High-Resolution Visualization of the Osteocyte Lacuno-Canalicular Network Juxtaposed to the Surface of Nanotextured Titanium Implants in Human

ACS Biomaterials Science and Engineering

Volumn 1, Issue 5, 2015, Pages 305-313

  Shah, Furqan A ^a,b   Wang, Xiaoyue ^c   Thomsen, Peter ^a,b   Grandfield, Kathryn ^c   Palmquist, Anders ^a,b  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

^c MCMASTER UNIVERSITY   (Canada)

Author keywords

bone remodelling; dental implant; electron microscopy; interface; osseointegration; osteocyte

Indexed keywords

APATITE;

ARTICLE; BONE GROWTH; BONE IMPLANT INTERFACE; BONE REGENERATION; CALCIUM SIGNALING; COLLAGEN FIBRIL; ELECTRON ENERGY LOSS SPECTROSCOPY; ELECTRON MICROSCOPY; HUMAN; HUMAN CELL; OSTEOCYTE; PRIORITY JOURNAL; TITANIUM DENTAL IMPLANT; TOOTH IMPLANT;

EID: 84969242614     PISSN: None     EISSN: 23739878     Source Type: Journal    
DOI: 10.1021/ab500127y     Document Type: Article

References (48)

1. Haïat, G.; Wang, H.-L.; Brunski, J. Effects of Biomechanical Properties of the Bone-Implant Interface on Dental Implant Stability: From In Silico Approaches to the Patient's Mouth Annu. Rev. Biomed. Eng. 2014, 16, 187-213 10.1146/annurev-bioeng-071813-104854
2. Astrand, P.; Ahlqvist, J.; Gunne, J.; Nilson, H. Implant treatment of patients with edentulous jaws: a 20-year follow-up Clin. Implant Dent. Relat. Res. 2008, 10, 207-17 10.1111/j.1708-8208.2007.00081.x
3. Brånemark, R.; Berlin, Ö.; Hagberg, K.; Bergh, P.; Gunterberg, B.; Rydevik, B. A novel osseointegrated percutaneous prosthetic system for the treatment of patients with transfemoral amputation: A prospective study of 51 patients Bone Joint J. 2014, 96b, 106-13 10.1302/0301-620X.96B1.31905
4. Weiner, S.; Wagner, H. D. The Material Bone: Structure-Mechanical Function Relations Annu. Rev. Mater. Sci. 1998, 28, 271-298 10.1146/annurev.matsci.28.1.271
5. Davies, J. E.; Ajami, E.; Moineddin, R.; Mendes, V. C. The roles of different scale ranges of surface implant topography on the stability of the bone/implant interface Biomaterials 2013, 34, 3535-46 10.1016/j.biomaterials.2013.01.024
6. Dalby, M. J.; Gadegaard, N.; Tare, R.; Andar, A.; Riehle, M. O.; Herzyk, P.; Wilkinson, C. D.; Oreffo, R. O. The control of human mesenchymal cell differentiation using nanoscale symmetry and disorder Nat. Mater. 2007, 6, 997-1003 10.1038/nmat2013
7. Ballo, A.; Agheli, H.; Lausmaa, J.; Thomsen, P.; Petronis, S. Nanostructured model implants for in vivo studies: influence of well-defined nanotopography on de novo bone formation on titanium implants Int. J. Nanomed. 2011, 6, 3415-28 10.2147/IJN.S25867
8. Neve, A.; Corrado, A.; Cantatore, F. P. Osteoblast physiology in normal and pathological conditions Cell Tissue Res. 2011, 343, 289-302 10.1007/s00441-010-1086-1
9. Silver, F. H.; Freeman, J. W.; Seehra, G. P. Collagen self-assembly and the development of tendon mechanical properties J. Biomech. 2003, 36, 1529-53 10.1016/S0021-9290(03)00135-0
10. Franz-Odendaal, T. A.; Hall, B. K.; Witten, P. E. Buried alive: how osteoblasts become osteocytes Dev. Dyn. 2006, 235, 176-90 10.1002/dvdy.20603
11. Kerschnitzki, M.; Wagermaier, W.; Roschger, P.; Seto, J.; Shahar, R.; Duda, G. N.; Mundlos, S.; Fratzl, P. The organization of the osteocyte network mirrors the extracellular matrix orientation in bone J. Struct. Biol. 2011, 173, 303-11 10.1016/j.jsb.2010.11.014
12. Klein-Nulend, J.; Bakker, A. D.; Bacabac, R. G.; Vatsa, A.; Weinbaum, S. Mechanosensation and transduction in osteocytes Bone 2013, 54, 182-90 10.1016/j.bone.2012.10.013
13. Webster, D. J.; Schneider, P.; Dallas, S. L.; Müller, R. Studying osteocytes within their environment Bone 2013, 54, 285-295 10.1016/j.bone.2013.01.004
14. Bonewald, L. F. The amazing osteocyte J. Bone Miner. Res. 2011, 26, 229-238 10.1002/jbmr.320
15. Han, Y.; Cowin, S. C.; Schaffler, M. B.; Weinbaum, S. Mechanotransduction and strain amplification in osteocyte cell processes Proc. Natl. Acad. Sci. U. S. A. 2004, 101, 16689-16694 10.1073/pnas.0407429101
16. Steflik, D. E.; Hanes, P. J.; Sisk, A. L.; Parr, G. R.; Song, M. J.; Lake, F. T.; McKinney, R. V. Transmission electron microscopic and high voltage electron microscopic observations of the bone and osteocyte activity adjacent to unloaded dental implants placed in dogs J. Periodontol. 1992, 63, 443-52 10.1902/jop.1992.63.5.443
17. Steflik, D. E.; Sisk, A. L.; Parr, G. R.; Lake, F. T.; Hanes, P. J.; Berkery, D. J.; Brewer, P. Transmission electron and high-voltage electron microscopy of osteocyte cellular processes extending to the dental implant surface J. Biomed. Mater. Res. 1994, 28, 1095-107 10.1002/jbm.820280915
18. Morinaga, K.; Kido, H.; Sato, A.; Watazu, A.; Matsuura, M. Chronological Changes in the Ultrastructure of Titanium-Bone Interfaces: Analysis by Light Microscopy, Transmission Electron Microscopy, and Micro-Computed Tomography Clinical Implant Dentistry and Related Research 2009, 11, 59-68 10.1111/j.1708-8208.2008.00093.x
19. Okamatsu, K.; Kido, H.; Sato, A.; Watazu, A.; Matsuura, M. Ultrastructure of the Interface Between Titanium and Surrounding Tissue in Rat Tibiae-A Comparison Study on Titanium-Coated and -Uncoated Plastic Implants Clin. Implant Dent. Relat. Res. 2007, 9, 100-111 10.1111/j.1708-8208.2007.00032.x
20. Shah, F. A.; Nilson, B.; Brånemark, R.; Thomsen, P.; Palmquist, A. The bone-implant interface-nanoscale analysis of clinically retrieved dental implants Nanomedicine 2014, 10, 1729-37 10.1016/j.nano.2014.05.015
21. Donath, K.; Breuner, G. A method for the study of undecalcified bones and teeth with attached soft tissues. The Sage-Schliff (sawing and grinding) technique J. Oral Pathol. Med. 1982, 11, 318-26 10.1111/j.1600-0714.1982.tb00172.x
22. Palmquist, A.; Engqvist, H.; Lausmaa, J.; Thomsen, P. Commercially Available Dental Implants: Review of Their Surface Characteristics J. Biomater. Tissue Eng. 2012, 2, 112-124 10.1166/jbt.2012.1033
23. Jarmar, T.; Palmquist, A.; Brånemark, R.; Hermansson, L.; Engqvist, H.; Thomsen, P. Technique for preparation and characterization in cross-section of oral titanium implant surfaces using focused ion beam and transmission electron microscopy J. Biomed. Mater. Res., Part A 2008, 87A, 1003-1009 10.1002/jbm.a.31856
24. Kubek, D. J.; Gattone, V. H.; Allen, M. R. Methodological assessment of acid-etching for visualizing the osteocyte lacunar-canalicular networks using scanning electron microscopy Microsc. Res. Tech. 2010, 73, 182-6 10.1002/jemt.20772
25. Reznikov, N.; Shahar, R.; Weiner, S. Three-dimensional structure of human lamellar bone: the presence of two different materials and new insights into the hierarchical organization Bone 2014, 59, 93-104 10.1016/j.bone.2013.10.023
26. Shah, F. A.; Johansson, B. R.; Thomsen, P.; Palmquist, A. Ultrastructural evaluation of shrinkage artefacts induced by fixatives and embedding resins on osteocyte processes and pericellular space dimensions J. Biomed Mater. Res. A 2014, 103, 1565-1564 10.1002/jbm.a.35287
27. Busse, B.; Djonic, D.; Milovanovic, P.; Hahn, M.; Puschel, K.; Ritchie, R. O.; Djuric, M.; Amling, M. Decrease in the osteocyte lacunar density accompanied by hypermineralized lacunar occlusion reveals failure and delay of remodeling in aged human bone Aging Cell 2010, 9, 1065-75 10.1111/j.1474-9726.2010.00633.x
28. Frost, H. M. Micropetrosis J. Bone Joint Surg. 1960, 42a, 144-50
29. Bell, L. S.; Kayser, M.; Jones, C. The mineralized osteocyte: A living fossil Am. J. Phys. Anthropol. 2008, 137, 449-456 10.1002/ajpa.20886
30. Milovanovic, P.; Zimmermann, E. A.; Hahn, M.; Djonic, D.; Püschel, K.; Djuric, M.; Amling, M.; Busse, B. Osteocytic Canalicular Networks: Morphological Implications for Altered Mechanosensitivity ACS Nano 2013, 7, 7542-7551 10.1021/nn401360u
31. You, L. D.; Weinbaum, S.; Cowin, S. C.; Schaffler, M. B. Ultrastructure of the osteocyte process and its pericellular matrix Anat. Rec. 2004, 278, 505-13 10.1002/ar.a.20050
32. McNamara, L. M.; Majeska, R. J.; Weinbaum, S.; Friedrich, V.; Schaffler, M. B. Attachment of osteocyte cell processes to the bone matrix Anat. Rec. 2009, 292, 355-63 10.1002/ar.20869
33. You, L.; Cowin, S. C.; Schaffler, M. B.; Weinbaum, S. A model for strain amplification in the actin cytoskeleton of osteocytes due to fluid drag on pericellular matrix J. Biomech. 2001, 34, 1375-1386 10.1016/S0021-9290(01)00107-5
34. Lau, E.; Al-Dujaili, S.; Guenther, A.; Liu, D.; Wang, L.; You, L. Effect of low-magnitude, high-frequency vibration on osteocytes in the regulation of osteoclasts Bone 2010, 46, 1508-1515 10.1016/j.bone.2010.02.031
35. Mann, V.; Huber, C.; Kogianni, G.; Jones, D.; Noble, B. The influence of mechanical stimulation on osteocyte apoptosis and bone viability in human trabecular bone J. Musculoskel. Neuron. Interact. 2006, 6, 408-417
36. Cardoso, L.; Herman, B. C.; Verborgt, O.; Laudier, D.; Majeska, R. J.; Schaffler, M. B. Osteocyte Apoptosis Controls Activation of Intracortical Resorption in Response to Bone Fatigue J. Bone Miner. Res. 2009, 24, 597-605 10.1359/jbmr.081210
37. Davies, J. E. Understanding peri-implant endosseous healing J. Dent. Educ. 2003, 67, 932-49
38. Du, Z.; Ivanovski, S.; Hamlet, S. M.; Feng, J. Q.; Xiao, Y. The Ultrastructural Relationship Between Osteocytes and Dental Implants Following Osseointegration Clin. Implant Dent. Relat. Res. 2014, 10.1111/cid.12257
39. Boyde, A., Scanning Electron Microscope Studies of Bone. In The Biochemistry and Physiology of Bone, 2 nd ed.; Bourne, G. H., Ed.; Academic Press: New York, 1972; Vol. I.
40. Palmquist, A.; Lindberg, F.; Emanuelsson, L.; Brånemark, R.; Engqvist, H.; Thomsen, P. Morphological studies on machined implants of commercially pure titanium and titanium alloy (Ti6Al4V) in the rabbit J. Biomed. Mater. Res., Part B 2009, 91B, 309-319 10.1002/jbm.b.31404
41. Palmquist, A.; Grandfield, K.; Norlindh, B.; Mattsson, T.; Brånemark, R.; Thomsen, P. Bone-titanium oxide interface in humans revealed by transmission electron microscopy and electron tomography J. R. Soc., Interface 2012, 9, 396-400 10.1098/rsif.2011.0420
42. Palmquist, A.; Jarmar, T.; Emanuelsson, L.; Brånemark, R.; Engqvist, H.; Thomsen, P. Forearm bone-anchored amputation prosthesis: a case study on the osseointegration Acta Orthopaedica 2008, 79, 78-85 10.1080/17453670710014806
43. Davies, J. E. Bone bonding at natural and biomaterial surfaces Biomaterials 2007, 28, 5058-5067 10.1016/j.biomaterials.2007.07.049
44. Burr, D. B.; Schaffler, M. B.; Frederickson, R. G. Composition of the cement line and its possible mechanical role as a local interface in human compact bone J. Biomech 1988, 21, 939-45 10.1016/0021-9290(88)90132-7
45. Skedros, J. G.; Holmes, J. L.; Vajda, E. G.; Bloebaum, R. D. Cement lines of secondary osteons in human bone are not mineral-deficient: New data in a historical perspective Anat. Rec., Part A 2005, 286A, 781-803 10.1002/ar.a.20214
46. Grandfield, K.; Gustafsson, S.; Palmquist, A. Where bone meets implant: the characterization of nano-osseointegration Nanoscale 2013, 5, 4302-8 10.1039/c3nr00826f
47. Grandfield, K.; McNally, E. A.; Palmquist, A.; Botton, G. A.; Thomsen, P.; Engqvist, H. Visualizing biointerfaces in three dimensions: electron tomography of the bone-hydroxyapatite interface J. R. Soc., Interface 2010, 7, 1497-1501 10.1098/rsif.2010.0213
48. Reznikov, N.; Shahar, R.; Weiner, S. Bone hierarchical structure in three dimensions Acta Biomater. 2014, 10, 3815-3826 10.1016/j.actbio.2014.05.024