Implant osseointegration; Implant anchorage; Bone remodeling; Metal artifacts; In vivo micro-computed tomography
Abstract :
[en] The mechanical integrity of the bone-implant system is maintained by the process of bone remodeling. Specifically, the interplay between bone resorption and bone formation is of paramount importance to fully understand the net changes in bone structure occurring in the pen-implant bone, which are eventually responsible for the mechanical stability of the bone-implant system. Using time-lapsed in vivo micro-computed tomography combined with new composite material implants, we were able to characterize the spatio-temporal changes of bone architecture and bone remodeling following implantation in living mice. After insertion, implant stability was attained by a quick and substantial thickening of the cortical shell which counteracted the observed loss of trabecular bone, probably due to the disruption of the trabecular network. Within the trabecular compartment, the rate of bone formation close to the implant was transiently higher than far from the implant mainly due to an increased mineral apposition rate which indicated a higher osteoblastic activity. Conversely, in cortical bone, the higher rate of bone formation close to the implant compared to far away was mostly related to the recruitment of new osteoblasts as indicated by a prevailing mineralizing surface. The behavior of bone resorption also showed dissimilarities between trabecular and cortical bone. In the former, the rate of bone resorption was higher in the pen-implant region and remained elevated during the entire monitoring period. In the latter, bone resorption rate had a bigger value away from the implant and decreased with time. Our approach may help to tune the development of smart implants that can attain a better long-term stability by a local and targeted manipulation of the remodeling process within the cortical and the trabecular compartments and, particularly, in bone of poor health. (C) 2015 Elsevier Inc. All rights reserved.
Ruffoni, Davide ; Université de Liège > Département d'aérospatiale et mécanique > Mécanique des matériaux biologiques et bioinspirés
Title :
In vivo monitoring of bone architecture and remodeling after implant insertion: The different responses of cortical and trabecular bone
Publication date :
2015
Journal title :
BONE
ISSN :
8756-3282
eISSN :
1873-2763
Publisher :
Elsevier Science Inc, New York, United States - New York
Volume :
81
Pages :
468-477
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
CSC - Chinese Scholarship Council
Funding text :
IOF-SERVIER Young Investigator Research Grant; ECTS Postdoctoral Fellowship
Commentary :
The authors would like to thank Harry van Lenthe from KU Leuven and Romano Matthys from RISystem for fruitful discussions. ZL acknowledges support of the Chinese Scholarship Council and DR of the IOF-SERVIER Young Investigator Research Grant as well as of the ECTS Postdoctoral Fellowship.
Ruffoni D., Fratzl P., Roschger P., Klaushofer K., Weinkamer R. The bone mineralization density distribution as a fingerprint of the mineralization process. Bone 2007, 40:1308-1319.
Lukas C., Ruffoni D., Lambers F.M., Schulte F.A., Kuhn G., Kollmannsberger P., Weinkamer R., Müller R. Mineralization kinetics in murine trabecular bone quantified by time-lapsed in vivo micro-computed tomography. Bone 2013, 56:55-60.
Schulte F.A., Ruffoni D., Lambers F.M., Christen D., Webster D.J., Kuhn G., Müller R. Local mechanical stimuli regulate bone formation and resorption in mice at the tissue level. Plos One 2013, 8.
Christen P., Ito K., Ellouz R., Boutroy S., Sornay-Rendu E., Chapurlat R.D., van Rietbergen B. Bone remodelling in humans is load-driven but not lazy. Nat. Commun. 2014, 5.
Schulte F.A., Zwahlen A., Lambers F.M., Kuhn G., Ruffoni D., Betts D., Webster D.J., Müller R. Strain-adaptive in silico modeling of bone adaptation - a computer simulation validated by in vivo micro-computed tomography data. Bone 2013, 52:485-492.
Marco F., Milena F., Gianluca G., Vittoria O. Peri-implant osteogenesis in health and osteoporosis. Micron 2005, 36:630-644.
Wang L., Ye T., Deng L., Shao J., Qi J., Zhou Q., Wei L., Qiu S. Repair of microdamage in osteonal cortical bone adjacent to bone screw. Plos One 2014, 9.
Berglundh T., Abrahamsson I., Lang N.P., Lindhe J. De novo alveolar bone formation adjacent to endosseous implants - a model study in the dog. Clin. Oral Implants Res. 2003, 14:251-262.
Palmquist A., Omar O.M., Esposito M., Lausmaa J., Thomsen P. Titanium oral implants: surface characteristics, interface biology and clinical outcome. J. R. Soc. Interface 2010, 7:S515-S527.
Degroot K. Clinical-applications of calcium-phosphate biomaterials - a review. Ceram. Int. 1993, 19:363-366.
Tresguerres I.F., Clemente C., Donado M., Gomez-Pellico L., Blanco L., Alobera M.A., Tresguerres J.A.F. Local administration of growth hormone enhances periimplant bone reaction in an osteoporotic rabbit model - an histologic, histomorphometric and densitometric study. Clin. Oral Implants Res. 2002, 13:631-636.
Wermelin K., Suska F., Tengvall P., Thomsen P., Aspenberg P. Stainless steel screws coated with bisphosphonates gave stronger fixation and more surrounding bone Histomorphometry in rats. Bone 2008, 42:365-371.
Kettenberger U., Ston J., Thein E., Procter P., Pioletti D.P. Does locally delivered Zoledronate influence pen-implant bone formation? - Spatio-temporal monitoring of bone remodeling in vivo. Biomaterials 2014, 35:9995-10006.
Sumner D.R. Long-term implant fixation and stress-shielding in total hip replacement. J. Biomech. 2015, 48:797-800.
Ruffoni D., Müller R., van Lenthe G.H. Mechanisms of reduced implant stability in osteoporotic bone. Biomech. Model. Mechanobiol. 2012, 11:313-323.
Ruffoni D., Wirth A.J., Steiner J.A., Parkinson I.H., Müller R., van Lenthe G.H. The different contributions of cortical and trabecular bone to implant anchorage in a human vertebra. Bone 2012, 50:733-738.
Lindsay R., Cosman F., Zhou H., Bostrom M.P., Shen V.W., Cruz J.D., Nieves J.W., Dempster D.W. A novel tetracycline labeling schedule for longitudinal evaluation of the short-term effects of anabolic therapy with a single iliac crest bone biopsy: early actions of teriparatide. J. Bone Miner. Res. 2006, 21:366-373.
Schulte F.A., Lambers F.M., Kuhn G., Müller R. In vivo micro-computed tomography allows direct three-dimensional quantification of both bone formation and bone resorption parameters using time-lapsed imaging. Bone 2011, 48:433-442.
Birkhold A.I., Razi H., Duda G.N., Weinkamer R., Checa S., Willie B.M. Mineralizing surface is the main target of mechanical stimulation independent of age: 3D dynamic in vivo morphometry. Bone 2014, 66:15-25.
David V., Laroche N., Boudignon B., Lafage-Proust M.H., Alexandre C., Ruegsegger P., Vico L. Noninvasive in vivo monitoring of bone architecture alterations in hindlimb-unloaded female rats using novel three-dimensional microcomputed tomography. J. Bone Miner. Res. 2003, 18:1622-1631.
Birkhold A.I., Razi H., Weinkamer R., Duda G.N., Checa S., Willie B.M. Monitoring in vivo (re)modeling: a computational approach using 4D microCT data to quantify bone surface movements. Bone 2015, 75:210-221.
Gabet Y., Müller R., Levy J., Dimarchi R., Chorev M., Bab I., Kohavi D. Parathyroid hormone 1-34 enhances titanium implant anchorage in low-density trabecular bone: a correlative micro-computed tomographic and biomechanical analysis. Bone 2006, 39:276-282.
Gabet Y., Kohavi D., Voide R., Mueller T.L., Müller R., Bab I. Endosseous implant anchorage is critically dependent on mechanostructural determinants of peri-implant bone trabeculae. J. Bone Miner. Res. 2010, 25:575-583.
Schouten C., Meijer G.J., van den Beucken J.J.J.P., Spauwen P.H.M., Jansen J.A. The quantitative assessment of peri-implant bone responses using histomorphometry and micro-computed tomography. Biomaterials 2009, 30:4539-4549.
Stadelmann V.A., Conway C.M., Boyd S.K. In vivo monitoring of bone-implant bond strength by microCT and finite element modelling. Comput. Method. Biomech. 2013, 16:993-1001.
Stoppie N., Wevers M., Naert I. Feasibility of detecting trabecular bone around percutaneous titanium implants in rabbits by in vivo microfocus computed tomography. J. Microsc. (Oxford) 2007, 228:55-61.
Riescher S., Wehner D., Schmid T., Zimmermann H., Hartmann B., Schmid C., Lehle K. Titaniumcarboxonitride layer increased biocompatibility of medical polyetherurethanes. J. Biomed. Mater. Res. B 2014, 102:141-148.
Webster D.J., Morley P.L., van Lenthe G.H., Müller R. A novel in vivo mouse model for mechanically stimulated bone adaptation - a combined experimental and computational validation study. Comput. Method. Biomech. 2008, 11:435-441.
Levchuk A., Zwahlen A., Weigt C., Lambers F.M., Badilatti S.D., Schulte F.A., Kuhn G., Muller R. The Clinical Biomechanics Award 2012-presented by the European Society of Biomechanics: large scale simulations of trabecular bone adaptation to loading and treatment. Clin. Biomech. 2014, 29:355-362.
Lambers F.M., Schulte F.A., Kuhn G., Webster D.J., Müller R. Mouse tail vertebrae adapt to cyclic mechanical loading by increasing bone formation rate and decreasing bone resorption rate as shown by time-lapsed in vivo imaging of dynamic bone morphometry. Bone 2011, 49:1340-1350.
Burghardt A.J., Kazakia G.J., Laib A., Majumdar S. Quantitative assessment of bone tissue mineralization with polychromatic micro-computed tomography. Calcif. Tissue Int. 2008, 83:129-138.
Schulte F.A., Lambers F.M., Mueller T.L., Stauber M., Müller R. Image interpolation allows accurate quantitative bone morphometry in registered micro-computed tomography scans. Comput. Method. Biomech. 2012, 1-10.
Lambers F.M., Koch K., Kuhn G., Ruffoni D., Weigt C., Schulte F.A., Müller R. Trabecular bone adapts to long-term cyclic loading by increasing stiffness and normalization of dynamic morphometric rates. Bone 2013, 55:325-334.
Bouxsein M.L., Boyd S.K., Christiansen B.A., Guldberg R.E., Jepsen K.J., Müller R. Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. J. Bone Miner. Res. 2010, 25:1468-1486.
Kohler T., Beyeler M., Webster D., Müller R. Compartmental bone morphometry in the mouse femur: reproducibility and resolution dependence of microtomographic measurements. Calcif. Tissue Int. 2005, 77:281-290.
Bernhardt R., Scharnweber D., Muller B., Thurner P., Schliephake H., Wyss P., Beckmann F., Goebbels J., Worch H. Comparison of microfocus- and synchrotron X-ray tomography for the analysis of osteointegration around Ti6Al4V implants. Eur. Cell. Mater. 2004, 7:42-51. discussion 51.
Liu S., Broucek J., Virdi A.S., Sumner D.R. Limitations of using micro-computed tomography to predict bone-implant contact and mechanical fixation. J. Microsc. 2012, 245:34-42.
Lienau J., Schmidt-Bleek K., Peters A., Haschke F., Duda G.N., Perka C., Bail H.J., Schutze N., Jakob F., Schell H. Differential regulation of blood vessel formation between standard and delayed bone healing. J. Orthop. Res. 2009, 27:1133-1140.
Irish J., Virdi A.S., Sena K., McNulty M.A., Sumner D.R. Implant placement increases bone remodeling transiently in a rat model. J. Orthop. Res. 2013, 31:800-806.
Kon T., Cho T.J., Aizawa T., Yamazaki M., Nooh N., Graves D., Gerstenfeld L.C., Einhorn T.A. Expression of osteoprotegerin, receptor activator of NF-kappa B ligand (osteoprotegerin ligand) and related proinflammatory cytokines during fracture healing. J. Bone Miner. Res. 2001, 16:1004-1014.
Raghavan M., Sahar N.D., Kohn D.H., Morris M.D. Age-specific profiles of tissue-level composition and mechanical properties in murine cortical bone. Bone 2012, 50:942-953.
Lambers F.M., Kuhn G., Weigt C., Koch K.M., Schulte F.A., Müller R. Bone adaptation to cyclic loading in murine caudal vertebrae is maintained with age and directly correlated to the local micromechanical environment. J. Biomech. 2015, 48:1179-1187.
Brouwers J.E.M., Van Rietbergen B., Huiskes R. No effects of in vivo micro-CT radiation on structural parameters and bone marrow cells in proximal tibia of Wistar rats detected after eight weekly scans. J. Orthop. Res. 2007, 25:1325-1332.
Willie B.M., Birkhold A.I., Razi H., Thiele T., Aido M., Kruck B., Schill A., Checa S., Main R.P., Duda G.N. Diminished response to in vivo mechanical loading in trabecular and not cortical bone in adulthood of female C57Bl/6 mice coincides with a reduction in deformation to load. Bone 2013, 55:335-346.
Leucht P., Kim J.B., Wazen R., Currey J.A., Nanci A., Brunski J.B., Heims J.A. Effect of mechanical stimuli on skeletal regeneration around implants. Bone 2007, 40:919-930.