Net change in periosteal strain during stance shift loading after surgery correlates to rapid de novo bone generation in critically sized defects

Annals of Biomedical Engineering

Volumn 39, Issue 5, 2011, Pages 1570-1581

  McBride, Sarah H ^a   Dolejs, Scott ^a   Brianza, Stefano ^b   Knothe, Ulf ^c   Knothe Tate, Melissa L ^a  

^a CASE WESTERN RESERVE UNIVERSITY   (United States)

^b AO FOUNDATION   (Switzerland)

^c LERNER RESEARCH INSTITUTE   (United States)

Author keywords

Endogenous tissue engineering; Mechanical loading; Mechanics; Mechanobiology; Periosteum; Progenitor cells

Indexed keywords

ENDOGENOUS TISSUE ENGINEERING; MECHANICAL LOADING; MECHANO-BIOLOGY; PERIOSTEUM; PROGENITOR CELLS;

ANIMALS; DEFECTS; LOADING; MECHANICS; STRAIN; SURGERY; TISSUE ENGINEERING;

BONE;

ANIMAL; ARTICLE; BONE DEVELOPMENT; BONE REGENERATION; FEMUR; INJURY; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PERIOSTEUM; SHEEP; WEIGHT BEARING;

ANIMALS; BONE REGENERATION; FEMUR; OSTEOGENESIS; PERIOSTEUM; SHEEP; WEIGHT-BEARING;

EID: 79954449018     PISSN: 00906964     EISSN: 15739686     Source Type: Journal    
DOI: 10.1007/s10439-010-0242-9     Document Type: Article

References (48)

1. D Alexander F Schäfer A Munz B Friedrich C Klein J Hoffmann H Buhring S Reinert 2009 LNGFR induction during osteogenesis of human jaw periosteum-derived cells Cell. Physiol. Biochem. 24 283 290 19710543 10.1159/000233253 1:CAS:528:DC%2BD1MXpsVaks7k%3D
2. MR Allen DB Burr 2005 Human femoral neck has less cellular periosteum, and more mineralized periosteum, than femoral diaphyseal bone Bone 36 311 316 15780957 10.1016/j.bone.2004.10.013 (Pubitemid 40283588)
3. MR Allen JM Hock DB Burr 2004 Periosteum: biology, regulation, and response to osteoporosis therapies Bone 35 1003 1012 15542024 10.1016/j.bone.2004.07.014 1:CAS:528:DC%2BD2cXpslOqt78%3D (Pubitemid 39487345)
4. EJ Anderson ML Knothe Tate 2007 Design of tissue engineering scaffolds as delivery devices for mechanical and mechanically modulated signals Tissue Eng. 13 2525 2538 17822359 10.1089/ten.2006.0443 1:CAS:528:DC%2BD2sXhtFSntbrL (Pubitemid 47577317)
5. EJ Arnsdorf LM Jones DR Carter CR Jacobs 2009 The periosteum as a cellular source for functional tissue engineering Tissue Eng. Part A 15 2637 2642 19207046 10.1089/ten.tea.2008.0244 1:CAS:528:DC%2BD1MXhtVKjs7nI
6. H Chang J Zimmermann ML Knothe Tate 2010 Mechanical adaptation of embryonic stem cells Trans. Orthop. Res. Soc. 35 0722
7. C Colnot 2009 Skeletal cell fate decisions within periosteum and bone marrow during bone regeneration J. Bone Miner. Res. 24 274 282 18847330 10.1359/jbmr.081003
8. N Datta QP Pham U Sharma VI Sikavitsas JA Jansen AG Mikos 2006 In vitro generated extracellular matrix and fluid shear stress synergistically enhance 3D osteoblastic differentiation Proc. Natl Acad. Sci. USA 103 2488 2493 16477044 10.1073/pnas.0505661103 1:CAS:528:DC%2BD28XksF2rsrc%3D
9. C De Bari F Dell'Accio A Karystinou PV Guillot NM Fisk EA Jones D McGonagle IM Khan CW Archer TA Mitsiadis AN Donaldson FP Luyten C Pitzalis 2008 A biomarker-based mathematical model to predict bone-forming potency of human synovial and periosteal mesenchymal stem cells Arthritis Rheum. 58 240 250 18163504 10.1002/art.23143
10. AJ Engler S Sen HL Sweeney DE Discher 2006 Extracellular matrix elasticity directs stem cell lineage specification Cell 126 677 689 16923388 10.1016/j.cell.2006.06.044 1:CAS:528:DC%2BD28Xpt1aktbg%3D (Pubitemid 44233625)
11. O Hayashi Y Katsube M Hirose H Ohgushi H Ito 2008 Comparison of osteogenic ability of rat mesenchymal stem cells from bone marrow, periosteum, and adipose tissue Calcif. Tissue Int. 82 238 247 18305886 10.1007/s00223-008- 9112-y 1:CAS:528:DC%2BD1cXjsF2gt7c%3D
12. HL Holtorf JA Jansen AG Mikos 2005 Flow perfusion culture induces the osteoblastic differentiation of marrow stroma cell-scaffold constructs in the absence of dexamethasone J. Biomed. Mater. Res. A 72 326 334 15657936 (Pubitemid 40271003)
13. DB Jones H Nolte JG Scholübbers E Turner D Veltel 1991 Biochemical signal transduction of mechanical strain in osteoblast-like cells Biomaterials 12 101 110 1652292 10.1016/0142-9612(91)90186-E 1:STN:280:DyaK3Mzks1aqtA%3D%3D
14. T Kanno T Takahashi W Ariyoshi T Tsujisawa M Haga T Nishihara 2005 Tensile mechanical strain up-regulates Runx2 and osteogenic factor expression in human periosteal cells: implications for distraction osteogenesis J. Oral Maxillofac. Surg. 63 499 504 15789322 10.1016/j.joms.2004.07.023 (Pubitemid 40409847)
15. P Kessler L Bumiller A Schlegel T Birkholz FW Neukam J Wiltfang 2007 Dynamic periosteal elevation Br. J. Oral Maxillofac. Surg. 45 284 287 17081664 10.1016/j.bjoms.2006.09.010 (Pubitemid 46661446)
16. UR Knothe S Dolejs RM Miller ML Knothe Tate 2010 Effects of mechanical loading patterns, bone graft, and proximity to periosteum on bone defect healing J. Biomech. 43 2728 2737 20673900 10.1016/j.jbiomech.2010.06.026
17. UR Knothe DS Springfield 2005 A novel surgical procedure for bridging of massive bone defects World J. Surg. Oncol. 3 7 15691380 10.1186/1477-7819-3-7 (Pubitemid 40251739)
18. ML Knothe Tate H Chang U Knothe 2010 Role of periosteal factors in long bone defect healing Trans. Orthop. Res. Soc. 35 0384
19. ML Knothe Tate TD Falls S Mishra R Atit 2010 Engineering an ecosystem: taking cues from nature's paradigm to build tissue in the lab and the body Fields Inst. Commun. 57 113 134
20. ML Knothe Tate TD Falls SH McBride R Atit UR Knothe 2008 Mechanical modulation of osteochondroprogenitor cell fate Int. J. Biochem. Cell Biol. 40 2720 2738 18620888 10.1016/j.biocel.2008.05.011 1:CAS:528:DC%2BD1cXhtFaisb7F
21. ML Knothe Tate TF Ritzman E Schneider UR Knothe 2007 Testing of a new one-stage bone-transport surgical procedure exploiting the periosteum for the repair of long-bone defects J. Bone Joint Surg. Am. 89 307 316 17272445 10.2106/JBJS.E.00512 (Pubitemid 46214349)
22. R McBeath DM Pirone CM Nelson K Bhadriraju CS Chen 2004 Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment Dev. Cell. 6 483 495 15068789 10.1016/S1534-5807(04)00075-9 1:CAS:528:DC%2BD2cXjsFeqsbk%3D (Pubitemid 38456178)
23. McBride, S. H., S. Dolejs, U. Knothe, and M. L. Knothe Tate. Major and minor centroidal axes serve as objective, automatable reference points to test mechanobiological hypotheses using histomorphometry. J. Biomech. 2011 (in press).
24. SH McBride S Evans ML Knothe Tate 2011 The material properties of ovine femoral periosteum Trans. Orthop. Res. Soc. 36 2212
25. SH McBride T Falls ML Knothe Tate 2008 Modulation of stem cell shape and fate B: mechanical modulation of cell shape and gene expression Tissue Eng. Part A 14 1573 1580 18774911 10.1089/ten.tea.2008.0113 1:CAS:528:DC%2BD1cXhtFWlt7vK
26. SH McBride ML Knothe Tate 2008 Modulation of stem cell shape and fate A: the role of density and seeding protocol on nucleus shape and gene expression Tissue Eng. Part A 14 1561 1572 18774910 10.1089/ten.tea.2008.0112 1:CAS:528:DC%2BD1cXhtFWlt7vF
27. RM Miller SH McBride S Dolejs UR Knothe M: Knothe Tate 2011 Modeling the mechanobiology of the periosteum to predict & harness its regenerative capacity Trans. Orthop. Res. Soc. 36 0384
28. AM Ng AB Saim K Tan GH Tan SA Mokhtar IM Rose F Othman RB Idrus 2005 Comparison of bioengineered human bone construct from four sources of osteogenic cells J. Orthop. Sci. 10 192 199 15815868 10.1007/s00776-004-0884-2 (Pubitemid 40562218)
29. A Ozaki M Tsunoda S Kinoshita R Saura 2000 Role of fracture hematoma and periosteum during fracture healing in rats: interaction of fracture hematoma and the periosteum in the initial step of the healing process J. Orthop. Sci. 5 64 70 10664441 10.1007/s007760050010 1:STN:280:DC%2BD3c7jtFSltw%3D%3D (Pubitemid 30133793)
30. CL Puckett JS Hurvitz MH Metzler D Silver 1979 Bone formation by revascularized periosteal and bone grafts, compared with traditional bone grafts Plast. Reconstruct. Surg. 64 361 365 10.1097/00006534-197909000-00013 1:STN:280:DyaE1M3ksleqsQ%3D%3D (Pubitemid 9242071)
31. Rahn, B. Intra vitam straining techniques. In: Handbook of Biomaterials Evaluation, edited by A. F. von Recum. New York: MacMillan, 1986, pp. 471-487.
32. B Rahn 2003 Fluorochrome labeling of bone dynamics Eur. Cells Mater. 5 41
33. F Rehfeldt AJ Engler A Eckhardt F Ahmed DE Discher 2007 Cell responses to the mechanochemical microenvironment-implications for regenerative medicine and drug delivery Adv. Drug Deliv. Rev. 59 1329 1339 17900747 10.1016/j.addr.2007. 08.007 1:CAS:528:DC%2BD2sXhtlals7bN (Pubitemid 350088256)
34. Y Sakaguchi I Sekiya K Yagishita T Muneta 2005 Comparison of human stem cells derived from various mesenchymal tissues: superiority of synovium as a cell source Arthritis Rheum. 52 2521 2529 16052568 10.1002/art.21212 (Pubitemid 41117441)
35. K Sato N Haruyama Y Shimizu J Hara H Kawamura 2010 Osteogenesis by gradually expanding the interface between bone surface and periosteum enhanced by bone marrow stem cell administration in rabbits Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod. 110 32 40 20188608 10.1016/j.tripleo.2009.11.005
36. Sauser, B. Technology review: faster healing for severe fractures. Technical Review. http://www.technologyreview.com/biomedicine/24711/?a=f. Accessed August 31, 2010.
37. BL Schmidt L Kung C Jones N Casap 2002 Induced osteogenesis by periosteal distraction J. Oral maxillofac. Surg. 60 1170 1175 12378493 10.1053/joms.2002.34993
38. E Seeman 2007 The periosteum-a surface for all seasons Osteoporos. Int. 18 123 128 17180552 10.1007/s00198-006-0296-6 1:STN:280:DC%2BD2s%2FitVWlsA%3D%3D (Pubitemid 46090217)
39. MJ Song D Dean ML Knothe Tate 2010 In situ spatiotemporal mapping of flow fields around seeded stem cells at the subcellular length scale PLoS ONE 5 e12796 20862249 10.1371/journal.pone.0012796
40. R Spitzer C Perka K Lindenhayn H Zippel 2002 Matrix engineering for osteogenic differentiation of rabbit periosteal cells using alpha-tricalcium phosphate particles in a three-dimensional fibrin culture J. Biomed. Mater. Res. 59 690 696 11774331 10.1002/jbm.1277 1:CAS:528:DC%2BD38XksFCitw%3D%3D (Pubitemid 34044472)
41. MM Stevens RP Marini D Schaefer J Aronson R Langer VP Shastri 2005 In vivo engineering of organs: the bone bioreactor Proc. Natl Acad. Sci. USA 102 11450 12455 16055556 10.1073/pnas.0504705102 1:CAS:528:DC%2BD2MXoslKitbc%3D (Pubitemid 41153840)
42. Taylor, J. The periosteum and bone growth. In: Bone: Bone Growth, Vol. 6, edited by B. K. Hall. Boca Raton, FL: CDC Press, 1992, pp. 21-52.
43. S Tepic AR Remiger K Morikawa M Predieri SM Perren 1997 Strength recovery in fractured sheep tibia treated with a plate or an internal fixator: an experimental study with a two-year follow-up J. Orthop. Trauma 11 14 23 8990027 10.1097/00005131-199701000-00005 1:STN:280:DyaK2s7ksVajsw%3D%3D (Pubitemid 127453358)
44. L Uddströmer V Ritsilä 1978 Osteogenic capacity of periosteal grafts. A qualitative and quantitative study of membranous and tubular bone periosteum in young rabbits Scand. J. Plast. Reconstr. Surg. 12 207 214 368970 10.3109/02844317809012996 (Pubitemid 9106769)
45. K Yamauchi T Takahashi K Funaki Y Yamashita 2008 Periosteal expansion osteogenesis using highly purified beta-tricalcium phosphate blocks: a pilot study in dogs J. Periodontol. 79 999 1005 18533776 10.1902/jop.2008.070536
46. CK Yiannakopoulos AD Kanellopoulos GP Trovas IA Dontas GP Lyritis 2008 The biomechanical capacity of the periosteum in intact long bones Arch. Orthop. Trauma Surg. 128 117 120 17874324 10.1007/s00402-007-0433-5 (Pubitemid 350055551)
47. X Zhang C Xie AS Lin H Ito H Awad JR Lieberman PT Rubery EM Schwarz RJ O'Keefe RE Guldberg 2005 Periosteal progenitor cell fate in segmental cortical bone graft transplantations: implications for functional tissue engineering J. Bone Miner. Res. 20 2124 2137 16294266 10.1359/JBMR.050806 1:CAS:528: DC%2BD2MXhtlWntrbP (Pubitemid 41698776)
48. J Zimmerman ML Knothe Tate 2011 Environment-enforced conformation alters stem cell nucleus shape Trans. Orthop. Res. Soc. 36 1764