Korean J Pain.  2021 Jun;34(3):250-261. 10.3344/kjp.2021.34.3.250.

Effects of photobiomodulation on different application points and different phases of complex regional pain syndrome type I in the experimental model

Affiliations
  • 1Background: Complex regional pain syndrome type I (CRPS-I) consists of disorders caused by spontaneous pain or induced by some stimulus. The objective was to verify the effects of photobiomodulation (PBM) using 830 nm wavelength light at the affected paw and involved spinal cord segments during the warm or acute phase. Methods: Fifty-six mice were randomized into seven groups. Group (G) 1 was the placebo group; G2 and G3 were treated with PBM on the paw in the warm and acute phase, respectively; G4 and G5 treated with PBM on involved spinal cord segments in the warm and acute phase, respectively; G6 and G7 treated with PBM on paw and involved spinal cord segments in the warm and acute phase, respectively. Edema degree, thermal and mechanical hyperalgesia, skin temperature, and functional quality of gait (Sciatic Static Index [SSI] and Sciatic Functional Index [SFI]) were evaluated. Results: Edema was lower in G3 and G7, and these were the only groups to return to baseline values at the end of treatment. For thermal hyperalgesia only G3 and G5 returned to baseline values. Regarding mechanical hyperalgesia, the groups did not show significant differences. Thermography showed increased temperature in all groups on the seventh day. In SSI and SFI assessment, G3 and G7 showed lower values when compared to G1, respectively. Conclusions: PBM irradiation in the acute phase and in the affected paw showed better results in reducing edema, thermal and mechanical hyperalgesia, and in improving gait quality, demonstrating efficacy in treatment of CRPS-I symptoms.
  • 2Postgraduate Program in Rehabilitation Sciences, Federal University of Santa Catarina, Araranguá, Brazil
  • 3Postgraduate Program in Rehabilitation and Functional Performance of the Departament of Health Sciences, Ribeirão Preto School of Medicine, University of São Paulo, Ribeirão Preto, Brazil

Abstract

Background
Complex regional pain syndrome type I (CRPS-I) consists of disorders caused by spontaneous pain or induced by some stimulus. The objective was to verify the effects of photobiomodulation (PBM) using 830 nm wavelength light at the affected paw and involved spinal cord segments during the warm or acute phase.
Methods
Fifty-six mice were randomized into seven groups. Group (G) 1 was the placebo group; G2 and G3 were treated with PBM on the paw in the warm and acute phase, respectively; G4 and G5 treated with PBM on involved spinal cord segments in the warm and acute phase, respectively; G6 and G7 treated with PBM on paw and involved spinal cord segments in the warm and acute phase, respectively. Edema degree, thermal and mechanical hyperalgesia, skin temperature, and functional quality of gait (Sciatic Static Index [SSI] and Sciatic Functional Index [SFI]) were evaluated.
Results
Edema was lower in G3 and G7, and these were the only groups to return to baseline values at the end of treatment. For thermal hyperalgesia only G3 and G5 returned to baseline values. Regarding mechanical hyperalgesia, the groups did not show significant differences. Thermography showed increased temperature in all groups on the seventh day. In SSI and SFI assessment, G3 and G7 showed lower values when compared to G1, respectively.
Conclusions
PBM irradiation in the acute phase and in the affected paw showed better results in reducing edema, thermal and mechanical hyperalgesia, and in improving gait quality, demonstrating efficacy in treatment of CRPS-I symptoms.

Keyword

Complex Regional Pain Syndromes; Edema; Hyperalgesia; Laser Therapy; Mice; Models; Animal; Pain; Pain Management; Reflex Sympathetic Dystrophy; Skin Temperature; Temperature; Thermography

Figure

  • Fig. 1 Representative photographs during tourniquet exposure (A), 2 after reperfusion (B) and 1 hour after tourniquet removal (C). Note in the second image the tissue hypoxia and in the third image, after tourniquet removal, hyperemia with apparent edema.

  • Fig. 2 Illustrative representation of the parameters used to calculate the Sciatic Static Index and Sciatic Functional Index. IT: intermediate finger opening, PL: footprint length, TS: full finger opening. Adapted from the article of Marcolino et al. (J Hand Microsurg 2013; 5: 49-53) [33].

  • Fig. 3 Average values of the edema variable between groups and evaluation days. Group (G) 1: control (placebo), G2: photobiomodulation (PBM) applied to the paw with complex regional pain syndrome type I (CRPS-I) from the warm phase, G3: PBM applied to the paw with CRPS-I from the acute phase, G4: PBM applied close to the area of the region between L4 and L5 from the warm phase, G5: PBM applied close to the area of the region between L4 and L5 from the acute phase, G6: PBM applied at two points: right paw and region between L4 and L5 from the warm phase, G7: PBM applied at two points: right paw and region between L4 and L5 from the acute phase. *P < 0.05.

  • Fig. 4 Average values referring to thermal hyperalgesia between groups and evaluations. Group (G) 1: control (placebo), G2: photobiomodulation (PBM) applied to the paw with complex regional pain syndrome type I (CRPS-I) from the warm phase, G3: PBM applied to the paw with CRPS-I from the acute phase, G4: PBM applied close to the area of the region between L4 and L5 from the warm phase, G5: PBM applied close to the area of the region between L4 and L5 from the acute phase, G6: PBM applied at two points: right paw and region between L4 and L5 from the warm phase, G7: PBM applied at two points: right paw and region between L4 and L5 from the acute phase. *P < 0.05.

  • Fig. 5 Average values of the mechanical hyperalgesia test (Von Frey) between groups and evaluations. Group (G) 1: control (placebo), G2: photobiomodulation (PBM) applied to the paw with complex regional pain syndrome type I (CRPS-I) from the warm phase, G3: PBM applied to the paw with CRPS-I from the acute phase, G4: PBM applied close to the area of the region between L4 and L5 from the warm phase, G5: PBM applied close to the area of the region between L4 and L5 from the acute phase, G6: PBM applied at two points: right paw and region between L4 and L5 from the warm phase, G7: PBM applied at two points: right paw and region between L4 and L5 from the acute phase.

  • Fig. 6 Average values of the thermographic evaluation between groups and evaluations. Group (G) 1: control (placebo), G2: photobiomodulation (PBM) applied to the paw with complex regional pain syndrome type I (CRPS-I) from the warm phase, G3: PBM applied to the paw with CRPS-I from the acute phase, G4: PBM applied close to the area of the region between L4 and L5 from the warm phase, G5: PBM applied close to the area of the region between L4 and L5 from the acute phase, G6: PBM applied at two points: right paw and region between L4 and L5 from the warm phase, G7: PBM applied at two points: right paw and region between L4 and L5 from the acute phase. *P < 0.05.

  • Fig. 7 Average values of Sciatic Functional Index (SFI) between groups and between evaluations. Group (G) 1: control (placebo), G2: photobiomodulation (PBM) applied to the paw with complex regional pain syndrome type I (CRPS-I) from the warm phase, G3: PBM applied to the paw with CRPS-I from the acute phase, G4: PBM applied close to the area of the region between L4 and L5 from the warm phase, G5: PBM applied close to the area of the region between L4 and L5 from the acute phase, G6: PBM applied at two points: right paw and region between L4 and L5 from the warm phase, G7: PBM applied at two points: right paw and region between L4 and L5 from the acute phase. *P < 0.05.

  • Fig. 8 Average values of Sciatic Static Index (SSI) between groups and between evaluations. Group (G) 1: control (placebo), G2: photobiomodulation (PBM) applied to the paw with complex regional pain syndrome type I (CRPS-I) from the warm phase, G3: PBM applied to the paw with CRPS-I from the acute phase, G4: PBM applied close to the area of the region between L4 and L5 from the warm phase, G5: PBM applied close to the area of the region between L4 and L5 from the acute phase, G6: PBM applied at two points: right paw and region between L4 and L5 from the warm phase, G7: PBM applied at two points: right paw and region between L4 and L5 from the acute phase. *P < 0.05.


Reference

1. De Prá SDT, Antoniazzi CTD, Ferro PR, Kudsi SQ, Camponogara C, Fialho MFP, et al. 2019; Nociceptive mechanisms involved in the acute and chronic phases of a complex regional pain syndrome type 1 model in mice. Eur J Pharmacol. 859:172555. DOI: 10.1016/j.ejphar.2019.172555. PMID: 31326377.
Article
2. Tajerian M, Clark JD. 2016; New concepts in complex regional pain syndrome. Hand Clin. 32:41–9. DOI: 10.1016/j.hcl.2015.08.003. PMID: 26611388. PMCID: PMC4662772.
Article
3. Birklein F, O'Neill D, Schlereth T. 2015; Complex regional pain syndrome: an optimistic perspective. Neurology. 84:89–96. DOI: 10.1212/WNL.0000000000001095. PMID: 25471395.
Article
4. Harden NR, Bruehl S, Perez RSGM, Birklein F, Marinus J, Maihofner C, et al. 2010; Validation of proposed diagnostic criteria (the "Budapest Criteria") for Complex Regional Pain Syndrome. Pain. 150:268–74. DOI: 10.1016/j.pain.2010.04.030. PMID: 20493633. PMCID: PMC2914601.
Article
5. Wei T, Guo TZ, Li WW, Kingery WS, Clark JD. 2016; Acute versus chronic phase mechanisms in a rat model of CRPS. J Neuroinflammation. 13:14. DOI: 10.1186/s12974-015-0472-8. PMID: 26785976. PMCID: PMC4719337.
Article
6. Goh EL, Chidambaram S, Ma D. 2017; Complex regional pain syndrome: a recent update. Burns Trauma. 5:2. DOI: 10.1186/s41038-016-0066-4. PMID: 28127572. PMCID: PMC5244710.
Article
7. Schwartzman RJ, Erwin KL, Alexander GM. 2009; The natural history of complex regional pain syndrome. Clin J Pain. 25:273–80. DOI: 10.1097/AJP.0b013e31818ecea5. PMID: 19590474.
Article
8. Lee WH. 2015; Complex regional pain syndrome: time to study the supraspinal role? Korean J Pain. 28:1–3. DOI: 10.3344/kjp.2015.28.1.1. PMID: 25589940. PMCID: PMC4293501.
Article
9. Karmarkar A, Lieberman I. 2006; Mirror box therapy for complex regional pain syndrome. Anaesthesia. 61:412–3. DOI: 10.1111/j.1365-2044.2006.04605.x. PMID: 16548982.
Article
10. Geurts JW, Smits H, Kemler MA, Brunner F, Kessels AG, van Kleef M. 2013; Spinal cord stimulation for complex regional pain syndrome type I: a prospective cohort study with long-term follow-up. Neuromodulation. 16:523–9. DOI: 10.1111/ner.12024. PMID: 23363081.
Article
11. Bodde MI, Dijkstra PU, den Dunnen WF, Geertzen JH. 2011; Therapy-resistant complex regional pain syndrome type I: to amputate or not? J Bone Joint Surg Am. 93:1799–805. DOI: 10.2106/JBJS.J.01329. PMID: 22005865.
Article
12. Krans-Schreuder HK, Bodde MI, Schrier E, Dijkstra PU, van den Dungen JA, den Dunnen WF, et al. 2012; Amputation for long-standing, therapy-resistant type-I complex regional pain syndrome. J Bone Joint Surg Am. 94:2263–8. DOI: 10.2106/JBJS.L.00532. PMID: 23318617.
Article
13. Rodrigues M, Cardoso RB, Kuriki HU, Marcolino AM, de Oliveira Guirro EC, Barbosa RI. 2020; Photobiomodulation decreases hyperalgesia in complex regional pain syndrome: an experimental mouse model subjected to nicotine. Lasers Surg Med. 52:890–6. DOI: 10.1002/lsm.23240. PMID: 32201964.
Article
14. Kocić M, Lazović M, Dimitrijević I, Mančić D, Stanković A. 2010; [Evaluation of low level laser and interferential current in the therapy of complex regional pain syndrome by infrared thermographic camera]. Vojnosanit Pregl. 67:755–60. Serbian. DOI: 10.2298/VSP1009755K. PMID: 20954414.
Article
15. Smart KM, Wand BM, O'Connell NE. 2016; Physiotherapy for pain and disability in adults with complex regional pain syndrome (CRPS) types I and II. Cochrane Database Syst Rev. 2:CD010853. DOI: 10.1002/14651858.CD010853.pub2. PMID: 26905470.
Article
16. Pires de Sousa MV, Ferraresi C, Kawakubo M, Kaippert B, Yoshimura EM, Hamblin MR. 2016; Transcranial low-level laser therapy (810 nm) temporarily inhibits peripheral nociception: photoneuromodulation of glutamate receptors, prostatic acid phophatase, and adenosine triphosphate. Neurophotonics. 3:015003. DOI: 10.1117/1.NPh.3.1.015003. PMID: 26835486. PMCID: PMC4725212.
17. de Sousa MVP, Kawakubo M, Ferraresi C, Kaippert B, Yoshimura EM, Hamblin MR. 2018; Pain management using photobiomodulation: mechanisms, location, and repeatability quantified by pain threshold and neural biomarkers in mice. J Biophotonics. 11:e201700370. DOI: 10.1002/jbio.201700370. PMID: 29484823. PMCID: PMC6037550.
Article
18. Tang C, Li J, Tai WL, Yao W, Zhao B, Hong J, et al. 2017; Sex differences in complex regional pain syndrome type I (CRPS-I) in mice. J Pain Res. 10:1811–9. DOI: 10.2147/JPR.S139365. PMID: 28831269. PMCID: PMC5548282.
Article
19. Coderre TJ, Xanthos DN, Francis L, Bennett GJ. 2004; Chronic post-ischemia pain (CPIP): a novel animal model of complex regional pain syndrome-type I (CRPS-I; reflex sympathetic dystrophy) produced by prolonged hindpaw ischemia and reperfusion in the rat. Pain. 112:94–105. DOI: 10.1016/j.pain.2004.08.001. PMID: 15494189.
Article
20. Drysch M, Wallner C, Schmidt SV, Reinkemeier F, Wagner JM, Lehnhardt M, et al. 2019; An optimized low-pressure tourniquet murine hind limb ischemia reperfusion model: inducing acute ischemia reperfusion injury in C57BL/6 wild type mice. PLoS One. 14:e0210961. DOI: 10.1371/journal.pone.0210961. PMID: 30677066. PMCID: PMC6345480.
Article
21. Gallagher JJ, Tajerian M, Guo T, Shi X, Li W, Zheng M, et al. 2013; Acute and chronic phases of complex regional pain syndrome in mice are accompanied by distinct transcriptional changes in the spinal cord. Mol Pain. 9:40. DOI: 10.1186/1744-8069-9-40. PMID: 23924076. PMCID: PMC3751593.
Article
22. Wei T, Li WW, Guo TZ, Zhao R, Wang L, Clark DJ, et al. 2009; Post-junctional facilitation of substance P signaling in a tibia fracture rat model of complex regional pain syndrome type I. Pain. 144:278–86. DOI: 10.1016/j.pain.2009.04.020. PMID: 19464118. PMCID: PMC2706925.
Article
23. Chen R, Yin C, Hu Q, Liu B, Tai Y, Zheng X, et al. 2020; Expression profiling of spinal cord dorsal horn in a rat model of complex regional pain syndrome type-I uncovers potential mechanisms mediating pain and neuroinflammation responses. J Neuroinflammation. 17:162. DOI: 10.1186/s12974-020-01834-0. PMID: 32446302. PMCID: PMC7245895.
Article
24. Barbosa RI, Guirro ECO, Bachmann L, Brandino HE, Guirro RRJ. 2020; Analysis of low-level laser transmission at wavelengths 660, 830 and 904 nm in biological tissue samples. J Photochem Photobiol B. 209:111914. DOI: 10.1016/j.jphotobiol.2020.111914. PMID: 32516626.
25. Shuaib A, Bourisly AK. 2018; Photobiomodulation optimization for spinal cord injury rat phantom model. Transl Neurosci. 9:67–71. DOI: 10.1515/tnsci-2018-0012. PMID: 29967691. PMCID: PMC6024694.
Article
26. Hudson DE, Hudson DO, Wininger JM, Richardson BD. 2013; Penetration of laser light at 808 and 980 nm in bovine tissue samples. Photomed Laser Surg. 31:163–8. DOI: 10.1089/pho.2012.3284. PMID: 23441909. PMCID: PMC3696948.
27. Hamblin MR, Ferraresi C, Huang YY, de Freitas LF, Carroll JD. 2018; Low-level light therapy: photobiomodulation. Bellingham. Society of Photo-Optical Instrumentation Engineers (SPIE). DOI: 10.1117/3.2295638.
28. Erthal V, Maria-Ferreira D, Werner MF, Baggio CH, Nohama P. 2016; Anti-inflammatory effect of laser acupuncture in ST36 (Zusanli) acupoint in mouse paw edema. Lasers Med Sci. 31:315–22. DOI: 10.1007/s10103-015-1845-z. PMID: 26738499.
Article
29. Hargreaves K, Dubner R, Brown F, Flores C, Joris J. 1988; A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain. 32:77–88. DOI: 10.1016/0304-3959(88)90026-7. PMID: 3340425.
Article
30. Minett MS, Eijkelkamp N, Wood JN. 2014; Significant determinants of mouse pain behaviour. PLoS One. 9:e104458. DOI: 10.1371/journal.pone.0104458. PMID: 25101983. PMCID: PMC4125188.
Article
31. Deuis JR, Dvorakova LS, Vetter I. 2017; Methods used to evaluate pain behaviors in rodents. Front Mol Neurosci. 10:284. DOI: 10.3389/fnmol.2017.00284. PMID: 28932184. PMCID: PMC5592204.
Article
32. de Souza LG, Marcolino AM, Kuriki HU, Gonçalves ECD, Fonseca MCR, Barbosa RI. 2018; Comparative effect of photobiomodulation associated with dexamethasone after sciatic nerve injury model. Lasers Med Sci. 33:1341–9. DOI: 10.1007/s10103-018-2494-9. PMID: 29611064.
Article
33. Marcolino AM, Barbosa RI, das Neves LM, Mazzer N, de Jesus Guirro RR, de Cássia Registro Fonseca M. 2013; Assessment of functional recovery of sciatic nerve in rats submitted to low-level laser therapy with different fluences. An experimental study: laser in functional recovery in rats. J Hand Microsurg. 5:49–53. DOI: 10.1007/s12593-013-0096-0. PMID: 24426674. PMCID: PMC3827659.
Article
34. de Medinaceli L, Freed WJ, Wyatt RJ. 1982; An index of the functional condition of rat sciatic nerve based on measurements made from walking tracks. Exp Neurol. 77:634–43. DOI: 10.1016/0014-4886(82)90234-5. PMID: 7117467.
Article
35. Bain JR, Mackinnon SE, Hunter DA. 1989; Functional evaluation of complete sciatic, peroneal, and posterior tibial nerve lesions in the rat. Plast Reconstr Surg. 83:129–36. DOI: 10.1097/00006534-198901000-00024. PMID: 2909054.
Article
36. Takhtfooladi MA, Jahanbakhsh F, Takhtfooladi HA, Yousefi K, Allahverdi A. 2015; Effect of low-level laser therapy (685 nm, 3 J/cm(2)) on functional recovery of the sciatic nerve in rats following crushing lesion. Lasers Med Sci. 30:1047–52. DOI: 10.1007/s10103-015-1709-6. PMID: 25595127.
Article
37. Smit X, van Neck JW, Ebeli MJ, Hovius SE. 2004; Static footprint analysis: a time-saving functional evaluation of nerve repair in rats. Scand J Plast Reconstr Surg Hand Surg. 38:321–5. DOI: 10.1080/02844310410034277. PMID: 15841798.
Article
38. National Institute of Neurological Disorders and Stroke. 2020. Complex regional pain syndrome fact sheet. National Institutes of Health;Bethesda:
39. Marcolino AM, Barbosa RI, das Neves LMS, Vinas TS, Duarte DTB, Mazzer N, et al. 2010; Low intensity laser (830 nm) functional to recover of the sciatic nerve in rats. Acta Ortop Bras. 18:207–11. DOI: 10.1590/S1413-78522010000400007.
40. Chow RT, David MA, Armati PJ. 2007; 830 nm laser irradiation induces varicosity formation, reduces mitochondrial membrane potential and blocks fast axonal flow in small and medium diameter rat dorsal root ganglion neurons: implications for the analgesic effects of 830 nm laser. J Peripher Nerv Syst. 12:28–39. DOI: 10.1111/j.1529-8027.2007.00114.x. PMID: 17374099.
Article
41. Pereira FC, Parisi JR, Maglioni CB, Machado GB, Barragán-Iglesias P, Silva JRT, et al. 2017; Antinociceptive effects of low-level laser therapy at 3 and 8 j/cm2 in a rat model of postoperative pain: possible role of endogenous opioids. Lasers Surg Med. 49:844–51. DOI: 10.1002/lsm.22696. PMID: 28671718.
42. Cotler HB, Chow RT, Hamblin MR, Carroll J. 2015; The use of low level laser therapy (LLLT) for musculoskeletal pain. MOJ Orthop Rheumatol. 2:00068. DOI: 10.15406/mojor.2015.02.00068. PMID: 26858986. PMCID: PMC4743666.
Article
43. Joensen J, Gjerdet NR, Hummelsund S, Iversen V, Lopes-Martins RA, Bjordal JM. 2012; An experimental study of low-level laser therapy in rat Achilles tendon injury. Lasers Med Sci. 27:103–11. DOI: 10.1007/s10103-011-0925-y. PMID: 21547473. PMCID: PMC3254871.
Article
44. Bjordal JM, Couppé C, Chow RT, Tunér J, Ljunggren EA. 2003; A systematic review of low level laser therapy with location-specific doses for pain from chronic joint disorders. Aust J Physiother. 49:107–16. DOI: 10.1016/S0004-9514(14)60127-6. PMID: 12775206.
Article
45. Barbosa RI, Marcolino AM, de Jesus Guirro RR, Mazzer N, Barbieri CH, de Cássia Registro Fonseca M. 2010; Comparative effects of wavelengths of low-power laser in regeneration of sciatic nerve in rats following crushing lesion. Lasers Med Sci. 25:423–30. DOI: 10.1007/s10103-009-0750-8. PMID: 20135336.
Article
46. Mandelbaum-Livnat MM, Almog M, Nissan M, Loeb E, Shapira Y, Rochkind S. 2016; Photobiomodulation triple treatment in peripheral nerve injury: nerve and muscle response. Photomed Laser Surg. 34:638–45. DOI: 10.1089/pho.2016.4095. PMID: 28001757.
Article
47. Neves LMS, Gonçalves ECD, Cavalli J, Vieira G, Laurindo LR, Simões RR, et al. 2018; Photobiomodulation therapy improves acute inflammatory response in mice: the role of cannabinoid receptors/ATP-sensitive K+ channel/p38-MAPK signalling pathway. Mol Neurobiol. 55:5580–93. DOI: 10.1007/s12035-017-0792-z. PMID: 28980210.
Article
Full Text Links
  • KJP
Actions
Cited
CITED
export Copy
Close
Share
  • Twitter
  • Facebook
Similar articles
Copyright © 2024 by Korean Association of Medical Journal Editors. All rights reserved.     E-mail: koreamed@kamje.or.kr