Spinal cord stimulation reduces hypersensitivity through activation of opioid receptors in a frequency-dependent manner

European Journal of Pain (United Kingdom)

Volumn 17, Issue 4, 2013, Pages 551-561

  Sato, K L ^a   King, E W ^a   Johanek, L M ^b   Sluka, K A ^a  

^a UNIVERSITY OF IOWA   (United States)

^b MEDTRONIC INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DELTA OPIATE RECEPTOR; MORPHINE; MU OPIATE RECEPTOR; NALOXONE; NALTRINDOLE; PLACEBO;

ANALGESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DRUG TOLERANCE; MOTOR PERFORMANCE; NEUROPATHIC PAIN; NONHUMAN; PAIN THRESHOLD; PRIORITY JOURNAL; RAT; SPINAL CORD STIMULATION; TREATMENT DURATION;

ANALGESICS, OPIOID; ANIMALS; HYPERALGESIA; MORPHINE; NALOXONE; NALTREXONE; NARCOTIC ANTAGONISTS; NEURALGIA; PAIN MEASUREMENT; PHYSICAL STIMULATION; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, OPIOID; SPINAL CORD; SPINAL CORD STIMULATION;

EID: 84879590489     PISSN: 10903801     EISSN: 15322149     Source Type: Journal    
DOI: 10.1002/j.1532-2149.2012.00220.x     Document Type: Article

References (66)

1. Arner, S., Meyerson, B.A. (1988). Lack of analgesic effect of opioids on neuropathic and idiopathic forms of pain. Pain 33, 11-23.
2. Bian, D., Nichols, M.L., Ossipov, M.H., Lai, J., Porreca, F. (1995). Characterization of the antiallodynic efficacy of morphine in a model of neuropathic pain in rats. Neuroreport 6, 1981-1984.
3. Cameron, T. (2004). Safety and efficacy of spinal cord stimulation for the treatment of chronic pain: A 20-year literature review. J Neurosurg 100, 254-267.
4. Chandran, P., Sluka, K.A. (2003). Development of opioid tolerance with repeated transcutaneous electrical nerve stimulation administration. Pain 102, 195-201.
5. Chen, X.H., Han, J.S. (1992a). Analgesia induced by electroacupuncture of different frequencies is mediated by different types of opioid receptors: Another cross-tolerance study. Behav Brain Res 47, 143-149.
6. Chen, X.H., Han, J.S. (1992b). All three types of opioid receptors in the spinal cord are important for 2/15 Hz electroacupuncture analgesia. Eur J Pharmacol 211, 203-210.
7. Christensen, D., Kayser, V. (2000). The development of painrelated behaviour and opioid tolerance after neuropathyinducing surgery and sham surgery. Pain 88, 231-238.
8. Compton, A.K., Shah, B., Hayek, S.M. (2012). Spinal cord stimulation: A review. Curr Pain Headache Rep 16, 35-42.
9. Cui, J.G., Linderoth, B., Meyerson, B.A. (1996). Effects of spinal cord stimulation on touch-evoked allodynia involve GABAergic mechanisms. An experimental study in the mononeuropathic rat. Pain 66, 287-295.
10. Cui, J.G., O'Connor, W.T., Ungerstedt, U., Linderoth, B., Meyerson, B.A. (1997). Spinal cord stimulation attenuates augmented dorsal horn release of excitatory amino acids in mononeuropathy via a GABAergic mechanism. Pain 73, 87-95.
11. Decosterd, I., Woolf, C.J. (2000). Spared nerve injury: An animal model of persistent peripheral neuropathic pain. Pain 87, 149- 158.
12. DeSantana, J.M., Da Silva, L.F., De Resende, M.A., Sluka, K.A. (2009). Transcutaneous electrical nerve stimulation at both high and low frequencies activates ventrolateral periaqueductal grey to decrease mechanical hyperalgesia in arthritic rats. Neuroscience 163, 1233-1241.
13. DeSantana, J.M., Walsh, D.M., Vance, C., Rakel, B.A., Sluka, K.A. (2008). Effectiveness of transcutaneous electrical nerve stimulation for treatment of hyperalgesia and pain. Curr Rheumatol Rep 10, 492-499.
14. Freeman, T.B., Campbell, J.N., Long, D.M. (1983). Naloxone does not affect pain relief induced by electrical stimulation in man. Pain 17, 189-195.
15. Goff, J.R., Burkey, A.R., Goff, D.J., Jasmin, L. (1998). Reorganization of the spinal dorsal horn in models of chronic pain: Correlation with behaviour. Neuroscience 82, 559-574.
16. Hunter, J.P., Ashby, P. (1994). Segmental effects of epidural spinal cord stimulation in humans. J Physiol 474, 407-419.
17. Jeon, Y., Huh, B.K. (2009). Spinal cord stimulation for chronic pain. Ann Acad Med Singapore 38, 998-1003.
18. Kalra, A., Urban, M.O., Sluka, K.A. (2001). Blockade of opioid receptors in rostral ventral medulla prevents antihyperalgesia produced by transcutaneous electrical nerve stimulation (TENS). J Pharmacol Exp Ther 298, 257-263.
19. Kim, J., Jung, J.I., Na, H.S., Hong, S.K., Yoon, Y.W. (2003). Effects of morphine on mechanical allodynia in a rat model of central neuropathic pain. Neuroreport 14, 1017-1020.
20. Kumar, K., Nath, R., Wyant, G.M. (1991). Treatment of chronic pain by epidural spinal cord stimulation: A 10-year experience. J Neurosurg 75, 402-407.
21. Kumar, K., Toth, C., Nath, R.K., Laing, P. (1998). Epidural spinal cord stimulation for treatment of chronic pain - some predictors of success. A 15-year experience. Surg Neurol 50, 110- 120.
22. Lanner, G., Spendel, M.C. (2007). Spinal cord stimulation for the treatment of chronic non-malignant pain. Acta Neurochir Suppl 97, 79-84.
23. Lee, C.Y., Perez, F.M., Wang, W., Guan, X., Zhao, X., Fisher, J.L., Guan, Y., Sweitzer, S.M., Raja, S.N., Tao, Y.X. (2011). Dynamic temporal and spatial regulation of mu opioid receptor expression in primary afferent neurons following spinal nerve injury. Eur J Pain 15, 669-675.
24. Leonard, G., Cloutier, C., Marchand, S. (2011). Reduced analgesic effect of acupuncture-like TENS but not conventional TENS in opioid-treated patients. J Pain 12, 213-221.
25. Li, D., Yang, H., Meyerson, B.A., Linderoth, B. (2006). Response to spinal cord stimulation in variants of the spared nerve injury pain model. Neurosci Lett 400, 115-120.
26. Lind, G., Meyerson, B.A., Winter, J., Linderoth, B. (2004). Intrathecal baclofen as adjuvant therapy to enhance the effect of spinal cord stimulation in neuropathic pain: A pilot study. Eur J Pain 8, 377-383.
27. Lind, G., Schechtmann, G., Winter, J., Linderoth, B. (2007). Drug-enhanced spinal stimulation for pain: A new strategy. Acta Neurochir Suppl 97, 57-63.
28. Lind, G., Schechtmann, G., Winter, J., Meyerson, B.A., Linderoth, B. (2008). Baclofen-enhanced spinal cord stimulation and intrathecal baclofen alone for neuropathic pain: Longterm outcome of a pilot study. Eur J Pain 12, 132-136.
29. Maeda, Y., Ikeuchi, M., Wacnik, P., Sluka, K.A. (2009). Increased c-fos immunoreactivity in the spinal cord and brain following spinal cord stimulation is frequency-dependent. Brain Res 1259, 40-50.
30. Maeda, Y., Wacnik, P.W., Sluka, K.A. (2008). Low frequencies, but not high frequencies of bi-polar spinal cord stimulation reduce cutaneous and muscle hyperalgesia induced by nerve injury. Pain 138, 143-152.
31. Makin, M.K., Ellershaw, J.E. (1998). Substitution of another opioid for morphine. Methadone can be used to manage neuropathic pain related to cancer. BMJ 317, 81.
32. Mao, J., Price, D.D., Mayer, D.J. (1995). Experimental mononeuropathy reduces the antinociceptive effects of morphine: Implications for common intracellular mechanisms involved in morphine tolerance and neuropathic pain. Pain 61, 353-364.
33. McQuay, H.J., Jadad, A.R., Carroll, D., Faura, C., Glynn, C.J., Moore, R.A., Liu, Y. (1992). Opioid sensitivity of chronic pain: A patient-controlled analgesia method. Anaesthesia 47, 757- 767.
34. Meyerson, B.A., Linderoth, B. (2000). Mechanisms of spinal cord stimulation in neuropathic pain. Neurol Res 22, 285-292.
35. Meyerson, B.A., Ren, B., Herregodts, P., Linderoth, B. (1995). Spinal cord stimulation in animal models of mononeuropathy: Effects on the withdrawal response and the flexor reflex. Pain 61, 229-243.
36. Moriyama, K., Murakawa, K., Uno, T., Oseto, K., Kawanishi, M., Saito, Y., Taira, T., Yamauchi, M. (2012). A prospective, openlabel, multicenter study to assess the efficacy of spinal cord stimulation and identify patients who would benefit. Neuromodulation 15, 7-11.
37. Obara, I., Parkitna, J.R., Korostynski, M., Makuch, W., Kaminska, D., Przewlocka, B., Przewlocki, R. (2009). Local peripheral opioid effects and expression of opioid genes in the spinal cord and dorsal root ganglia in neuropathic and inflammatory pain. Pain 141, 283-291.
38. Portenoy, R.K., Foley, K.M., Inturrisi, C.E. (1990). The nature of opioid responsiveness and its implications for neuropathic pain: New hypotheses derived from studies of opioid infusions. Pain 43, 273-286.
39. Qin, C., Farber, J.P., Foreman, R.D. (2007). Spinal cord stimulation modulates activity of lumbosacral spinal neurons receiving input from urinary bladder in rats. Neurosci Lett 428, 38-42.
40. Rashid, M.H., Inoue, M., Toda, K., Ueda, H. (2004). Loss of peripheral morphine analgesia contributes to the reduced effectiveness of systemic morphine in neuropathic pain. J Pharmacol Exp Ther 309, 380-387.
41. Reeta, K., Mediratta, P.K., Rathi, N., Jain, H., Chugh, C., Sharma, K.K. (2006). Role of kappa- and delta-opioid receptors in the antinociceptive effect of oxytocin in formalin-induced pain response in mice. Regul Pept 135, 85-90.
42. Sabino, G.S., Santos, C.M., Francischi, J.N., de Resende, M.A. (2008). Release of endogenous opioids following transcutaneous electric nerve stimulation in an experimental model of acute inflammatory pain. J Pain 9, 157-163.
43. Shrivastav, M., Musley, S. (2009). Spinal cord stimulation for complex regional pain syndrome. Conf Proc IEEE Eng Med Biol Soc 2009, 2033-2036.
44. Sluka, K.A., Chandran, P. (2002). Enhanced reduction in hyperalgesia by combined administration of clonidine and TENS. Pain 100, 183-190.
45. Sluka, K.A., Deacon, M., Stibal, A., Strissel, S., Terpstra, A. (1999). Spinal blockade of opioid receptors prevents the analgesia produced by TENS in arthritic rats. J Pharmacol Exp Ther 289, 840-846.
46. Sluka, K.A., Judge, M.A., McColley, M.M., Reveiz, P.M., Taylor, B.M. (2000). Low frequency TENS is less effective than high frequency TENS at reducing inflammationinduced hyperalgesia in morphine-tolerant rats. Eur J Pain 4, 185-193.
47. Song, Z., Meyerson, B.A., Linderoth, B. (2011a). Spinal 5-HT receptors that contribute to the pain-relieving effects of spinal cord stimulation in a rat model of neuropathy. Pain 152, 1666-1673.
48. Song, Z., Meyerson, B.A., Linderoth, B. (2011b). The interaction between antidepressant drugs and the pain-relieving effect of spinal cord stimulation in a rat model of neuropathy. Anesth Analg 113, 1260-1265.
49. Song, Z., Ultenius, C., Meyerson, B.A., Linderoth, B. (2009). Pain relief by spinal cord stimulation involves serotonergic mechanisms: An experimental study in a rat model of mononeuropathy. Pain 147, 241-248.
50. Stiller, C.O., Cui, J.G., O'Connor, W.T., Brodin, E., Meyerson, B.A., Linderoth, B. (1996). Release of gamma-aminobutyric acid in the dorsal horn and suppression of tactile allodynia by spinal cord stimulation in mononeuropathic rats. Neurosurgery 39, 367-374; discussion 374-5.
51. Stojanovic, M.P., Abdi, S. (2002). Spinal cord stimulation. Pain Physician 5, 156-166.
52. Stone, L.S., Vulchanova, L., Riedl, M.S., Williams, F.G., Wilcox, G.L., Elde, R. (2004). Effects of peripheral nerve injury on delta opioid receptor (DOR) immunoreactivity in the rat spinal cord. Neurosci Lett 361, 208-211.
53. Sun, S.L., Han, J.S. (1989). High and low frequency electroacupuncture analgesia are mediated by different types of opioid receptors at spinal level: A cross tolerance study. Sheng Li Xue Bao 41, 416-420.
54. Takasaki, I., Nojima, H., Shiraki, K., Kuraishi, Y. (2006). Specific down-regulation of spinal mu-opioid receptor and reduced analgesic effects of morphine in mice with postherpetic pain. Eur J Pharmacol 550, 62-67.
55. Tesfaye, S., Watt, J., Benbow, S.J., Pang, K.A., Miles, J., MacFarlane, I.A. (1996). Electrical spinal-cord stimulation for painful diabetic peripheral neuropathy. Lancet 348, 1698-1701.
56. Tonelli, L., Setti, T., Falasca, A., Martignoni, E., Torcia, E., Calcaterra, F.M., Merli, G.A., Facchinetti, F. (1988). Investigation on cerebrospinal fluid opioids and neurotransmitters related to spinal cord stimulation. Appl Neurophysiol 51, 324- 332.
57. Truin, M., Janssen, S.P., van Kleef, M., Joosten, E.A. (2011). Successful pain relief in non-responders to spinal cord stimulation: The combined use of ketamine and spinal cord stimulation. Eur J Pain 15, 1049.e1-1049.e9.
58. Wallin, J., Cui, J.G., Yakhnitsa, V., Schechtmann, G., Meyerson, B.A., Linderoth, B. (2002). Gabapentin and pregabalin suppress tactile allodynia and potentiate spinal cord stimulation in a model of neuropathy. Eur J Pain 6, 261-272.
59. Wallin, J., Fiska, A., Tjolsen, A., Linderoth, B., Hole, K. (2003). Spinal cord stimulation inhibits long-term potentiation of spinal wide dynamic range neurons. Brain Res 973, 39- 43.
60. Wolter, T., Kieselbach, K. (2011). Spinal cord stimulation for Raynaud's syndrome: Long-term alleviation of bilateral pain with a single cervical lead. Neuromodulation 14, 229- 233.
61. Wolter, T., Winkelmüller, M. (2012). Continuous versus intermittent spinal cord stimulation: An analysis of factors influencing clinical efficacy. Neuromodulation 15, 13-19.
62. Woolf, C.J., Barrett, G.D., Mitchell, D., Myers, R.A. (1977). Naloxone-reversible peripheral electroanalgesia in intact and spinal rats. Eur J Pharmacol 45, 311-314.
63. Xie, G.X., Han, J.S., Hollt, V. (1983). Electroacupuncture analgesia blocked by microinjection of anti-beta-endorphin antiserum into periaqueductal gray of the rabbit. Int J Neurosci 18, 287-291.
64. Yakhnitsa, V., Linderoth, B., Meyerson, B.A. (1999). Spinal cord stimulation attenuates dorsal horn neuronal hyperexcitability in a rat model of mononeuropathy. Pain 79, 223-233.
65. Yang, F., Carteret, A.F., Wacnik, P.W., Chung, C.Y., Xing, L., Dong, X., Meyer, R.A., Raja, S.N., Guan, Y. (2011). Bipolar spinal cord stimulation attenuates mechanical hypersensitivity at an intensity that activates a small portion of A-fiber afferents in spinal nerve-injured rats. Neuroscience 29, 470-480.
66. Yu, W., Hao, J.X., Xu, X.J., Wiesenfeld-Hallin, Z. (1997). The development of morphine tolerance and dependence in rats with chronic pain. Brain Res 756, 141-146.