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Erschienen in: Lasers in Medical Science 9/2019

10.04.2019 | Original Article

Photobiomodulation-induced analgesia in experimental temporomandibular disorder involves central inhibition of fractalkine

verfasst von: João Ignácio Ferrara-Jr, Everton Tiago de Souza, Adriano Cardozo Franciosi, Elaine Flamia Toniolo, Camila Squarzoni Dale

Erschienen in: Lasers in Medical Science | Ausgabe 9/2019

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Abstract

Temporomandibular disorder (TMD) is a collective term that encompasses a set of clinical problems that affect the masticatory muscles, the temporomandibular joint, and associated structures. Despite their high clinical prevalence, the mechanisms of chronic craniofacial muscle pain are not yet well understood. Treatments for TMD pain relief and control should be minimally invasive, reversible, and conservative. Photobiomodulation (PBM) is a promising option once it is known to inhibit inflammatory response and to relief painful symptoms. Herein, the effects of PBM (660 nm, 30 mW, 16 J/cm2, 0.2 cm2, 15 s in a continuous frequency) on the pain sensitivity of rats submitted to an experimental model of TMD induced by CFA was evaluated. Experimental TMD was induced in rats by the injection of complete Freund’s adjuvant (CFA) injection into the masseter muscle. Nociceptive behavior was evaluated by electronic von Frey before CFA and after 1 h, 3 h, 6 h, and 24 h and 7, 14, and 21 days after PBM treatment. Inflammatory infiltrate was evaluated by histology of the masseter muscle and fractalkine expression was evaluated by immunohistochemistry of the trigeminal ganglia. PBM reversed the mechanical hypersensitivity of the animals by inhibiting the local inflammatory response, observed by the decrease of the inflammatory infiltrate in the masseter muscle of rats and by a central inhibition of fractalkine observed in the trigeminal ganglion. These data provide new insights into the mechanisms involved in the effects of photobiomodulation therapy emphasizing its therapeutic potential in the treatment of TMD.
Literatur
1.
Zurück zum Zitat Köhler AA, Hugoson A, Magnusson T (2013) Clinical signs indicative of temporomandibular disorders in adults: time trends and associated factors. Swed Dent J 37:1–11PubMed Köhler AA, Hugoson A, Magnusson T (2013) Clinical signs indicative of temporomandibular disorders in adults: time trends and associated factors. Swed Dent J 37:1–11PubMed
2.
Zurück zum Zitat Macfarlane TV, Glenny AM, Worthington HV (2001) Systematic review of population-based epidemiological studies of oro-facial pain. J Dent 29:451–457PubMed Macfarlane TV, Glenny AM, Worthington HV (2001) Systematic review of population-based epidemiological studies of oro-facial pain. J Dent 29:451–457PubMed
3.
Zurück zum Zitat de Siqueira SR, Vilela TT, Florindo AA (2015) Prevalence of headache and orofacial pain in adults and elders in a Brazilian community: an epidemiological study. Gerodontology 32:123–131PubMed de Siqueira SR, Vilela TT, Florindo AA (2015) Prevalence of headache and orofacial pain in adults and elders in a Brazilian community: an epidemiological study. Gerodontology 32:123–131PubMed
4.
Zurück zum Zitat Gonçalves DA, Dal Fabbro AL, Campos JADB, Bigal ME, Speciali JG (2010) Symptoms of temporomandibular disorders in the population: an epidemiological study. J Orofac Pain 24:270–278PubMed Gonçalves DA, Dal Fabbro AL, Campos JADB, Bigal ME, Speciali JG (2010) Symptoms of temporomandibular disorders in the population: an epidemiological study. J Orofac Pain 24:270–278PubMed
5.
Zurück zum Zitat Machado LP, Nery Cde G, Leles CR, Nery MB, Okeson JP (2009) The prevalence of clinical diagnostic groups in patients with temporomandibular disorders. Cranio 27(3):194–199PubMed Machado LP, Nery Cde G, Leles CR, Nery MB, Okeson JP (2009) The prevalence of clinical diagnostic groups in patients with temporomandibular disorders. Cranio 27(3):194–199PubMed
6.
Zurück zum Zitat Ambalavanar R, Yallampalli C, Yallampalli U, Dessem D (2007) Injection of adjuvant but not acidic saline into craniofacial muscle evokes nociceptive behaviors and neuropeptide expression. Neuroscience 149(3):650–659PubMedPubMedCentral Ambalavanar R, Yallampalli C, Yallampalli U, Dessem D (2007) Injection of adjuvant but not acidic saline into craniofacial muscle evokes nociceptive behaviors and neuropeptide expression. Neuroscience 149(3):650–659PubMedPubMedCentral
7.
Zurück zum Zitat Barbe MF, Barr AE (2006) Inflammation and the pathophysiology of work-related musculoskeletal disorders. Brain Behav Immun 20(5):423–429PubMedPubMedCentral Barbe MF, Barr AE (2006) Inflammation and the pathophysiology of work-related musculoskeletal disorders. Brain Behav Immun 20(5):423–429PubMedPubMedCentral
8.
Zurück zum Zitat Carroll JD, Milward MR, Cooper PR, Hadis H, Palin WM (2014) Developments in low level light therapy (LLLT) for dentistry. Dent Mater 30(5):465–475PubMed Carroll JD, Milward MR, Cooper PR, Hadis H, Palin WM (2014) Developments in low level light therapy (LLLT) for dentistry. Dent Mater 30(5):465–475PubMed
9.
Zurück zum Zitat Herpich CM, Leal-Junior ECP, Amaral AP, Tosato JP, Glória IPS, Garcia MBS, Barbosa BRB, El Hage Y, Arruda EEC, Gomes CAFP, Rodrigues MS, de Sousa DFM, Carvalho PTC, Bussadori SK, Gonzalez TO, Politti F, Biasotto-Gonzalez DA (2015) Analysis of laser therapy and assessment methods in the rehabilitation of temporomandibular disorder: a systematic review of the literature. J Phys Ther Sci 27(1):295–301PubMedPubMedCentral Herpich CM, Leal-Junior ECP, Amaral AP, Tosato JP, Glória IPS, Garcia MBS, Barbosa BRB, El Hage Y, Arruda EEC, Gomes CAFP, Rodrigues MS, de Sousa DFM, Carvalho PTC, Bussadori SK, Gonzalez TO, Politti F, Biasotto-Gonzalez DA (2015) Analysis of laser therapy and assessment methods in the rehabilitation of temporomandibular disorder: a systematic review of the literature. J Phys Ther Sci 27(1):295–301PubMedPubMedCentral
10.
Zurück zum Zitat Melis M, Di Giosia M, Zawawi KH (2012) Low level laser therapy for the treatment of temporomandibular disorders: a systematic review of the literature. Cranio 30(4):304–312PubMed Melis M, Di Giosia M, Zawawi KH (2012) Low level laser therapy for the treatment of temporomandibular disorders: a systematic review of the literature. Cranio 30(4):304–312PubMed
11.
Zurück zum Zitat Carrasco TG, Mazzetto MO, Mazzetto RG, Mestriner W (2008) Low intensity laser therapy in temporomandibular disorder: a phase II double-blind study. Cranio 26:274–281PubMed Carrasco TG, Mazzetto MO, Mazzetto RG, Mestriner W (2008) Low intensity laser therapy in temporomandibular disorder: a phase II double-blind study. Cranio 26:274–281PubMed
12.
Zurück zum Zitat Mazzetto MO, Carrasco TG, Bidinelo EF, Pizzo RCA, Mazzetto RG (2007) Low intensity laser application in temporomandibular disorders: a phase I double-blind study. Cranio 25(3):186–192PubMed Mazzetto MO, Carrasco TG, Bidinelo EF, Pizzo RCA, Mazzetto RG (2007) Low intensity laser application in temporomandibular disorders: a phase I double-blind study. Cranio 25(3):186–192PubMed
13.
Zurück zum Zitat Melchior M de O, Venezian GC, Machado BC, Borges RF, Mazzetto MO (2013) Does low intensity laser therapy reduce pain and change orofacial myofunctional conditions? Cranio 31(2):133–139 Melchior M de O, Venezian GC, Machado BC, Borges RF, Mazzetto MO (2013) Does low intensity laser therapy reduce pain and change orofacial myofunctional conditions? Cranio 31(2):133–139
14.
Zurück zum Zitat Venezian GC, Silva ARM, Mazzetto RG, Mazzetto MO (2010) Low level laser effects on pain to palpation and electromyographic activity in TMD patients: a double-blind, randomized, placebo-controlled study. Cranio 28:84–91PubMed Venezian GC, Silva ARM, Mazzetto RG, Mazzetto MO (2010) Low level laser effects on pain to palpation and electromyographic activity in TMD patients: a double-blind, randomized, placebo-controlled study. Cranio 28:84–91PubMed
15.
Zurück zum Zitat Núñez SC, Garcez AS, Suzuki SS, Ribeiro MS (2006) Management of mouth opening in patients with temporomandibular disorders through low-level laser therapy and transcutaneous electrical neural stimulation. Photomed Laser Surg 24:45–49PubMed Núñez SC, Garcez AS, Suzuki SS, Ribeiro MS (2006) Management of mouth opening in patients with temporomandibular disorders through low-level laser therapy and transcutaneous electrical neural stimulation. Photomed Laser Surg 24:45–49PubMed
16.
Zurück zum Zitat Çetiner S, Kahraman SA, Yücetas S (2006) Evaluation of low-level laser therapy in the treatment of temporomandibular disorders. Photomed Laser Surg 24:637–641PubMed Çetiner S, Kahraman SA, Yücetas S (2006) Evaluation of low-level laser therapy in the treatment of temporomandibular disorders. Photomed Laser Surg 24:637–641PubMed
17.
Zurück zum Zitat da Silva MAMR, Botelho AL, Turim CV, da Silva AMR (2012) Low level laser therapy as an adjunctive technique in the management of temporomandibular disorders. Cranio 30:264–271PubMed da Silva MAMR, Botelho AL, Turim CV, da Silva AMR (2012) Low level laser therapy as an adjunctive technique in the management of temporomandibular disorders. Cranio 30:264–271PubMed
18.
Zurück zum Zitat Cao Y, Li K, Fu KY, Xie QF, Chiang CY, Sessle BJ (2013) Central sensitization and MAPKs are involved in occlusal interference-induced facial pain in rats. J Pain 14:793–807PubMedPubMedCentral Cao Y, Li K, Fu KY, Xie QF, Chiang CY, Sessle BJ (2013) Central sensitization and MAPKs are involved in occlusal interference-induced facial pain in rats. J Pain 14:793–807PubMedPubMedCentral
19.
Zurück zum Zitat Chiang CY, Dostrovsky DO, Iwata K, Sessle BJ (2011) Role of glia in orofacial pain. Neuroscientist 17:303–320PubMed Chiang CY, Dostrovsky DO, Iwata K, Sessle BJ (2011) Role of glia in orofacial pain. Neuroscientist 17:303–320PubMed
20.
Zurück zum Zitat Deguchi T, Adachi R, Kamioka H, Kim DG, Fields HW, Takano-Yamamoto T, Ichikawa H, Yamashiro T (2016) Effect of minocycline on induced glial activation by experimental tooth movement. Am J Orthod Dentofac Orthop 149:881–888 Deguchi T, Adachi R, Kamioka H, Kim DG, Fields HW, Takano-Yamamoto T, Ichikawa H, Yamashiro T (2016) Effect of minocycline on induced glial activation by experimental tooth movement. Am J Orthod Dentofac Orthop 149:881–888
21.
Zurück zum Zitat Kiyomoto M, Shinoda M, Honda K, Nakaya Y, Dezawa K, Katagiri A, Kamakura S, Inoue T, Iwata K (2015) p38 phosphorylation in medullary microglia mediates ectopic orofacial inflammatory pain in rats. Mol Pain 11:48PubMedPubMedCentral Kiyomoto M, Shinoda M, Honda K, Nakaya Y, Dezawa K, Katagiri A, Kamakura S, Inoue T, Iwata K (2015) p38 phosphorylation in medullary microglia mediates ectopic orofacial inflammatory pain in rats. Mol Pain 11:48PubMedPubMedCentral
22.
Zurück zum Zitat Lee S, Zhao YQ, Ribeiro-da-Silva A, Zhang J (2010) Distinctive response of CNS glial cells in oro-facial pain associated with injury, infection and inflammation. Mol Pain 6:79PubMedPubMedCentral Lee S, Zhao YQ, Ribeiro-da-Silva A, Zhang J (2010) Distinctive response of CNS glial cells in oro-facial pain associated with injury, infection and inflammation. Mol Pain 6:79PubMedPubMedCentral
23.
Zurück zum Zitat Sugiyo S, Takemura M, Dubner R, Ren K (2005) Trigeminal transition zone/rostral ventromedial medulla connections and facilitation of orofacial hyperalgesia after masseter inflammation in rats. J Comp Neurol 493:510–523PubMed Sugiyo S, Takemura M, Dubner R, Ren K (2005) Trigeminal transition zone/rostral ventromedial medulla connections and facilitation of orofacial hyperalgesia after masseter inflammation in rats. J Comp Neurol 493:510–523PubMed
24.
Zurück zum Zitat Clark AK, Staniland AA, Malcangio M (2011) Fractalkine/CX3CR1 signalling in chronic pain and inflammation. Curr Pharm Biotechnol 12:1707–1714PubMed Clark AK, Staniland AA, Malcangio M (2011) Fractalkine/CX3CR1 signalling in chronic pain and inflammation. Curr Pharm Biotechnol 12:1707–1714PubMed
25.
Zurück zum Zitat Hatori K, Nagai A, Heisel R, Ryu JK, Kim SU (2002) Fractalkine and fractalkine receptors in human neurons and glial cells. J Neurosci Res 69:418–426PubMed Hatori K, Nagai A, Heisel R, Ryu JK, Kim SU (2002) Fractalkine and fractalkine receptors in human neurons and glial cells. J Neurosci Res 69:418–426PubMed
26.
Zurück zum Zitat Hughes PM, Botham MS, Frentzel S, Mir A, Perry VH (2002) Expression of fractalkine (CX3CL1) and its receptor, CX3CR1, during acute and chronic inflammation in the rodent CNS. Glia 37:314–327PubMed Hughes PM, Botham MS, Frentzel S, Mir A, Perry VH (2002) Expression of fractalkine (CX3CL1) and its receptor, CX3CR1, during acute and chronic inflammation in the rodent CNS. Glia 37:314–327PubMed
27.
Zurück zum Zitat Jones BA, Beamer M, Ahmed S (2010) Fractalkine/CX3CL1: a potential new target for inflammatory diseases. Mol Interv 10:263–270PubMedPubMedCentral Jones BA, Beamer M, Ahmed S (2010) Fractalkine/CX3CL1: a potential new target for inflammatory diseases. Mol Interv 10:263–270PubMedPubMedCentral
28.
Zurück zum Zitat Milligan ED, Sloane EM, Watkins LR (2008) Glia in pathological pain: a role for fractalkine. J Neuroimmunol 198:113–120PubMedPubMedCentral Milligan ED, Sloane EM, Watkins LR (2008) Glia in pathological pain: a role for fractalkine. J Neuroimmunol 198:113–120PubMedPubMedCentral
29.
Zurück zum Zitat Souza GR, Talbot J, Lotufo CM, Cunha FQ, Cunha TM, Ferreira SH (2013) Fractalkine mediates inflammatory pain through activation of satellite glial cells. PNAS 110:11193–11198PubMed Souza GR, Talbot J, Lotufo CM, Cunha FQ, Cunha TM, Ferreira SH (2013) Fractalkine mediates inflammatory pain through activation of satellite glial cells. PNAS 110:11193–11198PubMed
30.
Zurück zum Zitat Kiyomoto M, Shinoda M, Okada-Ogawa A, Noma N, Shibuta K, Tsuboi Y, Sessle BJ, Imamura Y, Iwata K (2013) Fractalkine signaling in microglia contributes to ectopic orofacial pain following trapezius muscle inflammation. J Neurosci 33:7667–7680PubMedPubMedCentral Kiyomoto M, Shinoda M, Okada-Ogawa A, Noma N, Shibuta K, Tsuboi Y, Sessle BJ, Imamura Y, Iwata K (2013) Fractalkine signaling in microglia contributes to ectopic orofacial pain following trapezius muscle inflammation. J Neurosci 33:7667–7680PubMedPubMedCentral
31.
Zurück zum Zitat Cairns BE, O’Brien M, Dong XD, Gazerani P (2017) Elevated fractalkine (CX3CL1) levels in the trigeminal ganglion mechanically sensitize temporalis muscle nociceptors. Mol Neurobiol 54:3695–3706PubMed Cairns BE, O’Brien M, Dong XD, Gazerani P (2017) Elevated fractalkine (CX3CL1) levels in the trigeminal ganglion mechanically sensitize temporalis muscle nociceptors. Mol Neurobiol 54:3695–3706PubMed
32.
Zurück zum Zitat Denadai-Souza A, Camargo LL, Ribela MTCP, Keeble JE, Costa SKP, Muscará MN (2009) Participation of peripheral tachykinin NK1 receptors in the carrageenan-induced inflammation of the rat temporomandibular joint. Eur J Pain 13:812–819PubMed Denadai-Souza A, Camargo LL, Ribela MTCP, Keeble JE, Costa SKP, Muscará MN (2009) Participation of peripheral tachykinin NK1 receptors in the carrageenan-induced inflammation of the rat temporomandibular joint. Eur J Pain 13:812–819PubMed
33.
Zurück zum Zitat Capra NF, Ro JY (2004) Human and animal experimental models of acute and chronic muscle pain: intramuscular algesic injection. Pain 110:3–7PubMed Capra NF, Ro JY (2004) Human and animal experimental models of acute and chronic muscle pain: intramuscular algesic injection. Pain 110:3–7PubMed
34.
Zurück zum Zitat Imbe H, Iwata K, Zhou QQ, Zou S, Dubner R, Ren K (2001) Orofacial deep and cutaneous tissue inflammation and trigeminal neuronal activation. Implications for persistent temporomandibular pain. Cells Tissues Organs 169:238–247PubMed Imbe H, Iwata K, Zhou QQ, Zou S, Dubner R, Ren K (2001) Orofacial deep and cutaneous tissue inflammation and trigeminal neuronal activation. Implications for persistent temporomandibular pain. Cells Tissues Organs 169:238–247PubMed
35.
Zurück zum Zitat Okumura M, Iwata K, Yasuda K, Inoue K, Shinoda M, Honda K, Shibuta K, Yasuda M, Kondo E (2010) Alternation of gene expression in trigeminal ganglion neurons following complete Freund’s adjuvant or capsaicin injection into the rat face. J Mol Neurosci 42:200–209PubMed Okumura M, Iwata K, Yasuda K, Inoue K, Shinoda M, Honda K, Shibuta K, Yasuda M, Kondo E (2010) Alternation of gene expression in trigeminal ganglion neurons following complete Freund’s adjuvant or capsaicin injection into the rat face. J Mol Neurosci 42:200–209PubMed
36.
Zurück zum Zitat Ahrari F, Madani AS, Ghafouri ZS, Tunér J (2014) The efficacy of low-level laser therapy for the treatment of myogenous temporomandibular joint disorder. Lasers Med Sci 29:551–557PubMed Ahrari F, Madani AS, Ghafouri ZS, Tunér J (2014) The efficacy of low-level laser therapy for the treatment of myogenous temporomandibular joint disorder. Lasers Med Sci 29:551–557PubMed
37.
Zurück zum Zitat Moraes Maia ML, Ribeiro MA, Maia LG, Stuginski-Barbosa J, Costa YM, Porporatti AL, Conti PC, Bonjardim LR (2014) Evaluation of low-level laser therapy effectiveness on the pain and masticatory performance of patients with myofascial pain. Lasers Med Sci 29:29–35PubMed Moraes Maia ML, Ribeiro MA, Maia LG, Stuginski-Barbosa J, Costa YM, Porporatti AL, Conti PC, Bonjardim LR (2014) Evaluation of low-level laser therapy effectiveness on the pain and masticatory performance of patients with myofascial pain. Lasers Med Sci 29:29–35PubMed
38.
Zurück zum Zitat Rodrigues JH, Marques MM, Biasotto-Gonzalez DA, Moreira MS, Bussadori SK, Mesquita-Ferrari RA, Martins MD (2015) Evaluation of pain, jaw movements, and psychosocial factors in elderly individuals with temporomandibular disorder under laser phototherapy. Lasers Med Sci 30:953–959PubMed Rodrigues JH, Marques MM, Biasotto-Gonzalez DA, Moreira MS, Bussadori SK, Mesquita-Ferrari RA, Martins MD (2015) Evaluation of pain, jaw movements, and psychosocial factors in elderly individuals with temporomandibular disorder under laser phototherapy. Lasers Med Sci 30:953–959PubMed
39.
Zurück zum Zitat Salmos-Brito JA, Menezes RF, Teixeira CE, Gonzaga RK, Rodrigues BH, Braz R, Bessa-Nogueira RV, Gerbi ME (2013) Evaluation of low-level laser therapy in patients with acute and chronic temporomandibular disorders. Lasers Med Sci 28:57–64PubMed Salmos-Brito JA, Menezes RF, Teixeira CE, Gonzaga RK, Rodrigues BH, Braz R, Bessa-Nogueira RV, Gerbi ME (2013) Evaluation of low-level laser therapy in patients with acute and chronic temporomandibular disorders. Lasers Med Sci 28:57–64PubMed
40.
Zurück zum Zitat Shirani AM, Gutknecht N, Taghizadeh M, Mir M (2009) Low-level laser therapy and myofacial pain dysfunction syndrome: a randomized controlled clinical trial. Lasers Med Sci 24:715–720PubMed Shirani AM, Gutknecht N, Taghizadeh M, Mir M (2009) Low-level laser therapy and myofacial pain dysfunction syndrome: a randomized controlled clinical trial. Lasers Med Sci 24:715–720PubMed
41.
Zurück zum Zitat Peplow PV, Chung TY, Baxter GD (2012) Laser photostimulation (660 nm) of wound healing in diabetic mice is not brought about by ameliorating diabetes. Lasers Surg Med 44(1):26–29PubMed Peplow PV, Chung TY, Baxter GD (2012) Laser photostimulation (660 nm) of wound healing in diabetic mice is not brought about by ameliorating diabetes. Lasers Surg Med 44(1):26–29PubMed
42.
Zurück zum Zitat Ayuk SM, Houreld NN, Abrahamse H (2018) Effect of 660 nm visible red light on cell proliferation and viability in diabetic models in vitro under stressed conditions. Lasers Med Sci 33:1085–1093PubMed Ayuk SM, Houreld NN, Abrahamse H (2018) Effect of 660 nm visible red light on cell proliferation and viability in diabetic models in vitro under stressed conditions. Lasers Med Sci 33:1085–1093PubMed
43.
Zurück zum Zitat Houreld NN, Ayuk SM, Abrahamse H (2018) Cell adhesion molecules are mediated by photobiomodulation at 660 nm in diabetic wounded fibroblast cells. Cells 7:30PubMedCentral Houreld NN, Ayuk SM, Abrahamse H (2018) Cell adhesion molecules are mediated by photobiomodulation at 660 nm in diabetic wounded fibroblast cells. Cells 7:30PubMedCentral
44.
Zurück zum Zitat Oliveira ME, Santos FM, Bonifácio RP, Freitas MF, Martins DO, Chacur M (2017) Low level laser therapy alters satellite glial cell expression and reverses nociceptive behavior in rats with neuropathic pain. Photochem Photobiol Sci 16:547–554PubMed Oliveira ME, Santos FM, Bonifácio RP, Freitas MF, Martins DO, Chacur M (2017) Low level laser therapy alters satellite glial cell expression and reverses nociceptive behavior in rats with neuropathic pain. Photochem Photobiol Sci 16:547–554PubMed
45.
Zurück zum Zitat Johnston IN, Milligan ED, Wieseler-Frank J, Frank MG, Zapata V, Campisi J, Langer S, Martin D, Green P, Fleshner M, Leinwand L, Maier SF, Watkins LR (2004) A role for proinflammatory cytokines and fractalkine in analgesia, tolerance, and subsequent pain facilitation induced by chronic intrathecal morphine. J Neurosci 24:7353–7365PubMedPubMedCentral Johnston IN, Milligan ED, Wieseler-Frank J, Frank MG, Zapata V, Campisi J, Langer S, Martin D, Green P, Fleshner M, Leinwand L, Maier SF, Watkins LR (2004) A role for proinflammatory cytokines and fractalkine in analgesia, tolerance, and subsequent pain facilitation induced by chronic intrathecal morphine. J Neurosci 24:7353–7365PubMedPubMedCentral
46.
Zurück zum Zitat Milligan E, Zapata V, Schoeniger D, Chacur M, Green P, Poole S, Martin D, Maier SF, Watkins LR (2005) An initial investigation of spinal mechanisms underlying pain enhancement induced by fractalkine, a neuronally released chemokine. Eur J Neurosci 22:2775–2782PubMed Milligan E, Zapata V, Schoeniger D, Chacur M, Green P, Poole S, Martin D, Maier SF, Watkins LR (2005) An initial investigation of spinal mechanisms underlying pain enhancement induced by fractalkine, a neuronally released chemokine. Eur J Neurosci 22:2775–2782PubMed
47.
Zurück zum Zitat Milligan ED, Zapata V, Chacur M, Schoeniger D, Biedenkapp J, O’Connor KA, Verge GM, Chapman G, Green P, Foster AC, Naeve GS, Maier SF, Watkins LR (2004) Evidence that exogenous and endogenous fractalkine can induce spinal nociceptive facilitation in rats. Eur J Neurosci 20:2294–2302PubMed Milligan ED, Zapata V, Chacur M, Schoeniger D, Biedenkapp J, O’Connor KA, Verge GM, Chapman G, Green P, Foster AC, Naeve GS, Maier SF, Watkins LR (2004) Evidence that exogenous and endogenous fractalkine can induce spinal nociceptive facilitation in rats. Eur J Neurosci 20:2294–2302PubMed
Metadaten
Titel
Photobiomodulation-induced analgesia in experimental temporomandibular disorder involves central inhibition of fractalkine
verfasst von
João Ignácio Ferrara-Jr
Everton Tiago de Souza
Adriano Cardozo Franciosi
Elaine Flamia Toniolo
Camila Squarzoni Dale
Publikationsdatum
10.04.2019
Verlag
Springer London
Erschienen in
Lasers in Medical Science / Ausgabe 9/2019
Print ISSN: 0268-8921
Elektronische ISSN: 1435-604X
DOI
https://doi.org/10.1007/s10103-019-02785-6

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