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Bioheat Model of Spinal Column Heating During High-Density Spinal Cord Stimulation

      Abstract

      Introduction

      High-density (HD) spinal cord stimulation (SCS) delivers higher charge per time by increasing frequency and/or pulse duration, thus increasing stimulation energy. Previously, through phantom studies and computational modeling, we demonstrated that stimulation energy drives spinal tissue heating during kHz SCS. In this study, we predicted temperature increases in the spinal cord by HD SCS, the first step in considering the potential impact of heating on clinical outcomes.

      Materials and Methods

      We adapted a high-resolution computer-aided design–derived spinal cord model, both with and without a lead encapsulation layer, and applied bioheat transfer finite element method multiphysics to predict temperature increases during SCS. We simulated HD SCS using a commercial SCS lead (eight contacts) with clinically relevant intensities (voltage-controlled: 0.5–7 Vrms) and electrode configuration (proximal bipolar, distal bipolar, guarded tripolar [+−+], and guarded quadripolar [+−−+]). Results were compared with the conventional and 10-kHz SCS (current-controlled).

      Results

      HD SCS waveform energy (reflecting charge per second) governs joule heating in the spinal tissues, increasing temperature supralinearly with stimulation root mean square. Electrode configuration and tissue properties (an encapsulation layer) influence peak tissue temperature increase—but in a manner distinct for voltage-controlled (HD SCS) compared with current-controlled (conventional/10-kHz SCS) stimulation. Therefore, depending on conditions, HD SCS could produce heating greater than that of 10-kHz SCS. For example, with an encapsulation layer, using guarded tripolar configuration (500-Hz, 250-μs pulse width, 5-Vpeak HD SCS), the peak temperature increases were 0.36 °C at the spinal cord and 1.78 °C in the epidural space.

      Conclusions

      As a direct consequence of the higher charge, HD SCS increases tissue heating; voltage-controlled stimulation introduces special dependencies on electrode configuration and lead encapsulation (reflected in impedance). If validated with an in vivo measurement as a possible mechanism of action of SCS, bioheat models of HD SCS serve as tools for programming optimization.

      Keywords

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      References

        • Wille F.
        • Breel J.S.
        • Bakker E.W.P.
        • Hollmann M.W.
        Altering conventional to high density spinal cord stimulation: an energy dose-response relationship in neuropathic pain therapy.
        Neuromodulation. 2017; 20: 71-80https://doi.org/10.1111/ner.12529
        • Reddy C.G.
        • Dalm B.D.
        • Flouty O.E.
        • Gillies G.T.
        • Howard M.A.
        • Brennan T.J.
        Comparison of conventional and kilohertz frequency epidural stimulation in patients undergoing trialing for spinal cord stimulation: clinical considerations.
        World Neurosurg. 2016; 88: 586-591https://doi.org/10.1016/j.wneu.2015.10.088
      1. High-density spinal cord stimulation for the treatment of pain in the rehabilitation patient. Anesthesia Key. Accessed October 31, 2021. https://aneskey.com/high-density-spinal-cord-stimulation-for-the-treatment-of-pain-in-the-rehabilitation-patient/

        • Miller J.P.
        • Eldabe S.
        • Buchser E.
        • Johanek L.M.
        • Guan Y.
        • Linderoth B.
        Parameters of spinal cord stimulation and their role in electrical charge delivery: a review.
        Neuromodulation. 2016; 19: 373-384https://doi.org/10.1111/ner.12438
        • De Jaeger M.
        • van Hooff R.J.
        • Goudman L.
        • et al.
        High-density in spinal cord stimulation: virtual expert registry (DISCOVER): study protocol for a prospective observational trial.
        Anesth Pain Med. 2017; 7e13640https://doi.org/10.5812/aapm.13640
        • Sweet J.
        • Badjatiya A.
        • Tan D.
        • Miller J.
        Paresthesia-free high-density spinal cord stimulation for postlaminectomy syndrome in a prescreened population: a prospective case series.
        Neuromodulation. 2016; 19: 260-267https://doi.org/10.1111/ner.12357
        • Provenzano D.A.
        • Rebman J.
        • Kuhel C.
        • Trenz H.
        • Kilgore J.
        The efficacy of high-density spinal cord stimulation among trial, implant, and conversion patients: a retrospective case series.
        Neuromodulation. 2017; 20: 654-660https://doi.org/10.1111/ner.12612
        • Zannou A.L.
        • Khadka N.
        • Truong D.Q.
        • et al.
        Temperature increases by kilohertz frequency spinal cord stimulation.
        Brain Stimul. 2019; 12: 62-72https://doi.org/10.1016/j.brs.2018.10.007
        • Zannou A.L.
        • Khadka N.
        • FallahRad M.
        • Truong D.Q.
        • Kopell B.H.
        • Bikson M.
        Tissue temperature increases by a 10 kHz spinal cord stimulation system: phantom and bioheat model.
        Neuromodulation. 2021; 24: 1327-1335https://doi.org/10.1111/ner.12980
        • De Ridder D.
        • Vanneste S.
        • Plazier M.
        • van der Loo E.
        • Menovsky T.
        Burst spinal cord stimulation: toward paresthesia-free pain suppression.
        Neurosurgery. 2010; 66: 986-990https://doi.org/10.1227/01.NEU.0000368153.44883.B3
        • Al-Kaisy A.
        • Van Buyten J.P.
        • Smet I.
        • Palmisani S.
        • Pang D.
        • Smith T.
        Sustained effectiveness of 10 kHz high-frequency spinal cord stimulation for patients with chronic, low back pain: 24-month results of a prospective multicenter study.
        Pain Med. 2014; 15: 347-354https://doi.org/10.1111/pme.12294
        • Reynolds A.F.
        • Shetter A.G.
        Scarring around cervical epidural stimulating electrode.
        Neurosurgery. 1983; 13: 63-65https://doi.org/10.1227/00006123-198307000-00013
        • Butson C.R.
        • Maks C.B.
        • McIntyre C.C.
        Sources and effects of electrode impedance during deep brain stimulation.
        Clin Neurophysiol. 2006; 117: 447-454https://doi.org/10.1016/j.clinph.2005.10.007
      2. Electromagnetics, Volume 2. Virginia Tech. Accessed February 8, 2022. https://vtechworks.lib.vt.edu/handle/10919/93253

        • Elwassif M.M.
        • Kong Q.
        • Vazquez M.
        • Bikson M.
        Bio-heat transfer model of deep brain stimulation induced temperature changes.
        Conf Proc IEEE Eng Med Biol Soc. 2006; 2006: 3580-3583https://doi.org/10.1109/IEMBS.2006.259425
        • Chang I.
        Finite element analysis of hepatic radiofrequency ablation probes using temperature-dependent electrical conductivity.
        Biomed Eng OnLine. 2003; 2: 12https://doi.org/10.1186/1475-925X-2-12
        • Elwassif M.M.
        • Datta A.
        • Rahman A.
        • Bikson M.
        Temperature control at DBS electrodes using a heat sink: experimentally validated FEM model of DBS lead architecture.
        J Neural Eng. 2012; 9046009https://doi.org/10.1088/1741-2560/9/4/046009
        • Pennes H.H.
        Analysis of tissue and arterial blood temperatures in the resting human forearm.
        J Appl Physiol. 1948; 1: 93-122https://doi.org/10.1152/jappl.1948.1.2.93
        • Gabriel S.
        • Lau R.W.
        • Gabriel C.
        The dielectric properties of biological tissues: II. Measurements in the frequency range 10 Hz to 20 GHz.
        Phys Med Biol. 1996; 41: 2251-2269https://doi.org/10.1088/0031-9155/41/11/002
      3. IT'IS Foundation. Tissue Properties Database V3.0.
        • Mcintosh R.L.
        • Anderson V.
        A comprehensive tissue properties database provided for the thermal assessment of a human at rest.
        Biophys Rev Lett. 2010; 05: 129-151https://doi.org/10.1142/S1793048010001184
      4. Grill W, Mortimer J. Electrical impedance of electrode encapsulation tissue. Paper presented at: 14th Annual International Conference of the IEEE Engineering in Medicine and Biology Society; October 29–November 1, 1992; Paris, France.

        • Grill W.M.
        • Mortimer J.T.
        Electrical properties of implant encapsulation tissue.
        Ann Biomed Eng. 1994; 22: 23-33https://doi.org/10.1007/BF02368219
        • Sweet W.H.
        • Wepsic J.G.
        Treatment of chronic pain by stimulation of fibers of primary afferent neuron.
        Trans Am Neurol Assoc. 1968; 93: 103-107
        • Khadka N.
        • Harmsen I.E.
        • Lozano A.M.
        • Bikson M.
        Bio-heat model of kilohertz-frequency deep brain stimulation increases brain tissue temperature.
        Neuromodulation. 2020; 23: 489-495https://doi.org/10.1111/ner.13120
        • Zander H.J.
        • Graham R.D.
        • Anaya C.J.
        • Lempka S.F.
        Anatomical and technical factors affecting the neural response to epidural spinal cord stimulation.
        J Neural Eng. 2020; 17036019https://doi.org/10.1088/1741-2552/ab8fc4
        • Li S.
        • Farber J.P.
        • Linderoth B.
        • Chen J.
        • Foreman R.D.
        Spinal cord stimulation with ‘conventional clinical’ and higher frequencies on activity and responses of spinal neurons to noxious stimuli: an animal study.
        Neuromodulation. 2018; 21: 440-447https://doi.org/10.1111/ner.12725
        • Ahmed S.
        • Yearwood T.
        • De Ridder D.
        • Vanneste S.
        Burst and high frequency stimulation: underlying mechanism of action.
        Expert Rev Med Devices. 2018; 15: 61-70https://doi.org/10.1080/17434440.2018.1418662
        • de Jongste M.J.
        • Nagelkerke D.
        • Hooyschuur C.M.
        • et al.
        Stimulation characteristics, complications, and efficacy of spinal cord stimulation systems in patients with refractory angina: a prospective feasibility study.
        Pacing Clin Electrophysiol. 1994; 17: 1751-1760https://doi.org/10.1111/j.1540-8159.1994.tb03742.x
        • Alò K.
        • Varga C.
        • Krames E.
        • et al.
        Factors affecting impedance of percutaneous leads in spinal cord stimulation.
        Neuromodulation. 2006; 9: 128-135https://doi.org/10.1111/j.1525-1403.2006.00050.x
        • Khadka N.
        • Bikson M.
        Response to the Letter to the Editor by Caraway et al. on “Tissue temperature increases by a 10 kHz spinal cord stimulation system: phantom and bioheat model”.
        Neuromodulation. 2019; 22: 988https://doi.org/10.1111/ner.13079
      5. Ranson M, Pope J, Deer T. Reducing Risks and Complications of Interventional Pain Procedures: Volume 5: A Volume in the Interventional and Neuromodulatory Techniques for Pain Management Series; Expert Consult Online and Print. Elsevier Health Sciences; 2012.

        • Jotwani R.
        • Abd-Elsayed A.
        • Villegas K.
        • et al.
        Failure of SCS MR-conditional modes due to high impedance: a review of literature and case series.
        Pain Ther. 2021; 10: 729-737https://doi.org/10.1007/s40122-020-00219-8
        • Yearwood T.L.
        • Hershey B.
        • Bradley K.
        • Lee D.
        Pulse width programming in spinal cord stimulation: a clinical study.
        Pain Phys. 2010; 13: 321-335
        • Taccola G.
        • Barber S.
        • Horner P.J.
        • Bazo H.A.C.
        • Sayenko D.
        Complications of epidural spinal stimulation: lessons from the past and alternatives for the future.
        Spinal Cord. 2020; 58: 1049-1059https://doi.org/10.1038/s41393-020-0505-8
        • Abejón D.
        • Rueda P.
        • Vallejo R.
        Threshold evolution as an analysis of the different pulse frequencies in rechargeable systems for spinal cord stimulation.
        Neuromodulation. 2016; 19: 276-282https://doi.org/10.1111/ner.12401
        • Cameron T.
        • Alo K.M.
        Effects of posture on stimulation parameters in spinal cord stimulation.
        Neuromodulation. 1998; 1: 177-183https://doi.org/10.1111/j.1525-1403.1998.tb00014.x
        • Olin J.C.
        • Kidd D.H.
        • North R.B.
        Postural changes in spinal cord stimulation perceptual thresholds.
        Neuromodulation. 1998; 1: 171-175https://doi.org/10.1111/j.1525-1403.1998.tb00013.x
        • Lempka S.F.
        • Johnson M.D.
        • Miocinovic S.
        • Vitek J.L.
        • McIntyre C.C.
        Current-controlled deep brain stimulation reduces in vivo voltage fluctuations observed during voltage-controlled stimulation.
        Clin Neurophysiol. 2010; 121: 2128-2133https://doi.org/10.1016/j.clinph.2010.04.026