Dorsal Root Ganglion Stimulation in Experimental Painful Diabetic Polyneuropathy: Delayed Wash-Out of Pain Relief After Low-Frequency (1Hz) Stimulation.
Animal model
dorsal root ganglion stimulation
frequency
painful diabetic polyneuropathy
rats
Journal
Neuromodulation : journal of the International Neuromodulation Society
ISSN: 1525-1403
Titre abrégé: Neuromodulation
Pays: United States
ID NLM: 9804159
Informations de publication
Date de publication:
Feb 2020
Feb 2020
Historique:
received:
05
06
2019
revised:
24
07
2019
accepted:
19
08
2019
pubmed:
17
9
2019
medline:
15
12
2020
entrez:
17
9
2019
Statut:
ppublish
Résumé
Up until now there is little data about the pain relieving effect of different frequency settings in DRGS. The aim of this study was to compare the pain relieving effect of DRGS at low-, mid-, and high-frequencies and Sham-DRGS in an animal model of painful diabetic neuropathy (PDPN). Diabetes mellitus was induced by an intraperitoneal injection of streptozotocin in 8-week-old female Sprague-Dawley rats (n = 24; glucose ≥15 mmol/L: n = 20; mechanical hypersensitivity: n = 15). Five weeks later, a DRGS device was implanted at the L5 DRG. Ten animals were included for stimulation, alternating 30 minutes of low (1 Hz)-, mid (20 Hz)-, and high (1000 Hz)-frequencies and Sham-DRGS during four days, with a pulse width of 0.2 msec (average amplitude: 0.19 ± 0.01 mA), using a randomized cross-over design. The effect on mechanical hypersensitivity of the hind paw to von Frey filaments was evaluated. All DRGS frequencies resulted in a complete reversal of mechanical hypersensitivity and "a clinically relevant reduction" was achieved in 70-80% of animals. No significant differences in maximal pain relieving effect were found between the different frequency treatments (p = 0.24). Animals stimulated at 1000 and 20 Hz returned to baseline mechanical hypersensitivity values 15 and 30 min after stimulation cessation, respectively, while animals stimulated at 1 Hz did not. These results show that DRGS is equally effective when applied at low-, mid-, and high-frequency in an animal model of PDPN. However, low-frequency-(1 Hz)-DRGS resulted in a delayed wash-out effect, which suggests that this is the most optimal frequency for pain therapy in PDPN as compared to mid- and high-frequency.
Identifiants
pubmed: 31524325
doi: 10.1111/ner.13048
pii: S1094-7159(21)02104-8
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
177-184Informations de copyright
© 2019 International Neuromodulation Society.
Références
Peltier A, Goutman SA, Callaghan BC. Painful diabetic neuropathy. BMJ 2014;348:g1799.
Tesfaye S, Boulton AJM, Dickenson AH. Mechanisms and management of diabetic painful distal symmetrical polyneuropathy. Diabetes Car 2013;36:2456-2465.
Waldfogel JM, Nesbit SA, Dy SM et al. Pharmacotherapy for diabetic peripheral neuropathy pain and quality of life. Neurology 2017;90:1125.
Slangen R, Schaper NC, Faber CG et al. Spinal cord stimulation and pain relief in painful diabetic peripheral neuropathy: A prospective two-center randomized controlled trial. Diabetes Care 2014;37:3016-3024.
Van Beek M, Slangen R, Schaper NC et al. Sustained treatment effect of spinal cord stimulation in painful diabetic peripheral neuropathy: 24-month follow-up of a prospective two-center randomized controlled trial. Diabetes Care 2015;39:132-134.
De Vos CC, Meier K, Zaalberg PB et al. Spinal cord stimulation in patients with painful diabetic neuropathy: A multicentre randomized clinical trial. Pain 2014;155:2426-2431.
Deer TR, Grigsby E, Weiner RL, Wilcosky B, Kramer JM. A prospective study of dorsal root ganglion stimulation for the relief of chronic pain. Neuromodulation 2013;16:67-72.
Liem L, Russo M, Huygen FJPM et al. A multicenter, prospective trial to assess the safety and performance of the spinal modulation dorsal root ganglion neurostimulator system in the treatment of chronic pain. Neuromodulation 2013;16:471-482.
Pope JE, Deer TR, Kramer J. A systematic review: Current and future directions of dorsal root ganglion therapeutics to treat chronic pain. Pain Med 2013;14:1477-1496.
Eldabe S, Espinet A, Wahlstedt A et al. Retrospective case series on the treatment of painful diabetic peripheral neuropathy with dorsal root ganglion stimulation. Neuromodulation 2018;21:787-792.
Koetsier E, Franken G, Debets J et al. Effectiveness of dorsal root ganglion stimulation and dorsal column spinal cord stimulation in a model of experimental painful diabetic polyneuropathy. CNS Neurosci Ther 2018;25:367-374.
Calcutt NA. Modeling diabetic sensory neuropathy in rats. Methods Mol Med 2004;99:55-65.
Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL. Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 1994;53:55-63.
Beek M, Kleef M, Linderoth B et al. Spinal cord stimulation in experimental chronic painful diabetic polyneuropathy: Delayed effect of high-frequency stimulation. Eur J Pain 2017;21:795-803.
Mills C, Leblond D, Joshi S et al. Estimating efficacy and drug ED50's using von frey thresholds: Impact of Weber's law and log transformation. J Pain 2012;13:519-523.
Pluijms WA, Van Kleef M, Honig WM, Janssen SP, Joosten EA. The effect of spinal cord stimulation frequency in experimental painful diabetic polyneuropathy. Eur J Pain 2013;17:1338-1346.
Pan B, Yu H, Fischer GJ, Kramer JM, Hogan QH. Dorsal root ganglionic field stimulation relieves spontaneous and induced neuropathic pain in rats. J Pain 2016;17:1349-1358.
Wu M, Thorkilsen MM, Qin C, Farber JP, Linderoth B, Foreman RD. Effects of spinal cord stimulation on peripheral blood circulation in rats with streptozotocin-induced diabetes. Neuromodulation 2007;10:216-223.
Gao J, Wu M, Li L et al. Effects of spinal cord stimulation with “standard clinical” and higher frequencies on peripheral blood flow in rats. Brain Res 2010;1313:53-61.
Kao CH, Chen JJJ, Hsu YM, Bau DT, Yao CH, Chen YS. High-frequency electrical stimulation can be a complementary therapy to promote nerve regeneration in diabetic rats. PLoS One 2013;8:e79078.
Deer TR, Levy RM, Kramer J et al. Dorsal root ganglion stimulation yielded higher treatment success rate for CRPS and causalgia at 3 and 12 months. Pain 2016;158:669-681.
Huygen F, Liem L, Cusack W, Kramer J. Stimulation of the L2-L3 dorsal root ganglia induces effective pain relief in the low back. Pain Pract 2018;18:205-213.
Billet B, Wynendaele R, Vanquathem NE. Wireless neuromodulation for chronic back pain: delivery of high-frequency dorsal root ganglion stimulation by a minimally invasive technique. Case Rep Med 2017;2017:1-4.
Billet B, Hanssens K, De Coster O et al. Wireless high-frequency dorsal root ganglion stimulation for chronic low back pain: a pilot study. Acta Anaesthesiol Scand 2018; [Epub ahead of print;62:1133-1138.
Miller JP, Eldabe S, Buchser E, Johanek LM, Guan Y, Linderoth B. Parameters of spinal cord stimulation and their role in electrical charge delivery: a review. Neuromodulation 2016;19:373-384.
Geurts JW, Joosten EA, Van Kleef M. Current status and future perspectives of spinal cord stimulation in treatment of chronic pain. Pain 2017;158:771-774.
Koopmeiners AS, Mueller S, Kramer J, Hogan QH. Effect of electrical field stimulation on dorsal root ganglion neuronal function. Neuromodulation 2013;16:304-311. discussion 310-311.
Sandkühler J, Chen JG, Cheng G, Randić M. Low-frequency stimulation of afferent Adelta-fibers induces long-term depression at primary afferent synapses with substantia gelatinosa neurons in the rat. J Neurosci 1997;17:6483-6491.
Melzack R, Wall P. Pain mechanisms: a new theory. Science 1965;150:971-979.
Stiller CO, Cui JG, O'Connor WT, Brodin E, Meyerson BA, Linderoth B. Release of γ-aminobutyric acid in the dorsal horn and suppression of tactile allodynia by spinal cord stimulation in mononeuropathic rats. Neurosurgery 1996;39:367-375.
Cui JG, O'Connor WT, Ungerstedt U, Linderoth B, Meyerson BA. Spinal cord stimulation attenuates augmented dorsal horn release of excitatory amino acids in mononeuropathy via a GABAergic mechanism. Pain 1997;73:87-95.
Linderoth B, Stiller CO, Gunasekera L, O'Connor WT, Ungerstedt U, Brodin E. Gamma-aminobutyric acid is released in the dorsal horn by electrical spinal cord stimulation: an in vivo microdialysis study in the rat. Neurosurgery 1994;34:484-488.
Linderoth B, Foreman RD. Conventional and novel spinal stimulation algorithms: hypothetical mechanisms of action and comments on outcomes. Neuromodulation 2017;20:525-533.
Cui JG, Linderoth B, Meyerson BA. Effects of spinal cord stimulation on touch-evoked allodynia involve GABAergic mechanisms. an experimental study in the mononeuropathic rat. Pain 1996;66:287-295.
Janssen SP, Gerard S, Raijmakers ME, Truin M, Van Kleef M, Joosten EA. Decreased intracellular GABA levels contribute to spinal cord stimulation-induced analgesia in rats suffering from painful peripheral neuropathy: The role of KCC2 and GABAAreceptor-mediated inhibition. Neurochem Int 2012;60:21-30.
Krames ES. The dorsal root ganglion in chronic pain and as a target for neuromodulation: a review. Neuromodulation 2015;18:24-32.
Pawela CP, Kramer JM, Hogan QH. Dorsal root ganglion stimulation attenuates the BOLD signal response to noxious sensory input in specific brain regions: insights into a possible mechanism for analgesia. Neuroimage 2017;147:10-18.
van Beek M, Hermes D, Honig WM et al. Long-term spinal cord stimulation alleviates mechanical hypersensitivity and increases peripheral cutaneous blood perfusion in experimental painful diabetic polyneuropathy. Neuromodulation 2018;21:472-479.
Franken G, Debets J, Joosten EA. Dorsal root ganglion stimulation in experimental painful diabetic peripheral neuropathy: Burst vs. conventional stimulation paradigm. Neuromodulation 2018. https://doi.org/10.1111/ner.12908. [Epub ahead of print].