Spatial frequency analysis (SFA) is a quantitative ultrasound method that characterizes tissue organization. SFA has been used for research involving tendon injury, but may prove useful in similar research involving skeletal muscle. As a first step, we investigated if SFA could detect known architectural differences within hamstring muscles. Ultrasound B-mode images were collected bilaterally at locations corresponding to proximal, mid-belly, and distal thirds along the hamstrings from 10 healthy participants. Images were analyzed in the spatial frequency domain by applying a two-dimensional Fourier Transform in all 6.5 × 6.5 mm kernels in a region of interest corresponding to the central portion of the muscle. SFA parameters (peak spatial frequency radius [PSFR], maximum frequency amplitude [Mmax], sum of frequencies [Sum], and ratio of Mmax to Sum [Mmax%]) were extracted from each muscle location and analyzed by separate linear mixed effects models. Significant differences were observed proximo-distally in PSFR (p = .039), Mmax (p < .0001), and Sum (p < .0001), consistent with architectural descriptions of the hamstring muscles. These results suggest that SFA can detect regional differences of healthy tissue structure within the hamstrings—an important finding for future research in regional muscle structure and mechanics.
ThelenDGChumanovESHoerthDM, et al. Hamstring muscle kinematics during treadmill sprinting. Med Sci Sports Exerc. 2005;37:108-14.
2.
ChumanovESHeiderscheitBCThelenDG.The effect of speed and influence of individual muscles on hamstring mechanics during the swing phase of sprinting. J Biomech. 2007;40:3555-62.
3.
KellisEGalanisNKapetanosG, et al. Architectural differences between the hamstring muscles. J Electromyogr Kinesiol. 2012;22:520-6.
4.
WardSREngCMSmallwoodLH, et al. Are current measurements of lower extremity muscle architecture accurate?Clin Orthop Relat Res. 2009;467:1074-82.
5.
AziziEDeslauriersAR.Regional heterogeneity in muscle fiber strain: the role of fiber architecture. Front Physiol. 2014;5:303.
6.
LieberRLFridénJ.Functional and clinical significance of skeletal muscle architecture. Muscle Nerve. 2000;23:1647-66.
7.
GansC.Fiber architecture and muscle function. Exerc Sport Sci Rev. 1982;10:160-207.
8.
NariciM.Human skeletal muscle architecture studied in vivo by non-invasive imaging techniques: functional significance and applications. J Electromyogr Kinesiol. 1999;9:97-103.
9.
KellisEGalanisNNatsisK, et al. Muscle architecture variations along the human semitendinosus and biceps femoris (long head) length. J Electromyogr Kinesiol. 2010;20:1237-43.
10.
TosovicDMuirheadJCBrownJMM, et al. Anatomy of the long head of biceps femoris: an ultrasound study. Clin Anat. 2016;29:738-45.
11.
SilderAReederSBThelenDG.The influence of prior hamstring injury on lengthening muscle tissue mechanics. J Biomech. 2010;43:2254-60.
12.
KellisE.Intra- and inter-muscular variations in hamstring architecture and mechanics and their implications for injury: a narrative review. Sport Med. 2018;48:2271-83.
13.
RehornMRBlemkerSS.The effects of aponeurosis geometry on strain injury susceptibility explored with a 3D muscle model. J Biomech. 2010;43:2574-81.
14.
FiorentinoNMBlemkerSS.Musculotendon variability influences tissue strains experienced by the biceps femoris long head muscle during high-speed running. J Biomech. 2014;47:3325-33.
15.
TimminsRGShieldAJWilliamsMD, et al. Biceps femoris long head architecture: a reliability and retrospective injury study. Med Sci Sports Exerc. 2015;47:905-13.
16.
TimminsRGBourneMNShieldAJ, et al. Short biceps femoris fascicles and eccentric knee flexor weakness increase the risk of hamstring injury in elite football (soccer): a prospective cohort study. Br J Sports Med. 2016;50:1524-35.
17.
MiyamotoNKimuraNHirataK.Nonuniform distribution of passive muscle stiffness within hamstring. Scand J Med Sci Sports. 2020;30:1729-38.
18.
HegyiACsalaDPéterA, et al. High-density electromyography activity in various hamstring exercises. Scand J Med Sci Sport. 2019;29:34-43.
19.
ChlebounGSFranceARCrillMT, et al. In vivo measurement of fascicle length and pennation angle of the human biceps femoris muscle. Cells Tissues Organs. 2001;169:401-9.
20.
KwahLKPintoRZDiongJ, et al. Reliability and validity of ultrasound measurements of muscle fascicle length and pennation in humans: a systematic review. J Appl Physiol. 2013;114:761-9.
21.
KellisEGalanisNNatsisK, et al. Validity of architectural properties of the hamstring muscles: correlation of ultrasound findings with cadaveric dissection. J Biomech. 2009;42:2549-54.
22.
PotierTGAlexanderCMSeynnesOR.Effects of eccentric strength training on biceps femoris muscle architecture and knee joint range of movement. Eur J Appl Physiol. 2009;105: 939-44.
23.
SantosRValamatosMJMil-HomensP, et al. Muscle thickness and echo-intensity changes of the quadriceps femoris muscle during a strength training program. Radiography. 2018;24:e75-e84.
24.
BourneMNDuhigSJTimminsRG, et al. Impact of the Nordic hamstring and hip extension exercises on hamstring architecture and morphology: implications for injury prevention. Br J Sports Med. 2017;51:469-77.
25.
GaoJMemmottBPoulsonJ, et al. Quantitative ultrasound imaging to assess skeletal muscles in adults with multiple sclerosis: a feasibility study. J Ultrasound Med. 2019;38:2915-23.
26.
PillenSScholtenRRZwartsMJ, et al. Quantitative skeletal muscle ultrasonography in children with suspected neuromuscular disease. Muscle Nerve. 2003;27:699-705.
27.
PillenSTakROZwartsMJ, et al. Skeletal muscle ultrasound: correlation between fibrous tissue and echo intensity. Ultrasound Med Biol. 2009;35:443-6.
28.
BashfordGRTomsenNAryaS, et al. Tendinopathy discrimination by use of spatial frequency parameters in ultrasound B-mode images. IEEE Trans Med Imaging. 2008;27:608-15.
29.
KuligKLandelRChangYJ, et al. Patellar tendon morphology in volleyball athletes with and without patellar tendinopathy. Scand J Med Sci Sport. 2013;23:e81-8.
30.
CasselMRischLMayerF, et al. Achilles tendon morphology assessed using image based spatial frequency analysis is altered among healthy elite adolescent athletes compared to recreationally active controls. J Sci Med Sport. 2019;22: 882-6.
31.
CrawfordSKLeeKSBashfordGR, et al. Intra-session and inter-rater reliability of spatial frequency analysis methods in skeletal muscle. PLoS One. 2020;15:e0235924.
32.
WoodleySJMercerSR.Hamstring muscles: architecture and innervation. Cells Tissues Organs. 2005;179:125-41.
33.
PimentaRBlazevichAJFreitasSR.Biceps femoris long-head architecture assessed using different sonographic techniques. Med Sci Sports Exerc. 2018;50:2584-94.
34.
MauritsNMBollenAEWindhausenA, et al. Muscle ultrasound analysis: normal values and differentiation between myopathies and neuropathies. Ultrasound Med Biol. 2003;29:215-25.
35.
BlazevichAJGillNDZhouS.Intra- and intermuscular variation in human quadriceps femoris architecture assessed in vivo. J Anat. 2006;209:289-310.
36.
ZaidmanCMHollandMRAndersonCC, et al. Calibrated quantitative ultrasound imaging of skeletal muscle using backscatter analysis. Muscle Nerve. 2008;38:893-8.
37.
KuligKChangY-JWiniarskiS, et al. Ultrasound-based tendon micromorphology predicts mechanical characteristics of degenerated tendons. Ultrasound Med Biol. 2016;42:664-73.
38.
FaranJJ.Sound scattering by solid cylinders and spheres. J Acoust Soc Am. 1951;23:405-18.
39.
O’BrienPDO’BrienWDRhyneTL, et al. Relation of ultrasonic backscatter and acoustic propagation properties to myofibrillar length and myocardial thickness. Circulation. 1995;91:171-5.
40.
InsanaMFWagnerRFBrownDG, et al. Describing small-scale structure in random media using pulse-echo ultrasound. J Acoust Soc Am. 1990;87:179-92.
41.
van der MadeADWieldraaijerTKerkhoffsGM, et al. The hamstring muscle complex. Knee Surg Sports Traumatol Arthrosc. 2015;23:2115-22.
42.
GarrettWERichFRNikolaouPK, et al. Computed tomography of hamstring muscle strains. Med Sci Sports Exerc. 1989;21:506-14.
43.
CharlesJPSuntaxiFAnderstWJ.In vivo human lower limb muscle architecture dataset obtained using diffusion tensor imaging. PLoS One. 2019;14:e0223531.
44.
ScottSHEngstromCMLoebGE.Morphometry of human thigh muscles. Determination of fascicle architecture by magnetic resonance imaging. J Anat. 1993;182:249-57.
45.
BaliusRPedretCIriarteI, et al. Sonographic landmarks in hamstring muscles. Skeletal Radiol. 2019;48:1675-83.
46.
Binder-MarkeyBIBrodaNMLieberRL.Intramuscular anatomy drives collagen content variation within and between muscles. Front Physiol. 2020;11:293.
47.
CutlipRGBakerBAHollanderM, et al. Injury and adaptive mechanisms in skeletal muscle. J Electromyogr Kinesiol. 2009;19:358-72.
48.
NariciMVBordiniMCerretelliP.Effect of aging on human adductor pollicis muscle function. J Appl Physiol. 1991;71: 1277-81.
49.
LindleRSMetterEJLynchNA, et al. Age and gender comparisons of muscle strength in 654 women and men aged 20-93 yr. J Appl Physiol. 1997;83:1581-7.
Supplementary Material
Please find the following supplemental material available below.
For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.
For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.
