Skip to main content
Top
Published in: Journal of NeuroEngineering and Rehabilitation 1/2018

Open Access 01-12-2018 | Review

Advancing quantitative techniques to improve understanding of the skeletal structure-function relationship

Authors: Frances T. Sheehan, Elizabeth L. Brainerd, Karen L. Troy, Sandra J. Shefelbine, Janet L. Ronsky

Published in: Journal of NeuroEngineering and Rehabilitation | Issue 1/2018

Login to get access

Abstract

Although all functional movement arises from the interplay between the neurological, skeletal, and muscular systems, it is the skeletal system that forms the basic framework for functional movement. Central to understanding human neuromuscular development, along with the genesis of musculoskeletal pathologies, is quantifying how the human skeletal system adapts and mal-adapts to its mechanical environment. Advancing this understanding is hampered by an inability to directly and non-invasively measure in vivo strains, stresses, and forces on bone. Thus, we traditionally have turned to animal models to garner such information. These models enable direct in vivo measures that are not available for human subjects, providing information in regards to both skeletal adaptation and the interplay between the skeletal and muscular systems. Recently, there has been an explosion of new imaging and modeling techniques providing non-invasive, in vivo measures and estimates of skeletal form and function that have long been missing. Combining multiple modalities and techniques has proven to be one of our most valuable resources in enhancing our understanding of the form-function relationship of the human skeletal, muscular, and neurological systems. Thus, to continue advancing our knowledge of the structural-functional relationship, validation of current tools is needed, while development is required to limit the deficiencies in these tools and develop new ones.
Literature
1.
go back to reference Nishikawa K, Biewener AA, Aerts P, Ahn AN, Chiel HJ, Daley MA, Daniel TL, Full RJ, Hale ME, Hedrick TL, et al. Neuromechanics: an integrative approach for understanding motor control. Integr Comp Biol. 2007;47:16–54.CrossRefPubMed Nishikawa K, Biewener AA, Aerts P, Ahn AN, Chiel HJ, Daley MA, Daniel TL, Full RJ, Hale ME, Hedrick TL, et al. Neuromechanics: an integrative approach for understanding motor control. Integr Comp Biol. 2007;47:16–54.CrossRefPubMed
2.
go back to reference Ko D. Cinderella’s sisters: a revisionist history of Footbinding; 2005. p. 1–332. Ko D. Cinderella’s sisters: a revisionist history of Footbinding; 2005. p. 1–332.
3.
go back to reference Tiesler V. Studing cranial vault modifications in ancient Mesoamerica. J Anthropol Sci. 2012;90:33–58.PubMed Tiesler V. Studing cranial vault modifications in ancient Mesoamerica. J Anthropol Sci. 2012;90:33–58.PubMed
4.
go back to reference Wolff J. The law of bone remodelling. Berline, New York: Springer-Verlag; 1986.CrossRef Wolff J. The law of bone remodelling. Berline, New York: Springer-Verlag; 1986.CrossRef
5.
go back to reference Reddi AH. Cell biology and biochemistry of endochondral bone development. Coll Relat Res. 1981;1:209–26.CrossRefPubMed Reddi AH. Cell biology and biochemistry of endochondral bone development. Coll Relat Res. 1981;1:209–26.CrossRefPubMed
6.
go back to reference Erdemir A, McLean S, Herzog W, van den Bogert AJ. Model-based estimation of muscle forces exerted during movements. Clin Biomech. 2007;22:131–54.CrossRef Erdemir A, McLean S, Herzog W, van den Bogert AJ. Model-based estimation of muscle forces exerted during movements. Clin Biomech. 2007;22:131–54.CrossRef
7.
go back to reference Pandy MG. Computer modeling and simulation of human movement. Annu Rev Biomed Eng. 2001;3:245–73.CrossRefPubMed Pandy MG. Computer modeling and simulation of human movement. Annu Rev Biomed Eng. 2001;3:245–73.CrossRefPubMed
8.
go back to reference Dumas R, Moissenet F, Lafon Y, Cheze L. Multi-objective optimisation for musculoskeletal modelling: application to a planar elbow model. Proc Inst Mech Eng Part H-J EngMed. 2014;228:1108–13.CrossRef Dumas R, Moissenet F, Lafon Y, Cheze L. Multi-objective optimisation for musculoskeletal modelling: application to a planar elbow model. Proc Inst Mech Eng Part H-J EngMed. 2014;228:1108–13.CrossRef
9.
go back to reference Thelen DG, Anderson FC. Using computed muscle control to generate forward dynamic simulations of human walking from experimental data. J Biomech. 2006;39:1107–15.CrossRefPubMed Thelen DG, Anderson FC. Using computed muscle control to generate forward dynamic simulations of human walking from experimental data. J Biomech. 2006;39:1107–15.CrossRefPubMed
10.
go back to reference Giorgi M, Carriero A, Shefelbine SJ, Nowlan NC. Effects of normal and abnormal loading conditions on morphogenesis of the prenatal hip joint: application to hip dysplasia. J Biomech. 2015;48:3390–7.CrossRefPubMedPubMedCentral Giorgi M, Carriero A, Shefelbine SJ, Nowlan NC. Effects of normal and abnormal loading conditions on morphogenesis of the prenatal hip joint: application to hip dysplasia. J Biomech. 2015;48:3390–7.CrossRefPubMedPubMedCentral
11.
go back to reference Shefelbine SJ, Carter DR. Mechanobiological predictions of growth front morphology in developmental hip dysplasia. J Orthop Res. 2004;22:346–52.CrossRefPubMed Shefelbine SJ, Carter DR. Mechanobiological predictions of growth front morphology in developmental hip dysplasia. J Orthop Res. 2004;22:346–52.CrossRefPubMed
12.
go back to reference Shefelbine SJ, Carter DR. Mechanobiological predictions of femoral anteversion in cerebral palsy. Ann Biomed Eng. 2004;32:297–305.CrossRefPubMed Shefelbine SJ, Carter DR. Mechanobiological predictions of femoral anteversion in cerebral palsy. Ann Biomed Eng. 2004;32:297–305.CrossRefPubMed
13.
go back to reference Carriero A, Jonkers I, Shefelbine SJ. Mechanobiological prediction of proximal femoral deformities in children with cerebral palsy. Comput Methods Biomech Biomed Engin. 2011;14:253–62.CrossRefPubMed Carriero A, Jonkers I, Shefelbine SJ. Mechanobiological prediction of proximal femoral deformities in children with cerebral palsy. Comput Methods Biomech Biomed Engin. 2011;14:253–62.CrossRefPubMed
14.
go back to reference Lenaerts G, De Groote F, Demeulenaere B, Mulier M, Van der Perre G, Spaepen A, Jonkers I. Subject-specific hip geometry affects predicted hip joint contact forces during gait. J Biomech. 2008;41:1243–52.CrossRefPubMed Lenaerts G, De Groote F, Demeulenaere B, Mulier M, Van der Perre G, Spaepen A, Jonkers I. Subject-specific hip geometry affects predicted hip joint contact forces during gait. J Biomech. 2008;41:1243–52.CrossRefPubMed
15.
go back to reference Sheehan FT, Brochard S, Behnam AJ, Alter KE. Three-dimensional humeral morphologic alterations and atrophy associated with obstetrical brachial plexus palsy. J Shoulder Elb Surg. 2014;23:708–19.CrossRef Sheehan FT, Brochard S, Behnam AJ, Alter KE. Three-dimensional humeral morphologic alterations and atrophy associated with obstetrical brachial plexus palsy. J Shoulder Elb Surg. 2014;23:708–19.CrossRef
16.
go back to reference Wesseling M, De Groote F, Bosmans L, Bartels W, Meyer C, Desloovere K, Jonkers I. Subject-specific geometrical detail rather than cost function formulation affects hip loading calculation. Comput Methods Biomech Biomed Eng. 2016;19:1475–88.CrossRef Wesseling M, De Groote F, Bosmans L, Bartels W, Meyer C, Desloovere K, Jonkers I. Subject-specific geometrical detail rather than cost function formulation affects hip loading calculation. Comput Methods Biomech Biomed Eng. 2016;19:1475–88.CrossRef
17.
go back to reference Bartels W, Demol J, Gelaude F, Jonkers I, Vander Sloten J. Computed tomography-based joint locations affect calculation of joint moments during gait when compared to scaling approaches. Comput Methods Biomech Biomed Eng. 2015;18:1238–51.CrossRef Bartels W, Demol J, Gelaude F, Jonkers I, Vander Sloten J. Computed tomography-based joint locations affect calculation of joint moments during gait when compared to scaling approaches. Comput Methods Biomech Biomed Eng. 2015;18:1238–51.CrossRef
18.
go back to reference Bosmans L, Wesseling M, Desloovere K, Molenaers G, Scheys L, Jonkers I. Hip contact force in presence of aberrant bone geometry during normal and pathological gait. J Orthop Res. 2014;32:1406–15.CrossRefPubMed Bosmans L, Wesseling M, Desloovere K, Molenaers G, Scheys L, Jonkers I. Hip contact force in presence of aberrant bone geometry during normal and pathological gait. J Orthop Res. 2014;32:1406–15.CrossRefPubMed
19.
go back to reference Yadav P, Shefelbine SJ, Gutierrez-Farewik EM. Effect of growth plate geometry and growth direction on prediction of proximal femoral morphology. J Biomech. 2016;49:1613–9.CrossRefPubMed Yadav P, Shefelbine SJ, Gutierrez-Farewik EM. Effect of growth plate geometry and growth direction on prediction of proximal femoral morphology. J Biomech. 2016;49:1613–9.CrossRefPubMed
20.
go back to reference Frost HM. Bone's mechanostat: a 2003 update. Anat Rec A Discov Mol Cell Evol Biol. 2003;275:1081–101.CrossRefPubMed Frost HM. Bone's mechanostat: a 2003 update. Anat Rec A Discov Mol Cell Evol Biol. 2003;275:1081–101.CrossRefPubMed
21.
go back to reference Karlsson MK. Physical activity, skeletal health and fractures in a long term perspective. J Musculoskelet Neuronal Interact. 2004;4:12–21.PubMed Karlsson MK. Physical activity, skeletal health and fractures in a long term perspective. J Musculoskelet Neuronal Interact. 2004;4:12–21.PubMed
22.
go back to reference Karlsson MK, Magnusson H, Karlsson C, Seeman E. The duration of exercise as a regulator of bone mass. Bone. 2001;28:128–32.CrossRefPubMed Karlsson MK, Magnusson H, Karlsson C, Seeman E. The duration of exercise as a regulator of bone mass. Bone. 2001;28:128–32.CrossRefPubMed
23.
go back to reference Kontulainen S, Sievanen H, Kannus P, Pasanen M, Vuori I. Effect of long-term impact-loading on mass, size, and estimated strength of humerus and radius of female racquet-sports players: a peripheral quantitative computed tomography study between young and old starters and controls. J Bone Miner Res. 2003;18:352–9.CrossRefPubMed Kontulainen S, Sievanen H, Kannus P, Pasanen M, Vuori I. Effect of long-term impact-loading on mass, size, and estimated strength of humerus and radius of female racquet-sports players: a peripheral quantitative computed tomography study between young and old starters and controls. J Bone Miner Res. 2003;18:352–9.CrossRefPubMed
24.
go back to reference Troy KL, Edwards WB, Bhatia VA, Bareither ML. In vivo loading model to examine bone adaptation in humans: a pilot study. J Orthop Res. 2013;31:1406–13.CrossRefPubMed Troy KL, Edwards WB, Bhatia VA, Bareither ML. In vivo loading model to examine bone adaptation in humans: a pilot study. J Orthop Res. 2013;31:1406–13.CrossRefPubMed
25.
go back to reference Bhatia VA, Edwards WB, Johnson JE, Troy KL. Short-term bone formation is greatest within high strain regions of the human distal radius: a prospective pilot study. J Biomech Eng. 2015;137:1–5. Bhatia VA, Edwards WB, Johnson JE, Troy KL. Short-term bone formation is greatest within high strain regions of the human distal radius: a prospective pilot study. J Biomech Eng. 2015;137:1–5.
26.
go back to reference Meakin LB, Price JS, Lanyon LE. The contribution of experimental in vivo models to understanding the mechanisms of adaptation to mechanical loading in bone. Front Endocrinol (Lausanne). 2014;5:154. Meakin LB, Price JS, Lanyon LE. The contribution of experimental in vivo models to understanding the mechanisms of adaptation to mechanical loading in bone. Front Endocrinol (Lausanne). 2014;5:154.
27.
go back to reference Bailey CA, Kukuljan S, Daly RM. Effects of lifetime loading history on cortical bone density and its distribution in middle-aged and older men. Bone. 2010;47:673–80.CrossRefPubMed Bailey CA, Kukuljan S, Daly RM. Effects of lifetime loading history on cortical bone density and its distribution in middle-aged and older men. Bone. 2010;47:673–80.CrossRefPubMed
28.
go back to reference Dolan SH, Williams DP, Ainsworth BE, Shaw JM. Development and reproducibility of the bone loading history questionnaire. Med Sci Sports Exerc. 2006;38:1121–31.CrossRefPubMed Dolan SH, Williams DP, Ainsworth BE, Shaw JM. Development and reproducibility of the bone loading history questionnaire. Med Sci Sports Exerc. 2006;38:1121–31.CrossRefPubMed
29.
go back to reference Kemper HC, Bakker I, Twisk JW, van Mechelen W. Validation of a physical activity questionnaire to measure the effect of mechanical strain on bone mass. Bone. 2002;30:799–804.CrossRefPubMed Kemper HC, Bakker I, Twisk JW, van Mechelen W. Validation of a physical activity questionnaire to measure the effect of mechanical strain on bone mass. Bone. 2002;30:799–804.CrossRefPubMed
30.
go back to reference Turner CH, Robling AG. Designing exercise regimens to increase bone strength. Exerc Sport Sci Rev. 2003;31:45–50.CrossRefPubMed Turner CH, Robling AG. Designing exercise regimens to increase bone strength. Exerc Sport Sci Rev. 2003;31:45–50.CrossRefPubMed
31.
go back to reference Mancuso ME, Johnson JE, Ahmed SS, Butler TA, Troy KL. Distal radius microstructure and finite element bone strain are related to site-specific mechanical loading and areal bone mineral density in premenopausal women. Bone Reports. (in press). Mancuso ME, Johnson JE, Ahmed SS, Butler TA, Troy KL. Distal radius microstructure and finite element bone strain are related to site-specific mechanical loading and areal bone mineral density in premenopausal women. Bone Reports. (in press).
32.
go back to reference Bhatia VA, Edwards WB, Troy KL. Predicting surface strains at the human distal radius during an in vivo loading task--finite element model validation and application. J Biomech. 2014;47:2759–65.CrossRefPubMedPubMedCentral Bhatia VA, Edwards WB, Troy KL. Predicting surface strains at the human distal radius during an in vivo loading task--finite element model validation and application. J Biomech. 2014;47:2759–65.CrossRefPubMedPubMedCentral
33.
go back to reference Perilli E, Parkinson IH, Reynolds KJ. Micro-CT examination of human bone: from biopsies towards the entire organ. Ann Ist Super Sanita. 2012;48:75–82.PubMed Perilli E, Parkinson IH, Reynolds KJ. Micro-CT examination of human bone: from biopsies towards the entire organ. Ann Ist Super Sanita. 2012;48:75–82.PubMed
34.
go back to reference Tjong W, Kazakia GJ, Burghardt AJ, Majumdar S. The effect of voxel size on high-resolution peripheral computed tomography measurements of trabecular and cortical bone microstructure. Med Phys. 2012;39:1893–903.CrossRefPubMedPubMedCentral Tjong W, Kazakia GJ, Burghardt AJ, Majumdar S. The effect of voxel size on high-resolution peripheral computed tomography measurements of trabecular and cortical bone microstructure. Med Phys. 2012;39:1893–903.CrossRefPubMedPubMedCentral
35.
go back to reference Kim DG, Christopherson GT, Dong XN, Fyhrie DP, Yeni YN. The effect of microcomputed tomography scanning and reconstruction voxel size on the accuracy of stereological measurements in human cancellous bone. Bone. 2004;35:1375–82.CrossRefPubMed Kim DG, Christopherson GT, Dong XN, Fyhrie DP, Yeni YN. The effect of microcomputed tomography scanning and reconstruction voxel size on the accuracy of stereological measurements in human cancellous bone. Bone. 2004;35:1375–82.CrossRefPubMed
36.
go back to reference Muller R, Koller B, Hildebrand T, Laib A, Gianolini S, Ruegsegger P. Resolution dependency of microstructural properties of cancellous bone based on three-dimensional mu-tomography. Technol Health Care. 1996;4:113–9.PubMed Muller R, Koller B, Hildebrand T, Laib A, Gianolini S, Ruegsegger P. Resolution dependency of microstructural properties of cancellous bone based on three-dimensional mu-tomography. Technol Health Care. 1996;4:113–9.PubMed
37.
go back to reference Newitt DC, Majumdar S, van Rietbergen B, von Ingersleben G, Harris ST, Genant HK, Chesnut C, Garnero P, MacDonald B. In vivo assessment of architecture and micro-finite element analysis derived indices of mechanical properties of trabecular bone in the radius. Osteoporos Int. 2002;13:6–17.CrossRefPubMed Newitt DC, Majumdar S, van Rietbergen B, von Ingersleben G, Harris ST, Genant HK, Chesnut C, Garnero P, MacDonald B. In vivo assessment of architecture and micro-finite element analysis derived indices of mechanical properties of trabecular bone in the radius. Osteoporos Int. 2002;13:6–17.CrossRefPubMed
38.
go back to reference Edwards WB, Troy KL. Finite element prediction of surface strain and fracture strength at the distal radius. Med Eng Phys. 2012;34:290–8.CrossRefPubMed Edwards WB, Troy KL. Finite element prediction of surface strain and fracture strength at the distal radius. Med Eng Phys. 2012;34:290–8.CrossRefPubMed
39.
go back to reference Schileo E, Taddei F, Malandrino A, Cristofolini L, Viceconti M. Subject-specific finite element models can accurately predict strain levels in long bones. J Biomech. 2007;40:2982–9.CrossRefPubMed Schileo E, Taddei F, Malandrino A, Cristofolini L, Viceconti M. Subject-specific finite element models can accurately predict strain levels in long bones. J Biomech. 2007;40:2982–9.CrossRefPubMed
40.
go back to reference Carter DR, Hayes WC. The compressive behavior of bone as a two-phase porous structure. J Bone Joint Surg Am. 1977;59:954–62.CrossRefPubMed Carter DR, Hayes WC. The compressive behavior of bone as a two-phase porous structure. J Bone Joint Surg Am. 1977;59:954–62.CrossRefPubMed
41.
go back to reference Dalstra M, Huiskes R, Odgaard A, van Erning L. Mechanical and textural properties of pelvic trabecular bone. J Biomech. 1993;26:523–35.CrossRefPubMed Dalstra M, Huiskes R, Odgaard A, van Erning L. Mechanical and textural properties of pelvic trabecular bone. J Biomech. 1993;26:523–35.CrossRefPubMed
42.
go back to reference Morgan EF, Bayraktar HH, Keaveny TM. Trabecular bone modulus-density relationships depend on anatomic site. J Biomech. 2003;36:897–904.CrossRefPubMed Morgan EF, Bayraktar HH, Keaveny TM. Trabecular bone modulus-density relationships depend on anatomic site. J Biomech. 2003;36:897–904.CrossRefPubMed
43.
go back to reference Rho JY. Ultrasonic characterisation in determining elastic modulus of trabecular bone material. Med Biol Eng Comput. 1998;36:57–9.CrossRefPubMed Rho JY. Ultrasonic characterisation in determining elastic modulus of trabecular bone material. Med Biol Eng Comput. 1998;36:57–9.CrossRefPubMed
44.
go back to reference Heilmeier U, Cheng K, Pasco C, Parrish R, Nirody J, Patsch JM, Zhang CA, Joseph GB, Burghardt AJ, Schwartz AV, et al. Cortical bone laminar analysis reveals increased midcortical and periosteal porosity in type 2 diabetic postmenopausal women with history of fragility fractures compared to fracture-free diabetics. Osteoporos Int. 2016;27:2791–802.CrossRefPubMed Heilmeier U, Cheng K, Pasco C, Parrish R, Nirody J, Patsch JM, Zhang CA, Joseph GB, Burghardt AJ, Schwartz AV, et al. Cortical bone laminar analysis reveals increased midcortical and periosteal porosity in type 2 diabetic postmenopausal women with history of fragility fractures compared to fracture-free diabetics. Osteoporos Int. 2016;27:2791–802.CrossRefPubMed
45.
go back to reference Weaver CM, Gordon CM, Janz KF, Kalkwarf HJ, Lappe JM, Lewis R, O'Karma M, Wallace TC, Zemel BS. The National Osteoporosis Foundation's position statement on peak bone mass development and lifestyle factors: a systematic review and implementation recommendations. Osteoporos Int. 2016;27:1281–386.CrossRefPubMedPubMedCentral Weaver CM, Gordon CM, Janz KF, Kalkwarf HJ, Lappe JM, Lewis R, O'Karma M, Wallace TC, Zemel BS. The National Osteoporosis Foundation's position statement on peak bone mass development and lifestyle factors: a systematic review and implementation recommendations. Osteoporos Int. 2016;27:1281–386.CrossRefPubMedPubMedCentral
46.
go back to reference Behnam AJ, Herzka DA, Sheehan FT. Assessing the accuracy and precision of musculoskeletal motion tracking using cine-PC MRI on a 3.0T platform. J Biomech. 2011;44:193–7.CrossRefPubMed Behnam AJ, Herzka DA, Sheehan FT. Assessing the accuracy and precision of musculoskeletal motion tracking using cine-PC MRI on a 3.0T platform. J Biomech. 2011;44:193–7.CrossRefPubMed
47.
go back to reference Borotikar BS, Sipprell WH 3rd, Wible EE, Sheehan FT. A methodology to accurately quantify patellofemoral cartilage contact kinematics by combining 3D image shape registration and cine-PC MRI velocity data. J Biomech. 2012;45:1117–22.CrossRefPubMedPubMedCentral Borotikar BS, Sipprell WH 3rd, Wible EE, Sheehan FT. A methodology to accurately quantify patellofemoral cartilage contact kinematics by combining 3D image shape registration and cine-PC MRI velocity data. J Biomech. 2012;45:1117–22.CrossRefPubMedPubMedCentral
48.
go back to reference Cuesta-Vargas AI. Development of a new ultrasound-based system for tracking motion of the human lumbar spine: reliability, stability and repeatability during forward bending movement trials. Ultrasound Med Biol. 2015;41:2049–56.CrossRefPubMed Cuesta-Vargas AI. Development of a new ultrasound-based system for tracking motion of the human lumbar spine: reliability, stability and repeatability during forward bending movement trials. Ultrasound Med Biol. 2015;41:2049–56.CrossRefPubMed
49.
go back to reference Defrate LE, Papannagari R, Gill TJ, Moses JM, Pathare NP, Li G. The 6 degrees of freedom kinematics of the knee after anterior cruciate ligament deficiency: an in vivo imaging analysis. Am J Sports Med. 2006;34:1240–6.CrossRefPubMed Defrate LE, Papannagari R, Gill TJ, Moses JM, Pathare NP, Li G. The 6 degrees of freedom kinematics of the knee after anterior cruciate ligament deficiency: an in vivo imaging analysis. Am J Sports Med. 2006;34:1240–6.CrossRefPubMed
50.
go back to reference Eckstein F, Lemberger B, Stammberger T, Englmeier K, Reiser M. Patellar cartilage deformation in vivo after static versus dynamic loading. J Biomech. 2000;33:819–25.CrossRefPubMed Eckstein F, Lemberger B, Stammberger T, Englmeier K, Reiser M. Patellar cartilage deformation in vivo after static versus dynamic loading. J Biomech. 2000;33:819–25.CrossRefPubMed
51.
go back to reference Sharma GB, Beveridge JE, Kuntze G, Bhatla C, Shank J, Ronsky JL. Structural and functional characterization of tibiofemoral cartilage: a dual fluoroscopy and magnetic imaging approach. In: Proc Comp Meth Biomech & Biomedical Eng & Imaging & Visualization; 9/15/2015. Montreal: Springer International Research; 2015. Sharma GB, Beveridge JE, Kuntze G, Bhatla C, Shank J, Ronsky JL. Structural and functional characterization of tibiofemoral cartilage: a dual fluoroscopy and magnetic imaging approach. In: Proc Comp Meth Biomech & Biomedical Eng & Imaging & Visualization; 9/15/2015. Montreal: Springer International Research; 2015.
52.
go back to reference Sharma GB, Kuntze G, Beveridge JE, Bhatla C, Frayne R, Ronsky JL. Subject-specific 3D T2 relaxation mapping of the tibiofemoral contact regions during walking: a dual fluoroscopy and magnetic resonance imaging approach. In: Orthopaedic Research Society; 2015. Sharma GB, Kuntze G, Beveridge JE, Bhatla C, Frayne R, Ronsky JL. Subject-specific 3D T2 relaxation mapping of the tibiofemoral contact regions during walking: a dual fluoroscopy and magnetic resonance imaging approach. In: Orthopaedic Research Society; 2015.
53.
go back to reference Sheehan FT, Smith RM. 3D musculoskeletal kinematics using dynamic MRI. In: Müller B, Wolf SI, Brueggemann G-P, Deng Z, McIntosh A, Miller F, Selbie WS, editors. Handbook of human motion. Cham: Springer International Publishing; 2017. p. 1–17. Sheehan FT, Smith RM. 3D musculoskeletal kinematics using dynamic MRI. In: Müller B, Wolf SI, Brueggemann G-P, Deng Z, McIntosh A, Miller F, Selbie WS, editors. Handbook of human motion. Cham: Springer International Publishing; 2017. p. 1–17.
54.
go back to reference Smith RM, Sheehan FT. Cross platform comparison of imaging Technologies for Measuring Musculoskeletal Motion. In: Müller B, Wolf SI, Brueggemann G-P, Deng Z, McIntosh A, Miller F, Selbie WS, editors. Handbook of human motion. Cham: Springer International Publishing; 2017. p. 1–22. Smith RM, Sheehan FT. Cross platform comparison of imaging Technologies for Measuring Musculoskeletal Motion. In: Müller B, Wolf SI, Brueggemann G-P, Deng Z, McIntosh A, Miller F, Selbie WS, editors. Handbook of human motion. Cham: Springer International Publishing; 2017. p. 1–22.
55.
go back to reference Benoit DL, Ramsey DK, Lamontagne M, Xu L, Wretenberg P, Renstrom P. In vivo knee kinematics during gait reveals new rotation profiles and smaller translations. Clin Orthop Relat Res. 2007;454:81–8.CrossRefPubMed Benoit DL, Ramsey DK, Lamontagne M, Xu L, Wretenberg P, Renstrom P. In vivo knee kinematics during gait reveals new rotation profiles and smaller translations. Clin Orthop Relat Res. 2007;454:81–8.CrossRefPubMed
56.
go back to reference Tashman S, Collon D, Anderson K, Kolowich P, Anderst W. Abnormal rotational knee motion during running after anterior cruciate ligament reconstruction. Am J Sports Med. 2004;32:975–83.CrossRefPubMed Tashman S, Collon D, Anderson K, Kolowich P, Anderst W. Abnormal rotational knee motion during running after anterior cruciate ligament reconstruction. Am J Sports Med. 2004;32:975–83.CrossRefPubMed
57.
go back to reference Vergis A, Gillquist J. Sagittal plane translation of the knee during stair walking. Comparison of healthy and anterior cruciate ligament--deficient subjects. Am J Sports Med. 1998;26:841–6.CrossRefPubMed Vergis A, Gillquist J. Sagittal plane translation of the knee during stair walking. Comparison of healthy and anterior cruciate ligament--deficient subjects. Am J Sports Med. 1998;26:841–6.CrossRefPubMed
58.
go back to reference Georgoulis AD, Papadonikolakis A, Papageorgiou CD, Mitsou A, Stergiou N. Three-dimensional tibiofemoral kinematics of the anterior cruciate ligament-deficient and reconstructed knee during walking. Am J Sports Med. 2003;31:75–9.CrossRefPubMed Georgoulis AD, Papadonikolakis A, Papageorgiou CD, Mitsou A, Stergiou N. Three-dimensional tibiofemoral kinematics of the anterior cruciate ligament-deficient and reconstructed knee during walking. Am J Sports Med. 2003;31:75–9.CrossRefPubMed
59.
go back to reference Andriacchi TP, Dyrby CO. Interactions between kinematics and loading during walking for the normal and ACL deficient knee. J Biomech. 2005;38:293–8.CrossRefPubMed Andriacchi TP, Dyrby CO. Interactions between kinematics and loading during walking for the normal and ACL deficient knee. J Biomech. 2005;38:293–8.CrossRefPubMed
60.
go back to reference Andriacchi TP, Mundermann A, Smith RL, Alexander EJ, Dyrby CO, Koo S. A framework for the in vivo pathomechanics of osteoarthritis at the knee. Ann Biomed Eng. 2004;32:447–57.CrossRefPubMed Andriacchi TP, Mundermann A, Smith RL, Alexander EJ, Dyrby CO, Koo S. A framework for the in vivo pathomechanics of osteoarthritis at the knee. Ann Biomed Eng. 2004;32:447–57.CrossRefPubMed
61.
go back to reference Anderst WJ, Tashman S. The association between velocity of the center of closest proximity on subchondral bones and osteoarthritis progression. J Orthop Res. 2009;27:71–7.CrossRefPubMedPubMedCentral Anderst WJ, Tashman S. The association between velocity of the center of closest proximity on subchondral bones and osteoarthritis progression. J Orthop Res. 2009;27:71–7.CrossRefPubMedPubMedCentral
62.
go back to reference Maniwa S, Nishikori T, Furukawa S, Kajitani K, Ochi M. Alteration of collagen network and negative charge of articular cartilage surface in the early stage of experimental osteoarthritis. Arch Orthop Trauma Surg. 2001;121:181–5.CrossRefPubMed Maniwa S, Nishikori T, Furukawa S, Kajitani K, Ochi M. Alteration of collagen network and negative charge of articular cartilage surface in the early stage of experimental osteoarthritis. Arch Orthop Trauma Surg. 2001;121:181–5.CrossRefPubMed
63.
go back to reference Akizuki S, Mow VC, Muller F, Pita JC, Howell DS, Manicourt DH. Tensile properties of human knee joint cartilage: I. Influence of ionic conditions, weight bearing, and fibrillation on the tensile modulus. J Orthop Res. 1986;4:379–92.CrossRefPubMed Akizuki S, Mow VC, Muller F, Pita JC, Howell DS, Manicourt DH. Tensile properties of human knee joint cartilage: I. Influence of ionic conditions, weight bearing, and fibrillation on the tensile modulus. J Orthop Res. 1986;4:379–92.CrossRefPubMed
64.
go back to reference Chaudhari AM, Briant PL, Bevill SL, Koo S, Andriacchi TP. Knee kinematics, cartilage morphology, and osteoarthritis after ACL injury. Med Sci Sports Exerc. 2008;40:215–22.CrossRefPubMed Chaudhari AM, Briant PL, Bevill SL, Koo S, Andriacchi TP. Knee kinematics, cartilage morphology, and osteoarthritis after ACL injury. Med Sci Sports Exerc. 2008;40:215–22.CrossRefPubMed
65.
go back to reference Sharma GB, Kuntze G, Kukulski D, Ronsky JL. Validating dual fluoroscopy system capabilities for determining in-vivo knee joint soft tissue deformation: a strategy for registration error management. J Biomech. 2015;48:2181–5.CrossRefPubMed Sharma GB, Kuntze G, Kukulski D, Ronsky JL. Validating dual fluoroscopy system capabilities for determining in-vivo knee joint soft tissue deformation: a strategy for registration error management. J Biomech. 2015;48:2181–5.CrossRefPubMed
66.
go back to reference Anderst W, Zauel R, Bishop J, Demps E, Tashman S. Validation of three-dimensional model-based tibio-femoral tracking during running. Med Eng Phys. 2009;31:10–6.CrossRefPubMed Anderst W, Zauel R, Bishop J, Demps E, Tashman S. Validation of three-dimensional model-based tibio-femoral tracking during running. Med Eng Phys. 2009;31:10–6.CrossRefPubMed
67.
go back to reference Lichti DD, Sharma GB, Kuntze G, Mund B, Beveridge JE, Ronsky JL. Rigorous geometric self-calibrating bundle adjustment for a dual fluoroscopic imaging system. IEEE Trans Med Imaging. 2015;34:589–98.CrossRefPubMed Lichti DD, Sharma GB, Kuntze G, Mund B, Beveridge JE, Ronsky JL. Rigorous geometric self-calibrating bundle adjustment for a dual fluoroscopic imaging system. IEEE Trans Med Imaging. 2015;34:589–98.CrossRefPubMed
68.
go back to reference Miranda DL, Schwartz JB, Loomis AC, Brainerd EL, Fleming BC, Crisco JJ. Static and dynamic error of a biplanar videoradiography system using marker-based and markerless tracking techniques. J Biomech Eng. 2011;133:121002.CrossRefPubMedPubMedCentral Miranda DL, Schwartz JB, Loomis AC, Brainerd EL, Fleming BC, Crisco JJ. Static and dynamic error of a biplanar videoradiography system using marker-based and markerless tracking techniques. J Biomech Eng. 2011;133:121002.CrossRefPubMedPubMedCentral
69.
go back to reference Calvo E, Palacios I, Delgado E, Sanchez-Pernaute O, Largo R, Egido J, Herrero-Beaumont G. Histopathological correlation of cartilage swelling detected by magnetic resonance imaging in early experimental osteoarthritis. Osteoarthr Cartil. 2004;12:878–86.CrossRefPubMed Calvo E, Palacios I, Delgado E, Sanchez-Pernaute O, Largo R, Egido J, Herrero-Beaumont G. Histopathological correlation of cartilage swelling detected by magnetic resonance imaging in early experimental osteoarthritis. Osteoarthr Cartil. 2004;12:878–86.CrossRefPubMed
70.
go back to reference Mow VC, Gu WY, Chen FH. Structure and function of articular cartilage and meniscus. In: Mow VC, Huiskes R, editors. Basic orthopaedic biomechanics & mechano-biology. 3rd ed. Philadelphia, PA: Lippincott Williams & Wilkins; 2005. p. 181–225. Mow VC, Gu WY, Chen FH. Structure and function of articular cartilage and meniscus. In: Mow VC, Huiskes R, editors. Basic orthopaedic biomechanics & mechano-biology. 3rd ed. Philadelphia, PA: Lippincott Williams & Wilkins; 2005. p. 181–225.
71.
go back to reference Li X, Cheng J, Lin K, Saadat E, Bolbos RI, Jobke B, Ries MD, Horvai A, Link TM, Majumdar S. Quantitative MRI using T1rho and T2 in human osteoarthritic cartilage specimens: correlation with biochemical measurements and histology. Magn Reson Imaging. 2011;29:324–34.CrossRefPubMed Li X, Cheng J, Lin K, Saadat E, Bolbos RI, Jobke B, Ries MD, Horvai A, Link TM, Majumdar S. Quantitative MRI using T1rho and T2 in human osteoarthritic cartilage specimens: correlation with biochemical measurements and histology. Magn Reson Imaging. 2011;29:324–34.CrossRefPubMed
72.
go back to reference Nishioka H, Hirose J, Nakamura E, Oniki Y, Takada K, Yamashita Y, Mizuta H. T1rho and T2 mapping reveal the in vivo extracellular matrix of articular cartilage. J Magn Reson Imaging. 2012;35:147–55.CrossRefPubMed Nishioka H, Hirose J, Nakamura E, Oniki Y, Takada K, Yamashita Y, Mizuta H. T1rho and T2 mapping reveal the in vivo extracellular matrix of articular cartilage. J Magn Reson Imaging. 2012;35:147–55.CrossRefPubMed
73.
go back to reference Klocke NF, Amendola A, Thedens DR, Williams GN, Luty CM, Martin JA, Pedersen DR. Comparison of T1rho, dGEMRIC, and quantitative T2 MRI in preoperative ACL rupture patients. Acad Radiol. 2013;20:99–107.CrossRefPubMed Klocke NF, Amendola A, Thedens DR, Williams GN, Luty CM, Martin JA, Pedersen DR. Comparison of T1rho, dGEMRIC, and quantitative T2 MRI in preoperative ACL rupture patients. Acad Radiol. 2013;20:99–107.CrossRefPubMed
74.
go back to reference Zarins ZA, Bolbos RI, Pialat JB, Link TM, Li X, Souza RB, Majumdar S. Cartilage and meniscus assessment using T1rho and T2 measurements in healthy subjects and patients with osteoarthritis. Osteoarthr Cartil. 2010;18:1408–16.CrossRefPubMedPubMedCentral Zarins ZA, Bolbos RI, Pialat JB, Link TM, Li X, Souza RB, Majumdar S. Cartilage and meniscus assessment using T1rho and T2 measurements in healthy subjects and patients with osteoarthritis. Osteoarthr Cartil. 2010;18:1408–16.CrossRefPubMedPubMedCentral
75.
go back to reference Brainerd EL, Baier DB, Gatesy SM, Hedrick TL, Metzger KA, Gilbert SL, Crisco JJ. X-ray reconstruction of moving morphology (XROMM): precision, accuracy and applications in comparative biomechanics research. J Exp Zool. 2010;313A:262–79. Brainerd EL, Baier DB, Gatesy SM, Hedrick TL, Metzger KA, Gilbert SL, Crisco JJ. X-ray reconstruction of moving morphology (XROMM): precision, accuracy and applications in comparative biomechanics research. J Exp Zool. 2010;313A:262–79.
76.
go back to reference Knorlein BJ, Baier DB, Gatesy SM, Laurence-Chasen JD, Brainerd EL. Validation of XMALab software for marker-based XROMM. J Exp Biol. 2016;219:3701–11.CrossRefPubMed Knorlein BJ, Baier DB, Gatesy SM, Laurence-Chasen JD, Brainerd EL. Validation of XMALab software for marker-based XROMM. J Exp Biol. 2016;219:3701–11.CrossRefPubMed
77.
go back to reference Miranda DL, Rainbow MJ, Leventhal EL, Crisco JJ, Fleming BC. Automatic determination of anatomical coordinate systems for three-dimensional bone models of the isolated human knee. J Biomech. 2010;43:1623–6.CrossRefPubMedPubMedCentral Miranda DL, Rainbow MJ, Leventhal EL, Crisco JJ, Fleming BC. Automatic determination of anatomical coordinate systems for three-dimensional bone models of the isolated human knee. J Biomech. 2010;43:1623–6.CrossRefPubMedPubMedCentral
78.
go back to reference You BM, Siy P, Anderst W, Tashman S. In vivo measurement of 3-D skeletal kinematics from sequences of biplane radiographs: application to knee kinematics. IEEE Trans Med Imaging. 2001;20:514–25.CrossRefPubMed You BM, Siy P, Anderst W, Tashman S. In vivo measurement of 3-D skeletal kinematics from sequences of biplane radiographs: application to knee kinematics. IEEE Trans Med Imaging. 2001;20:514–25.CrossRefPubMed
79.
go back to reference Tashman S, Anderst W. In-vivo measurement of dynamic joint motion using high speed biplane radiography and CT: application to canine ACL deficiency. J Biomech Eng. 2003;125:238–45.CrossRefPubMed Tashman S, Anderst W. In-vivo measurement of dynamic joint motion using high speed biplane radiography and CT: application to canine ACL deficiency. J Biomech Eng. 2003;125:238–45.CrossRefPubMed
80.
go back to reference Brainerd EL. Major transformations in vertebrate breathing mechanisms. In: Dial KP, Shubin N, Brainerd EL, editors. Great transformations in vertebrate evolution. Chicago: Chicago University Press; 2015. p. 47–62. Brainerd EL. Major transformations in vertebrate breathing mechanisms. In: Dial KP, Shubin N, Brainerd EL, editors. Great transformations in vertebrate evolution. Chicago: Chicago University Press; 2015. p. 47–62.
81.
go back to reference Brainerd EL, Moritz S, Ritter DA. XROMM analysis of rib kinematics during lung ventilation in the green iguana, Iguana iguana. J Exp Biol. 2016;219:404–11.CrossRefPubMed Brainerd EL, Moritz S, Ritter DA. XROMM analysis of rib kinematics during lung ventilation in the green iguana, Iguana iguana. J Exp Biol. 2016;219:404–11.CrossRefPubMed
82.
go back to reference Brainerd EL, Blob RW, Hedrick TL, Creamer AT, Muller UK. Data management rubric for video data in organismal biology. Integr Comp Biol. 2017;57:33–47.CrossRefPubMed Brainerd EL, Blob RW, Hedrick TL, Creamer AT, Muller UK. Data management rubric for video data in organismal biology. Integr Comp Biol. 2017;57:33–47.CrossRefPubMed
83.
go back to reference Olsen A, Hernandez P, Camp A, Brainerd E. Linking morphology and motion: testing multibody simulations against in vivo cranial kinematics in suction feeding fishes using XROMM. FASEB J. 2017;31 Olsen A, Hernandez P, Camp A, Brainerd E. Linking morphology and motion: testing multibody simulations against in vivo cranial kinematics in suction feeding fishes using XROMM. FASEB J. 2017;31
Metadata
Title
Advancing quantitative techniques to improve understanding of the skeletal structure-function relationship
Authors
Frances T. Sheehan
Elizabeth L. Brainerd
Karen L. Troy
Sandra J. Shefelbine
Janet L. Ronsky
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Journal of NeuroEngineering and Rehabilitation / Issue 1/2018
Electronic ISSN: 1743-0003
DOI
https://doi.org/10.1186/s12984-018-0368-9

Other articles of this Issue 1/2018

Journal of NeuroEngineering and Rehabilitation 1/2018 Go to the issue