Stress-induced hyperalgesia

Jennings, Elaine M.; Okine, Bright N.; Roche, Michelle; Finn, David P.

doi:10.1016/j.pneurobio.2014.06.003

Cited by 318Pain Mechanisms and TreatmentsStress Responses and CortisolPain Management and Treatment

Stress-induced hyperalgesia

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Jennings, Elaine M., Okine, Bright N., Roche, Michelle, Finn, David P.·2014·Progress in Neurobiology

DOI 10.1016/j.pneurobio.2014.06.003

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Abstract

The importance of the modulation of pain by emotion is now widely recognised. In particular, stress and anxiety, depending on their nature, duration and intensity, can exert potent, but complex, modulatory influences typified by either a reduction or exacerbation of the pain state. Exposure to either acute or chronic stress can increase pain responding under experimental conditions and exacerbate clinical pain disorders. There is evidence that exposure to chronic or repeated stress can produce maladaptive neurobiological changes in pathways associated with pain processing, resulting in stress-induced hyperalgesia (SIH). Preclinical studies of SIH are essential for our understanding of the mechanisms underpinning stress-related pain syndromes and for the identification of neural pathways and substrates, and the development of novel therapeutic agents for their clinical management. In this review, we describe clinical and pre-clinical models used to study SIH and discuss the neural substrates, neurotransmitters and neuromodulatory systems involved in this phenomenon.

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Dysregulation of allostatic systems can manifest as either hypo- or hyper-responsiveness to stress later in life, with consequent impairment in endogenous pain regulation.
“However, dysregulation of allostatic systems can manifest as either hypo- or hyper- responsiveness to stress later in life,(14–16) with consequent impairment in endogenous pain regulation.(17–19)”
From Effects of Mindfulness-Based Stress Reduction on Experimental Pain Sensitivity and Cortisol Responses in Women with Early Life Abuse: A Randomized Controlled Trial (2021) · cites this paper as [18]

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Experimental hypoglycemia is a human model of stress-induced hyperalgesia
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Stress enhances muscle nociceptor activity in the rat
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Alterations in Prefrontal-Limbic Functional Activation and Connectivity in Chronic Stress-Induced Visceral Hyperalgesia
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Activation of Extracellular Signal-Regulated Protein Kinase is Associated with Colorectal Distension-Induced Spinal and Supraspinal Neuronal Response and Neonatal Maternal Separation-Induced Visceral Hyperalgesia in Rats
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Deletion of the CCK2 receptor gene reduces mechanical sensitivity and abolishes the development of hyperalgesia in mononeuropathic mice
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Chronic stress mediators act synergistically on colonic nociceptive mouse dorsal root ganglia neurons to increase excitability
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Involvement of post‐translational modification of neuronal plasticity‐related proteins in hyperalgesia revealed by a proteomic analysis
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Neonatal Maternal Separation Increases Brain-Derived Neurotrophic Factor and Tyrosine Kinase Receptor B Expression in the Descending Pain Modulatory System
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Depressive State With Anxiety in Repeated Cold-Stressed Mice in Forced Swimming Tests
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Lateralized amygdala activation: Importance in the regulation of anxiety and pain behavior
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Selective ablation of mu-opioid receptor expressing neurons in the rostral ventromedial medulla attenuates stress-induced mechanical hypersensitivity
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Resiniferatoxin (RTX) Causes a Uniquely Protracted Musculoskeletal Hyperalgesia in Mice by Activation of TRPV1 Receptors
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PKCγ Receptor Mediates Visceral Nociception and Hyperalgesia following Exposure to PTSD-Like Stress in the Spinal Cord of Rats
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Neck pain: global epidemiology, trends and risk factors
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Fibromyalgia: Pathogenesis, Mechanisms, Diagnosis and Treatment Options Update
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A Brainstem-Spinal Cord Inhibitory Circuit for Mechanical Pain Modulation by GABA and Enkephalins
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The cannabinoid system and pain
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Psychological stress in early life as a predisposing factor for the development of chronic pain: clinical and preclinical evidence and neurobiological mechanisms
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Social transfer of pain in mice
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Emotion regulation and the salience network: a hypothetical integrative model of fibromyalgia
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Managing Chronic Pain in Children and Adolescents: A Clinical Review
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Discrimination hurts: The effect of discrimination on the development of chronic pain
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Stress-induced modulation of pain: Role of the endogenous opioid system
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Emotional and Cognitive Influences on Pain Experience
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Different contexts, different pains, different experiences
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The gut microbiota as a key regulator of visceral pain
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The Role of the Brain's Endocannabinoid System in Pain and Its Modulation by Stress
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Can positive affect attenuate (persistent) pain? State of the art and clinical implications
Hanssen, M. M., Peters, M. L., Boselie, J. J. L. M., & Meulders, A. (2017) · Current Rheumatology Reports · doi:10.1007/s11926-017-0703-3 · Cited by 83 · see citing works
Neuropathic pain, mood, and stress-related disorders: A literature review of comorbidity and co-pathogenesis
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Nociceptive Cortical Activity Is Dissociated from Nociceptive Behavior in Newborn Human Infants under Stress
Jones, L., Lorenzo Fabrizi, D., Laudiano‐Dray, M. P., Whitehead, K., Meek, J. H., Verriotis, M., & Fitzgerald, M. (2017) · Current Biology · doi:10.1016/j.cub.2017.10.063 · Cited by 77 · see citing works
Chronic stress exacerbates neuropathic pain via the integration of stress-affect–related information with nociceptive information in the central nucleus of the amygdala
Li, M.-J., Liu, L., Chen, L., Cai, J., Wan, Y., & Xing, G. (2016) · Pain · doi:10.1097/j.pain.0000000000000827 · Cited by 75 · see citing works
PPARs and pain
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The Early Impact of COVID-19 on Chronic Pain: A Cross-Sectional Investigation of a Large Online Sample of Individuals with Chronic Pain in the United States, April to May, 2020
Mun, C. J., Campbell, C., McGill, L., & Aaron, R. V. (2021) · Pain medicine (Malden, Mass.) · doi:10.1093/pm/pnaa446 · Cited by 67 · see citing works
Pain in Times of Stress.
Ahmad, A. H., & Zakaria, R. (2015) · Europe PMC (PubMed Central) · Cited by 63 · see citing works
Hippocampal activation of microglia may underlie the shared neurobiology of comorbid posttraumatic stress disorder and chronic pain
Sun, R., Zhang, Z., Lei, Y., Liu, Y., Lu, C., Rong, H., Sun, Y., Zhang, W., Ma, Z., & Gu, X. (2016) · Molecular Pain · doi:10.1177/1744806916679166 · Cited by 63 · see citing works
Challenges and opportunities in translational pain research – An opinion paper of the working group on translational pain research of the European pain federation (EFIC)
Mouraux, A., Bannister, K., Becker, S., Finn, D. P., Pickering, G. P., Pogatzki-Zahn, E. M., & Graven‐Nielsen, T. (2021) · European Journal of Pain · doi:10.1002/ejp.1730 · Cited by 61 · see citing works
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Activation of acid-sensing ion channel 3 by lysophosphatidylcholine 16:0 mediates psychological stress-induced fibromyalgia-like pain
Hung, C.-H., Lee, C.-H., Tsai, M.-H., Chen, C.-H., Lin, H.-F., Hsu, C.-Y., Lai, C.-L., & Chen, C.-C. (2020) · Annals of the Rheumatic Diseases · doi:10.1136/annrheumdis-2020-218329 · Cited by 65 · see citing works
Short-Term Sleep Disturbance–Induced Stress Does not Affect Basal Pain Perception, but Does Delay Postsurgical Pain Recovery
Wang, P., Cao, J., Wang, H., Liang, L., Zhang, J., Lutz, B. M., Shieh, K.-R., Bekker, A., & Tao, Y. (2015) · Journal of Pain · doi:10.1016/j.jpain.2015.07.006 · Cited by 60 · see citing works
High Times for Painful Blues: The Endocannabinoid System in Pain-Depression Comorbidity
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Chloride – The Underrated Ion in Nociceptors
Wilke, B. U., Kummer, K. K., Leitner, M. G., & Kress, M. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.00287 · Cited by 56 · see citing works
Neuroimmune interactions in chronic pain – An interdisciplinary perspective
Hore, Z. L., & Denk, F. (2019) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2019.04.033 · Cited by 54 · see citing works
Psychogenic stress in hospitalized veterinary patients: Causation, implications, and therapies
Lefman, S. H., & Prittie, J. E. (2019) · Journal of Veterinary Emergency and Critical Care · doi:10.1111/vec.12821 · Cited by 61 · see citing works
Stressinduzierte Hyperalgesie (SIH) als Folge von emotionaler Deprivation und psychischer Traumatisierung in der Kindheit
Egle, U. T., Egloff, N., & von Känel, R. (2016) · Der Schmerz · doi:10.1007/s00482-016-0107-8 · Cited by 52 · see citing works
Effect of transportation and social isolation on facial expressions of healthy horses
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Stress Induces Pain Transition by Potentiation of AMPA Receptor Phosphorylation
Li, C., Yang, Y., Liu, S., Fang, H., Zhang, Y., Furmanski, O., SKINNER, J. T., Xing, Y., Johns, R. A., Huganir, R. L., et al. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.2130-14.2014 · Cited by 52 · see citing works
From Pavlov to pain: How predictability affects the anticipation and processing of visceral pain in a fear conditioning paradigm
Labrenz, F., Icenhour, A., Schlamann, M. U., Forsting, M., Bingel, U., & Elsenbruch, S. (2016) · NeuroImage · doi:10.1016/j.neuroimage.2016.01.064 · Cited by 46 · see citing works
Chronic stress‐induced mechanical hyperalgesia is controlled by capsaicin‐sensitive neurones in the mouse
Scheich, B., Vincze, P., Szőke, É., Borbély, É., Hunyady, Á., Szolcsányi, J., Dénes, Á., Környei, Z., Gaszner, B., & Helyes, Z. (2017) · European Journal of Pain · doi:10.1002/ejp.1043 · Cited by 48 · see citing works
A refinement to the formalin test in mice
Lopes, D. M., Cater, H. L., Thakur, M., Wells, S. E., & McMahon, S. B. (2019) · F1000Research · doi:10.12688/f1000research.18338.1 · Cited by 48 · see citing works
Switch of serotonergic descending inhibition into facilitation by a spinal chloride imbalance in neuropathic pain
Aby, F., Lorenzo, L.-É., Grivet, Z., Bouali‐Benazzouz, R., Martin, H., Valério, S., Whitestone, S., Isabel, D., Idi, W., Bouchatta, O., et al. (2022) · Science Advances · doi:10.1126/sciadv.abo0689 · Cited by 47 · see citing works
Gesundheitliche Langzeitfolgen psychosozialer Belastungen in der Kindheit – ein Update
Egle, U. T., Franz, M., Joraschky, P., Lampe, A., Seiffge‐Krenke, I., & Cierpka, M. (2016) · Bundesgesundheitsblatt - Gesundheitsforschung - Gesundheitsschutz · doi:10.1007/s00103-016-2421-9 · Cited by 47 · see citing works
Comparing Central Pain Processing in Individuals With Non-Traumatic Neck Pain and Healthy Individuals: A Systematic Review and Meta-Analysis
Xie, Y., Jun, D., Thomas, L. C., Coombes, B. K., & Johnston, V. (2020) · Journal of Pain · doi:10.1016/j.jpain.2020.02.007 · Cited by 47 · see citing works
Anxious anticipation and pain: the influence of instructed vs conditioned threat on pain
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Glucocorticoid-Potentiated Spinal Microglia Activation Contributes to Preoperative Anxiety-Induced Postoperative Hyperalgesia
Sun, R., Zhao, Z., Feng, J., Bo, J., Rong, H., Lei, Y., Lu, C., Zhang, X., Hou, B., Sun, Y., et al. (2016) · Molecular Neurobiology · doi:10.1007/s12035-016-9976-1 · Cited by 45 · see citing works
Experiencing early life maternal separation increases pain sensitivity in adult offspring
Vilela, F. C., Vieira, J. S., Giusti‐Paiva, A., & da Silva, M. L. (2017) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2017.07.003 · Cited by 45 · see citing works
The Neurobiology of Stress
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The Locus Coeruleus–Norepinephrine System Mediates Empathy for Pain through Selective Up-Regulation of P2X3 Receptor in Dorsal Root Ganglia in Rats
Lü, Y.-F., Yang, Y. L., Li, C.-L., Wang, Y., Li, Z., & Chen, J. (2017) · Frontiers in Neural Circuits · doi:10.3389/fncir.2017.00066 · Cited by 44 · see citing works
Cannabinoids and the endocannabinoid system in fibromyalgia: A review of preclinical and clinical research
Bourke, S. L., Schlag, A. K., O’Sullivan, S. E., Nutt, D., & Finn, D. P. (2022) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2022.108216 · Cited by 45 · see citing works
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Restraint training for awake functional brain scanning of rodents can cause long-lasting changes in pain and stress responses
Low, L. A., Bauer, L. C., Pitcher, M. H., & Bushnell, M. C. (2016) · Pain · doi:10.1097/j.pain.0000000000000579 · Cited by 43 · see citing works
Experiencing neonatal maternal separation increased pain sensitivity in adult male mice: Involvement of oxytocinergic system
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Authors: Jennings, E. M., Okine, B. N., Roche, M., & Finn, D. P.
Affiliations: Ollscoil na Gaillimhe – University of Galway (IE)
Corresponding author: Finn, David P.
ORCID: Okine, Bright N.
Roche, Michelle
Finn, David P.
Venue: Progress in Neurobiology
Publisher: Elsevier BV
Published: 2014-10
Volume: 121
Pages: 1-18
ISSN: 0301-0082 (ISSN-L)
DOI: 10.1016/j.pneurobio.2014.06.003
OpenAlex: W2035912882
Cited by: 318
References: 218
Citations by year: 2026: 25 · 2025: 25 · 2024: 35 · 2023: 26 · 2022: 29 · 2021: 21 · 2020: 26 · 2019: 21 · 2018: 17 · 2017: 40 · 2016: 31 · 2015: 19 · 2014: 1 · 2013: 1
FWCI: 3.55
Type: journal article
Language: en
Open access: green
doi.org
Licence: cc-by-nc-nd
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Progress in Neurobiology (publishedVersion)
PubMed (publishedVersion)
ARAN (University of Galway Research Repository) (Ollscoil na Gaillimhe – University of Galway) (acceptedVersion, cc-by-nc-nd)
Arrow@dit (Dublin Institute of Technology) (acceptedVersion)
University of Galway Research Repository (submittedVersion, cc-by)
Funders: Science Foundation Ireland (10/IN.1/B2976)
Topics: Health Sciences › Medicine › Physiology › Pain Mechanisms and Treatments
Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Health Sciences › Medicine › Anesthesiology and Pain Medicine › Pain Management and Treatment
Keywords: stress-induced hyperalgesia, chronic stress, anxiety, pain modulation, emotional pain, pain processing, neural correlates, neurotransmitters, neuromodulatory systems, preclinical models, clinical model
MeSH terms: Animals, Brain, Humans, Hyperalgesia, Pain, Spinal Cord, Stress, Psychological

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Stress-induced hyperalgesia

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