Foreground Detection Analysis of Ultrasound Image Sequences Identifies Markers of Motor Neurone Disease across Diagnostically Relevant Skeletal Muscles
Kate Bibbings, Peter J Harding, Ian D Loram, Nicholas Combes, Emma F Hodson-Tole, Kate Bibbings, Peter J Harding, Ian D Loram, Nicholas Combes, Emma F Hodson-Tole
Abstract
Diagnosis of motor neurone disease (MND) includes detection of small, involuntary muscle excitations, termed fasciculations. There is need to improve diagnosis and monitoring of MND through provision of objective markers of change. Fasciculations are visible in ultrasound image sequences. However, few approaches that objectively measure their occurrence have been proposed; their performance has been evaluated in only a few muscles; and their agreement with the clinical gold standard for fasciculation detection, intramuscular electromyography, has not been tested. We present a new application of adaptive foreground detection using a Gaussian mixture model (GMM), evaluating its accuracy across five skeletal muscles in healthy and MND-affected participants. The GMM provided good to excellent accuracy with the electromyography ground truth (80.17%-92.01%) and was robust to different ultrasound probe orientations. The GMM provides objective measurement of fasciculations in each of the body segments necessary for MND diagnosis and hence could provide a new, clinically relevant disease marker.
Keywords: Amyotrophic lateral sclerosis; Diagnostics; Electromyography; Feature tracking; Gaussian mixture model; Image processing; Myosonography; Neuromuscular; Ultrasonography.
Copyright © 2019 The Authors. Published by Elsevier Inc. All rights reserved.
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References
- Arts I.M., Overeem S., Pillen S., Kleine B.U., Boekestein W.A., Zwarts M.J., Jurgen Schelhaas H. Muscle ultrasonography: A diagnostic tool for amyotrophic lateral sclerosis. Clin Neurophysiol. 2012;123:1662–1667.
- Baumer D., Talbot K., Turner M.R. Advances in motor neurone disease. J R Soc Med. 2014;107:14–21.
- Botter A., Vieira T.M.M., Loram I.D., Merletti R., Hodson-Tole E.F. A novel system of electrodes transparent to ultrasound for simultaneous detection of myoelectric activity and B-mode ultrasound images of skeletal muscles. J Appl Physiol. 2013;115:1203–1214.
- Darby J., Hodson-Tole E.F., Costen N., Loram I.D. Automated regional analysis of B-mode ultrasound images of skeletal muscle movement. J Appl Physiol. 2012;112:313–327.
- Darby J., Li B., Costen N., Loram I., Hodson-Tole E. Estimating skeletal muscle fascicle curvature from B-mode Ultrasound image sequences. IEEE Trans Biomed Eng. 2013;60:1935–1945.
- de Carvalho M., Dengler R., Eisen A., England J.D., Kaji R., Kimura J., Mills K., Mitsumoto H., Nodera H., Shefner J., Swash M. Electrodiagnostic criteria for diagnosis of ALS. Clin Neurophysiol. 2008;119:497–503.
- de Carvalho M., Swash M. Fasciculation discharge frequency in amyotrophic lateral sclerosis and related disorders. Clin Neurophysiol. 2016;127:2257–2262.
- Fermont J., Arts I.M.P., Overeem S., Kleine B.U., Schelhaas H.J., Zwarts M.J. Prevalence and distribution of fasciculations in healthy adults: Effect of age, caffeine consumption and exercise. Amyotrophic Lateral Scler. 2010;11:181–186.
- Grimm A., Prell T., Décard B.F., Schumacher U., Witte O.W., Axer H., Grosskreutz J. Muscle ultrasonography as an additional diagnostic tool for the diagnosis of amyotrophic lateral sclerosis. Clin Neurophysiol. 2015;126:820–827.
- Hanley J.A., McNeil B.J. The meaning and use of the area under a receiver operating characteristic (ROC) curve. Radiology. 1982;143:29–36.
- Harding P.J., Hodson-Tole E.F., Cunningham R., Loram I., Costen N. Automated detection of skeletal muscle twitches from B-mode ultrasound images: An application to motor neuron disease. Proceedings, 21st International Conference on Pattern Recognition (ICPR 2012); Piscataway, NJ; IEEE; 2012. pp. 2630–2633.
- Harding P.J., Loram I.D., Combes N., Hodson-Tole E.F. Ultrasound-based detection of fasciculations in healthy and diseased muscles. IEEE Trans Biomed Eng. 2016;63:512–518.
- Jahanmiri-Nezhad F., Barkhaus P.E., Rymer W.Z., Zhou P. Sensitivity of fasciculation potential detection is dramatically reduced by spatial filtering of surface electromyography. Clin Neurophysiol. 2014;125:1498–1500.
- Johansson M.T., Ellegaard H.R., Tankisi H., Fuglsang-Frederiksen A., Qerama E. Fasciculations in nerve and muscle disorders: A prospective study of muscle ultrasound compared to electromyography. Clin Neurophysiol. 2017;128:2250–2257.
- KaewTraKulPong P., Bowden R. 2nd European Workshop on Advanced Video Based Surveillance Systems. Kluwer Academic; 2001. An improved adaptive background mixture model for realtime tracking with shadow detection; pp. 1–5.
- Kiernan M.C., Vucic S., Cheah B.C., Turner M.R., Eisen A., Hardiman O., Burrell J.R., Zoing M.C. Amyotrophic lateral sclerosis. Lancet. 2011;377:942–955.
- Krämer H.H., Vlazak A., Döring K., Tanislav C., Allendörfer J., Kaps M. Excellent interrater agreement for the differentiation of fasciculations and artefacts: A dynamic myosonography study. Clin Neurophysiol. 2014;125 2441–2145.
- Lucas B.D., Kanade T. An iterative image registration technique with an application to stereo vision. Proceedings of the 1981 DARPA Image Understanding Workshop; Washington, DC; 1981. pp. 121–130.
- Maurits N.M., Bollen A.E., Windhausen A., De Jager A.E.J., Van Der Hoeven J.H. Muscle ultrasound analysis: Normal values and differentiation between myopathies and neuropathies. Ultrasound Med Biol. 2003;29:215–225.
- McGill K.C., Cummins K.L., Dorfman L.J. Automatic Decomposition of the Clinical Electromyogram. IEEE Trans. Biomedical Engineering. 1985;32:470–477.
- Miguez D., Hodson-Tole E.F., Loram I., Harding P.J. A technical note on variable inter-frame interval as a cause of non-physiological experimental artefacts in ultrasound. R Soc Open Sci. 2017;4
- Mills K.R. Characteristics of fasciculations in amyotrophic lateral sclerosis and the benign fasciculation syndrome. Brain. 2010;133:3458–3469.
- Misawa S., Noto Y., Shibuya K., Isose S., Sekiguchi Y., Nasu S., Kuwabara S. Ultrasonographic detection of fasciculations markedly increases diagnostic sensitivity of ALS. Neurology. 2011;77:1532–1537.
- Namburete A.I.L., Rana M., Wakeling J.M. Computational methods for quantifying in vivo muscle fascicle curvature from ultrasound images. J Biomech. 2011;44:2538–2543.
- Noto Y., Shibuya K., Shahrizaila N., Huynh W., Matamala J.M., Dharmadasa T., Kiernan M.C. Detection of fasciculations in amyotrophic lateral sclerosis: The optimal ultrasound scan time. Muscle Nerve. 2017;56:1068–1071.
- Pillen S., Arts I.M.P., Zwarts M.J. Muscle ultrasound in neuromuscular disorders. Muscle Nerve. 2008;37:679–693.
- Rana M., Wakeling J.M. In-vivo determination of 3D muscle architecture of human muscle using free hand ultrasound. J Biomech. 2011;44:2129–2135.
- Rana M., Hamarneh G., Wakeling J.M. Automated tracking of muscle fascicle orientation in B-mode ultrasound images. J Biomech. 2009;42:2068–2073.
- Reimers C.D., Ziemann U., Scheel A., Rieckmann P., Kunkel M., Kurth C. Fasciculations: Clinical, electromyographic, and ultrasonographic assessment. J Neurol. 1996;243:579–584.
- Shi J., Tomasi C. Good features to track. Proceedings, IEEE Conference on Computer Vision and Pattern Recognition; Piscataway, NJ; IEEE; 1994. pp. 593–600.
- Stauffer C., Grimson W.E.L. Adaptive background mixture models for real-time tracking. Proceedings, 1999 IEEE Computer Society Conference on Computer Vision and Pattern Recognition (Cat. No PR00149); Piscataway, NJ; IEEE; 1999. pp. 1–252.
- Takamatsu N., Nodera H., Mori A., Maruyama-Saladini K., Osaki Y., Shimatani Y., Oda M., Izumi Y., Kaji R. Which muscle shows fasciculations by ultrasound in patients with ALS? J Med Invest. 2016;63:49–53.
- Tsugawa J., Dharmadasa T., Ma Y., Huynh W., Vucic S., Kiernan M.C. Fasciculation intensity and disease progression in amyotrophic lateral sclerosis. Clin Neurophysiol. 2018;129:2149–2154.
- Tsuji Y., Noto Y.I., Shiga K., Teramukai S., Nakagawa M., Mizuno T. A muscle ultrasound score in the diagnosis of amyotrophic lateral sclerosis. Clin Neurophysiol. 2017;128:1069–1074.
- Wagner R.F., Smith S.W., Sandrik J.M., Lopez H. Statistics of speckle in ultrasound B-scans. IEEE Trans Sonics Ultrason. 1983;30:156–163.
- Walker F.O., Donofrio P.D., Harpold G.J., Ferrell W.G. Sonographic imaging of muscle contraction and fasciculations: A correlation with electromyography. Muscle Nerve. 1990;13:33–39.
Source: PubMed