Effects of transcranial direct current stimulation (tDCS) on pro-inflammatory cytokines: a systematic review

Authors

DOI:

https://doi.org/10.33448/rsd-v11i13.35013

Keywords:

TDCS; Animals; Citokines.

Abstract

Transcranial direct current stimulation (tDCS) is a neuromodulation technique that causes alterations in the synthesis of several proteins, including cytokines (e.g., Interleukins). Pro-inflammatory cytokines are associated with the presence of pain and their reduction occurs in several pathologies. The aim of this study was to investigate the effects of tDCS on the variation of tissue and serum blood levels of pro-inflammatory cytokines and its relationship with behavioral changes, through a systematic review. PubMed, Embase and Lilacs database searches were performed for articles published in all languages ​​before October 1, 2020. The search was based on the keywords "Transcranial Direct Current Stimulation" or "tDCS" and "IL-1alpha " or "IL-1Beta" or "IL-6" or "IL-8" or "IL-17" or "Tumoral necrosis factor alpha" or "TNF-alpha". The systematic review protocol was registered in PROSPERO (CRD42021283417). Initially, 416 studies were identified in the electronic databases, of which 40 were eliminated because they were duplicates. Of the remaining 376, 358 were excluded after analyzing the title and abstract (selection stage) and 09 were excluded after a complete reading. Nine studies were considered for evaluation. The results demonstrate that tDCS can alter the levels of pro-inflammatory cytokines and modify behaviors in animals, however these findings are variable. Still, the cause and effect relationship between cytokine levels and behavioral changes found was not conclusive. Further studies are needed to establish the mechanisms involved in the action of tDCS on the levels of pro-inflammatory cytokines.

References

Abbas, A. K., Lichtman, A. H., & Pillai, S. (2014). Imunologia Básica: Funções e distúrbios do sistema imunológico. Elsevier, 539.

Allard-chamard, H., Mishra, H. K., Nandi, M., & Mayhue, M. (2020). Cytokine Interleukin-15 in autoimmunity. Cytokine, 136(August), 155258. https://doi.org/10.1016/j.cyto.2020.155258

Anderson, D. M., Kumaki, S., Ahdieh, M., Bertles, J., Tometsko, M., Loomis, A., Giri, J., Copeland, N. G., Gilbert, D. J., Jenkins, N. A., Valentine, V., Shapiro, D. N., Morris, S. W., Park, L. S., & Cosman, D. (1995). Functional characterization of the human interleukin-15 receptor α chain and close linkage of IL15RA and IL2RA genes. Journal of Biological Chemistry, 270(50), 29862–29869. https://doi.org/10.1074/jbc.270.50.29862

Baggiolini, M., & Clark-Lewis, I. (1992). Interleukin-8, a chemotactic and inflammatory cytokine. FEBS Letters, 307(1), 97–101. https://doi.org/10.1016/0014-5793(92)80909-Z

Barres, B. A., & Barde, Y. (2000). Neuronal and glial cell biology. 642–648.

Bingham, C. O. (2002). The pathogenesis of rheumatoid arthritis: Pivotal cytokines involved in bone degradation and imflammation. Journal of Rheumatology, 29(SUPPL. 65), 3–9.

Callai, E. M. M., Scarabelot, V. L., Fernandes Medeiros, L., de Oliveira, C., de Souza, A., Macedo, I. C., Cioato, S. G., Finamor, F., Caumo, W., Quevedo, A. da S., & Torres, I. L. S. (2019). Transcranial direct current stimulation (tDCS) and trigeminal pain: A preclinical study. Oral Diseases, 25(3), 888–897. https://doi.org/10.1111/odi.13038

Campos Kraychete, D., Thais de Andrade Calasans, M., & Motta Leal Valente, C. (2006). Citocinas Pró-inflamatórias e Dor Pro-inflammatory Cytokines and Pain. Rev Bras Reumatol, 46(3), 199–206.

Carswell, E. A., & Old, L. J. (1975). An endotoxin-induced serum factor that causes necrosis of tumors Immunology : 72(9), 3666–3670.

Cioato, S. G., Medeiros, L. F., Marques Filho, P. R., Vercelino, R., De Souza, A., Scarabelot, V. L., De Oliveira, C., Adachi, L. N. S., Fregni, F., Caumo, W., & Torres, I. L. S. (2016). Long-Lasting Effect of Transcranial Direct Current Stimulation in the Reversal of Hyperalgesia and Cytokine Alterations Induced by the Neuropathic Pain Model. Brain Stimulation, 9(2), 209–217. https://doi.org/10.1016/j.brs.2015.12.001

Covey, W. C., Ignatowski, T. A., Knight, P. R., & Spengler, R. N. (2000). Brain-derived TNFα : Involvement in neuroplastic changes implicated in the conscious perception of persistent pain. Brain Research, 859(1), 113–122. https://doi.org/10.1016/S0006-8993(00)01965-X

Cunha, F. Q., Poole, S., Lorenzetti, B. B., & Ferreira, S. H. (1992). The pivotal role of tumour necrosis factor a in the development of inflammatory hyperalgesia. 660–664.

Cycles, S. (1989). Chapter 9 Chapter 9. Cycle, 1897(Figure 1), 44–45.

de Oliveira, C., de Freitas, J. S., Macedo, I. C., Scarabelot, V. L., Ströher, R., Santos, D. S., Souza, A., Fregni, F., Caumo, W., & Torres, I. L. S. (2019). Transcranial direct current stimulation (tDCS) modulates biometric and inflammatory parameters and anxiety-like behavior in obese rats. Neuropeptides, 73(April 2018), 1–10. https://doi.org/10.1016/j.npep.2018.09.006

de Oliveira, C. M. B., Sakata, R. K., Issy, A. M., Gerola, L. R., & Salomão, R. (2011). Cytokines and Pain. Brazilian Journal of Anesthesiology, 61(2), 255–265. https://doi.org/10.1016/s0034-7094(11)70029-0

Deuis, J. R., Dvorakova, L. S., & Vetter, I. (2017). Methods used to evaluate pain behaviors in rodents. Frontiers in Molecular Neuroscience, 10(September), 1–17. https://doi.org/10.3389/fnmol.2017.00284

Dubový, P., Brázda, V., Klusáková, I., & Hradilová-Svíženská, I. (2013). Bilateral elevation of interleukin-6 protein and mRNA in both lumbar and cervical dorsal root ganglia following unilateral chronic compression injury of the sciatic nerve. Journal of Neuroinflammation, 10, 1–22. https://doi.org/10.1186/1742-2094-10-55

Floege, J., Lüscher, B., & Müller-newen, G. (2012). European Journal of Cell Biology Cytokines and inflammation. European Journal of Cell Biology, 91(6–7), 427. https://doi.org/10.1016/j.ejcb.2012.01.003

Fossiez, F., Djossou, O., Chomarat, P., Flores-Romo, L., Ait-Yahia, S., Maat, C., Pin, J. J., Garrone, P., Garcia, E., Saeland, S., Blanchard, D., Gaillard, C., Das Mahapatra, B., Rouvier, E., Golstein, P., Banchereau, J., & Lebecque, S. (1996). T cell interleukin-17 induces stromal cells to produce proinflammatory and hematopoietic cytokines. Journal of Experimental Medicine, 183(6), 2593–2603. https://doi.org/10.1084/jem.183.6.2593

Fregni, F., Boggio, P. S., Lima, M. C., Ferreira, M. J. L., Wagner, T., Rigonatti, S. P., Castro, A. W., Souza, D. R., Riberto, M., Freedman, S. D., Nitsche, M. A., & Pascual-Leone, A. (2006). A sham-controlled, phase II trial of transcranial direct current stimulation for the treatment of central pain in traumatic spinal cord injury. Pain, 122(1–2), 197–209. https://doi.org/10.1016/j.pain.2006.02.023

Gu, C., Wu, L., & Li, X. (2013). IL-17 family: Cytokines, receptors and signaling. Cytokine, 64(2), 477–485. https://doi.org/10.1016/j.cyto.2013.07.022

Guo, T., Fang, J., Tong, Z. Y., He, S., & Luo, Y. (2020). Transcranial Direct Current Stimulation Ameliorates Cognitive Impairment via Modulating Oxidative Stress, Inflammation, and Autophagy in a Rat Model of Vascular Dementia. Frontiers in Neuroscience, 14(January). https://doi.org/10.3389/fnins.2020.00028

Hedges, J. C., Singer, C. A., & Gerthoffer, W. T. (2000). Mitogen-activated protein kinases regulate cytokine gene expression in human airway myocytes. American Journal of Respiratory Cell and Molecular Biology, 23(1), 86–94. https://doi.org/10.1165/ajrcmb.23.1.4014

Heinricher, M. ., Tavares, I., Leith, J. L., & Lumb, B. M. (2010). Descending control of nociception. Brain, 60(1), 214–225. https://doi.org/10.1016/j.brainresrev.2008.12.009.Descending

Hooijmans, C. R., Rovers, M. M., De Vries, R. B. M., Leenaars, M., Ritskes-Hoitinga, M., & Langendam, M. W. (2014). SYRCLE’s risk of bias tool for animal studies. BMC Medical Research Methodology, 14(1), 1–9. https://doi.org/10.1186/1471-2288-14-43

Horváth, G., Gölöncsér, F., Csölle, C., Király, K., Andó, R. D., Baranyi, M., Koványi, B., Máté, Z., Hoffmann, K., Algaier, I., Baqi, Y., Müller, C. E., Von Kügelgen, I., & Sperlágh, B. (2014). Central P2Y12 receptor blockade alleviates inflammatory and neuropathic pain and cytokine production in rodents. Neurobiology of Disease, 70, 162–178. https://doi.org/10.1016/j.nbd.2014.06.011

Ignatowski, T. A., Covey, W. C., Knight, P. R., Severin, C. M., Nickola, T. J., & Spengler, R. N. (1999). Brain-derived TNFα mediates neuropathic pain. Brain Research, 841(1–2), 70–77. https://doi.org/10.1016/S0006-8993(99)01782-5

Jaiswal. (2014). 基因的改变NIH Public Access. Bone, 23(1), 1–7. https://doi.org/10.1016/j.cyto.2013.07.022.IL-17

Kostrzewa-Janicka, J., Jurkowski, P., Nedzi-Gora, M., & Mierzwinska-Nastalska, E. (2012). Inflammatory markers in temporomandibular joint disorders. Central-European Journal of Immunology, 37(3), 290–293. https://doi.org/10.5114/ceji.2012.30809

Kumolosasi, E., Bonhomme, A., Beorchia, A., Foudrinier, F., Marx, C., Pluot, M., & Pinon, J. M. (1996). Kinetics study of the localization and quantitation of target antigens of immunoglobulin a antibodies in acquired and congenital toxoplasmosis. Parasitology Research, 82(5), 402–409. https://doi.org/10.1007/s004360050136

Laste, G., Caumo, W., Adachi, L. N. S., Rozisky, J. R., De MacEdo, I. C., Filho, P. R. M., Partata, W. A., Fregni, F., & Torres, I. L. S. (2012). After-effects of consecutive sessions of transcranial direct current stimulation (tDCS) in a rat model of chronic inflammation. Experimental Brain Research, 221(1), 75–83. https://doi.org/10.1007/s00221-012-3149-x

Lefaucheur, J. P. (2006). Myoclonus and transcranial magnetic stimulation. Neurophysiologie Clinique, 36(5–6), 293–297. https://doi.org/10.1016/j.neucli.2006.12.008

Li, Q. Y., Xu, H. Y., & Yang, H. J. (2017). Effect of proinflammatory factors TNF-α,IL-1β, IL-6 on neuropathic pain. Zhongguo Zhong Yao Za Zhi = Zhongguo Zhongyao Zazhi = China Journal of Chinese Materia Medica, 42(19), 3709–3712. https://doi.org/10.19540/j.cnki.cjcmm.20170907.004

Liebetanz, D. (2002). Pharmacological approach to the mechanisms of transcranial DC-stimulation-induced after-effects of human motor cortex excitability. Brain, 125(10), 2238–2247. https://doi.org/10.1093/brain/awf238

Lima, M. C., & Fregni, F. (2008). Motor cortex stimulation for chronic pain: Systematic review and meta-analysis of the literature. Neurology, 70(24), 2329–2337. https://doi.org/10.1212/01.wnl.0000314649.38527.93

Lin, E., Calvano, S. E., & Lowry, S. F. (2000). Inflammatory cytokines and cell response in surgery. Surgery, 127(2), 117–126. https://doi.org/10.1067/msy.2000.101584

Lüttjohann, A., Fabene, P. F., & van Luijtelaar, G. (2009). A revised Racine’s scale for PTZ-induced seizures in rats. Physiology and Behavior, 98(5), 579–586. https://doi.org/10.1016/j.physbeh.2009.09.005

Machado, S., Bittencourt, J., Minc, D., Portella, C. E., Velasques, B., Cunha, M., Budde, H., Basile, L. F., Chadi, G., Cagy, M., Piedade, R., & Ribeiro, P. (2008). Therapeutic applications of repetitive transcranial magnetic stimulation in clinical neurorehabilitation. Functional Neurology, 23(3), 113–122.

Migliorini, P., Italiani, P., Pratesi, F., Puxeddu, I., & Boraschi, D. (2020). The IL-1 family cytokines and receptors in autoimmune diseases. Autoimmunity Reviews, 19(9), 102617. https://doi.org/10.1016/j.autrev.2020.102617

Mihara, M., Hashizume, M., Yoshida, H., Suzuki, M., & Shiina, M. (2012). IL-6/IL-6 receptor system and its role in physiological and pathological conditions. Clinical Science, 122(4), 143–159. https://doi.org/10.1042/CS20110340

Nitsche, M. A., & Paulus, W. (2000). Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. Journal of Physiology, 527(3), 633–639. https://doi.org/10.1111/j.1469-7793.2000.t01-1-00633.x

Nitsche, Michael A., Cohen, L. G., Wassermann, E. M., Priori, A., Lang, N., Antal, A., Paulus, W., Hummel, F., Boggio, P. S., Fregni, F., & Pascual-Leone, A. (2008). Transcranial direct current stimulation: State of the art 2008. Brain Stimulation, 1(3), 206–223. https://doi.org/10.1016/j.brs.2008.06.004

Nitsche, Michael A., & Paulus, W. (2001). Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans. Neurology, 57(10), 1899–1901. https://doi.org/10.1212/WNL.57.10.1899

Page, M. J., Moher, D., Bossuyt, P. M., Boutron, I., Hoffmann, T. C., Mulrow, C. D., Shamseer, L., Tetzlaff, J. M., Akl, E. A., Brennan, S. E., Chou, R., Glanville, J., Grimshaw, J. M., Hróbjartsson, A., Lalu, M. M., Li, T., Loder, E. W., Mayo-Wilson, E., Mcdonald, S., & Mckenzie, J. E. (2021). PRISMA 2020 explanation and elaboration: Updated guidance and exemplars for reporting systematic reviews. The BMJ, 372. https://doi.org/10.1136/bmj.n160

Patidar, M., Yadav, N., & Dalai, S. K. (2016). Interleukin 15: A key cytokine for immunotherapy. Cytokine and Growth Factor Reviews, 31, 49–59. https://doi.org/10.1016/j.cytogfr.2016.06.001

Plow, E. B., Pascual-Leone, A., & MacHado, A. (2012). Brain stimulation in the treatment of chronic neuropathic and non-cancerous pain. Journal of Pain, 13(5), 411–424. https://doi.org/10.1016/j.jpain.2012.02.001

Regner, G. G., Torres, I. L. S., de Oliveira, C., Pflüger, P., da Silva, L. S., Scarabelot, V. L., Ströher, R., de Souza, A., Fregni, F., & Pereira, P. (2020). Transcranial direct current stimulation (tDCS) affects neuroinflammation parameters and behavioral seizure activity in pentylenetetrazole-induced kindling in rats. Neuroscience Letters, 735. https://doi.org/10.1016/j.neulet.2020.135162

Rice, T., Larsen, J., Rivest, S., & Yong, V. W. (2007). Characterization of the early neuroinflammation after spinal cord injury in mice. Journal of Neuropathology and Experimental Neurology, 66(3), 184–195. https://doi.org/10.1097/01.jnen.0000248552.07338.7f

Russo, R. C., Garcia, C. C., Teixeira, M. M., & Amaral, F. A. (2014). The CXCL8/IL-8 chemokine family and its receptors in inflammatory diseases. Expert Review of Clinical Immunology, 10(5), 593–619. https://doi.org/10.1586/1744666X.2014.894886

Scarabelot, V. L., de Oliveira, C., Medeiros, L. F., de Macedo, I. C., Cioato, S. G., Adachi, L. N. S., Paz, A. H., de Souza, A., Caumo, W., & Torres, I. L. S. (2019). Transcranial direct-current stimulation reduces nociceptive behaviour in an orofacial pain model. Journal of Oral Rehabilitation, 46(1), 40–50. https://doi.org/10.1111/joor.12726

Silvetti, M., Alexander, W., Verguts, T., & Brown, J. W. (2014). From conflict management to reward-based decision making: Actors and critics in primate medial frontal cortex. Neuroscience and Biobehavioral Reviews, 46(P1), 44–57. https://doi.org/10.1016/j.neubiorev.2013.11.003

Spezia Adachi, L. N., Quevedo, A. S., de Souza, A., Scarabelot, V. L., Rozisky, J. R., de Oliveira, C., Marques Filho, P. R., Medeiros, L. F., Fregni, F., Caumo, W., & Torres, I. L. S. (2015). Exogenously induced brain activation regulates neuronal activity by top-down modulation: conceptualized model for electrical brain stimulation. Experimental Brain Research, 233(5), 1377–1389. https://doi.org/10.1007/s00221-015-4212-1

Stagg, C. J., & Nitsche, M. A. (2011). Physiological basis of transcranial direct current stimulation. Neuroscientist, 17(1), 37–53. https://doi.org/10.1177/1073858410386614

Thelin, E. P., Hall, C. E., Tyzack, G. E., Frostell, A., Giorgi-Coll, S., Alam, A., Carpenter, K. L. H., Mitchell, J., Tajsic, T., Hutchinson, P. J., Patani, R., & Helmy, A. (2020). Delineating astrocytic cytokine responses in a human stem cell model of neural trauma. Journal of Neurotrauma, 37(1), 93–105. https://doi.org/10.1089/neu.2019.6480

Thornberry, C., Cimadevilla, J. M., & Commins, S. (2021). Virtual Morris water maze: Opportunities and challenges. Reviews in the Neurosciences, 32(8), 887–903. https://doi.org/10.1515/revneuro-2020-0149

Vanderwall, A. G., Milligan, E. D., & Talbot, S. (2019). Cytokines in Pain : Harnessing Endogenous Anti-Inflammatory Signaling for Improved Pain Management Peripheral Immune Actions in Pathological. 10(December), 1–15. https://doi.org/10.3389/fimmu.2019.03009

Watkins, L. R., Wiertelak, E. P., Goehler, L. E., Mooney-Heiberger, K., Martinez, J., Furness, L., Smith, K. P., & Maier, S. F. (1994). Neurocircuitry of illness-induced hyperalgesia. Brain Research, 639(2), 283–299. https://doi.org/10.1016/0006-8993(94)91742-6

Watkins, Linda R., & Maier, S. F. (2002). Beyond neurons: Evidence that immune and glial cells contribute to pathological pain states. Physiological Reviews, 82(4), 981–1011. https://doi.org/10.1152/physrev.00011.2002

Wieseler-Frank, J., Maier, S. F., & Watkins, L. R. (2005). Central proinflammatory cytokines and pain enhancement. NeuroSignals, 14(4), 166–174. https://doi.org/10.1159/000087655

Yana, H. Q., Banes, M. A., Herregodtso, P., Hooghe, R., & Hooghe-petersb, E. L. (1992). Expression of interleukin ( IL ) = lp , IL-6 and their respective receptors in the normal rat brain and after injury ". 2963–2971.

Yasuda, K., Nakanishi, K., & Tsutsui, H. (2019). Interleukin-18 in health and disease. International Journal of Molecular Sciences, 20(3). https://doi.org/10.3390/ijms20030649

Zhou, H., & Rigoutsos, I. (2014). The emerging roles of GPRC5A in diseases. Oncoscience, 1(12), 765–776. https://doi.org/10.18632/oncoscience.104

Downloads

Published

28/09/2022

How to Cite

GALVAGNI, L. E. .; ANDRADE, I. N. .; BRUNHERI, V.; CALLAI, E. M. M.; CATARINA , L. S. .; QUEVEDO, D. M. de; PONZONI, D.; QUEVEDO, A. S. . Effects of transcranial direct current stimulation (tDCS) on pro-inflammatory cytokines: a systematic review. Research, Society and Development, [S. l.], v. 11, n. 13, p. e72111335013, 2022. DOI: 10.33448/rsd-v11i13.35013. Disponível em: https://rsdjournal.org/index.php/rsd/article/view/35013. Acesso em: 23 nov. 2024.

Issue

Section

Health Sciences