Meccanica

, Volume 52, Issue 3, pp 665–676 | Cite as

Application of ultrasound imaging to subject-specific modelling of the human musculoskeletal system

  • Elyse Passmore
  • Adrian Lai
  • Morgan Sangeux
  • Anthony G. Schache
  • Marcus G. Pandy
Advances in Biomechanics: from foundations to applications

Abstract

Ultrasound imaging is relatively inexpensive, does not involve ionising radiation, and requires much shorter scan times compared with other imaging modalities such as magnetic resonance imaging and computed tomography. These advantages make it an appealing option in both clinical and research settings. Computational models of the human musculoskeletal system are used for a wide range of applications in biomechanics, from studies of muscle function during locomotion to pre-operative planning of orthopaedic surgeries. The integration of ultrasound imaging with musculoskeletal modelling has the potential to create new opportunities in the study of human movement science. Subject-specific measures of muscle–tendon properties and bone geometry obtained from ultrasound imaging are now being used in conjunction with detailed models of the musculoskeletal system to better understand muscle–tendon function during normal and pathological movement. This approach also allows more rigorous validation studies to be performed to quantify the accuracy of musculoskeletal modelling predictions. We have been using ultrasound imaging to create subject-specific models of the human musculoskeletal system for the purpose of simulating normal and pathological gait. This review describes our experiences in using ultrasound imaging to measure muscle–tendon architecture and bone geometry in vivo. Recent studies focused on integrating ultrasound imaging and musculoskeletal modelling to determine muscle–tendon function in human walking and running are also described.

Keywords

Bone geometry Muscle–tendon architecture Muscle–tendon function Muscle properties Musculoskeletal modelling Gait biomechanics 

References

  1. 1.
    Davis R, Ounpuu S, Tyburski D, Gage J (1991) A gait analysis data collection and reduction technique. Hum Mov Sci 10:575–587CrossRefGoogle Scholar
  2. 2.
    Howry DH, Bliss WR (1952) Ultrasonic visualization of soft tissue structures of the body. J Lab Clin Med 40:579–592Google Scholar
  3. 3.
    Shung KK (2006) Diagnostic ultrasound: imaging and blood flow measurements. CRC Press, Boca RatonGoogle Scholar
  4. 4.
    Maganaris CN (2001) Force–length characteristics of in vivo human skeletal muscle. Acta Physiol Scand 172:279–285CrossRefGoogle Scholar
  5. 5.
    Ito M, Akima H, Fukunaga T (2000) In vivo moment arm determination using B-mode ultrasonography. J Biomech 33:215–218CrossRefGoogle Scholar
  6. 6.
    Maganaris CN, Paul JP (2000) In vivo human tendinous tissue stretch upon maximum muscle force generation. J Biomech 33:1453–1459CrossRefGoogle Scholar
  7. 7.
    Lichtwark GA, Wilson AM (2005) In vivo mechanical properties of the human Achilles tendon during one-legged hopping. J Exp Biol 208:4715–4725CrossRefGoogle Scholar
  8. 8.
    Maganaris CN (2002) Tensile properties of in vivo human tendinous tissue. J Biomech 35:1019–1027CrossRefGoogle Scholar
  9. 9.
    Magnusson SP, Hansen P, Aagaard P, Brønd J, Dyhre-Poulsen P, Bojsen-Moller J et al (2003) Differential strain patterns of the human gastrocnemius aponeurosis and free tendon, in vivo. Acta Physiol Scand 177:185–195CrossRefGoogle Scholar
  10. 10.
    Muraoka T, Muramatsu T, Fukunaga T, Kanehisa H (2005) Elastic properties of human Achilles tendon are correlated to muscle strength. J Appl Physiol 99:665–669CrossRefGoogle Scholar
  11. 11.
    Bråten M, Rossvoll I, Terjesen T (1992) Femoral anteversion in normal adults. Acta Orthop 63:29–32CrossRefGoogle Scholar
  12. 12.
    Hudson D (2008) A comparison of ultrasound to goniometric and inclinometer measurements of torsion in the tibia and femur. Gait Posture 28:708–710CrossRefGoogle Scholar
  13. 13.
    Kulig K, Harper-Hanigan K, Souza RB, Powers CM (2010) Measurement of femoral torsion by ultrasound and magnetic resonance imaging: concurrent validity. Phys Ther 90:1641–1648CrossRefGoogle Scholar
  14. 14.
    Cronin NJ, Lichtwark G (2013) The use of ultrasound to study muscle–tendon function in human posture and locomotion. Gait Posture 37:305–312CrossRefGoogle Scholar
  15. 15.
    Fukunaga T, Kubo K, Kawakami Y, Fukashiro S, Kanehisa H, Maganaris CN (2001) In vivo behaviour of human muscle tendon during walking. Proc R Soc B Biol Sci 268:229–233CrossRefGoogle Scholar
  16. 16.
    Ishikawa M, Komi PV, Grey MJ, Lepola V, Bruggemann G-P (2005) Muscle–tendon interaction and elastic energy usage in human walking. J Appl Physiol 99:603–608CrossRefGoogle Scholar
  17. 17.
    Lichtwark GA, Bougoulias K, Wilson AM (2007) Muscle fascicle and series elastic element length changes along the length of the human gastrocnemius during walking and running. J Biomech 40:157–164CrossRefGoogle Scholar
  18. 18.
    Delp SL, Loan JP, Hoy MG, Zajac FE, Topp EL, Rosen JM (1990) An interactive graphics-based model of the lower extremity to study orthopaedic surgical procedures. IEEE Trans Biomed Eng 37:757–767CrossRefGoogle Scholar
  19. 19.
    Arnold EM, Ward SR, Lieber RL, Delp SL (2010) A model of the lower limb for analysis of human movement. Ann Biomed Eng 38:269–279CrossRefGoogle Scholar
  20. 20.
    Pandy MG (2001) Computer modeling and simulation of human movement. Annu Rev Biomed Eng 3:245–273CrossRefGoogle Scholar
  21. 21.
    Pandy MG, Andriacchi TP (2010) Muscle and joint function in human locomotion. Annu Rev Biomed Eng 12:401–433CrossRefGoogle Scholar
  22. 22.
    Barber L, Hastings-Ison T, Baker R, Barrett R, Lichtwark G (2011) Medial gastrocnemius muscle volume and fascicle length in children aged 2–5 years with cerebral palsy. Dev Med Child Neurol 53:543–548CrossRefGoogle Scholar
  23. 23.
    Peters A, Baker R, Morris ME, Sangeux M (2012) A comparison of hip joint centre localisation techniques with 3-DUS for clinical gait analysis in children with cerebral palsy. Gait Posture 36:282–286CrossRefGoogle Scholar
  24. 24.
    Fry NR, Childs CR, Eve LC, Gough M, Robinson RO, Shortland AP (2003) Accurate measurement of muscle belly length in the motion analysis laboratory: potential for the assessment of contracture. Gait Posture 17:119–124CrossRefGoogle Scholar
  25. 25.
    Halar EM, Stolov WC, Venkatesh B, Brozovich FV, Harley JD (1978) Gastrocnemius muscle belly and tendon length in stroke patients and able-bodied persons. Arch Phys Med Rehabil 59:476–484Google Scholar
  26. 26.
    Ackland DC, Lin Y-C, Pandy MG (2012) Sensitivity of model predictions of muscle function to changes in moment arms and muscle–tendon properties: a Monte-Carlo analysis. J Biomech 45:1463–1471CrossRefGoogle Scholar
  27. 27.
    Redl C, Gfoehler M, Pandy MG (2007) Sensitivity of muscle force estimates to variations in muscle–tendon properties. Hum Mov Sci 26:306–319CrossRefGoogle Scholar
  28. 28.
    Peters A, Baker R, Sangeux M (2010) Validation of 3-D freehand ultrasound for the determination of the hip joint centre. Gait Posture 31:530–532CrossRefGoogle Scholar
  29. 29.
    Hsu P-W, Prager RW, Gee AH, Treece GM (2009) Freehand 3D ultrasound calibration: a review. In: Sensen CW, Hallgrímsson B (eds) Advanced imaging in biology and medicine. Springer, Berlin, pp 47–84CrossRefGoogle Scholar
  30. 30.
    Hsu P-W, Treece GM, Prager RW, Houghton NE, Gee AH (2008) Comparison of freehand 3-D ultrasound calibration techniques using a stylus. Ultrasound Med Biol 34:1610–1621CrossRefGoogle Scholar
  31. 31.
    Harrington ME, Zavatsky AB, Lawson SEM, Yuan Z, Theologis TN (2007) Prediction of the hip joint centre in adults, children, and patients with cerebral palsy based on magnetic resonance imaging. J Biomech 40:595–602CrossRefGoogle Scholar
  32. 32.
    Delp SL, Anderson FC, Arnold AS, Loan P, Habib A, John CT et al (2007) OpenSim: open-source software to create and analyze dynamic simulations of movement. IEEE Trans Biomed Eng 54:1940–1950CrossRefGoogle Scholar
  33. 33.
    Sangeux M, Peters A, Baker R (2011) Hip joint centre localization: evaluation on normal subjects in the context of gait analysis. Gait Posture 34:324–328CrossRefGoogle Scholar
  34. 34.
    Gee A, Prager R, Treece G, Cash C, Berman L (2004) Processing and visualizing three-dimensional ultrasound data. Br J Radiol 77:S186–S193CrossRefGoogle Scholar
  35. 35.
    Stagni R, Leardini A, Cappozzo A, Grazia Benedetti M, Cappello A (2000) Effects of hip joint centre mislocation on gait analysis results. J Biomech 33:1479–1487CrossRefGoogle Scholar
  36. 36.
    Delp SL, Maloney W (1993) Effects of hip center location on the moment-generating capacity of the muscles. J Biomech 26:485–499CrossRefGoogle Scholar
  37. 37.
    Lenaerts G, Bartels W, Gelaude F, Mulier M, Spaepen A, Van der Perre G et al (2009) Subject-specific hip geometry and hip joint centre location affects calculated contact forces at the hip during gait. J Biomech 42:1246–1251CrossRefGoogle Scholar
  38. 38.
    McGinley JL, Baker R, Wolfe R, Morris ME (2009) The reliability of three-dimensional kinematic gait measurements: a systematic review. Gait Posture 29:360–369CrossRefGoogle Scholar
  39. 39.
    Schwartz MH, Trost JP, Wervey RA (2004) Measurement and management of errors in quantitative gait data. Gait Posture 20:196–203CrossRefGoogle Scholar
  40. 40.
    Grood ES, Suntay WJ (1983) A joint coordinate system for the clinical description of three-dimensional motions: application to the knee. J Biomech Eng 105:136–144CrossRefGoogle Scholar
  41. 41.
    Ehrig RM, Taylor WR, Duda GN, Heller MO (2007) A survey of formal methods for determining functional joint axes. J Biomech 40:2150–2157CrossRefGoogle Scholar
  42. 42.
    Schwartz MH, Rozumalski A, Novacheck TF (2014) Femoral derotational osteotomy: surgical indications and outcomes in children with cerebral palsy. Gait Posture 39:778–783CrossRefGoogle Scholar
  43. 43.
    Passmore E, Sangeux M (2016) Defining the medial-lateral axis of an anatomical femur coordinate system using freehand 3D ultrasound imaging. Gait Posture 45:211–216CrossRefGoogle Scholar
  44. 44.
    Eckhoff DG, Bach JM, Spitzer VM, Reinig KD, Bagur MM, Baldini TH et al (2005) Three-dimensional mechanics, kinematics, and morphology of the knee viewed in virtual reality. J Bone Joint Surg Am 87(Suppl. 2):71–80Google Scholar
  45. 45.
    Hancock CW, Winston MJ, Bach JM, Davidson BS, Eckhoff DG (2013) Cylindrical axis, not epicondyles, approximates perpendicular to knee axes. Clin Orthop Relat Res 471:2278–2283CrossRefGoogle Scholar
  46. 46.
    Iwaki H, Pinskerova V, Freeman MA (2000) Tibiofemoral movement 1: the shapes and relative movements of the femur and tibia in the unloaded cadaver knee. J Bone Joint Surg Br 82:1189–1195CrossRefGoogle Scholar
  47. 47.
    Freeman MAR, Pinskerova V (2005) The movement of the normal tibio-femoral joint. J Biomech 38:197–208CrossRefGoogle Scholar
  48. 48.
    Hill PF, Vedi V, Williams A, Iwaki H, Pinskerova V, Freeman MA (2000) Tibiofemoral movement 2: the loaded and unloaded living knee studied by MRI. J Bone Joint Surg Br 82:1196–1198CrossRefGoogle Scholar
  49. 49.
    Johal P, Williams A, Wragg P, Hunt D, Gedroyc W (2005) Tibio-femoral movement in the living knee. A study of weight bearing and non-weight bearing knee kinematics using “interventional” MRI. J Biomech 38:269–276CrossRefGoogle Scholar
  50. 50.
    Schutte LM, Hayden SW, Gage JR (1997) Lengths of hamstrings and psoas muscles during crouch gait: effects of femoral anteversion. J Orthop Res 15:615–621CrossRefGoogle Scholar
  51. 51.
    Arnold AS, Komattu AV, Delp SL (1997) Internal rotation gait: a compensatory mechanism to restore abduction capacity decreased by bone deformity. Dev Med Child Neurol 39:40–44CrossRefGoogle Scholar
  52. 52.
    Davids JR, Benfanti P, Blackhurst DW, Allen BL (2002) Assessment of femoral anteversion in children with cerebral palsy: accuracy of the trochanteric prominence angle test. J Pediatr Orthop 22:173–178Google Scholar
  53. 53.
    Seber S, Hazer B, Köse N, Göktürk E, Günal I, Turgut A (2000) Rotational profile of the lower extremity and foot progression angle: computerized tomographic examination of 50 male adults. Arch Orthop Trauma Surg 120:255–258CrossRefGoogle Scholar
  54. 54.
    Passmore E, Pandy MG, Graham HK, Sangeux M (2016) Measuring femoral torsion in vivo using freehand 3-D ultrasound imaging. Ultrasound Med Biol 42:619–623CrossRefGoogle Scholar
  55. 55.
    Robin J, Graham HK, Selber P, Dobson F, Smith K, Baker R (2008) Proximal femoral geometry in cerebral palsy: a population-based cross-sectional study. J Bone Joint Surg Br 90:1372–1379CrossRefGoogle Scholar
  56. 56.
    Aktas S, Aiona MD, Orendurff M (2000) Evaluation of rotational gait abnormality in the patients cerebral palsy. J Pediatr Orthop 20:217–220Google Scholar
  57. 57.
    Maganaris CN, Baltzopoulos V, Sargeant AJ (1998) In vivo measurements of the triceps surae complex architecture in man: implications for muscle function. J Physiol 512:603–614CrossRefGoogle Scholar
  58. 58.
    Bénard MR, Becher JG, Harlaar J, Huijing PA, Jaspers RT (2009) Anatomical information is needed in ultrasound imaging of muscle to avoid potentially substantial errors in measurement of muscle geometry. Muscle Nerve 39:652–665CrossRefGoogle Scholar
  59. 59.
    Klimstra M, Dowling J, Durkin JL, MacDonald M (2007) The effect of ultrasound probe orientation on muscle architecture measurement. J Electromyogr Kinesiol 17:504–514CrossRefGoogle Scholar
  60. 60.
    Seynnes OR, Bojsen-Moller J, Albracht K, Arndt A, Cronin N, Finni T et al (2015) Ultrasound-based testing of tendon mechanical properties: a critical evaluation. J Appl Physiol 118:133–141CrossRefGoogle Scholar
  61. 61.
    Gillett JG, Barrett RS, Lichtwark GA (2013) Reliability and accuracy of an automated tracking algorithm to measure controlled passive and active muscle fascicle length changes from ultrasound. Comput Methods Biomech Biomed Eng 16:678–687CrossRefGoogle Scholar
  62. 62.
    Cronin NJ, Carty CP, Barrett RS, Lichtwark G (2011) Automatic tracking of medial gastrocnemius fascicle length during human locomotion. J Appl Physiol 111:1491–1496CrossRefGoogle Scholar
  63. 63.
    Maganaris CN, Paul JP (2000) Load-elongation characteristics of in vivo human tendon and aponeurosis. J Exp Biol 203:751–756Google Scholar
  64. 64.
    Gerus P, Rao G, Berton E (2012) Subject-specific tendon-aponeurosis definition in hill-type model predicts higher muscle forces in dynamic tasks. PLoS One 7:e44406ADSCrossRefGoogle Scholar
  65. 65.
    Zajac FE (1989) Muscle and tendon: properties, models, scaling, and application to biomechanics and motor control. Crit Rev Biomed Eng 17:359–411Google Scholar
  66. 66.
    Domire ZJ, Challis JH (2007) The influence of an elastic tendon on the force producing capabilities of a muscle during dynamic movements. Comput Methods Biomech Biomed Eng 10:337–341CrossRefGoogle Scholar
  67. 67.
    Gerus P, Rao G, Berton E (2015) Ultrasound-based subject-specific parameters improve fascicle behaviour estimation in Hill-type muscle model. Comput Methods Biomech Biomed Eng 18:116–123Google Scholar
  68. 68.
    de Oliveira LF, Menegaldo LL (2010) Individual-specific muscle maximum force estimation using ultrasound for ankle joint torque prediction using an EMG-driven Hill-type model. J Biomech 43:2816–2821CrossRefGoogle Scholar
  69. 69.
    Li L, Tong K, Song R, Koo TKK (2007) Is maximum isometric muscle stress the same among prime elbow flexors? Clin Biomech 22:874–883CrossRefGoogle Scholar
  70. 70.
    Li L, Tong KY, Hu XL, Hung LK, Koo TKK (2009) Incorporating ultrasound-measured musculotendon parameters to subject-specific EMG-driven model to simulate voluntary elbow flexion for persons after stroke. Clin Biomech 24:101–109CrossRefGoogle Scholar
  71. 71.
    Lai A, Lichtwark GA, Schache AG, Lin Y-C, Brown NAT, Pandy MG (2015) In vivo behavior of the human soleus muscle with increasing walking and running speeds. J Appl Physiol 118:1266–1275CrossRefGoogle Scholar
  72. 72.
    Farris DJ, Sawicki GS (2012) Human medial gastrocnemius force–velocity behavior shifts with locomotion speed and gait. Proc Natl Acad Sci 109:977–982ADSCrossRefGoogle Scholar
  73. 73.
    Farris DJ, Robertson BD, Sawicki GS (2013) Elastic ankle exoskeletons reduce soleus muscle force but not work in human hopping. J Appl Physiol 115:579–585CrossRefGoogle Scholar
  74. 74.
    Arnold EM, Hamner SR, Seth A, Millard M, Delp SL (2013) How muscle fiber lengths and velocities affect muscle force generation as humans walk and run at different speeds. J Exp Biol 216:2150–2160CrossRefGoogle Scholar
  75. 75.
    Farris DJ, Hicks JL, Delp SL, Sawicki GS (2014) Musculoskeletal modelling deconstructs the paradoxical effects of elastic ankle exoskeletons on plantar–flexor mechanics and energetics during hopping. J Exp Biol 217:4018–4028CrossRefGoogle Scholar
  76. 76.
    Lai A, Schache AG, Lin Y-C, Pandy MG (2014) Tendon elastic strain energy in the human ankle plantar-flexors and its role with increased running speed. J Exp Biol 217:3159–3168CrossRefGoogle Scholar
  77. 77.
    Hicks JL, Uchida TK, Seth A, Rajagopal A, Delp SL (2014) Is my model good enough? Best practices for verification and validation of musculoskeletal models and simulations of human movement. J Biomech Eng 137:1–24Google Scholar
  78. 78.
    Herbert RD, Clarke J, Kwah LK, Diong J, Martin J, Clarke EC et al (2011) In vivo passive mechanical behaviour of muscle fascicles and tendons in human gastrocnemius muscle–tendon units. J Physiol 589:5257–5267CrossRefGoogle Scholar
  79. 79.
    Bolsterlee B, Gandevia SC, Herbert RD (2016) Ultrasound imaging of the human medial gastrocnemius muscle: how to orient the transducer so that muscle fascicles lie in the image plane. J Biomech 49:1002–1008Google Scholar
  80. 80.
    Huijing PA, Baan GC (1992) Stimulation level-dependent length-force and architectural characteristics of rat gastrocnemius muscle. J Electromyogr Kinesiol 2:112–120CrossRefGoogle Scholar
  81. 81.
    Lieber RL, Jacobson MD, Fazeli BM, Abrams RA, Botte MJ (1992) Architecture of selected muscles of the arm and forearm: anatomy and implications for tendon transfer. J Hand Surg Am 17:787–798CrossRefGoogle Scholar
  82. 82.
    Esformes JI, Narici MV, Maganaris CN (2002) Measurement of human muscle volume using ultrasonography. Eur J Appl Physiol 87:90–92CrossRefGoogle Scholar
  83. 83.
    Zheng N, Fleisig GS, Escamilla RF, Barrentine SW (1998) An analytical model of the knee for estimation of internal forces during exercise. J Biomech 31:963–967CrossRefGoogle Scholar
  84. 84.
    Blemker SS, Pinsky PM, Delp SL (2005) A 3D model of muscle reveals the causes of nonuniform strains in the biceps brachii. J Biomech 38:657–665CrossRefGoogle Scholar
  85. 85.
    Korstanje JWH, Selles RW, Stam HJ, Hovius SER, Bosch JG (2010) Development and validation of ultrasound speckle tracking to quantify tendon displacement. J Biomech 43:1373–1379CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  1. 1.Department of Mechanical EngineeringUniversity of MelbourneMelbourneAustralia
  2. 2.Hugh Williamson Gait Analysis LaboratoryThe Royal Children’s HospitalMelbourneAustralia
  3. 3.Gait Lab and OrthopaedicsThe Murdoch Childrens Research InstituteMelbourneAustralia
  4. 4.Neuromuscular Mechanics Laboratory, Department of Biomedical Physiology and KinesiologySimon Fraser UniversityBurnabyCanada

Personalised recommendations