Skip to main content
Top
Published in: BMC Medical Imaging 1/2021

Open Access 01-12-2021 | Magnetic Resonance Imaging | Research

Spatial frequency analysis detects altered tissue organization following hamstring strain injury at time of injury but not return to sport

Authors: Scott K. Crawford, Christa M. Wille, Mikel R. Stiffler-Joachim, Kenneth S. Lee, Greg R. Bashford, Bryan C. Heiderscheit

Published in: BMC Medical Imaging | Issue 1/2021

Login to get access

Abstract

Background

Hamstring strain injury (HSI) diagnosis is often corroborated using ultrasound. Spatial frequency analysis (SFA) is a quantitative ultrasound method that has proven useful in characterizing altered tissue organization. The purpose of this study was to determine changes in muscular tissue organization using SFA following HSI.

Methods

Ultrasound B-mode images were captured at time of injury (TOI) and return to sport (RTS) in collegiate athletes who sustained an HSI. Spatial frequency parameters extracted from two-dimensional Fourier Transforms in user-defined regions of interest (ROI) were analyzed. Separate ROIs encompassed injured and adjacent tissue within the same image of the injured limb and mirrored locations in the contralateral limb at TOI. The ROIs for RTS images were drawn to correspond to the injury-matched location determined from TOI imaging. Peak spatial frequency radius (PSFR) and the fascicular banded pattern relative to image background (Mmax%) were compared between injured and adjacent portions within the same image with separate paired t-tests. Within-image differences of SFA parameters in the injured limb were calculated and compared between TOI and RTS with Wilcoxon rank sum tests.

Results

Within the injured limb at TOI, PSFR differences in injured and healthy regions did not strictly meet statistical significance (p = 0.06), while Mmax% was different between regions (p < 0.001). No differences were observed between regions in the contralateral limb at TOI (PSFR, p = 0.16; Mmax%, p = 0.30). Significant within-image differences in PSFR (p = 0.03) and Mmax% (p = 0.04) at RTS were detected relative to TOI.

Conclusions

These findings are a first step in determining the usefulness of SFA in muscle injury characterization and provide quantitative assessment of both fascicular disruption and edema presence in acute HSI.
Literature
1.
go back to reference Pollock N, James SLJ, Lee JC, Chakraverty R. British athletics muscle injury classification: a new grading system. Br J Sport Med. 2014;48:1347–51.CrossRef Pollock N, James SLJ, Lee JC, Chakraverty R. British athletics muscle injury classification: a new grading system. Br J Sport Med. 2014;48:1347–51.CrossRef
2.
go back to reference Valle X, Alentorn-Geli E, Tol JL, Hamilton B, Garrett WE, Pruna R, et al. Muscle injuries in sports: a new evidence-informed and expert consensus-based classification with clinical application. Sport Med. 2017;47:1241–53.CrossRef Valle X, Alentorn-Geli E, Tol JL, Hamilton B, Garrett WE, Pruna R, et al. Muscle injuries in sports: a new evidence-informed and expert consensus-based classification with clinical application. Sport Med. 2017;47:1241–53.CrossRef
3.
go back to reference Mueller-Wohlfahrt H-W, Haensel L, Mithoefer K, Ekstrand J, English B, McNally S, et al. Terminology and classification of muscle injuries in sport: the Munich consensus statement. Br J Sports Med. 2013;47:342–50.CrossRef Mueller-Wohlfahrt H-W, Haensel L, Mithoefer K, Ekstrand J, English B, McNally S, et al. Terminology and classification of muscle injuries in sport: the Munich consensus statement. Br J Sports Med. 2013;47:342–50.CrossRef
4.
go back to reference Petersen J, Thorborg K, Nielsen MB, Skjødt T, Bolvig L, Bang N, et al. The diagnostic and prognostic value of ultrasonography in soccer players with acute hamstring injuries. Am J Sports Med. 2014;42:399–404.CrossRef Petersen J, Thorborg K, Nielsen MB, Skjødt T, Bolvig L, Bang N, et al. The diagnostic and prognostic value of ultrasonography in soccer players with acute hamstring injuries. Am J Sports Med. 2014;42:399–404.CrossRef
5.
go back to reference van Heumen M, Tol JL, de Vos R-J, Moen MH, Weir A, Orchard J, et al. The prognostic value of MRI in determining reinjury risk following acute hamstring injury: a systematic review. Br J Sports Med. 2017;51:1355–63.CrossRef van Heumen M, Tol JL, de Vos R-J, Moen MH, Weir A, Orchard J, et al. The prognostic value of MRI in determining reinjury risk following acute hamstring injury: a systematic review. Br J Sports Med. 2017;51:1355–63.CrossRef
6.
go back to reference Connell DA, Schneider-Kolsky ME, Hoving JL, Malara F, Buchbinder R, Koulouris G, et al. Longitudinal study comparing sonographic and MRI assessments of acute and healing hamstring injuries. Am J Roentgenol. 2004;183:975–84.CrossRef Connell DA, Schneider-Kolsky ME, Hoving JL, Malara F, Buchbinder R, Koulouris G, et al. Longitudinal study comparing sonographic and MRI assessments of acute and healing hamstring injuries. Am J Roentgenol. 2004;183:975–84.CrossRef
7.
go back to reference Whittaker JL, Ellis R, Hodges PW, Osullivan C, Hides J, Fernandez-Carnero S, et al. Imaging with ultrasound in physical therapy: What is the PT’s scope of practice? A competency-based educational model and training recommendations. Br J Sports Med. 2019;53:1447–53.CrossRef Whittaker JL, Ellis R, Hodges PW, Osullivan C, Hides J, Fernandez-Carnero S, et al. Imaging with ultrasound in physical therapy: What is the PT’s scope of practice? A competency-based educational model and training recommendations. Br J Sports Med. 2019;53:1447–53.CrossRef
8.
go back to reference Lee JC, Healy J. Sonography of Lower Limb Muscle Injury. Am J Roentgenol. 2004;182:341–51.CrossRef Lee JC, Healy J. Sonography of Lower Limb Muscle Injury. Am J Roentgenol. 2004;182:341–51.CrossRef
9.
go back to reference Crema MD, Yamada AF, Guermazi A, Roemer FW, Skaf AY. Imaging techniques for muscle injury in sports medicine and clinical relevance. Curr Rev Musculoskelet Med. 2015;8:154–61.CrossRef Crema MD, Yamada AF, Guermazi A, Roemer FW, Skaf AY. Imaging techniques for muscle injury in sports medicine and clinical relevance. Curr Rev Musculoskelet Med. 2015;8:154–61.CrossRef
10.
go back to reference Chopp-Hurley JN, Wiebenga EG, Bulbrook BD, Keir PJ, Maly MR. Evaluating the relationship between quadriceps muscle quality captured using ultrasound with clinical severity in women with knee osteoarthritis. Clin Biomech. 2020;80:105165.CrossRef Chopp-Hurley JN, Wiebenga EG, Bulbrook BD, Keir PJ, Maly MR. Evaluating the relationship between quadriceps muscle quality captured using ultrasound with clinical severity in women with knee osteoarthritis. Clin Biomech. 2020;80:105165.CrossRef
11.
go back to reference Watanabe Y, Yamada Y, Fukumoto Y, Ishihara T, Yokoyama K, Yoshida T, et al. Echo intensity obtained from ultrasonography images reflecting muscle strength in elderly men. Clin Interv Aging. 2013;8:993–8.CrossRef Watanabe Y, Yamada Y, Fukumoto Y, Ishihara T, Yokoyama K, Yoshida T, et al. Echo intensity obtained from ultrasonography images reflecting muscle strength in elderly men. Clin Interv Aging. 2013;8:993–8.CrossRef
12.
go back to reference Ismail C, Zabal J, Hernandez HJ, Woletz P, Manning H, Teixeira C, et al. Diagnostic ultrasound estimates of muscle mass and muscle quality discriminate between women with and without sarcopenia. Front Physiol. 2015;6:302.CrossRef Ismail C, Zabal J, Hernandez HJ, Woletz P, Manning H, Teixeira C, et al. Diagnostic ultrasound estimates of muscle mass and muscle quality discriminate between women with and without sarcopenia. Front Physiol. 2015;6:302.CrossRef
13.
go back to reference Fukumoto Y, Ikezoe T, Yamada Y, Tsukagoshi R, Nakamura M, Mori N, et al. Skeletal muscle quality assessed from echo intensity is associated with muscle strength of middle-aged and elderly persons. Eur J Appl Physiol. 2012;112:1519–25.CrossRef Fukumoto Y, Ikezoe T, Yamada Y, Tsukagoshi R, Nakamura M, Mori N, et al. Skeletal muscle quality assessed from echo intensity is associated with muscle strength of middle-aged and elderly persons. Eur J Appl Physiol. 2012;112:1519–25.CrossRef
14.
go back to reference Strasser EM, Draskovits T, Praschak M, Quittan M, Graf A. Association between ultrasound measurements of muscle thickness, pennation angle, echogenicity and skeletal muscle strength in the elderly. Age. 2013;35:2377–88.CrossRef Strasser EM, Draskovits T, Praschak M, Quittan M, Graf A. Association between ultrasound measurements of muscle thickness, pennation angle, echogenicity and skeletal muscle strength in the elderly. Age. 2013;35:2377–88.CrossRef
15.
go back to reference Bashford GR, Tomsen N, Arya S, Burnfield JM, Kulig K. Tendinopathy discrimination by use of spatial frequency parameters in ultrasound B-mode images. IEEE Trans Med Imaging. 2008;27:608–15.CrossRef Bashford GR, Tomsen N, Arya S, Burnfield JM, Kulig K. Tendinopathy discrimination by use of spatial frequency parameters in ultrasound B-mode images. IEEE Trans Med Imaging. 2008;27:608–15.CrossRef
16.
go back to reference Kulig K, Chang Y-J, Winiarski S, Bashford GR. Ultrasound-based tendon micromorphology predicts mechanical characteristics of degenerated tendons. Ultrasound Med Biol. 2016;42:664–73.CrossRef Kulig K, Chang Y-J, Winiarski S, Bashford GR. Ultrasound-based tendon micromorphology predicts mechanical characteristics of degenerated tendons. Ultrasound Med Biol. 2016;42:664–73.CrossRef
17.
go back to reference Kulig K, Landel R, Chang YJ, Hannanvash N, Reischl SF, Song P, et al. Patellar tendon morphology in volleyball athletes with and without patellar tendinopathy. Scand J Med Sci Sport. 2013;23:e81–8.CrossRef Kulig K, Landel R, Chang YJ, Hannanvash N, Reischl SF, Song P, et al. Patellar tendon morphology in volleyball athletes with and without patellar tendinopathy. Scand J Med Sci Sport. 2013;23:e81–8.CrossRef
18.
go back to reference Crawford SK, Lee KS, Bashford GR, Heiderscheit BC. Spatial-frequency analysis of the anatomical differences in hamstring muscles. Ultrason Imaging. 2021;43:100–8.CrossRef Crawford SK, Lee KS, Bashford GR, Heiderscheit BC. Spatial-frequency analysis of the anatomical differences in hamstring muscles. Ultrason Imaging. 2021;43:100–8.CrossRef
19.
go back to reference Cassel M, Risch L, Mayer F, Kaplick H, Engel A, Kulig K, 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.CrossRef Cassel M, Risch L, Mayer F, Kaplick H, Engel A, Kulig K, 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.CrossRef
20.
go back to reference Crawford SK, Lee KS, Bashford GR, Heiderscheit BC. Intra-session and inter-rater reliability of spatial frequency analysis methods in skeletal muscle. PLoS ONE. 2020;15:e0235924.CrossRef Crawford SK, Lee KS, Bashford GR, Heiderscheit BC. Intra-session and inter-rater reliability of spatial frequency analysis methods in skeletal muscle. PLoS ONE. 2020;15:e0235924.CrossRef
21.
go back to reference Wangensteen A, Bahr R, Van Linschoten R, Almusa E, Whiteley R, Witvrouw E, et al. MRI appearance does not change in the first 7 days after acute hamstring injury—a prospective study. Br J Sports Med. 2017;51:1087–92.CrossRef Wangensteen A, Bahr R, Van Linschoten R, Almusa E, Whiteley R, Witvrouw E, et al. MRI appearance does not change in the first 7 days after acute hamstring injury—a prospective study. Br J Sports Med. 2017;51:1087–92.CrossRef
22.
go back to reference Heiderscheit BC, Sherry MA, Silder A, Chumanov ES, Thelen DG. Hamstring strain injuries: recommendations for diagnosis, rehabilitation, and injury prevention. J Orthop Sports Phys Ther. 2010;40:67–81.CrossRef Heiderscheit BC, Sherry MA, Silder A, Chumanov ES, Thelen DG. Hamstring strain injuries: recommendations for diagnosis, rehabilitation, and injury prevention. J Orthop Sports Phys Ther. 2010;40:67–81.CrossRef
23.
go back to reference Gielen JL, Robinson P, Van Dyck P, Van der Stappen A, Vanhoenacker FM. Muscle Injuries. In: Imaging of Orthopedic Sports Injuries. Berlin: Springer; 2007. p. 15–39. Gielen JL, Robinson P, Van Dyck P, Van der Stappen A, Vanhoenacker FM. Muscle Injuries. In: Imaging of Orthopedic Sports Injuries. Berlin: Springer; 2007. p. 15–39.
24.
go back to reference Takebayashi S, Takasawa H, Banzai Y, Miki H, Sasaki R, Itoh Y, et al. Sonographic findings in muscle strain injury: clinical and MR imaging correlation. J Ultrasound Med. 1995;14:899–905.CrossRef Takebayashi S, Takasawa H, Banzai Y, Miki H, Sasaki R, Itoh Y, et al. Sonographic findings in muscle strain injury: clinical and MR imaging correlation. J Ultrasound Med. 1995;14:899–905.CrossRef
25.
go back to reference Zaidman CM, Holland MR, Hughes MS. Quantitative ultrasound of skeletal muscle: reliable measurements of calibrated muscle backscatter from different ultrasound systems. Ultrasound Med Biol. 2012;38:1618–25.CrossRef Zaidman CM, Holland MR, Hughes MS. Quantitative ultrasound of skeletal muscle: reliable measurements of calibrated muscle backscatter from different ultrasound systems. Ultrasound Med Biol. 2012;38:1618–25.CrossRef
26.
go back to reference Ho K-Y, Baquet A, Chang Y-J, Chien L-C, Harty M, Bashford G, et al. Factors related to intra-tendinous morphology of Achilles tendon in runners. PLoS ONE. 2019;14:e0221183.CrossRef Ho K-Y, Baquet A, Chang Y-J, Chien L-C, Harty M, Bashford G, et al. Factors related to intra-tendinous morphology of Achilles tendon in runners. PLoS ONE. 2019;14:e0221183.CrossRef
27.
go back to reference Malliaropoulos N, Papacostas E, Kiritsi O, Papalada A, Gougoulias N, Maffulli N. Posterior thigh muscle injuries in elite track and field athletes. Am J Sports Med. 2010;38:1813–9.CrossRef Malliaropoulos N, Papacostas E, Kiritsi O, Papalada A, Gougoulias N, Maffulli N. Posterior thigh muscle injuries in elite track and field athletes. Am J Sports Med. 2010;38:1813–9.CrossRef
28.
go back to reference De Vos RJ, Reurink G, Goudswaard GJ, Moen MH, Weir A, Tol JL. Clinical findings just after return to play predict hamstring re-injury, but baseline MRI findings do not. Br J Sports Med. 2014;48:1377–84.CrossRef De Vos RJ, Reurink G, Goudswaard GJ, Moen MH, Weir A, Tol JL. Clinical findings just after return to play predict hamstring re-injury, but baseline MRI findings do not. Br J Sports Med. 2014;48:1377–84.CrossRef
29.
go back to reference De Smet AA, Best TM. MR imaging of the distribution and location of acute hamstring injuries in athletes. Am J Roentgenol. 2000;174:393–9.CrossRef De Smet AA, Best TM. MR imaging of the distribution and location of acute hamstring injuries in athletes. Am J Roentgenol. 2000;174:393–9.CrossRef
Metadata
Title
Spatial frequency analysis detects altered tissue organization following hamstring strain injury at time of injury but not return to sport
Authors
Scott K. Crawford
Christa M. Wille
Mikel R. Stiffler-Joachim
Kenneth S. Lee
Greg R. Bashford
Bryan C. Heiderscheit
Publication date
01-12-2021
Publisher
BioMed Central
Published in
BMC Medical Imaging / Issue 1/2021
Electronic ISSN: 1471-2342
DOI
https://doi.org/10.1186/s12880-021-00721-1

Other articles of this Issue 1/2021

BMC Medical Imaging 1/2021 Go to the issue