Korean J Pain.  2020 Apr;33(2):121-130. 10.3344/kjp.2020.33.2.121.

Transcutaneous electrical nerve stimulation, acupuncture, and spinal cord stimulation on neuropathic, inflammatory and, noninflammatory pain in rat models

Affiliations
  • 1Department of Physical Therapy, Federal University of Sergipe, Sao Cristovao, Brazil
  • 2Department of Physical Therapy, Physiotherapy Postgraduate Program, Santa Catarina State University, Florianopolis, Brazil
  • 3Department of Physical Therapy, Federal University of Pampa, Uruguaiana, Brazil
  • 4Department of Physical Therapy and Rehabilitation Science, Pain Research Program, University of Iowa, Iowa City, IA, USA

Abstract

Background
Transcutaneous electrical nerve stimulation (TENS), manual acupuncture (MA), and spinal cord stimulation (SCS) are used to treat a variety of pain conditions. These non-pharmacological treatments are often thought to work through similar mechanisms, and thus should have similar effects for different types of pain. However, it is unclear if each of these treatments work equally well on each type of pain condition. The purpose of this study was to compared the effects of TENS, MA, and SCS on neuropathic, inflammatory, and non-inflammatory pain models.
Methods
TENS 60 Hz, 200 μs, 90% motor threshold (MT), SCS was applied at 60 Hz, an intensity of 90% MT, and a 0.25 ms pulse width. MA was performed by inserting a stainless-steel needle to a depth of about 4-5 mm at the Sanyinjiao (SP6) and Zusanli (ST36) acupoints on a spared nerve injury (SNI), knee joint inflammation (3% carrageenan), and non-inflammatory muscle pain (intramuscular pH 4.0 injections) in rats. Mechanical withdrawal thresholds of the paw, muscle, and/or joint were assessed before and after induction of the pain model, and daily before and after treatment.
Results
The reduced withdrawal thresholds were significantly reversed by application of either TENS or SCS (P < 0.05). MA, on the other hand, increased the withdrawal threshold in animals with SNI and joint inflammation, but not chronic muscle pain.
Conclusions
TENS and SCS produce similar effects in neuropathic, inflammatory and non-inflammatory muscle pain models while MA is only effective in inflammatory and neuropathic pain models.

Keyword

Acupuncture Therapy; Inflammation; Knee Joint; Myalgia; Neuralgia; Pain; Spinal Cord Stimulation; Transcutaneous Electric Nerve Stimulation

Figure

  • Fig. 1 Average paw withdrawal thresholds in the SNI group (A), joint inflammation group (B), and the non-inflammatory muscle pain group (C). Each graph shows the effects before and after induction of the model, and before and after treatment on each day. A significant decrease in withdrawal thresholds occurred after induction of the models, and this reduced withdrawal thresholds was increased after treatment on each day for the SNI and the joint inflammation model. For the acid model, a significant decrease occurred in all groups, and this decreased threshold was reversed by TENS and SCS but not by MA. SNI: spared nerve injury, TENS: transcutaneous electrical nerve stimulation, SCS: spinal cord stimulation, MA: manual acupuncture. ***P < 0.001.

  • Fig. 2 (A) Average joint withdrawal thresholds before (baseline) and after induction of knee joint inflammation, and before and after treatment on each day with TENS, MA, or SCS. Significant increases occurred after treatment on each day. TENS was significantly higher than SCS and MA. (B) Average muscle withdrawal thresholds before (baseline) and after the second injection of acidic saline (pH 4.0), and before and after treatment on each day with TENS, MA, SCS. Significant increases occurred after treatment on each day. SCS and TENS were significantly greater than MA. TENS: transcutaneous electrical nerve stimulation, MA: manual acupuncture, SCS: spinal cord stimulation. ***P < 0.001.


Reference

1. Orr PM, Shank BC, Black AC. 2017; The role of pain classification systems in pain management. Crit Care Nurs Clin North Am. 29:407–18. DOI: 10.1016/j.cnc.2017.08.002. PMID: 29107304.
Article
2. Decosterd I, Woolf CJ. 2000; Spared nerve injury: an animal model of persistent peripheral neuropathic pain. Pain. 87:149–58. DOI: 10.1016/S0304-3959(00)00276-1. PMID: 10924808.
Article
3. Radhakrishnan R, Moore SA, Sluka KA. 2003; Unilateral carrageenan injection into muscle or joint induces chronic bilateral hyperalgesia in rats. Pain. 104:567–77. DOI: 10.1016/S0304-3959(03)00114-3. PMID: 12927629. PMCID: PMC2732018.
Article
4. Sluka KA, Kalra A, Moore SA. 2001; Unilateral intramuscular injections of acidic saline produce a bilateral, long-lasting hyperalgesia. Muscle Nerve. 24:37–46. DOI: 10.1002/1097-4598(200101)24:1<37::AID-MUS4>3.0.CO;2-8. PMID: 11150964.
Article
5. Lee JB, Choi SS, Ahn EH, Hahm KD, Suh JH, Leem JG, et al. 2010; Effect of perioperative perineural injection of dexamethasone and bupivacaine on a rat spared nerve injury model. Korean J Pain. 23:166–71. DOI: 10.3344/kjp.2010.23.3.166. PMID: 20830261. PMCID: PMC2935977.
Article
6. Radhakrishnan R, Bement MK, Skyba D, Sluka KA, Kehl LJ. 2004; Models of muscle pain: carrageenan model and acidic saline model. Curr Protoc Pharmacol. 25:5.35.1–28. DOI: 10.1002/0471141755.ph0535s25. PMID: 22294122.
Article
7. Dailey DL, Rakel BA, Vance CG, Liebano RE, Amrit AS, Bush HM, et al. 2013; Transcutaneous electrical nerve stimulation reduces pain, fatigue and hyperalgesia while restoring central inhibition in primary fibromyalgia. Pain. 154:2554–62. DOI: 10.1016/j.pain.2013.07.043. PMID: 23900134. PMCID: PMC3972497.
Article
8. Beyaz SG, Bal NŞ. 2017; Spinal cord stimulation for a patient with neuropathic pain related to congenital syringomyelia. Korean J Pain. 30:229–30. DOI: 10.3344/kjp.2017.30.3.229. PMID: 28757924. PMCID: PMC5532531.
Article
9. Lee SJ, Yoo YM, You JA, Shin SW, Kim TK, Abdi S, et al. 2019; Successful removal of permanent spinal cord stimulators in patients with complex regional pain syndrome after complete relief of pain. Korean J Pain. 32:47–50. DOI: 10.3344/kjp.2019.32.1.47. PMID: 30671203. PMCID: PMC6333578.
Article
10. Sato KL, Johanek LM, Sanada LS, Sluka KA. 2014; Spinal cord stimulation (SCS) improves decreased physical activity induced by nerve injury. Behav Neurosci. 128:625–32. DOI: 10.1037/bne0000004. PMID: 24911318.
Article
11. Ezzo J, Hadhazy V, Birch S, Lao L, Kaplan G, Hochberg M, et al. 2001; Acupuncture for osteoarthritis of the knee: a systematic review. Arthritis Rheum. 44:819–25. DOI: 10.1002/1529-0131(200104)44:4<819::AID-ANR138>3.0.CO;2-P. PMID: 11315921.
Article
12. Cidral-Filho FJ, da Silva MD, Moré AO, Córdova MM, Werner MF, Santos AR. 2011; Manual acupuncture inhibits mechanical hypersensitivity induced by spinal nerve ligation in rats. Neuroscience. 193:370–6. DOI: 10.1016/j.neuroscience.2011.07.076. PMID: 21835228.
Article
13. Kalra A, Urban MO, Sluka KA. 2001; Blockade of opioid receptors in rostral ventral medulla prevents antihyperalgesia produced by transcutaneous electrical nerve stimulation (TENS). J Pharmacol Exp Ther. 298:257–63. PMID: 11408550.
14. Maeda Y, Lisi TL, Vance CG, Sluka KA. 2007; Release of GABA and activation of GABA(A) in the spinal cord mediates the effects of TENS in rats. Brain Res. 1136:43–50. DOI: 10.1016/j.brainres.2006.11.061. PMID: 17234163. PMCID: PMC2746639.
Article
15. Song Z, Ansah OB, Meyerson BA, Pertovaara A, Linderoth B. 2013; Exploration of supraspinal mechanisms in effects of spinal cord stimulation: role of the locus coeruleus. Neuroscience. 253:426–34. DOI: 10.1016/j.neuroscience.2013.09.006. PMID: 24036376.
Article
16. Takeshige C, Sato T, Mera T, Hisamitsu T, Fang J. 1992; Descending pain inhibitory system involved in acupuncture analgesia. Brain Res Bull. 29:617–34. DOI: 10.1016/0361-9230(92)90131-G. PMID: 1422859.
Article
17. Mayer DJ. 2000; Biological mechanisms of acupuncture. Prog Brain Res. 122:457–77. DOI: 10.1016/S0079-6123(08)62157-3. PMID: 10737077.
Article
18. Zhao ZQ. 2008; Neural mechanism underlying acupuncture analgesia. Prog Neurobiol. 85:355–75. DOI: 10.1016/j.pneurobio.2008.05.004. PMID: 18582529.
Article
19. da Silva MD, Bobinski F, Sato KL, Kolker SJ, Sluka KA, Santos AR. 2015; IL-10 cytokine released from M2 macrophages is crucial for analgesic and anti-inflammatory effects of acupuncture in a model of inflammatory muscle pain. Mol Neurobiol. 51:19–31. DOI: 10.1007/s12035-014-8790-x. PMID: 24961568. PMCID: PMC4276737.
Article
20. Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL. 1994; Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods. 53:55–63. DOI: 10.1016/0165-0270(94)90144-9. PMID: 7990513.
Article
21. Sluka KA. 1998; Blockade of N- and P/Q-type calcium channels reduces the secondary heat hyperalgesia induced by acute inflammation. J Pharmacol Exp Ther. 287:232–7. PMID: 9765342.
22. Gopalkrishnan P, Sluka KA. 2000; Effect of varying frequency, intensity, and pulse duration of transcutaneous electrical nerve stimulation on primary hyperalgesia in inflamed rats. Arch Phys Med Rehabil. 81:984–90. DOI: 10.1053/apmr.2000.5576. PMID: 10896017.
Article
23. Yu YC, Koo ST, Kim CH, Lyu Y, Grady JJ, Chung JM. 2002; Two variables that can be used as pain indices in experimental animal models of arthritis. J Neurosci Methods. 115:107–13. DOI: 10.1016/S0165-0270(02)00011-0. PMID: 11897370.
Article
24. Skyba DA, Radhakrishnan R, Sluka KA. 2005; Characterization of a method for measuring primary hyperalgesia of deep somatic tissue. J Pain. 6:41–7. DOI: 10.1016/j.jpain.2004.10.002. PMID: 15629417.
Article
25. Gong W, Johanek LM, Sluka KA. 2014; Spinal cord stimulation reduces mechanical hyperalgesia and restores physical activity levels in animals with noninflammatory muscle pain in a frequency-dependent manner. Anesth Analg. 119:186–95. DOI: 10.1213/ANE.0000000000000239. PMID: 24797123.
Article
26. da Silva MD, Guginski G, Werner MF, Baggio CH, Marcon R, Santos AR. 2011; Involvement of interleukin-10 in the anti-inflammatory effect of Sanyinjiao (SP6) acupuncture in a mouse model of peritonitis. Evid Based Complement Alternat Med. 2011:217946. DOI: 10.1093/ecam/neq036. PMID: 21799673. PMCID: PMC3135881.
Article
27. Sluka KA, Judge MA, McColley MM, Reveiz PM, Taylor BM. 2000; Low frequency TENS is less effective than high frequency TENS at reducing inflammation-induced hyperalgesia in morphine-tolerant rats. Eur J Pain. 4:185–93. DOI: 10.1053/eujp.2000.0172. PMID: 10957699.
Article
28. Ma YT, Sluka KA. 2001; Reduction in inflammation-induced sensitization of dorsal horn neurons by transcutaneous electrical nerve stimulation in anesthetized rats. Exp Brain Res. 137:94–102. DOI: 10.1007/s002210000629. PMID: 11310176.
Article
29. Matsuo H, Uchida K, Nakajima H, Guerrero AR, Watanabe S, Takeura N, et al. 2014; Early transcutaneous electrical nerve stimulation reduces hyperalgesia and decreases activation of spinal glial cells in mice with neuropathic pain. Pain. 155:1888–901. DOI: 10.1016/j.pain.2014.06.022. PMID: 25010326.
Article
30. Gibson W, Wand BM, Meads C, Catley MJ, O’Connell NE. 2019; Transcutaneous electrical nerve stimulation (TENS) for chronic pain - an overview of Cochrane Reviews. Cochrane Database Syst Rev. 4:CD011890. DOI: 10.1002/14651858.CD011890.pub3. PMCID: PMC6446021.
Article
31. Nnoaham KE, Kumbang J. 2008; Transcutaneous electrical nerve stimulation (TENS) for chronic pain. Cochrane Database Syst Rev. 3:CD003222. DOI: 10.1002/14651858.CD003222.pub2. PMID: 18646088.
Article
32. Sluka KA, Bjordal JM, Marchand S, Rakel BA. 2013; What makes transcutaneous electrical nerve stimulation work? Making sense of the mixed results in the clinical literature. Phys Ther. 93:1397–402. DOI: 10.2522/ptj.20120281. PMID: 23641031. PMCID: PMC3788712.
Article
33. Cheing GL, Tsui AY, Lo SK, Hui-Chan CW. 2003; Optimal stimulation duration of tens in the management of osteoarthritic knee pain. J Rehabil Med. 35:62–8. DOI: 10.1080/16501970306116. PMID: 12691335.
Article
34. Johnson MI, Mulvey MR, Bagnall AM. 2015; Transcutaneous electrical nerve stimulation (TENS) for phantom pain and stump pain following amputation in adults. Cochrane Database Syst Rev. 8:CD007264. DOI: 10.1002/14651858.CD007264.pub3. PMID: 26284511.
Article
35. Jin DM, Xu Y, Geng DF, Yan TB. 2010; Effect of transcutaneous electrical nerve stimulation on symptomatic diabetic peripheral neuropathy: a meta-analysis of randomized controlled trials. Diabetes Res Clin Pract. 89:10–5. DOI: 10.1016/j.diabres.2010.03.021. PMID: 20510476.
Article
36. Tokuda M, Tabira K, Masuda T, Nishiwada T, Shomoto K. 2014; Effect of modulated-frequency and modulated-intensity transcutaneous electrical nerve stimulation after abdominal surgery: a randomized controlled trial. Clin J Pain. 30:565–70. DOI: 10.1097/AJP.0b013e31829ea151. PMID: 24901753.
37. Celik EC, Erhan B, Gunduz B, Lakse E. 2013; The effect of low-frequency TENS in the treatment of neuropathic pain in patients with spinal cord injury. Spinal Cord. 51:334–7. DOI: 10.1038/sc.2012.159. PMID: 23295472.
Article
38. Yameen F, Shahbaz NN, Hasan Y, Fauz R, Abdullah M. 2011; Efficacy of transcutaneous electrical nerve stimulation and its different modes in patients with trigeminal neuralgia. J Pak Med Assoc. 61:437–9. PMID: 22204173.
39. Vance CG, Rakel BA, Blodgett NP, DeSantana JM, Amendola A, Zimmerman MB, et al. 2012; Effects of transcutaneous electrical nerve stimulation on pain, pain sensitivity, and function in people with knee osteoarthritis: a randomized controlled trial. Phys Ther. 92:898–910. DOI: 10.2522/ptj.20110183. PMID: 22466027. PMCID: PMC3386514.
Article
40. Johnson M, Martinson M. 2007; Efficacy of electrical nerve stimulation for chronic musculoskeletal pain: a meta-analysis of randomized controlled trials. Pain. 130:157–65. DOI: 10.1016/j.pain.2007.02.007. PMID: 17383095.
Article
41. Sdrulla AD, Guan Y, Raja SN. 2018; Spinal cord stimulation: clinical efficacy and potential mechanisms. Pain Pract. 18:1048–67. DOI: 10.1111/papr.12692. PMID: 29526043. PMCID: PMC6391880.
42. Buonocore M, Bonezzi C, Barolat G. 2008; Neurophysiological evidence of antidromic activation of large myelinated fibres in lower limbs during spinal cord stimulation. Spine (Phila Pa 1976). 33:E90–3. DOI: 10.1097/BRS.0b013e3181642a97. PMID: 18277861.
Article
43. Vallejo R, Bradley K, Kapural L. 2017; Spinal cord stimulation in chronic pain: mode of action. Spine (Phila Pa 1976). 42(Suppl 14):S53–60. DOI: 10.1097/BRS.0000000000002179. PMID: 28368982.
44. Cha MH, Choi JS, Bai SJ, Shim I, Lee HJ, Choi SM, et al. 2006; Antiallodynic effects of acupuncture in neuropathic rats. Yonsei Med J. 47:359–66. DOI: 10.3349/ymj.2006.47.3.359. PMID: 16807985. PMCID: PMC2688155.
Article
45. Plaster R, Vieira WB, Alencar FA, Nakano EY, Liebano RE. 2014; Immediate effects of electroacupuncture and manual acupuncture on pain, mobility and muscle strength in patients with knee osteoarthritis: a randomised controlled trial. Acupunct Med. 32:236–41. DOI: 10.1136/acupmed-2013-010489. PMID: 24566612.
Article
46. Goldman N, Chen M, Fujita T, Xu Q, Peng W, Liu W, et al. 2010; Adenosine A1 receptors mediate local anti-nociceptive effects of acupuncture. Nat Neurosci. 13:883–8. DOI: 10.1038/nn.2562. PMID: 20512135. PMCID: PMC3467968.
Article
47. Norrbrink C, Lundeberg T. 2011; Acupuncture and massage therapy for neuropathic pain following spinal cord injury: an exploratory study. Acupunct Med. 29:108–15. DOI: 10.1136/aim.2010.003269. PMID: 21474490.
Article
48. Berman BM, Singh BB, Lao L, Langenberg P, Li H, Hadhazy V, et al. 1999; A randomized trial of acupuncture as an adjunctive therapy in osteoarthritis of the knee. Rheumatology (Oxford). 38:346–54. DOI: 10.1093/rheumatology/38.4.346. PMID: 10378713.
Article
49. Witt C, Brinkhaus B, Jena S, Linde K, Streng A, Wagenpfeil S, et al. 2005; Acupuncture in patients with osteoarthritis of the knee: a randomised trial. Lancet. 366:136–43. DOI: 10.1016/S0140-6736(05)66871-7. PMID: 16005336.
Article
50. Vas J, Modesto M, Aguilar I, Santos-Rey K, Benítez-Parejo N, Rivas-Ruiz F. 2011; Effects of acupuncture on patients with fibromyalgia: study protocol of a multicentre randomized controlled trial. Trials. 12:59. DOI: 10.1186/1745-6215-12-59. PMID: 21356075. PMCID: PMC3055832.
Article
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