Alignment of magnetic sensing and clinical magnetomyography

Neuromuscular diseases are a prevalent cause of prolonged and severe suffering for patients, and with the global population aging, it is increasingly becoming a pressing concern. To assess muscle activity in NMDs, clinicians and researchers typically use electromyography (EMG), which can be either non-invasive using surface EMG, or invasive through needle EMG. Surface EMG signals have a low spatial resolution, and while the needle EMG provides a higher resolution, it can be painful for the patients, with an additional risk of infection. The pain associated with the needle EMG can pose a risk for certain patient groups, such as children. For example, children with spinal muscular atrophy (type of NMD) require regular monitoring of treatment efficacy through needle EMG; however, due to the pain caused by the procedure, clinicians often rely on a clinical assessment rather than needle EMG. Magnetomyography (MMG), the magnetic counterpart of the EMG, measures muscle activity non-invasively using magnetic signals. With super-resolution capabilities, MMG has the potential to improve spatial resolution and, in the meantime, address the limitations of EMG. This article discusses the challenges in developing magnetic sensors for MMG, including sensor design and technology advancements that allow for more specific recordings, targeting of individual motor units, and reduction of magnetic noise. In addition, we cover the motor unit behavior and activation pattern, an overview of magnetic sensing technologies, and evaluations of wearable, non-invasive magnetic sensors for MMG.

[1]  Mathilde Bonnefond,et al.  A New Generation of OPM for High Dynamic and Large Bandwidth MEG: The 4He OPMs—First Applications in Healthy Volunteers , 2023, Sensors.

[2]  C. Braun,et al.  Optically pumped magnetometers detect altered maximal muscle activity in neuromuscular disease , 2022, Frontiers in Neuroscience.

[3]  K. Nazarpour,et al.  Wearable super-resolution muscle–machine interfacing , 2022, Frontiers in Neuroscience.

[4]  K. Nazarpour,et al.  Investigating the Volume Conduction Effect in MMG and EMG during Action Potential Recording , 2022, 2022 29th IEEE International Conference on Electronics, Circuits and Systems (ICECS).

[5]  R. Bowtell,et al.  Magnetoencephalography with optically pumped magnetometers (OPM-MEG): the next generation of functional neuroimaging , 2022, Trends in Neurosciences.

[6]  Todd P. Coleman,et al.  Peripheral Nerve Magnetoneurography With Optically Pumped Magnetometers , 2022, bioRxiv.

[7]  C. Braun,et al.  Muscle Fatigue Revisited – Insights From Optically Pumped Magnetometers , 2021, Frontiers in Physiology.

[8]  L. Gizzi,et al.  Investigating the spatial resolution of EMG and MMG based on a systemic multi-scale model , 2021, Biomechanics and Modeling in Mechanobiology.

[9]  C. Braun,et al.  Optically pumped magnetometers reveal fasciculations non-invasively , 2021, Clinical Neurophysiology.

[10]  C. Braun,et al.  Investigation of the temporal and spatial dynamics of muscular action potentials through optically pumped magnetometers. , 2021, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[11]  M. Farah,et al.  Axonal regeneration and sprouting as a potential therapeutic target for nervous system disorders , 2021, Neural regeneration research.

[12]  T. Vos,et al.  Global estimates of the need for rehabilitation based on the Global Burden of Disease study 2019: a systematic analysis for the Global Burden of Disease Study 2019 , 2020, The Lancet.

[13]  U. Andersen,et al.  Detection of biological signals from a live mammalian muscle using an early stage diamond quantum sensor , 2020, Scientific Reports.

[14]  A. Wickenbrock,et al.  Sensitive magnetometry in challenging environments , 2020, 2008.00082.

[15]  Dario Farina,et al.  Miniaturized Magnetic Sensors for Implantable Magnetomyography , 2020, Advanced Materials Technologies.

[16]  Matthew J. Brookes,et al.  Multi-channel whole-head OPM-MEG: Helmet design and a comparison with a conventional system , 2020, NeuroImage.

[17]  A. Scholey,et al.  Vitamins and Minerals for Energy, Fatigue and Cognition: A Narrative Review of the Biochemical and Clinical Evidence , 2020, Nutrients.

[18]  Igor Savukov,et al.  Diamond magnetometer enhanced by ferrite flux concentrators , 2019, Physical review research.

[19]  Matthew J. Brookes,et al.  Optically pumped magnetometers: From quantum origins to multi-channel magnetoencephalography , 2019, NeuroImage.

[20]  Hari Eswaran,et al.  Magnetomyographic Recordings of Pelvic Floor Activity During Pregnancy and Postpartum: A Novel Non-invasive Approach , 2019, 2019 41st Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC).

[21]  H. Eswaran,et al.  Characterizing pelvic floor muscles activities using magnetomyography , 2018, Neurourology and urodynamics.

[22]  Svenja Knappe,et al.  Optically Pumped Magnetometers for Magneto-Myography to Study the Innervation of the Hand , 2018, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[23]  Robert Oostenveld,et al.  Localizing on-scalp MEG sensors using an array of magnetic dipole coils , 2018, PloS one.

[24]  P. Lumbiganon,et al.  The global epidemiology of preterm birth. , 2018, Best practice & research. Clinical obstetrics & gynaecology.

[25]  D. You,et al.  Levels and trends in child mortality : report 2017 , 2017 .

[26]  University of California,et al.  Miniature cavity-enhanced diamond magnetometer , 2017, 1706.02201.

[27]  Igor Savukov,et al.  High-sensitivity operation of single-beam optically pumped magnetometer in a kHz frequency range , 2017 .

[28]  Thierry Bal,et al.  Local recording of biological magnetic fields using Giant Magneto Resistance-based micro-probes , 2016, Scientific Reports.

[29]  Keiji Enpuku,et al.  SQUIDs in biomagnetism: a roadmap towards improved healthcare , 2016 .

[30]  Roberto Merletti,et al.  Surface Electromyography: Physiology, engineering, and applications , 2016 .

[31]  Ronald L. Walsworth,et al.  Optical magnetic detection of single-neuron action potentials using quantum defects in diamond , 2016, Proceedings of the National Academy of Sciences.

[32]  Hari Eswaran,et al.  Tracking the Changes in Synchrony of the Electrophysiological Activity as the Uterus Approaches Labor Using Magnetomyographic Technique , 2015, Reproductive Sciences.

[33]  Ivana Y. Kuo,et al.  Signaling in muscle contraction. , 2015, Cold Spring Harbor perspectives in biology.

[34]  T. Wolf,et al.  Subpicotesla Diamond Magnetometry , 2014, 1411.6553.

[35]  B. Barrick,et al.  Patients with neuromuscular disorder. , 2013, The Medical clinics of North America.

[36]  André Fabio Kohn,et al.  Experimental and Simulated EMG Responses in the Study of the Human Spinal Cord , 2013 .

[37]  R. Enoka,et al.  Human motor unit recordings: Origins and insight into the integrated motor system , 2011, Brain Research.

[38]  Morton B. Brown,et al.  Correlation between levator ani muscle injuries on magnetic resonance imaging and fecal incontinence, pelvic organ prolapse, and urinary incontinence in primiparous women. , 2010, American journal of obstetrics and gynecology.

[39]  Jau-Shin Lou,et al.  Assessment and Management of Fatigue in Neuromuscular Disease , 2010, The American journal of hospice & palliative care.

[40]  J D Wilson,et al.  Magnetomyographic recording and identification of uterine contractions using Hilbert-wavelet transforms , 2009, Physiological measurement.

[41]  Mario Cifrek,et al.  Surface EMG based muscle fatigue evaluation in biomechanics. , 2009, Clinical biomechanics.

[42]  Hari Eswaran,et al.  Extraction, quantification and characterization of uterine magnetomyographic activity--a proof of concept case study. , 2009, European journal of obstetrics, gynecology, and reproductive biology.

[43]  D. Farina,et al.  Estimating motor unit discharge patterns from high-density surface electromyogram , 2009, Clinical Neurophysiology.

[44]  D. Farina,et al.  Analysis of motor units with high-density surface electromyography. , 2008, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[45]  Y. So,et al.  American Association of Neuromuscular & Electrodiagnostic Medicine evidenced‐based review: Use of surface electromyography in the diagnosis and study of neuromuscular disorders , 2008, Muscle & nerve.

[46]  A. Fletcher Action potential: generation and propagation , 2008, Anaesthesia & Intensive Care Medicine.

[47]  Bert U Kleine,et al.  Using two-dimensional spatial information in decomposition of surface EMG signals. , 2007, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[48]  D. Budker,et al.  Optical magnetometry - eScholarship , 2006, physics/0611246.

[49]  Joshua C. Kline,et al.  Decomposition of surface EMG signals. , 2006, Journal of neurophysiology.

[50]  J. Casillas,et al.  Fatigue in patients with cardiovascular disease. , 2006, Annales de readaptation et de medecine physique : revue scientifique de la Societe francaise de reeducation fonctionnelle de readaptation et de medecine physique.

[51]  S. Ransom,et al.  Childbirth and pelvic floor dysfunction: an epidemiologic approach to the assessment of prevention opportunities at delivery. , 2006, American journal of obstetrics and gynecology.

[52]  Claude Fermon,et al.  Optimised GMR sensors for low and high frequencies applications , 2006 .

[53]  Alex I. Braginski,et al.  Biomagnetism using SQUIDs: status and perspectives , 2006 .

[54]  Hubert Preissl,et al.  Synchronization analysis of the uterine magnetic activity during contractions , 2005, Biomedical engineering online.

[55]  Jean-Yves Hogrel,et al.  Clinical applications of surface electromyography in neuromuscular disorders , 2005, Neurophysiologie Clinique/Clinical Neurophysiology.

[56]  K. Mills,et al.  The basics of electromyography , 2005, Journal of Neurology, Neurosurgery & Psychiatry.

[57]  R. Stein,et al.  The resilience of the size principle in the organization of motor unit properties in normal and reinnervated adult skeletal muscles. , 2004, Canadian journal of physiology and pharmacology.

[58]  Hubert Preissl,et al.  Prediction of labor in term and preterm pregnancies using non-invasive magnetomyographic recordings of uterine contractions. , 2004, American journal of obstetrics and gynecology.

[59]  Dario Farina,et al.  Estimation of average muscle fiber conduction velocity from two-dimensional surface EMG recordings , 2004, Journal of Neuroscience Methods.

[60]  John Clarke,et al.  Superconducting quantum interference devices: State of the art and applications , 2003, Proceedings of the IEEE.

[61]  J D Wilson,et al.  First magnetomyographic recordings of uterine activity with spatial-temporal information using 151 channel sensor array (SARA). , 2003, The Journal of the Arkansas Medical Society.

[62]  D. Farina,et al.  The linear electrode array: a useful tool with many applications. , 2003, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[63]  Hubert Preissl,et al.  First magnetomyographic recordings of uterine activity with spatial-temporal information with a 151-channel sensor array. , 2002, American journal of obstetrics and gynecology.

[64]  E L Morin,et al.  Sampling, noise-reduction and amplitude estimation issues in surface electromyography. , 2002, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[65]  Vladimir Medved,et al.  Standards for Reporting EMG Data , 2000, Journal of Electromyography and Kinesiology.

[66]  J P Clarys,et al.  Electromyography in sports and occupational settings: an update of its limits and possibilities , 2000, Ergonomics.

[67]  V L Towle,et al.  Reorganization of the hand somatosensory cortex following perinatal unilateral brain injury. , 2000, Neuropediatrics.

[68]  M. Godschalk,et al.  Changes in the compound action current amplitudes in relation to the conduction velocity and functional recovery in the reconstructed peripheral nerve , 1999, Muscle & nerve.

[69]  John Clarke,et al.  High-transition-temperature superconducting quantum interference devices , 1999 .

[70]  Gabriel Curio,et al.  Magnetometry of injury currents from human nerve and muscle specimens using Superconducting Quantum Interferences Devices , 1999, Neuroscience Letters.

[71]  Tsunehiro Takeda,et al.  Magnetic fields produced by single motor units in human skeletal muscles , 1999, Clinical Neurophysiology.

[72]  G. Rau,et al.  Estimation of the relationship between the noninvasively detected activity of single motor units and their characteristic pathological changes by modelling. , 1998, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[73]  G. Saade,et al.  Uterine activity during pregnancy and labor assessed by simultaneous recordings from the myometrium and abdominal surface in the rat. , 1998, American journal of obstetrics and gynecology.

[74]  J. Wikswo,et al.  A model of the magnetic fields created by single motor unit compound action potentials in skeletal muscle , 1997, IEEE Transactions on Biomedical Engineering.

[75]  R. Garfield,et al.  Electrical Activity of the Human Uterus During Pregnancy as Recorded from the Abdominal Surface , 1997, Obstetrics and gynecology.

[76]  Carlo J. De Luca,et al.  The Use of Surface Electromyography in Biomechanics , 1997 .

[77]  R. Enoka Morphological Features and Activation Patterns of Motor Units , 1995, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[78]  C Marque,et al.  Uterine electromyography: a critical review. , 1993, American journal of obstetrics and gynecology.

[79]  H P Clamann,et al.  Motor unit recruitment and the gradation of muscle force. , 1993, Physical therapy.

[80]  G Sjøgaard,et al.  Role of exercise-induced potassium fluxes underlying muscle fatigue: a brief review. , 1991, Canadian journal of physiology and pharmacology.

[81]  J. Lenz A review of magnetic sensors , 1990, Proc. IEEE.

[82]  J P Wikswo,et al.  Magnetic field of a single muscle fiber. First measurements and a core conductor model. , 1990, Biophysical journal.

[83]  L J Dorfman,et al.  Motor unit firing rates and firing rate variability in the detection of neuromuscular disorders. , 1989, Electroencephalography and clinical neurophysiology.

[84]  J P Wikswo,et al.  Magnetic field of a nerve impulse: first measurements. , 1980, Science.

[85]  G. Wolfs,et al.  Electromyographic Observations on the Human Uterus during Labour , 1979, Acta obstetricia et gynecologica Scandinavica. Supplement.

[86]  T. Mcguire,et al.  Anisotropic magnetoresistance in ferromagnetic 3d alloys , 1975 .

[87]  D. Cohen,et al.  Magnetomyography: magnetic fields around the human body produced by skeletal muscles , 1972 .

[88]  R. Person,et al.  Discharge frequency and discharge pattern of human motor units during voluntary contraction of muscle. , 1972, Electroencephalography and clinical neurophysiology.

[89]  John Lambe,et al.  QUANTUM INTERFERENCE EFFECTS IN JOSEPHSON TUNNELING , 1964 .

[90]  D. Rubin Normal and abnormal spontaneous activity. , 2019, Handbook of clinical neurology.

[91]  S. Cnattingius,et al.  Risks of stress urinary incontinence and pelvic organ prolapse surgery in relation to mode of childbirth. , 2011, American journal of obstetrics and gynecology.

[92]  T. Cansever,et al.  Anatomic variations of the median nerve in the carpal tunnel: a brief review of the literature. , 2011, Turkish neurosurgery.

[93]  L. Mendell,et al.  Functional Organization of Motoneuron Pool and its Inputs , 2011 .

[94]  Nicola S. Clayton,et al.  What Do Jays Know About Other Minds and Other Times , 2009 .

[95]  ScienceDirect Annales de réadaptation et de médecine physique , 2008 .

[96]  Kurt Jørgensen,et al.  Electromyography and fatigue during prolonged, low-level static contractions , 2004, European Journal of Applied Physiology and Occupational Physiology.

[97]  A. Boxtel,et al.  Optimal signal bandwidth for the recording of surface EMG activity of facial, jaw, oral, and neck muscles. , 2001 .

[98]  G. Saade,et al.  Instrumentation for the diagnosis of term and preterm labour , 1998, Journal of perinatal medicine.

[99]  Robert Plonsey,et al.  Bioelectromagnetism: Principles and Applications of Bioelectric and Biomagnetic Fields , 1995 .

[100]  J P Clarys,et al.  Electrology and localized electrization revisited. , 1994, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[101]  C Marque,et al.  Human abdominal EHG processing for uterine contraction monitoring. , 1989, Biotechnology.

[102]  B Bigland-Ritchie,et al.  Fatigue of submaximal static contractions. , 1986, Acta physiologica Scandinavica. Supplementum.

[103]  V. Zahn Uterine contractions during pregnancy. , 1984, Journal of perinatal medicine.