In vivo human lower limb muscle architecture dataset obtained using diffusion tensor imaging

Autoři: James P. Charles aff001;  Felipe Suntaxi aff002;  William J. Anderst aff002
Působiště autorů: Evolutionary Morphology and Biomechanics Lab, Institute of Aging and Chronic Disease, University of Liverpool, Liverpool, United Kingdom aff001;  Biodynamics Lab, Department of Orthopaedic Surgery, University of Pittsburgh, Pennsylvania, United States of America aff002
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: 10.1371/journal.pone.0223531


‘Gold standard’ reference sets of human muscle architecture are based on elderly cadaveric specimens, which are unlikely to be representative of a large proportion of the human population. This is important for musculoskeletal modeling, where the muscle force-generating properties of generic models are defined by these data but may not be valid when applied to models of young, healthy individuals. Obtaining individualized muscle architecture data in vivo is difficult, however diffusion tensor magnetic resonance imaging (DTI) has recently emerged as a valid method of achieving this. DTI was used here to provide an architecture data set of 20 lower limb muscles from 10 healthy adults, including muscle fiber lengths, which are important inputs for Hill-type muscle models commonly used in musculoskeletal modeling. Maximum isometric force and muscle fiber lengths were found not to scale with subject anthropometry, suggesting that these factors may be difficult to predict using scaling or optimization algorithms. These data also highlight the high level of anatomical variation that exists between individuals in terms of lower limb muscle architecture, which supports the need of incorporating subject-specific force-generating properties into musculoskeletal models to optimize their accuracy for clinical evaluation.

Klíčová slova:

Body limbs – Diffusion tensor imaging – Magnetic resonance imaging – Muscle analysis – Muscle fibers – Muscle functions – Sarcomeres – Information architecture


1. Lieber RL, Fridén J. Functional and clinical significance of skeletal muscle architecture. Muscle Nerve. 2000;23(11):1647–66. doi: 10.1002/1097-4598(200011)23:11<1647::aid-mus1>;2-m 11054744.

2. Wickiewicz TL, Roy RR, Powell PL, Edgerton VR. Muscle architecture of the human lower limb. Clin Orthop Relat Res. 1983;(179):275–83. 6617027.

3. Ward SR, Eng CM, Smallwood LH, Lieber RL. Are current measurements of lower extremity muscle architecture accurate? Clin Orthop Relat Res. 2009;467(4):1074–82. doi: 10.1007/s11999-008-0594-8 18972175.

4. Narici MV, Maganaris CN, Reeves ND, Capodaglio P. Effect of aging on human muscle architecture. J Appl Physiol (1985). 2003;95(6):2229–34. Epub 2003/07/08. doi: 10.1152/japplphysiol.00433.2003 12844499.

5. Tate CM, Williams GN, Barrance PJ, Buchanan TS. Lower extremity muscle morphology in young athletes: an MRI-based analysis. Med Sci Sports Exerc. 2006;38(1):122–8. Epub 2006/01/06. doi: 10.1249/01.mss.0000179400.67734.01 16394964.

6. Handsfield GG, Meyer CH, Hart JM, Abel MF, Blemker SS. Relationships of 35 lower limb muscles to height and body mass quantified using MRI. J Biomech. 2014;47(3):631–8. Epub 2013/12/26. doi: 10.1016/j.jbiomech.2013.12.002 24368144.

7. Zajac FE. Muscle and tendon: properties, models, scaling, and application to biomechanics and motor control. Crit Rev Biomed Eng. 1989;17(4):359–411. 2676342.

8. Scovil CY, Ronsky JL. Sensitivity of a Hill-based muscle model to perturbations in model parameters. J Biomech. 2006;39(11):2055–63. Epub 2005/08/09. doi: 10.1016/j.jbiomech.2005.06.005 16084520.

9. Ackland DC, Lin YC, Pandy MG. Sensitivity of model predictions of muscle function to changes in moment arms and muscle-tendon properties: a Monte-Carlo analysis. J Biomech. 2012;45(8):1463–71. Epub 2012/04/14. doi: 10.1016/j.jbiomech.2012.02.023 22507351.

10. O’Neill MC, Lee LF, Larson SG, Demes B, Stern JT, Umberger BR. A three-dimensional musculoskeletal model of the chimpanzee (Pan troglodytes) pelvis and hind limb. J Exp Biol. 2013;216(Pt 19):3709–23. doi: 10.1242/jeb.079665 24006347.

11. Valente G, Pitto L, Testi D, Seth A, Delp SL, Stagni R, et al. Are subject-specific musculoskeletal models robust to the uncertainties in parameter identification? PLoS One. 2014;9(11):e112625. Epub 2014/11/12. doi: 10.1371/journal.pone.0112625 25390896.

12. Navacchia A, Myers CA, Rullkoetter PJ, Shelburne KB. Prediction of In Vivo Knee Joint Loads Using a Global Probabilistic Analysis. J Biomech Eng. 2016;138(3):4032379. doi: 10.1115/1.4032379 26720096.

13. Charles JP, Cappellari O, Spence AJ, Wells DJ, Hutchinson JR. Muscle moment arms and sensitivity analysis of a mouse hindlimb musculoskeletal model. J Anat. 2016;229(4):514–35. doi: 10.1111/joa.12461 27173448.

14. Bujalski P, Martins J, Stirling L. A Monte Carlo analysis of muscle force estimation sensitivity to muscle-tendon properties using a Hill-based muscle model. J Biomech. 2018. Epub 2018/08/28. doi: 10.1016/j.jbiomech.2018.07.045 30146173.

15. Ward SR, Smallwood LH, Lieber RL. Scaling of human lower extremity muscle architecture to skeletal dimensions. In: ISB XXth Congress Cleveland, Ohio. 2005.

16. Modenese L, Ceseracciu E, Reggiani M, Lloyd DG. Estimation of musculotendon parameters for scaled and subject specific musculoskeletal models using an optimization technique. J Biomech. 2016;49(2):141–8. Epub 2015/11/18. doi: 10.1016/j.jbiomech.2015.11.006 26776930.

17. Manal K, Buchanan T. Subject-specific estimates of tendon slack length: A numerical method. Journal of Applied Biomechanics. 2004;20(2):195–203.

18. Winby CR, Lloyd DG, Kirk TB. Evaluation of different analytical methods for subject-specific scaling of musculotendon parameters. J Biomech. 2008;41(8):1682–8. Epub 2008/05/06. doi: 10.1016/j.jbiomech.2008.03.008 18456272.

19. Wu W, Lee PV, Bryant AL, Galea M, Ackland DC. Subject-specific musculoskeletal modeling in the evaluation of shoulder muscle and joint function. J Biomech. 2016;49(15):3626–34. Epub 2016/09/23. doi: 10.1016/j.jbiomech.2016.09.025 28327299.

20. Charles JP, Moon CH, Anderst W. Determining subject-specific lower-limb muscle architecture data for musculoskeletal models using diffusion tensor MRI. J Biomech Eng. 2019;141(6):060905–9. 30098157.

21. Preibisch S, Saalfeld S, Tomancak P. Globally optimal stitching of tiled 3D microscopic image acquisitions. Bioinformatics. 2009;25(11):1463–5. Epub 2009/04/07. doi: 10.1093/bioinformatics/btp184 19346324.

22. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods. 2012;9(7):676–82. Epub 2012/06/30. doi: 10.1038/nmeth.2019 22743772.

23. Jiang H, van Zijl PC, Kim J, Pearlson GD, Mori S. DtiStudio: resource program for diffusion tensor computation and fiber bundle tracking. Comput Methods Programs Biomed. 2006;81(2):106–16. Epub 2006/01/18. doi: 10.1016/j.cmpb.2005.08.004 16413083.

24. Aja-Fernandez S, Niethammer M, Kubicki M, Shenton ME, Westin CF. Restoration of DWI data using a Rician LMMSE estimator. IEEE Trans Med Imaging. 2008;27(10):1389–403. Epub 2008/09/26. doi: 10.1109/TMI.2008.920609 18815091.

25. Cook P, Bai Y, Nedjati-Gilani S, Seunarine K, Hall M, Parker G, et al. Camino: Open-Source Diffusion-MRI Reconstruction and Processing. 14th Scientific Meeting of the International Society for Magnetic Resonance in Medicine, Seattle, WA, USA2006. p. 2759.

26. Bodine SC, Roy RR, Meadows DA, Zernicke RF, Sacks RD, Fournier M, et al. Architectural, histochemical, and contractile characteristics of a unique biarticular muscle: the cat semitendinosus. J Neurophysiol. 1982;48(1):192–201. doi: 10.1152/jn.1982.48.1.192 7119845.

27. Charles JP, Cappellari O, Spence AJ, Hutchinson JR, Wells DJ. Musculoskeletal Geometry, Muscle Architecture and Functional Specialisations of the Mouse Hindlimb. PLoS One. 2016;11(4):e0147669. doi: 10.1371/journal.pone.0147669 27115354.

28. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012;9(7):671–5. doi: 10.1038/nmeth.2089 22930834.

29. Felder A, Ward SR, Lieber RL. Sarcomere length measurement permits high resolution normalization of muscle fiber length in architectural studies. J Exp Biol. 2005;208(Pt 17):3275–9. Epub 2005/08/20. doi: 10.1242/jeb.01763 16109889.

30. Sacks RD, Roy RR. Architecture of the hind limb muscles of cats: functional significance. J Morphol. 1982;173(2):185–95. doi: 10.1002/jmor.1051730206 7120421.

31. Hutchinson JR. Biomechanical modeling and sensitivity analysis of bipedal running ability. I. Extant taxa. J Morphol. 2004;262(1):421–40. doi: 10.1002/jmor.10241 15352201.

32. Medler S. Comparative trends in shortening velocity and force production in skeletal muscles. Am J Physiol Regul Integr Comp Physiol. 2002;283(2):R368–78. doi: 10.1152/ajpregu.00689.2001 12121850.

33. Fukunaga T, Roy RR, Shellock FG, Hodgson JA, Edgerton VR. Specific tension of human plantar flexors and dorsiflexors. J Appl Physiol (1985). 1996;80(1):158–65. Epub 1996/01/01. doi: 10.1152/jappl.1996.80.1.158 8847297.

34. Maganaris CN, Baltzopoulos V, Ball D, Sargeant AJ. In vivo specific tension of human skeletal muscle. J Appl Physiol (1985). 2001;90(3):865–72. Epub 2001/02/22. doi: 10.1152/jappl.2001.90.3.865 11181594.

35. Powell PL, Roy RR, Kanim P, Bello MA, Edgerton VR. Predictability of skeletal muscle tension from architectural determinations in guinea pig hindlimbs. J Appl Physiol Respir Environ Exerc Physiol. 1984;57(6):1715–21. doi: 10.1152/jappl.1984.57.6.1715 6511546.

36. Lieber RL, Blevins FT. Skeletal muscle architecture of the rabbit hindlimb: functional implications of muscle design. J Morphol. 1989;199(1):93–101. doi: 10.1002/jmor.1051990108 2921772.

37. Payne RC, Hutchinson JR, Robilliard JJ, Smith NC, Wilson AM. Functional specialisation of pelvic limb anatomy in horses (Equus caballus). J Anat. 2005;206(6):557–74. doi: 10.1111/j.1469-7580.2005.00420.x 15960766.

38. Williams SB, Wilson AM, Rhodes L, Andrews J, Payne RC. Functional anatomy and muscle moment arms of the pelvic limb of an elite sprinting athlete: the racing greyhound (Canis familiaris). J Anat. 2008;213(4):361–72. doi: 10.1111/j.1469-7580.2008.00961.x 18657259.

39. Williams SB, Payne RC, Wilson AM. Functional specialisation of the pelvic limb of the hare (Lepus europeus). J Anat. 2007;210(4):472–90. doi: 10.1111/j.1469-7580.2007.00704.x 17362487.

40. Allen V, Elsey RM, Jones N, Wright J, Hutchinson JR. Functional specialization and ontogenetic scaling of limb anatomy in Alligator mississippiensis. J Anat. 2010;216(4):423–45. doi: 10.1111/j.1469-7580.2009.01202.x 20148991.

41. Paxton H, Anthony NB, Corr SA, Hutchinson JR. The effects of selective breeding on the architectural properties of the pelvic limb in broiler chickens: a comparative study across modern and ancestral populations. J Anat. 2010;217(2):153–66. doi: 10.1111/j.1469-7580.2010.01251.x 20557402.

42. Hsu EW, Mori S. Analytical expressions for the NMR apparent diffusion coefficients in an anisotropic system and a simplified method for determining fiber orientation. Magn Reson Med. 1995;34(2):194–200. doi: 10.1002/mrm.1910340210 7476078.

43. Damon BM, Ding Z, Anderson AW, Freyer AS, Gore JC. Validation of diffusion tensor MRI-based muscle fiber tracking. Magn Reson Med. 2002;48(1):97–104. doi: 10.1002/mrm.10198 12111936.

44. Deux JF, Malzy P, Paragios N, Bassez G, Luciani A, Zerbib P, et al. Assessment of calf muscle contraction by diffusion tensor imaging. Eur Radiol. 2008;18(10):2303–10. Epub 2008/05/09. doi: 10.1007/s00330-008-1012-z 18463875.

45. Heemskerk AM, Sinha TK, Wilson KJ, Ding Z, Damon BM. Repeatability of DTI-based skeletal muscle fiber tracking. NMR Biomed. 2010;23(3):294–303. doi: 10.1002/nbm.1463 20099372.

46. Sinha U, Sinha S, Hodgson JA, Edgerton RV. Human soleus muscle architecture at different ankle joint angles from magnetic resonance diffusion tensor imaging. J Appl Physiol (1985). 2011;110(3):807–19. doi: 10.1152/japplphysiol.00923.2010 21164150.

47. Froeling M, Nederveen AJ, Heijtel DF, Lataster A, Bos C, Nicolay K, et al. Diffusion-tensor MRI reveals the complex muscle architecture of the human forearm. J Magn Reson Imaging. 2012;36(1):237–48. doi: 10.1002/jmri.23608 22334539.

48. Soares JM, Marques P, Alves V, Sousa N. A hitchhiker’s guide to diffusion tensor imaging. Front Neurosci. 2013;7:31. doi: 10.3389/fnins.2013.00031 23486659.

49. Bolsterlee B, Veeger HE, van der Helm FC, Gandevia SC, Herbert RD. Comparison of measurements of medial gastrocnemius architectural parameters from ultrasound and diffusion tensor images. J Biomech. 2015;48(6):1133–40. Epub 2015/02/16. doi: 10.1016/j.jbiomech.2015.01.012 25682540.

50. Froeling M, Oudeman J, Strijkers GJ, Maas M, Drost MR, Nicolay K, et al. Muscle changes detected with diffusion-tensor imaging after long-distance running. Radiology. 2015;274(2):548–62. Epub 2014/10/03. doi: 10.1148/radiol.14140702 25279435.

51. Damon BM, Froeling M, Buck AK, Oudeman J, Ding Z, Nederveen AJ, et al. Skeletal muscle diffusion tensor-MRI fiber tracking: rationale, data acquisition and analysis methods, applications and future directions. NMR Biomed. 2016. Epub 2016/06/03. doi: 10.1002/nbm.3563 27257975.

52. Sieben JM, van Otten I, Lataster A, Froeling M, Nederveen AJ, Strijkers GJ, et al. In Vivo Reconstruction of Lumbar Erector Spinae Architecture Using Diffusion Tensor MRI. Clin Spine Surg. 2016;29(3):E139–45. doi: 10.1097/BSD.0000000000000036 27007789.

53. Bolsterlee B, Finni T, D’Souza A, Eguchi J, Clarke EC, Herbert RD. Three-dimensional architecture of the whole human soleus muscle in vivo. PeerJ. 2018;6:e4610. Epub 2018/04/24. doi: 10.7717/peerj.4610 29682414.

54. Sahrmann AS, Stott NS, Besier TF, Fernandez JW, Handsfield GG. Soleus muscle weakness in cerebral palsy: Muscle architecture revealed with Diffusion Tensor Imaging. PLoS One. 2019;14(2):e0205944. Epub 2019/02/26. doi: 10.1371/journal.pone.0205944 30802250.

55. Bolsterlee B, D’Souza A, Herbert RD. Reliability and robustness of muscle architecture measurements obtained using diffusion tensor imaging with anatomically constrained tractography. J Biomech. 2019;86:71–8. Epub 2019/02/12. doi: 10.1016/j.jbiomech.2019.01.043 30739766.

56. Bolsterlee B, D’Souza A, Gandevia SC, Herbert RD. How does passive lengthening change the architecture of the human medial gastrocnemius muscle? J Appl Physiol (1985). 2017;122(4):727–38. Epub 2017/01/21. doi: 10.1152/japplphysiol.00976.2016 28104754.

57. Matsukiyo A, Goh AC, Asagai Y. Relationship between muscle-tendon length, range of motion, and resistance to passive movement in children with normal and increased tone. J Phys Ther Sci. 2017;29(2):349–55. Epub 2017/03/08. doi: 10.1589/jpts.29.349 28265172.

58. DeVita P, Hortobagyi T. Age causes a redistribution of joint torques and powers during gait. J Appl Physiol (1985). 2000;88(5):1804–11. Epub 2000/05/08. doi: 10.1152/jappl.2000.88.5.1804 10797145.

59. Scheys L, Spaepen A, Suetens P, Jonkers I. Calculated moment-arm and muscle-tendon lengths during gait differ substantially using MR based versus rescaled generic lower-limb musculoskeletal models. Gait Posture. 2008;28(4):640–8. Epub 2008/06/04. doi: 10.1016/j.gaitpost.2008.04.010 18534855.

60. Scheys L, Loeckx D, Spaepen A, Suetens P, Jonkers I. Atlas-based non-rigid image registration to automatically define line-of-action muscle models: a validation study. J Biomech. 2009;42(5):565–72. Epub 2009/02/24. doi: 10.1016/j.jbiomech.2008.12.014 19232618.

61. Scheys L, Desloovere K, Suetens P, Jonkers I. Level of subject-specific detail in musculoskeletal models affects hip moment arm length calculation during gait in pediatric subjects with increased femoral anteversion. J Biomech. 2011;44(7):1346–53. Epub 2011/02/03. doi: 10.1016/j.jbiomech.2011.01.001 21295307.

62. Prinold JA, Mazzà C, Di Marco R, Hannah I, Malattia C, Magni-Manzoni S, et al. A Patient-Specific Foot Model for the Estimate of Ankle Joint Forces in Patients with Juvenile Idiopathic Arthritis. Ann Biomed Eng. 2016;44(1):247–57. Epub 2015/09/15. doi: 10.1007/s10439-015-1451-z 26374518.

63. Chen X, Sanchez GN, Schnitzer MJ, Delp SL. Changes in sarcomere lengths of the human vastus lateralis muscle with knee flexion measured using in vivo microendoscopy. J Biomech. 2016;49(13):2989–94. Epub 2016/08/03. doi: 10.1016/j.jbiomech.2016.07.013 27481293.

64. Chen X, Delp SL. Human soleus sarcomere lengths measured using in vivo microendoscopy at two ankle flexion angles. J Biomech. 2016;49(16):4164–7. Epub 2016/11/22. doi: 10.1016/j.jbiomech.2016.11.010 27866676.

65. Herbert RD, Heroux ME, Diong J, Bilston LE, Gandevia SC, Lichtwark GA. Changes in the length and three-dimensional orientation of muscle fascicles and aponeuroses with passive length changes in human gastrocnemius muscles. J Physiol. 2015;593(2):441–55. Epub 2015/01/30. doi: 10.1113/jphysiol.2014.279166 25630264.

66. Maganaris CN, Baltzopoulos V, Sargeant AJ. In vivo measurements of the triceps surae complex architecture in man: implications for muscle function. J Physiol. 1998;512 (Pt 2):603–14. Epub 1998/10/09. doi: 10.1111/j.1469-7793.1998.603be.x 9763648.

67. Narici MV, Binzoni T, Hiltbrand E, Fasel J, Terrier F, Cerretelli P. In vivo human gastrocnemius architecture with changing joint angle at rest and during graded isometric contraction. J Physiol. 1996;496 (Pt 1):287–97. Epub 1996/10/01. doi: 10.1113/jphysiol.1996.sp021685 8910216.

68. Chen JS, Basava RR, Zhang Y, Csapo R, Malis V, Sinha U, et al. Pixel-based meshfree modelling of skeletal muscles. Comput Methods Biomech Biomed Eng Imaging Vis. 2016;4(2):73–85. Epub 2016/01/01. doi: 10.1080/21681163.2015.1049712 28748126.

69. Malis V, Sinha U, Csapo R, Narici M, Smitaman E, Sinha S. Diffusion tensor imaging and diffusion modeling: Application to monitoring changes in the medial gastrocnemius in disuse atrophy induced by unilateral limb suspension. J Magn Reson Imaging. 2019;49(6):1655–64. Epub 2018/12/21. doi: 10.1002/jmri.26295 30569482.

70. Ponrartana S, Ramos-Platt L, Wren TA, Hu HH, Perkins TG, Chia JM, et al. Effectiveness of diffusion tensor imaging in assessing disease severity in Duchenne muscular dystrophy: preliminary study. Pediatr Radiol. 2015;45(4):582–9. Epub 2014/09/24. doi: 10.1007/s00247-014-3187-6 25246097.

71. Sinha U, Csapo R, Malis V, Xue Y, Sinha S. Age-related differences in diffusion tensor indices and fiber architecture in the medial and lateral gastrocnemius. J Magn Reson Imaging. 2015;41(4):941–53. Epub 2014/04/29. doi: 10.1002/jmri.24641 24771672.

72. Rosenberg M, Steele KM. Simulated impacts of ankle foot orthoses on muscle demand and recruitment in typically-developing children and children with cerebral palsy and crouch gait. PLoS One. 2017;12(7):e0180219. Epub 2017/07/14. doi: 10.1371/journal.pone.0180219 28704464.

73. Steele KM, Seth A, Hicks JL, Schwartz MS, Delp SL. Muscle contributions to support and progression during single-limb stance in crouch gait. J Biomech. 2010;43(11):2099–105. Epub 2010/05/25. doi: 10.1016/j.jbiomech.2010.04.003 20493489.

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