Transcranial Direct Current Stimulation to Improve the Dysfunction of Descending Pain Modulatory System Related to Opioids in Chronic Non-cancer Pain: An Integrative Review of Neurobiology and Meta-Analysis

Maxciel Zortea, Leticia Ramalho, Rael Lopes Alves, Camila Fernanda da Silveira Alves, Gilberto Braulio, Iraci Lucena da Silva Torres, Felipe Fregni, Wolnei Caumo, Maxciel Zortea, Leticia Ramalho, Rael Lopes Alves, Camila Fernanda da Silveira Alves, Gilberto Braulio, Iraci Lucena da Silva Torres, Felipe Fregni, Wolnei Caumo

Abstract

Background: Opioid long-term therapy can produce tolerance, opioid-induced hyperalgesia (OIH), and it induces dysfunction in pain descending pain inhibitory system (DPIS). Objectives: This integrative review with meta-analysis aimed: (i) To discuss the potential mechanisms involved in analgesic tolerance and opioid-induced hyperalgesia (OIH). (ii) To examine how the opioid can affect the function of DPIS. (ii) To show evidence about the tDCS as an approach to treat acute and chronic pain. (iii) To discuss the effect of tDCS on DPIS and how it can counter-regulate the OIH. (iv) To draw perspectives for the future about the tDCS effects as an approach to improve the dysfunction in the DPIS in chronic non-cancer pain. Methods: Relevant published randomized clinical trials (RCT) comparing active (irrespective of the stimulation protocol) to sham tDCS for treating chronic non-cancer pain were identified, and risk of bias was assessed. We searched trials in PubMed, EMBASE and Cochrane trials databases. tDCS protocols accepted were application in areas of the primary motor cortex (M1), dorsolateral prefrontal cortex (DLPFC), or occipital area. Results: Fifty-nine studies were fully reviewed, and 24 with moderate to the high-quality methodology were included. tDCS improved chronic pain with a moderate effect size [pooled standardized mean difference; -0.66; 95% confidence interval (CI) -0.91 to -0.41]. On average, active protocols led to 27.26% less pain at the end of treatment compared to sham [95% CI; 15.89-32.90%]. Protocol varied in terms of anodal or cathodal stimulation, areas of stimulation (M1 and DLPFC the most common), number of sessions (from 5 to 20) and current intensity (from 1 to 2 mA). The time of application was 20 min in 92% of protocols. Conclusion: In comparison with sham stimulation, tDCS demonstrated a superior effect in reducing chronic pain conditions. They give perspectives that the top-down neuromodulator effects of tDCS are a promising approach to improve management in refractory chronic not-cancer related pain and to enhance dysfunctional neuronal circuitries involved in the DPIS and other pain dimensions and improve pain control with a therapeutic opioid-free. However, further studies are needed to determine individualized protocols according to a biopsychosocial perspective.

Keywords: descending pain inhibitory system; hyperalgesia; opioid; pain; tDCS.

Copyright © 2019 Zortea, Ramalho, Alves, Alves, Braulio, Torres, Fregni and Caumo.

Figures

Figure 1
Figure 1
Cell mechanisms of opioids action. In presynaptic neuron have inhibition of intracellular calcium influx and impairment in neurotransmitters release. In a postsynaptic neuron, cascade events induce to hyperpolarization state. cAMP, cyclic adenosine monophosphate; RPBE, response of cAMP to the protein binding element; Ca2+, calcium; K+, potassium; Na+, sodium; +, excitatory; –, inhibitory. 1. Inhibition of adenylate cyclase reduces the cyclic adenosine monophosphate (cAMP); and second messengers. 2. With this, cAMP reduction allow the openness of the potassium channels and promote the postsynaptic cell hyperpolarization. 3. The concomitant activation of presynaptic opioid receptors of C and Aδ fiber inhibits indirectly calcium influx, which decreases cAMP levels and blocks neurotransmitters release—glutamate, substance P and calcitonin gene-related peptide (CGRP).
Figure 2
Figure 2
Schematic representation of neuronal mechanisms underlying opioid tolerance development. Tolerance event: Decreases membrane potential threshold, increases the action-potential duration (APD), and increases neurotransmitter release. APD, action-potential duration; IEG, immediate early genes (c-Fos, FosB); PKA, protein Kinase A; CREB, cAMP response element-binding protein; pCREB, phosphorylated CREB protein; Gi/o, inhibitory G protein; Gs, excitatory G protein; CaMK-II, calcium/calmodulin dependent protein kinase II; PLA2, phospholipase A2; NO, nitric oxide; nNOS, neuronal nitric oxide synthase; HPETE, hydroperoxyeicosatetraenoic acid; +, excitatory; –, inhibitory.
Figure 3
Figure 3
Mechanisms engaged in the formation and maintenance of OIH. OIH, Hyperalgesia induced by opioids; BDNF, brain derived neurotrophic factor; Cx3Cl1, chemokine Cx3Cl1; EAAC1, glutamate transporter EAAC1; GABAR, gamma aminobutyric acid receptor; GRK, G protein coupled receptor kinase; IL1β, interleukin beta; IP3, inositol triphosphate; KCC2, K+/Cl cotransporter 2; LTP, long-term potentiation; MOR, mu-opioid receptor; mTOR, mammalian target of rapamycin; NO, nitric oxide; NOS, nitric oxide synthase; NK1, neurokinin 1 receptor; NMDAR, N-methyl-D-aspartic acid receptor; PKC, protein kinase C; SP, substance P; TNFα, tumor necrosis factor alpha; TrkB, tyrosine kinase B; TRPV1, transient receptor potential vanilloid 1; Ca2+, calcium; Cl−, chlorine; +, excitatory; –, inhibitory. (1) Morphine activates the neuronal MOR and generates an intracellular process that culminates in the OIH; (2) Signaling mTOR is activated by morphine engaged in neuroexcitation that lead to OIH; (3) The synaptic concentration of glutamate is elevated when the glutamate transporter EEAC1 are blocked by morphine. (4) Glutamate coupling in your NMDA receptors activates the calcium influx inducing the LTP that lead an OIH. (5) The BDNF receptor TrkB reduces the action of the cotransporter KCC2 evolved in ions chlorine homeostasis that modifies the inhibitory function of GABA for an excitatory function that which promote OIH. (6) Morphine also activates the glial cells and neurons that generate pro-inflammatory cytokines (IL1β and TNFα) that induce LTP and lead to OIH.
Figure 4
Figure 4
Areas of the brain that induction the descending pain inhibitory system composed by PAG-RVM-spinal cord pathway. TH, Thalamus; HT, hypothalamus; AMY, amygdala; NCF, nucleus cuneiforms; PAG, periaqueductal gray matter; DLPT, dorsolateral pontine tegmentum; RVM, rostral ventromedial medulla. (1) Cortical regions as cingulate and insula cortex as also the subcortical regions how the thalamus, hypothalamus, and amygdala project signals for the PAG, gray substance located in the midbrain, that receives stimulus and send inhibitory impulses across the medial and lateral tracts of the CNS. (2) Medial tract: inhibitory and facilitatory influence of the neurotransmitter serotonin in the pain activeness. (3) Lateral tract: dominant activity of neurotransmitter noradrenaline. (4) Fired inhibitory stimulus go down throughout dorsal horn of the spinal cord segment. The painful stimuli are sent to the second order neurons. Endorphins, noradrenaline, and serotonin, inhibitory neurotransmitters, are released activation of the inhibitory interneurons.
Figure 5
Figure 5
M1, Primary motor cortex; DLPFC, dorsolateral prefrontal cortex; S1, primary somatosensory cortex; S2, secondary somatosensory cortex; PFC, prefrontal cortex; ACC, anterior cingulate cortex; PCC, posterior cingulate cortex; INS, Insula; TH–VPL, thalamus-ventral posterolateral nucleus; TH-MD, thalamus-medial dorsal nucleus; HT, hypothalamus; AMY, Amygdala; PAG, periaqueductal gray matter;RVM, rostral ventromedial medulla; NMDAR, N-methyl-D-aspartate receptor; AMPAR, α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor; Trk, Tropomyosin receptor kinase; Ca2+, calcium; K+, potassium; Na+, sodium; Mg2, magnesium; +, excitatory; -, inhibitory; L-LTP, late long-term potentiation. (1) The anodal tDCS increases the intracellular Ca2+ flow that releases more neurotransmitters. (2) The positive regulation of neurotransmitters facilitates the openness of AMPA channels and indirectly of NMDA channels, which characterizes the long-term potentiation (LTP). (3) Activation of tropomyosin receptor (Trk) indicates the role of brain-derived neurotrophic factor (BDNF) in the anodal tDCS; its effect increases the production of the synaptic vesicles and the neurotransmitter release. (4) Increase of Ca2+ flow promotes the release of neurotrophic factors for the synaptic cleft. (5) Post-synaptic Trk receptor induces the late LTP (L-LTP) and favors the openness of the NMDA channels, which reinforces the L-LTP. (6) Both L-LTP and L-LTD are highly dependent on the modification of gene expression.
Figure 6
Figure 6
Flowchart of the systematized search.
Figure 7
Figure 7
Forest plot of the effects of tDCS on pain levels for all studies reviewed (n = 23).
Figure 8
Figure 8
Forest plot of the effects of anodal M1 tDCS on pain levels (n = 20).
Figure 9
Figure 9
Forest plot of the effects of anodal DLPFC tDCS on pain levels (n = 4).
Figure 10
Figure 10
Assessment of risk of bias from the reviewed studies (n = 24).

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