DOI QR코드

DOI QR Code

Antinociceptive Effect of Memantine and Morphine on Vincristine-induced Peripheral Neuropathy in Rats

  • Park, Byoung-Yoon (Department of Anesthesiology and Pain Medicine, Chonnam National University, Medical School) ;
  • Park, Sang-Hee (Department of Anesthesiology and Pain Medicine, Chonnam National University, Medical School) ;
  • Kim, Woong-Mo (Department of Anesthesiology and Pain Medicine, Chonnam National University, Medical School) ;
  • Yoon, Myung-Ha (Department of Anesthesiology and Pain Medicine, Chonnam National University, Medical School) ;
  • Lee, Hyung-Gon (Department of Anesthesiology and Pain Medicine, Chonnam National University, Medical School)
  • Received : 2010.06.04
  • Accepted : 2010.08.03
  • Published : 2010.09.01

Abstract

Background: Vincristine-induced peripheral neuropathy is a major dose limiting side effect and thus effective therapeutic strategy is required. In this study, we investigated the antinociceptive effect of memantine and morphine on a vincristine-induced peripheral neuropathy model in rats. Methods: Male Sprague-Dawley rats weighing 220-240 g were used in all experiments. Rats subsequently received daily intraperitoneal injections of either vincristine sulfate (0.1 ml/kg/day) or saline (0.1 ml/kg/day) over 12 days, immediately following behavioral testing. For assessment of mechanical allodynia, mechanical stimuli using von Frey filament was applied to the paw to measure withdrawal threshold. The effects of N-methyl-D-aspartate receptors antagonist (memantine; 2.5, 5, 10 mg/kg intraperitoneal), opioid agonist (morphine; 2.5, 5, 10 mg/kg intraperitoneal) and vehicle (saline) on vicristine-induced neuropathy were evaluated. Results: Mechanical allodynia developed over the course of ten daily injections of vincristine relative to groups receiving saline at the same time. Morphine abolished the reduction in paw withdrawal threshold compared to vehicle and produced dose-responsiveness. Only the highest dose of memantine (10 mg/kg) was able to increase paw withdrawal threshold compared to vehicle. Conclusions: Systemic morphine and memantine have an antinociceptive effect on the vincristine-induced peripheral neuropathy model in rats. These results suggest morphine and memantine may be an alternative approach for the treatment of vincristine-induced peripheral neuropathic pain.

Keywords

References

  1. Quasthoff S, Hartung HP. Chemotherapy-induced peripheral neuropathy. J Neurol 2002; 249: 9-17. https://doi.org/10.1007/PL00007853
  2. Postma TJ, Benard BA, Huijgens PC, Ossenkoppele GJ, Heimans JJ. Long-term effects of vincristine on the peripheral nervous system. J Neurooncol 1993; 15: 23-7. https://doi.org/10.1007/BF01050259
  3. Himes RH, Kersey RN, Heller-Bettinger I, Samson FE. Action of the vinca alkaloids vincristine, vinblastine, and desacetyl vinblastine amide on microtubules in vitro. Cancer Res 1976; 36: 3798-802
  4. Owellen RJ, Hartke CA, Dickerson RM, Hains FO. Inhibition of tubulin-microtubule polymerization by drugs of the Vinca alkaloid class. Cancer Res 1976; 36: 1499-502.
  5. Casey EB, Jellife AM, Le Quesne PM, Millett YL. Vincristine neuropathy. Clinical and electrophysiological observations. Brain 1973; 96: 69-86. https://doi.org/10.1093/brain/96.1.69
  6. Weiden PL, Wright SE. Vincristine neurotoxicity. N Engl J Med 1972; 286: 1369-70.
  7. Forman A. Peripheral neuropathy in cancer patients: clinical types, etiology, and presentation. Part 2. Oncology (Williston Park) 1990; 4: 85-9.
  8. Sandler SG, Tobin W, Henderson ES. Vincristine-induced neuropathy. A clinical study of fifty leukemic patients. Neurology 1969; 19: 367-74. https://doi.org/10.1212/WNL.19.4.367
  9. Wolf S, Barton D, Kottschade L, Grothey A, Loprinzi C. Chemotherapy-induced peripheral neuropathy: prevention and treatment strategies. Eur J Cancer 2008; 44: 1507-15. https://doi.org/10.1016/j.ejca.2008.04.018
  10. Ogawa T, Mimura Y, Kato H, Ootsubo S, Murakoshi M. The usefulness of rabbits as an animal model for the neuropathological assessment of neurotoxicity following the administration of vincristine. Neurotoxicology 2000; 21: 501-11.
  11. Topp KS, Tanner KD, Levine JD. Damage to the cytoskeleton of large diameter sensory neurons and myelinated axons in vincristine-induced painful peripheral neuropathy in the rat. J Comp Neurol 2000; 424: 563-76. https://doi.org/10.1002/1096-9861(20000904)424:4<563::AID-CNE1>3.0.CO;2-U
  12. Weng HR, Cordella JV, Dougherty PM. Changes in sensory processing in the spinal dorsal horn accompany vincristineinduced hyperalgesia and allodynia. Pain 2003; 103: 131-8. https://doi.org/10.1016/S0304-3959(02)00445-1
  13. Lynch JJ 3rd, Wade CL, Zhong CM, Mikusa JP, Honore P. Attenuation of mechanical allodynia by clinically utilized drugs in a rat chemotherapy-induced neuropathic pain model. Pain 2004; 110: 56-63. https://doi.org/10.1016/j.pain.2004.03.010
  14. Kaley TJ, Deangelis LM. Therapy of chemotherapy-induced peripheral neuropathy. Br J Haematol 2009; 145: 3-14. https://doi.org/10.1111/j.1365-2141.2008.07558.x
  15. Arné.r S, Meyerson BA. Lack of analgesic effect of opioids on neuropathic and idiopathic forms of pain. Pain 1988; 33: 11-23. https://doi.org/10.1016/0304-3959(88)90198-4
  16. Dellemijn P. Are opioids effective in relieving neuropathic pain? Pain 1999; 80: 453-62. https://doi.org/10.1016/S0304-3959(98)00256-5
  17. Obara I, Makuch W, Spetea M, Schu-tz J, Schmidhammer H, Przewlocki R, et al. Local peripheral antinociceptive effects of 14-O-methyloxymorphone derivatives in inflammatory and neuropathic pain in the rat. Eur J Pharmacol 2007; 558: 60-7. https://doi.org/10.1016/j.ejphar.2006.11.037
  18. Eisenberg E, McNicol ED, Carr DB. Efficacy and safety of opioid agonists in the treatment of neuropathic pain of nonmalignant origin: systematic review and meta-analysis of randomized controlled trials. JAMA 2005; 293: 3043-52. https://doi.org/10.1001/jama.293.24.3043
  19. Chizh BA, Headley PM. NMDA antagonists and neuropathic pain--multiple drug targets and multiple uses. Curr Pharm Des 2005; 11: 2977-94. https://doi.org/10.2174/1381612054865082
  20. Eide PK. Wind-up and the NMDA receptor complex from a clinical perspective. Eur J Pain 2000; 4: 5-15. https://doi.org/10.1053/eujp.1999.0154
  21. Buvanendran A, Kroin JS. Early use of memantine for neuropathic pain. Anesth Analg 2008; 107: 1093-4. https://doi.org/10.1213/ane.0b013e318180ebfe
  22. Finkel JC, Pestieau SR, Quezado ZM. Ketamine as an adjuvant for treatment of cancer pain in children and adolescents. J Pain 2007; 8: 515-21. https://doi.org/10.1016/j.jpain.2007.02.429
  23. Lipton SA. Failures and successes of NMDA receptor antagonists: molecular basis for the use of open-channel blockers like memantine in the treatment of acute and chronic neurologic insults. NeuroRx 2004; 1: 101-10. https://doi.org/10.1602/neurorx.1.1.101
  24. Chaplan SR, Malmberg AB, Yaksh TL. Efficacy of spinal NMDA receptor antagonism in formalin hyperalgesia and nerve injury evoked allodynia in the rat. J Pharmacol Exp Ther 1997; 280: 829-38.
  25. Zimmermann M. Ethical guidelines for investigations on experimental pain in conscious animals. Pain 1983; 16: 109-10. https://doi.org/10.1016/0304-3959(83)90201-4
  26. 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. https://doi.org/10.1016/0165-0270(94)90144-9
  27. Cata JP, Weng HR, Lee BN, Reuben JM, Dougherty PM. Clinical and experimental findings in humans and animals with chemotherapy-induced peripheral neuropathy. Minerva Anestesiol 2006; 72: 151-69.
  28. Polomano RC, Bennett GJ. Chemotherapy-evoked painful peripheral neuropathy. Pain Med 2001; 2: 8-14. https://doi.org/10.1046/j.1526-4637.2001.002001008.x
  29. Rahn EJ, Makriyannis A, Hohmann AG. Activation of cannabinoid CB1 and CB2 receptors suppresses neuro pathic nociception evoked by the chemotherapeutic agent vincristine in rats. Br J Pharmacol 2007; 152: 765-77.
  30. Reisberg B, Doody R, Stöffler A, Schmitt F, Ferris S, Möbius HJ; Memantine Study Group. Memantine in moderate-tosevere Alzheimer's disease. N Engl J Med 2003; 348: 1333-41. https://doi.org/10.1056/NEJMoa013128
  31. Tariot PN, Farlow MR, Grossberg GT, Graham SM, McDonald S, Gergel I; Memantine Study Group. Memantine treatment in patients with moderate to severe Alzheimer disease already receiving donepezil: a randomized controlled trial. JAMA 2004; 291: 317-24. https://doi.org/10.1001/jama.291.3.317
  32. Sinis N, Birbaumer N, Gustin S, Schwarz A, Bredanger S, Becker ST, et al. Memantine treatment of complex regional pain syndrome: a preliminary report of six cases. Clin J Pain 2007; 23: 237-43. https://doi.org/10.1097/AJP.0b013e31802f67a7
  33. Hackworth RJ, Tokarz KA, Fowler IM, Wallace SC, Stedje-Larsen ET. Profound pain reduction after induction of memantine treatment in two patients with severe phantom limb pain. Anesth Analg 2008; 107: 1377-9. https://doi.org/10.1213/ane.0b013e31817f90f1
  34. Carlton SM, Hargett GL. Treatment with the NMDA antagonist memantine attenuates nociceptive responses to mechanical stimulation in neuropathic rats. Neurosci Lett 1995; 198: 115-8. https://doi.org/10.1016/0304-3940(95)11980-B
  35. Suzuki R, Matthews EA, Dickenson AH. Comparison of the effects of MK-801, ketamine and memantine on responses of spinal dorsal horn neurones in a rat model of mononeuropathy. Pain 2001; 91: 101-9. https://doi.org/10.1016/S0304-3959(00)00423-1
  36. Medvedev IO, Malyshkin AA, Belozertseva IV, Sukhotina IA, Sevostianova NY, Aliev K, et al. Effects of low-affinity NMDA receptor channel blockers in two rat models of chronic pain. Neuropharmacology 2004; 47: 175-83. https://doi.org/10.1016/j.neuropharm.2004.01.019
  37. Bulka A, Plesan A, Xu XJ, Wiesenfeld-Hallin Z. Reduced tolerance to the anti-hyperalgesic effect of methadone in comparison to morphine in a rat model of mononeuropathy. Pain 2002; 95: 103-9. https://doi.org/10.1016/S0304-3959(01)00382-7
  38. Erichsen HK, Hao JX, Xu XJ, Blackburn-Munro G. Comparative actions of the opioid analgesics morphine, methadone and codeine in rat models of peripheral and central neuropathic pain. Pain 2005; 116: 347-58. https://doi.org/10.1016/j.pain.2005.05.004
  39. Bujalska M, Makulska-Nowak H, Gumulka SW. Magnesium ions and opioid agonists in vincristine-induced neuropathy. Pharmacol Rep 2009; 61: 1096-104. https://doi.org/10.1016/S1734-1140(09)70172-0

Cited by

  1. Ginkgo biloba Extract Attenuates Hyperalgesia in a Rat Model of Vincristine-Induced Peripheral Neuropathy vol.115, pp.5, 2012, https://doi.org/10.1213/ANE.0b013e318262e170
  2. on vincristine-induced neuropathic pain model in rats vol.29, pp.1, 2013, https://doi.org/10.1177/0748233711432573
  3. Optimization and pharmacological characterization of a refined cisplatin-induced rat model of peripheral neuropathic pain vol.25, pp.8, 2014, https://doi.org/10.1097/FBP.0000000000000090
  4. in vincristine-induced painful neuropathy in rats vol.30, pp.9, 2014, https://doi.org/10.1177/0748233712463779
  5. Antinociceptive effect of matrine on vincristine-induced neuropathic pain model in mice vol.35, pp.6, 2014, https://doi.org/10.1007/s10072-013-1603-6
  6. The effect of thioctic acid on allodynia in a rat vincristine-induced neuropathy model vol.43, pp.3, 2015, https://doi.org/10.1177/0300060515569287
  7. Comparison of the Analgesic Activity of Antiparkinsonian Aminoadamantane Derivatives Amantadine and Hemantane vol.05, pp.03, 2016, https://doi.org/10.4236/apd.2016.53007
  8. Analgesic Effects of Dexmedetomidine in Vincristine-Evoked Painful Neuropathic Rats vol.27, pp.11, 2012, https://doi.org/10.3346/jkms.2012.27.11.1411
  9. Endogenous opiates and behavior: 2010 vol.32, pp.12, 2010, https://doi.org/10.1016/j.peptides.2011.09.020
  10. High-Intensity Ultrasound Treatment for Vincristine-Induced Neuropathic Pain vol.83, pp.5, 2010, https://doi.org/10.1093/neuros/nyx488
  11. Neuropharmacological Properties of the Essential Oil of Bergamot for the Clinical Management of Pain-Related BPSDs vol.26, pp.20, 2010, https://doi.org/10.2174/0929867325666180307115546
  12. The effect of analgesics on stimulus evoked pain-like behaviour in animal models for chemotherapy induced peripheral neuropathy- a meta-analysis vol.9, pp.1, 2010, https://doi.org/10.1038/s41598-019-54152-8
  13. The Antiallodynic Effect of Nefopam on Vincristine-Induced Neuropathy in Mice vol.13, pp.None, 2010, https://doi.org/10.2147/jpr.s224478
  14. Emerging pharmacological strategies for the management of chemotherapy-induced peripheral neurotoxicity (CIPN), based on novel CIPN mechanisms vol.20, pp.10, 2010, https://doi.org/10.1080/14737175.2020.1796639
  15. Protective effect of gastrodin on peripheral neuropathy induced by anti-tumor treatment with vincristine in rat models vol.44, pp.1, 2010, https://doi.org/10.1080/01480545.2018.1547739