280: DyaK2c3ls1ahsg%3D%3D 8197867
48. G Bridgeman M Brookes 1996 Blood supply to the human femoral diaphysis in youth and senescence J Anat 188 611 621 8763478
49. I McCarthy 2006 The physiology of bone blood flow: a review J Bone Joint Surg Am 88 Suppl 3 4 9 10.2106/JBJS.F.00890 17079361
50. W Jelkmann 1992 Erythropoietin: structure, control of production, and function Physiol Rev 72 449 489 1:CAS:528:DyaK38XisVylsro%3D 1557429
51. JK Perloff 1993 Systemic complications of cyanosis in adults with congenital heart disease Cardiol Clin 11 689 699 1:STN:280: DyaK2c%2Fntl2jtA%3D%3D 8252568
52. JL Tuttle RD Nachreiner AS Bhuller KW Condict BA Connors BP Herring MC Dalsing JL Unthank 1997 Shear level influences resistance artery remodeling: wall dimensions, cell density, and eNOS expression Am J Physiol Heart Circ Physiol 273 H628 H633
53. A Koller 2006 Flow-dependent remodeling of small arteries: the stimuli and the sensors are (still) in question Circ Res 99 6 9 1:CAS:528: DC%2BD28XotVSiu7s%3D 10.1161/01.RES.0000233144.65663.23 16825584
54. JD Humphrey 2008 Mechanisms of arterial remodeling in hypertension: coupled roles of wall shear and intramural stress Hypertension 52 195 200 1:CAS:528:DC%2BD1cXosF2jsrc%3D 10.1161/HYPERTENSIONAHA.107.103440 18541735
55. JG Skedros KJ Hunt PE Hughes H Winet 2003 Ontogenetic and regional morphologic variations in the turkey ulna diaphysis: implications for functional adaptation of cortical bone Anat Rec A Discov Mol Cell Evol Biol 273 609 629 10.1002/ar.a.10073 12808646