Freehand three-dimensional ultrasound to assess semitendinosus muscle morphology

Helga Haberfehlner, Huub Maas, Jaap Harlaar, Jules G Becher, Annemieke I Buizer, Richard T Jaspers, Helga Haberfehlner, Huub Maas, Jaap Harlaar, Jules G Becher, Annemieke I Buizer, Richard T Jaspers

Abstract

In several neurological disorders and muscle injuries, morphological changes of the m. semitendinosus (ST) are presumed to contribute to movement limitations around the knee. Freehand three-dimensional (3D) ultrasound (US), using position tracking of two-dimensional US images to reconstruct a 3D voxel array, can be used to assess muscle morphology in vivo. The aims of this study were: (i) to introduce a newly developed 3D US protocol for ST; and (ii) provide a first comparison of morphological characteristics determined by 3D US with those measured on dissected cadaveric muscles. Morphological characteristics of ST (e.g. muscle belly length, tendon length, fascicle length and whole muscle volume, and volumes of both compartments) were assessed in six cadavers using a 3D US protocol. Subsequently, ST muscles were removed from the body to measure the same morphological characteristics. Mean differences between morphological characteristics measured by 3D US and after dissection were smaller than 10%. Intra-class correlation coefficients (ICCs) were higher than 0.75 for all variables except for the lengths of proximal fascicles (ICC = 0.58). Measurement of the volume of proximal compartment by 3D US was not feasible, due to low US image quality proximally. We conclude that the presented 3D US protocol allows for reasonably accurate measurements of key morphological characteristics of ST muscle.

Keywords: geometry; hamstrings; muscle architecture; three-dimensional ultrasonography.

© 2016 The Authors. Journal of Anatomy published by John Wiley & Sons Ltd on behalf of Anatomical Society.

Figures

Figure 1
Figure 1
Typical example of semitendinosus muscle (ST) in situ, of a mid‐longitudinal transection of ST and illustration of morphological characteristics. (A) The ST was made visible by removing the skin, subcutaneous tissues, gluteus muscle and the fasciae of ST. Posterior view, proximal of knee axis. (B) Photographic image demonstrating the transection. Starting from the distal end of the most distal fascicle, the blade was perpendicularly orientated on the apex of the oval‐shaped distal aponeurosis. The muscle was cut in the direction of the proximal end of the tendinous inscription. (C) Photographic image of the longitudinal section of ST. (D) Two‐dimensional planimetric model of the morphological variables measured in the mid‐longitudinal plane: distal aponeurosis (ℓadist), proximal aponeurosis (ℓaprox), most distal fascicle of distal compartment (ℓfascdist_d), most proximal fascicles of distal compartment (ℓfascdist_p), most distal fascicle of proximal compartment (ℓfascprox_d), most proximal fascicles of proximal compartment (ℓfascprox_p), intermediate fascicles (ℓfascdist_m, ℓfascprox_m) and tendinous inscription (ℓti). The gray dotted line indicates the muscle line of pull, defined as the line between the proximal end of the most proximal fascicles and the distal end of the most distal fascicle. The blue dotted line indicates the location for the transversal section of ST for assessment of anatomical cross‐sectional area (ACSA). d, distal; l, lateral; m, medial; p, proximal; TI, tendinous inscription.
Figure 2
Figure 2
Typical example of segmented semitendinosus muscle (ST) based on transversal images. ST segmented into the proximal (STprox) (red) and distal compartment (STdist) (yellow), which are separated by the tendinous inscription (TI) (green) viewed from posterior–medial. Top: three representative transversal US images used for segmentation. The concave TI is indicated by a green arrow, visible between the two compartments, the distal aponeurosis (apodist) – also shaped concavely – by a white arrow. Segmentation was performed on transversal images every 5 mm along the muscle belly. Bottom: the image shows the TI (green) and the distal aponeurosis (white), which are orientated in parallel to each other, but opposite in orientation of their concave shapes. Note that the image of this example for the method section was taken from a subject in vivo. In the voxel arrays of the cadavers a segmentation of the proximal compartment was not possible. a, anterior; BF, biceps femoris muscle; l, lateral; m, medial; p, posterior; SM, semimembranosus muscle.
Figure 3
Figure 3
Illustration of anatomical points used for analyzing three‐dimensional ultrasound (3D US) imaging of semitendinosus muscle (ST). Bony landmarks (blue) and points at the ST (red): 1: ischial tuberosity; 2: medial epicondyle; 3: lateral epicondyle; 2–3: estimated knee axis; 4: proximal end of the tendinous inscription; 5: distal end of the tendinous inscription; 6: proximal end of the distal aponeurosis; 7: distal end of the most distal fascicle (i.e. distal end of muscle belly); 8: most distal point of ST tendon visible by ultrasound; 9: point where tendon passes the knee axis. Variables measured as distance between points: 1–7: muscle belly length (ℓm); 1–4: most proximal fascicle of proximal compartment (ℓfascprox_p); 4–6: most proximal fascicle of distal compartment (ℓfascdist_p); 5–7: most distal fascicle of distal compartment (ℓfascdist_d); 6–7: distal aponeurosis (ℓadist); and 7–9: distal tendon length till estimated knee axis (ℓtdist_p). Note that the image of this example for the method section was taken from a subject in vivo. In the voxel arrays of the cadavers, a segmentation of the proximal compartment was not possible.

References

    1. Alexander RM, Vernon A (1975) The dimensions of knee and ankle muscles and the forces they exert. J Hum Mov Stud 1, 115–123.
    1. Baldwin SL, Marutyan KR, Yang M, et al. (2006) Measurements of the anisotropy of ultrasonic attenuation in freshly excised myocardium. J Acoust Soc Am 119, 3130–3139.
    1. Bamber JC, Hill CR, King JA, et al. (1979) Ultrasonic propagation through fixed and unfixed tissues. Ultrasound Med Biol 5, 159–165.
    1. Barber L, Barrett R, Lichtwark G (2009) Validation of a freehand 3D ultrasound system for morphological measures of the medial gastrocnemius muscle. J Biomech 42, 1313–1319.
    1. Bénard MR, Harlaar J, Becher JG, et al. (2011) Effects of growth on geometry of gastrocnemius muscle in children: a three‐dimensional ultrasound analysis. J Anat 219, 388–402.
    1. Bland JM, Altman DG (1986) Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 1, 307–310.
    1. Brand RA, Pedersen DR, Friederich JA (1986) The sensitivity of muscle force predictions to changes in physiologic cross‐sectional area. J Biomech 19, 589–596.
    1. Cutts A (1988) The range of sarcomere lengths in the muscles of the human lower limb. J Anat 160, 79–88.
    1. Faul F, Erdfelder E, Lang AG, et al. (2007) G*Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods 39, 175–191.
    1. Friederich JA, Brand RA (1990) Muscle fiber architecture in the human lower limb. J Biomech 23, 91–95.
    1. Fry NR, Gough M, Shortland AP (2004) Three‐dimensional realisation of muscle morphology and architecture using ultrasound. Gait Posture 20, 177–182.
    1. Gage JR, Schwartz MH, Koop SE, et al. (2009) The identification and treatment of gait problems in cerebral palsy. Mac Keith: Cambridge University Press, London.
    1. Gans C, Bock WJ (1965) The functional significance of muscle architecture – a theoretical analysis. Ergeb Anat Entwicklungsgesch 38, 115–142.
    1. Gans C, Gaunt AS (1991) Muscle architecture in relation to function. J Biomech 24(Suppl 1), 53–65.
    1. Haberfehlner H, Maas H, Harlaar J, et al. (2015) Assessment of net knee moment‐angle characteristics by instrumented hand‐held dynamometry in children with spastic cerebral palsy and typically developing children. J Neuroeng Rehabil 12, 67.
    1. Huijing PA (1985) Architecture of the human gastrocnemius muscle and some functional consequences. Acta Anat (Basel) 123, 101–107.
    1. Huijing PA (1996) Important experimental factors for skeletal muscle modelling: non‐linear changes of muscle length force characteristics as a function of degree of activity. Eur J Morphol 34, 47–54.
    1. Keenan MA, Ure K, Smith CW, et al. (1988) Hamstring release for knee flexion contracture in spastic adults. Clin Orthop Relat Res 236, 221–226.
    1. Kellis E, Galanis N, Natsis K, et al. (2009) Validity of architectural properties of the hamstring muscles: correlation of ultrasound findings with cadaveric dissection. J Biomech 42, 2549–2554.
    1. Kellis E, Galanis N, Natsis K, et al. (2010) Muscle architecture variations along the human semitendinosus and biceps femoris (long head) length. J Electromyogr Kinesiol 20, 1237–1243.
    1. Kellis E, Galanis N, Natsis K, et al. (2012) In vivo and in vitro examination of the tendinous inscription of the human semitendinosus muscle. Cells Tissues Organs 195, 365–376.
    1. Lakens D (2013) Calculating and reporting effect sizes to facilitate cumulative science: a practical primer for t‐tests and ANOVAs. Front Psychol 4, 863.
    1. Lee TC, O'Driscoll KJ, McGettigan P, et al. (1988) The site of the tendinous interruption in semitendinosus in man. J Anat 157, 229–231.
    1. Lieber RL, Loren GJ, Friden J (1994) In vivo measurement of human wrist extensor muscle sarcomere length changes. J Neurophysiol 71, 874–881.
    1. MacGillivray TJ, Ross E, Simpson HA, et al. (2009) 3D freehand ultrasound for in vivo determination of human skeletal muscle volume. Ultrasound Med Biol 35, 928–935.
    1. van der Made AD, Wieldraaijer T, Kerkhoffs GM, et al. (2015) The hamstring muscle complex. Knee Surg Sports Traumatol Arthrosc 23, 2115–2122.
    1. Markee JE, Logue JT Jr, Williams M, et al. (1955) Two‐joint muscles of the thigh. J Bone Joint Surg Am, 37‐A, 125–142.
    1. Martin JN, Vialle R, Denormandie P, et al. (2006) Treatment of knee flexion contracture due to central nervous system disorders in adults. J Bone Joint Surg Am 88, 840–845.
    1. Nishino A, Sanada A, Kanehisa H, et al. (2006) Knee‐flexion torque and morphology of the semitendinosus after ACL reconstruction. Med Sci Sports Exerc 38, 1895–1900.
    1. Pettersen EF, Goddard TD, Huang CC, et al. (2004) UCSF Chimera – a visualization system for exploratory research and analysis. J Comput Chem 25, 1605–1612.
    1. Prager RW, Rohling RN, Gee AH, et al. (1998) Rapid calibration for 3‐D freehand ultrasound. Ultrasound Med Biol 24, 855–869.
    1. Rassier DE, MacIntosh BR, Herzog W (1999) Length dependence of active force production in skeletal muscle. J Appl Physiol (1985) 86, 1445–1457.
    1. Schindelin J, Arganda‐Carreras I, Frise E, et al. (2012) Fiji: an open‐source platform for biological‐image analysis. Nat Methods 9, 676–682.
    1. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9, 671–675.
    1. Silder A, Heiderscheit BC, Thelen DG, et al. (2008) MR observations of long‐term musculotendon remodeling following a hamstring strain injury. Skeletal Radiol 37, 1101–1109.
    1. Straube WL, Arthur RM (1994) Theoretical estimation of the temperature dependence of backscattered ultrasonic power for noninvasive thermometry. Ultrasound Med Biol 20, 915–922.
    1. Tijs C, van Dieen JH, Maas H (2015) Effects of epimuscular myofascial force transmission on sarcomere length of passive muscles in the rat hindlimb. Physiol Rep 3, e12608.
    1. Tsui BC, Dillane D, Pillay J, et al. (2007) Cadaveric ultrasound imaging for training in ultrasound‐guided peripheral nerve blocks: lower extremity. Can J Anaesth 54, 475–480.
    1. Vet HCW, Terwee CB, Mokkink LB, et al. (2011) Measurement in Medicine. New York: Cambridge University Press.
    1. Walker SM, Schrodt GR (1974) I segment lengths and thin filament periods in skeletal muscle fibers of the Rhesus monkey and the human. Anat Rec 178, 63–81.
    1. Ward SR, Eng CM, Smallwood LH, et al. (2009) Are current measurements of lower extremity muscle architecture accurate? Clin Orthop Relat Res 467, 1074–1082.
    1. Weide G, Huijing PA, Maas JC, et al. (2015) Medial gastrocnemius muscle growth during adolescence is mediated by increased fascicle diameter rather than by longitudinal fascicle growth. J Anat 226, 530–541.
    1. Weller R, Pfau T, Ferrari M, et al. (2007) The determination of muscle volume with a freehand 3D ultrasonography system. Ultrasound Med Biol 33, 402–407.
    1. Wickiewicz TL, Roy RR, Powell PL, et al. (1983) Muscle architecture of the human lower limb. Clin Orthop Relat Res 179, 275–283.
    1. Winters TM, Takahashi M, Lieber RL, et al. (2011) Whole muscle length‐tension relationships are accurately modeled as scaled sarcomeres in rabbit hindlimb muscles. J Biomech 44, 109–115.
    1. Woittiez RD, Huijing PA, Rozendal RH (1983) Influence of muscle architecture on the length‐force diagram of mammalian muscle. Pflugers Arch 399, 275–279.
    1. Woodley SJ, Mercer SR (2005) Hamstring muscles: architecture and innervation. Cells Tissues Organs 179, 125–141.

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